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Fiber Pathways of the Brain$

Jeremy D. Schmahmann and Deepak N. Pandya

Print publication date: 2006

Print ISBN-13: 9780195104233

Published to Oxford Scholarship Online: May 2009

DOI: 10.1093/acprof:oso/9780195104233.001.0001

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Fronto-Occipital Fasciculus

Fronto-Occipital Fasciculus

Chapter:
(p.455) 19 Fronto-Occipital Fasciculus
Source:
Fiber Pathways of the Brain
Author(s):

Jeremy D. Schmahmann

Deepak N. Pandya

Publisher:
Oxford University Press
DOI:10.1093/acprof:oso/9780195104233.003.0019

Abstract and Keywords

The fronto-occipital fasciculus (FOF), also known as the occipitofrontal fasciculus, is one of the long association systems of the dorsal visual stream. The subcallosal fasciculus of Muratoff that links the cerebral cortex with the caudate nucleus was mistaken for the FOF, and this conceptual and terminological confusion continues to the present day. This chapter begins with historical accounts of the FOF and Muratoff bundles. It then presents the results of the investigation of the FOF of rhesus monkey brain. Observations confirm the existence of the FOF where Dejerine located it in the human, and provide compelling evidence that it is a true association fasciculus linking parieto-occipital regions with the dorsolateral premotor and prefrontal areas. The present study also adds detail to the understanding of its location and to the origin and termination of its fibers.

Keywords:   Muratoff, cerebral cortex, rhesus monkey brain, fibers, dorsal visual stream, Dejerine

The Fronto-Occipital Fasciculus and the Subcallosal Fasciculus of Muratoff: Separate Pathways with a Shared History

The fronto-occipital fasciculus (FOF), also known as the occipitofrontal fasciculus, is one of the long association systems of the dorsal visual stream. Like the inferior longitudinal fasciculus (ILF) that subserves the ventral visual stream in the occipitotemporal region, the existence, course, and composition of the FOF have long been mired in controversy. The confusion surrounding the FOF, as well as the probably spurious “inferior fronto-occipital fasciculus” (see chapter 18), has persisted in current anatomical texts and is being propagated in contemporary DTI literature. The subcallosal fasciculus of Muratoff that links the cerebral cortex with the caudate nucleus was mistaken for the FOF, and this conceptual and terminological confusion continues to the present day. The tapetum is the extension into the hemispheres of the corpus callosum, lying adjacent to the ventricular ependyma. This is not dealt with in detail in our work but is included in this historical review because it featured prominently in earlier discussions as a part of the FOF. In the text that follows the FOF and Muratoff bundle are discussed individually, but the historical accounts of these bundles and also of the tapetum are so interwoven that it is useful first to consider them together to understand the difficulties encountered by earlier anatomists.

“Sachs-Probst Bundles “Mistaken for the FOF

The initial misidentification of the FOF arose as a consequence of a frank error in logic while studying the fiber tracts in brains of individuals with agenesis of the corpus callosum. The subsequent clear understanding of the FOF was also hampered by the methodologies available to earlier investigators. Congenital absence of the corpus callosum was first described by Reil (1812b) and in later subsequent reports, all of which contained scant clinical and pathological information (see Bruce, 1887–1888). In 1875, Knox studied such a brain and described a medially situated “lamina of white matter of considerable thickness, apparently having no attachment to corpus striatum.” This observation was replicated by Eichler (1878) and Urquhart (1880).

In 1881 Forel presented a report on a case of agenesis of the corpus callosum to the Assembly of German Natural Scientists and Physicians in Salzburg. The contribution of Forel’s student, Onufrowicz, in 1887 is of considerable historical as well as contemporary interest.1 He presented a clinical account of this patient’s course2 before describing the anatomical features of the brain. The preservation of the brain was suboptimal,3 but Onufrowicz was nevertheless able to describe its anatomic features:

(p.456)

                         Fronto-Occipital Fasciculus

Figure 19-1 Reproductions of the original diagrams showing the longitudinal callosal bundle in cases of callosal agenesis that were misidentified as an association fiber tract linking the frontal and occipital lobes. The misplaced callosal fibers (the correct identification of which may be attributed to Sachs and Probst) are shown in A, figure 5 from Onufrowicz’s (1887) original paper, a coronal section in which he labeled the callosal fibers the “Ass. occ. front” (arrow). B, Figure 7 from Onufrowicz (1887) as reproduced by Dejerine (1895), in which “OF” points to the aberrant callosal fibers in a more caudal coronal section of the same brain (arrow). C, Coronal section of figure IX from the brain studied by Kaufmann (1888), who also misidentified the Sachs-Probst callosal fibers as the FOF (arrow and asterisk).

The septum pellucidum borders directly on the medial aspect of the cortex as well as the hemispheric white matter. The latter, i.e., the hemispheric white matter, forms at this location, a peculiar, massive, pear-shaped structure, sharply delineated in coronal section (the occipital frontal association system) which instead of the corpus callosum, forms the dorsal wall of the anterior horn of the lateral ventricle. The dorsal as well as the ventral leaf of the corpus callosum is missing completely (Onufrowicz, 1887, p. 316; figure 19-1A,B).

In addition to our fiber bundle, we recognized here the projection fibers of the occipital lobe in the posterior part of the internal capsule (optic radiations of Gratiolet/bundle H of Flechsig/projection tracts). We also see the well-developed inferior longitudinal fasciculus (association fibers of the temporal lobe to the occipital lobe). [See chapter 18 for discussion of the inferior longitudinal fasciculus. Onufrowicz here refers to what we now understand to be the sagittal stratum.] Furthermore, the comparison of coronal sections of a normal brain with those of our case of agenesis of the corpus callosum leads us to recognize that the tapetum of the corpus callosum in the normal brain is in fact the direct continuation of our occipital frontal association bundle, and the tapetum certainly does not belong to the callosal fibers (Onufrowicz, p. 318).

Despite the complete absence of the corpus callosum, the tapetum of the corpus callosum and the lateral appendix of the forceps of the corpus callosum have not disappeared, rather they are strongly developed, while the actual forceps (p.457) of the corpus callosum is missing completely. This is clear evidence that the fibers in the tapetum of the corpus callosum do not belong to the corpus callosum, but to the longer association fiber systems of the hemisphere. We have thus seen that the part of the tapetum of the corpus callosum positioned close to the posterior horn seems to transition into the forceps, and in fact belongs to our occipital frontal association bundle. Because the radiation of the corpus callosum into the corona radiata is missing, a massive association system of the frontal lobe to the occipital lobe is clearly seen, isolated with utmost clarity. In the normal brain, this structure is intermingled with callosal fibers so that it cannot be distinguished from the other diffuse fibers of the corona radiata, and for this reason, it has been overlooked until the present time. In the occipital lobe, this bundle is represented by the so-called tapetum of the corpus callosum and the lateral continuation of the forceps of the corpus callosum, which gradually diminishes caudally. This fiber tract should best be termed the frontal occipital association bundle or the true superior longitudinal fasciculus. The genius Burdach recognized this fiber tract, or more accurately, he probably guessed it, and called it the arcuate fasciculus or the superior longitudinal fasciculus. But neither his nor Meynert’s descriptions of this bundle are clear, and the fact is that it is impossible to see it in a normal brain. We were able to recognize its location between the fibers of the corpus callosum only after comparison with our experiment of nature, in the case of agenesis of the corpus callosum (Onufrowicz, p. 322).

Eduard Kaufmann (1887, 1888) concurred with Onufrowicz. He sectioned the brain of a patient with callosal agenesis (1888, p. 229):

in the frontal plane. Special consideration was given to the previously discussed association systems of the gyrus fornicatus [cingulate gyrus]. It soon became clear that the initial interpretation of this system, which seemed to be obvious before frontal cuts were performed, was incorrect, and in fact, this is a massive bundle that courses from the frontal lobe to the occipital lobe, that we together with Onufrowicz, would like to call the “frontal occipital association bundle” or true superior longitudinal fasciculus (see figure 19-1C).

Heinrich Hochhaus (1893) joined the fray (p. 92):

On the coronal sections we see medial to the sparse callosal fibers as initially described by Onufrowicz, the association bundle that on all cuts is clearly visible, as well as the tapetum of the posterior horn. There is almost no doubt about the accuracy of this interpretation by Onufrowicz, and possibly Burdach has interpreted it the same way. It is a long fiber system that mainly connects the frontal and occipital lobes, and in our case it also seems without doubt that the tapetum is very nicely preserved, and that it is in fact part of the association fiber bundle.

This confusion was confounded by Bruce (1887–1888), who described a “marginal arch” in his own case of agenesis but found untenable the view of Onufrowicz and Kaufman that (p. 338) “the fibers occupying its [marginal arch] position belong to the (p.458) system of fronto-occipital association fibres … [and] that they are, in fact, the fibres of the cingulum of Burdach, no longer concealed by the fibres of the corpus callosum.”

Thus, some 65 years after Burdach’s lucid descriptions, a series of investigators became thoroughly muddled in their conceptions of the arcuate fasciculus, the superior longitudinal fasciculus, the cingulum bundle, and the tapetum and the displaced callosal fibers that they mistakenly thought was an association system linking the frontal lobe with the occipital lobe (i.e., a fronto-occipital fasciculus).

Callosal agenesis is a complex condition that is wholly unsuitable for deriving conclusions regarding normal brain anatomy because it may be associated with a number of morphological and clinical aberrations (Aicardi and Chevrie, 1994; Andermann and Andermann, 1994; Geoffroy, 1994; Hyndman and Penfield, 1937; Probst, 1973; Sauerwein and Lassonde, 1994). The obvious fallacy inherent in this approach was recognized within a few short years by astute investigators of the time.

Heinrich Sachs (1892), who was consistently and remarkably accurate in many of his observations, concluded that Onufrowicz’s system was nothing more than a heterotopia, entirely lacking in normal brains, and consisting of callosal fibers “transformed into a sagittal bundle which does not leave the hemisphere in which the fibres belong” (translated and quoted in Barker, 1899, p. 1067). Carl Wernicke (1897) concurred with Sachs and emphatically denied that the subcallosal fascicle of Forel and Onufrowicz was an association system. He termed it the “longitudinal callosal bundle” and regarded it as carrying fibers of the corpus callosum radiating into the frontal lobe.

Dejerine Describes the Fronto-Occipital Fasciculus

Dejerine (1895) attempted to reconcile the findings of Forel, Onufrowicz, and others with his own observations (Dejerine, pp. 758–765):

Forel and Onufrowicz identified [their] fascicle as the superior longitudinal fasciculus or arcuate fasciculus of Burdach, and their position was accepted by Kaufman and Hochhaus. We cannot agree with this opinion. Indeed … the superior longitudinal fasciculus of Burdach is located lateral to the corona radiata, and its more inferior fibers cover the lateral aspect of the external capsule. The occipital frontal fascicle, on the other hand, is located medial to the corona radiata and contributes to the formation of the roof of the lateral ventricle. We think that the occipital frontal fascicle of Forel and Onufrowicz is part of a sagittally oriented fascicle that runs, in a normal hemisphere, along the external angle of the lateral ventricle. This fascicle is located medial to the corona radiata, above the caudate nucleus, below and lateral to the corpus callosum, and it is separated from the ventricular cavity by sub-ependymal gray matter.

[T]he occipital frontal fascicle is a sagittally oriented long association fascicle located between the cingulum and the arcuate fascicle or superior longitudinal fascicle of Burdach. It is separated from the cingulum by the whole thickness of the corpus callosum, and from the superior longitudinal fascicle by the foot of the corona radiata … It exhibits a curved shape open rostrally and ventrally, and is covered along its entire length by ependymal lining and by sub-ependymal gray matter, where it gives off numerous fibers. The fascicle then runs along the external angle of the lateral ventricle, located above the (p.459) caudate nucleus, medial to the corona radiata below the U, or the hook, that the callosal fibers make around the external angle of the lateral ventricles. On coronal section its surface is pyriform and about half a centimeter thick at its base … Clearly delineated at the level of the head and body of the caudate nucleus, this fascicle is in part dissociated at the level of the tail of the caudate, or separated by the fibers of the corona radiata and by the callosal fibers. Rostrally the occipital-frontal fascicle originates from the whole frontal lobe—external aspect, frontal pole, and orbital aspect. It receives a large number of fibers from the superior border of the hemisphere and from the external aspect of the convolutions. These fibers travel through the callosal fibers and through the fibers of the corona radiata. [A] large number of fine, lightly stained fibers leave the principal fascicle, move dorsally and medially, and completely fill the clear space situated between the fibers of the corona radiata and the corpus callosum that surrounds the lateral ventricle. Other fibers cross the sub-ependymal gray matter, and rostral to the frontal horn they cross the fibers of the corpus callosum and corona radiata and radiate within the anterior part of the extremity of the frontal lobe. From the base of the occipitofrontal fascicle some fibers leave in the ventral and lateral direction. They cross the foot of the corona radiata and enter the main part of the external capsule [see figures 2-10B,C and 2-11B].

Dejerine noted that the occipitofrontal fascicle degenerates following lesions of the occipital lobe, and (ibid.)

only partially following lesions of the temporal lobe and the convexity of the hemisphere … The occipito-frontal fascicle therefore constitutes a long associative fascicle that connects the temporo-occipital lobe to the frontal lobe, to the convexity of the hemisphere, and to the insula (through the fibers going to the external capsule). This fascicle is formed by fibers of different lengths that belong to the occipitofrontal fascicle only for a portion of their path. The occipitofrontal fascicle can thus be distinguished from other long association fascicles because it is more deeply located and is sub-ependymal, and because it is located medial to the projection system whereas the other long associative fascicles are more eccentric with regard to this system.

Dejerine thus rejected both arguments of Forel and Onufrowicz: that the FOF linking the occipital and frontal lobes was in the location they described, and that it was equivalent to the arcuate fasciculus of Burdach. He provided the first detailed account and illustrations of the location of the true FOF, described its shape and dimensions, and placed it medial to the corona radiata, whereas the arcuate fascicle of Burdach is lateral to the corona radiata. Further, Dejerine’s FOF was not nestled immediately adjacent to the ventricle and the cingulum bundle, as Forel and Onufrowicz indicated, but rather it was ventral and lateral to the callosum, at some distance from the white matter of the cingulate gyrus. In attempting to reconcile his conclusions with those of Forel and Onufrowicz, however, as well as those of Meynert and Wernicke,4 Dejerine concluded that the true FOF was identical to the subcallosal fasciculus of Muratoff.5 By conflating these two fiber tracts (the FOF and the Muratoff subcallosal fasciculus), confusion regarding their course and composition persisted for over a century. Like many (p.460) of his contemporaries, Dejerine also believed, incorrectly, that the FOF was continuous with the tapetum.6

Schröder (1901) provided a withering critique of Onufrowicz’s conclusions.7 As to the assertion that the FOF represents the superior longitudinal fasciculus, Schröder (1901, p. 83) acknowledged that it was Sachs who exposed the folly of this conclusion and who “first proved that this statement is untenable by pointing out that Burdach’s fasciculus longitudinalis superior was situated lateral to the corona radiata, between the short association fibers of the cortex and the corona radiata, whereas Onufrowicz’s fasciculus fronto-occipitalis lies medial to the corona radiata, and in the frontal lobe even medial to the ventricle, adjacent to the cingulum.” He added his own interpretation based on volume I of Wernicke’s (1897) atlas to which he contributed (Schröder, 1901, p. 81): “A number of association fiber bundles that connect distant parts of the cortex are an established fact. Among those, a new bundle has recently established a new place, the so-called fronto-occipital association bundle. The literature on this fiber tract is a reflection of our knowledge of the brain fiber tracts in general: imprecise descriptions, misunderstanding of earlier descriptions of other authors, hasty generalization and precipitate physiological application of the results play a role here.” Schröder disapproved of the methods and conclusions of Onufrowicz, Kaufmann, and Hochhaus and lamented the fact that investigators were trying to determine the location of the fronto-occipital bundle in normal brain without first asking whether a fronto-occipital bundle in the sense of Onufrowicz exists. He dismissed Onufrowicz’s claims in total and instead identified a region lateral and superior to the subcallosal fasciculus/fasciculus of the caudate nucleus, that he labeled “area r.” He equated this area, at least in part, with the region that Dejerine identified as the location of the FOF. Schröder disputed Dejerine’s claim, however, that this location contained association fibers traveling between the frontal and occipital lobes. Rather, Schröder agreed with Sachs that this area was part of the corona radiata.8

Moriz Probst (1901a) provided a definitive understanding of Onufrowicz’s robust myelinated bundle in the agenesis brain that reflected precisely what Sachs had suggested almost a decade earlier. Probst regarded it as misplaced callosal fibers, which, being unable to cross to the opposite hemisphere, were directed in the rostral—caudal plane instead. He adopted the same term used by Wernicke (the “longitudinal callosal bundle”) and observed that it “forms, anteriorly as well as posteriorly, a similar forceps-like continuation as does the normal corpus callosum” (translated and referenced in Probst FP, 1973, p. 13). These misdirected callosal fibers, subsequently termed the bundles of Probst, can be visualized on MRI (Kuker et al., 2003) and have been studied in the mutant mouse model of callosal agenesis (Wahlsten and Ozaki, 1994). They are not present in the normal brain. The nature of these misplaced bundles was first clearly articulated by Heinrich Sachs almost a decade earlier, and it therefore seems appropriate to refer to the longitudinal callosal bundles in cases of agenesis of the corpus callosum as the bundles of Sachs and Probst, or the Sachs-Probst bundles.

Thus, the fiber bundle that Forel and Onufrowicz described was not what is now known to be the FOF. Although there is indeed a fiber system linking the occipital and frontal regions, this is not what Forel and Onufrowicz observed. The proximity of Dejerine’s FOF to the Sachs-Probst bundle is a matter of serendipity, and the resulting confusion is well demonstrated in these conflicting accounts in the original contributions above, as well as in authoritative texts of the time (Barker, 1899, pp. 1067–1069; Gordinier, 1899, pp. 369–370).

(p.461) Dejerine’s identification of an FOF that carried association fibers between the frontal and occipital lobes was not universally adopted, as reflected in the analysis of Schröder (1901).9 Obersteiner and Redlich (1902), who surveyed the literature and compared it with their own experience, were also unable to agree with Dejerine in the determination of the FOF as an association fascicle. They concluded instead that the area in their work that corresponded to the location of Dejerine’s FOF is a corticocaudate fascicle.10

Thus, despite Dejerine’s attempt to define the anatomical features of the FOF, his findings remained a matter of debate, and several problems persisted, particularly regarding its differentiation from the tapetum and the Muratoff bundle.

The Tapetum

Forel and Onufrowicz stated that their medially lying system was the occipitofrontal fascicle and that the “tapetum” was a part of that (FOF) bundle, because both the FOF and the tapetum were preserved in their case of callosal agenesis. Bechterew (1899, 1900) agreed that the tapetum, being preserved in callosal agenesis, was not a callosal system but was the caudal extension of the medially lying system. Dejerine, too, believed that (p. 763) “[w]hen it reaches the confluence of the ventricles, this [FOF] fascicle curves ventrally and rostrally and its fibers spread over the inferior and external wall of the sphenoid (temporal) horn, forming the tapetum of previous authors” (see figure 2-11B, “OF[Ta]“). Muratoff (1893a, p. 722) reviewed the literature “to develop a consensus on the term ‘tapetum of the corpus callosum’ [and was able to] convince [him]self that the subcallosal fasciculus and the tapetum are one and the same, an anatomically indivisible system.”11 According to Schröder (1901, p. 90), von Monakow thought that the “tapetum and superior longitudinal fasciculus [constitute] a continuous fiber system that runs through the normal brain in its entire length and corresponds to the fronto-occipital bundle of brains without a corpus callosum.”12 Obersteiner and Redlich (1902) described the uncertainties at the turn of the 20th century concerning the tapetum, the FOF, and the subcallosal fasciculus of Muratoff13 and concluded that (p. 307) “it appears more correct to abandon the term tapetum, which only is of historical significance, and designate the single layer that lines the lower horn according to its significance, as stratum subcallosum, callosal layer etc.”

All these authors would have been well advised to pay closer heed to Burdach (1822, p. 148, paragraph 193), who wrote the following regarding the

posterior portion of the corpus callosum and the splenium. The tapetum is the lateral extension of the lower layer of the body that lies above the anterior portion of the splenium and the extension of the anterior portion of the splenium itself … The tapetum is a fiber layer 1\2 to 1 Line thick that extends to cover part of the lateral wall of the lateral ventricle, where it is lined by epithelium [ependyma]. It runs posteriorly in an oblique fashion on each side of the corpus callosum within the roof of the entrance to the lower horn [temporal horn of the lateral ventricle], lateral and inferior to the posterior lateral corner of the thalamus. It then curves forwards, runs in the lateral wall of the lower horn, leaning towards the inner surface of the corona radiata along the lateral side of Ammon’s horn and parallel to it, anteriorly and inferiorly to reach the apex of the temporal lobe.

(p.462) These observations of Burdach have been repeatedly confirmed and validated by subsequent investigators (Ariëns-Kappers et al., 1936; Brodal, 1981; Carpenter, 1976; Cipolloni and Pandya, 1985; Crosby and Schnitzlein, 1982; Demeter et al., 1985, 1990; Rockland and Pandya, 1986; Seltzer and Pandya, 1983; Tusa and Ungerleider, 1988), and the confusion over the tapetum has abated. It is now known that the tapetum is a thin rim of bidirectional callosal fibers derived from and leading to the temporal and occipital lobes, lying laterally adjacent to the ependymal lining of the inferior and posterior horns of the lateral ventricles. There is no controversy today about these callosal fibers, and the tapetum is not dealt with further in detail in this work. Perhaps what was seen in agenesis of the corpus callosum were the tapetal fibers of the corpus callosum not crossing to the opposite hemisphere but remaining connected with the aberrant callosal fibers (not the FOF fibers), precisely as postulated by Sachs and Wernicke.

The Confusion Surrounding the Subcallosal Fasciculus of Muratoff

In 1893, Wladimir Muratoff (Muratoff, 1893a,b; Muratow, 1893) described a bundle of fibers situated directly above the caudate nucleus and beneath the corpus callosum. Uncertain as to whether the bundle he observed was an occipital frontal association system or a projection system, Muratoff designated this fiber bundle by its anatomic location and called it the subcallosal fasciculus. Muratoff’s discussion set the stage for the debates that followed, as well as the persistent uncertainties.

Muratoff followed the tradition of investigators at the time and performed physiologically defined anatomic experiments in dogs with excitation and ablation of the motor cortex.14 He noted degenerated fibers in the lesioned left hemisphere in the cortical U-fibers or arcuate fibers, in the corona radiata, and in the corpus callosum. In addition, Muratoff (1893b, p. 98) observed that

below the corpus callosum one sees a transected nerve fiber bundle bordered superiorly by the corpus callosum. On our cuts it appears to be crescent shaped. It begins at the midline with its narrow end, enlarges in circumference in the middle portion, and is situated in the angle which is formed by the corpus callosum superiorly, the corona radiata laterally and by the caudate body inferiorly. At this location, the bundle broadens and its terminations cover the caudate nucleus. This bundle has been designated as “fasciculus fronto-occipitalis” by Onufrowicz [see below]. I will call it subcallosal fascicle.15 I chose the name “fasciculus subcallosus” because the term of Onufrowicz “fasciculus fronto-occipitalis” is anatomically incorrect. These fibers by no means represent a particular fronto-occipital association tract. Fibers from different areas of the cortex run in it, for example from the suprasylvian gyrus, and these run only sagittally in the fronto-occipital direction. The mid-portion of this bundle is occupied by fibers from the cortical motor area. The designation “fasciculus subcallosus” has the advantage that it refers only to the anatomical position of this system without making implications regarding its function.

In a later publication devoted to the pattern of secondary degeneration following transection of the corpus callosum, Muratoff noted that the corpus callosum actually contains two systems. He wrote (Muratoff, 1893a, p. 721) that

(p.463)

One system of transverse fibers proceeds from right to left in the frontal plane. Another system consists of longitudinal fibers that lie in the rostrocaudal direction; in my last work [Muratoff, 1893b] I called this system the “subcallosal fasciculus”…. We will further see that this system contains fibers of different significance. On the anterior frontal cuts, one can separate the system into three components. A superior horizontal part is positioned below the corpus callosum; a laterally placed descending part fills the angle between the corona radiata and the corpus callosum; and a lower part is adjacent to the basal ganglia.16

Muratoff’s observations led him to conclude that his subcallosal bundle did not convey fibers between the frontal and occipital lobes.17

The elucidation of the subcallosal fasciculus by Muratoff based on the location of the bundle and the degeneration within it following motor cortex lesions is thus clear and comprehensive. Unfortunately, and perhaps inescapably, the description is then intermingled and conflated with the fiber systems of the corpus callosum, including the tapetum, and the elusive FOF. Despite Muratoff’s use of the innovative experimental approach that combined clinical deficit with the anatomic study of the degeneration following lesion placement, it was still not possible to state with certainty what fiber system the subcallosal fasciculus conveyed. Muratoff’s conclusions were as accurate as the contemporary understanding would permit, and in the end he cautiously named the bundle for its location rather than its constituents.

Sachs (1893) named the bundle that Muratoff observed the “fasciculus nuclei caudati,” or fasciculus of the caudate nucleus. He correctly concluded that the fasciculus of the caudate nucleus, situated in the same location as Muratoff’s subcallosal fasciculus, was not a frontal-occipital association bundle but rather an important fiber system linking the cerebral cortex with the corpus striatum.18 Dejerine recognized the existence of the subcallosal fasciculus of Muratoff, but he equated it in terms of the fibers it conveys with his FOF.19 Flechsig, by contrast, viewed the Muratoff bundle as part of the corona radiata.20 Meynert (1865) and Bechterew (1900), like Sachs, viewed this fasciculus as a corticostriatal bundle, the “fasciculus nuclei caudati,” but Meynert perpetuated the terminological difficulties by calling the FOF the “corona radiata of the caudate nucleus” (see Dejerine, p. 760). Anton and Zingerle (1902, p. 160) also regarded the subcallosal fasciculus as synonymous with the fronto-occipital fiber bundle, named it the medial longitudinal fasciculus, and concluded that it linked the posterior portion of the temporal lobe with the frontal lobe. Niessel von Mayendorf (1919) later concluded that the medial longitudinal fasciculus was not identical with the FOF, and that neither of these bundles was an association system.

Oskar Vogt (1895) accurately identified the two fiber systems adjacent to the caudate nucleus. He recognized the narrow fascicle covering the caudate nucleus, which he regarded as an association system of this nucleus. The other fascicle he believed to be a long association fiber system. Vogt’s anatomic observations were hampered by the use of incorrect terminology—that is, he called the long association fiber system the subcallosal fascicle, whereas it should have been called the FOF; and he had no name for the corticocaudate system that should have been termed the subcallosal fascicle.21

In his evaluation of the earlier literature concerning the FOF and subcallosal fasciculus of Muratoff, Schröder (1901) acknowledged the accuracy of Muratoff’s descriptions, distinguished it from the corpus callosum, and concluded that it was “the analog (p.464) of the fasciculus nuclei caudati that has been described by Sachs.” However, Schröder continued,

Muratoff goes one step further by identifying his subcallosal fascicle with Sachs’ fasciculus nuclei caudati, and he also unscrupulously identifies it with the fronto-occipital association bundle of Onufrowicz … This was crucial for the further development of the question regarding the fronto-occipital bundle—the fronto-occipital bundle was therefore found also in the normal brain [and not only in the callosal agenesis brain]. But if one takes a closer look, Muratoff’s bundle has nothing more in common with the bundle postulated by Onufrowicz for the normal brain than its sagittal orientation.

Schröder proceeded to argue eloquently for the subcallosal fascicle as a striatal bundle. He marshaled three anatomic observations to support his contention: the intimate relationship in terms of location and size of the subcallosal fasciculus to the caudate nucleus; the morphologic appearance of the subcallosal fasciculus itself, which was unlike the other long association tracts; and the low probability of a long association tract diving deep into the periventricular region.22

Obersteiner and Redlich (1902, p. 289) noted Muratoff’s view that “according to pathological findings on the human brain, the construction of the subcallosal fasciculus in the human is identical with the one in the dog, “but they declared the direct comparison between dogs and humans to be

completely illegitimate…. Muratoff’s statements will also need correction in many other aspects. Unfortunately Muratoff’s short descriptions and his sparse illustrations do not allow exact verification of his statements on the degeneration of this system after extirpation of cortex, especially pertaining to its association with the cortex. If one considers how difficult it is to create circumscribed lesions in the cortex, the lack of detailed descriptions carries especially heavy weight.

In their ablation–degeneration experiments, Obersteiner and Redlich found no evidence to support the assertion that the subcallosal fasciculus conveyed fibers from the frontal lobe to the occipital lobe, and they differentiated the subcallosal fasciculus from a “stratum zonale” that was more closely adjacent to the caudate nucleus.23 Further, they made the prescient observation that (p. 300)

Muratoff … includes the subcallosal fascicle among the association fiber systems. (If one considers the subcallosal fascicle as a connection between cortex and caudate nucleus, the designation association bundle seems more correct, as the caudate nucleus can be considered modified cortex, and this would mean that the subcallosal fascicle would represent a connection between two cortical areas, therefore representing association fibers).24 One could also regard those fibers that apparently leave the subcallosal fascicle and break through the corona radiata as evidence that the subcallosal fascicle represents an association fiber system between cortex and caudate nucleus … An ultimate decision regarding this question cannot be made in our opinion. It is our speculation that collaterals of fibers of neighboring systems are also embodied here, including fibers from the corona radiata that enter the caudate nucleus and possibly also the lentiform nucleus and the thalamus.

(p.465) In Rosett’s (1933) paper provocatively entitled “The Myth of the Occipitofrontal Association Tract,” he described his work based on microscopic sections prepared from flattened gross dissections. He concluded (p. 1257)

that the subcallosal bundle is not an occipitofrontal association system, a radiation of the caudate nucleus or a contingent of the corpus callosum … [T]he mesial and more superficial portion of this bundle [are] made up of thalamic fibers. Its deeper and more lateral portion is made up of fibers which proceed from the prefrontal and frontal and perhaps the anterior portion of the parietal regions of the cerebral cortex to contribute to the formation of the pes pedunculi of the midbrain. They are, in other words, corticospinal and corticopontile fibers.

This reinterpretation by Rosett of the earlier work dealing with the subcallosal fasciculus was wholly fallacious. One subsequent study that included an appropriate notion of the subcallosal bundle was that by Yakovlev and Locke (1961a). This work, based on careful anatomic analysis using the ablation–degeneration technique, showed that the anterior cingulate gyrus gives rise to ventrally directed fibers that traverse the corpus callosum, travel in the stratum subcallosum, and enter the capsule of the caudate nucleus.

Authoritative sources in the more contemporary literature have perpetuated the uncertainty in their consideration of the FOF and Muratoff bundles. Riley (1960, p. 672) based his comments regarding the Muratoff bundle in large part on the investigations of Mettler and concluded that “its constituents are not clear.” Crosby and Schnitzlein (1982) postulated two separate fronto-occipital fiber systems, one superior and one inferior. We have been unable to find evidence in support of the existence of an inferior FOF, as discussed in chapter 18. As there is no “inferior FOF,” the qualifying “superior” adjective is superfluous when describing the actual FOF. Further, Crosby equated the “superior fronto-occipital fasciculus” with the subcallosal bundle and perpetuated the initial misconception by describing the FOF (not the Muratoff bundle) as conveying primarily frontocaudate fibers. Relying on previous anatomic studies for validation, the DT-MRI literature has already continued this conflation of the two bundles (e.g., “the superior fronto-occipital [subcallosal] fasciculus” in Catani et al., 2002).

Summary of Historical Accounts

Burdach provided clear descriptions, later elaborated upon, regarding the cingulum bundle, the arcuate fasciculus/superior longitudinal fasciculus, the corona radiata, and the tapetum and other components of the corpus callosum.

The paper by Onufrowicz and others purporting to describe a new association fiber bundle in cases of callosal agenesis that linked the frontal lobe directly with the occipital lobe threw the contemporary understanding of these systems into disarray. The “fronto-occipital fasciculus” of Forel and Onufrowicz was, in fact, an aberrant bundle present only in cases of callosal agenesis that contained misdirected callosal fibers oriented in the sagittal plane. Sachs, Dejerine, Wernicke, and Probst recognized this error. We elect to refer to these aberrant fascicles as the bundles of Sachs and Probst.

The dissection technique and even the lesion-degeneration studies comprehensively and carefully performed by some of the preeminent scientists of the day were unable to (p.466) disentangle the FOF, the subcallosal fasciculus of Muratoff, and the tapetum that is a part of the corpus callosum. Dejerine described and illustrated the FOF, which he believed to be a long association fiber tract. However, he thought it was identical with the subcallosal fasciculus of Muratoff situated above the caudate nucleus, while Flechsig regarded the FOF as part of the corona radiata. The descriptions of a spurious and probably nonexistent “inferior fronto-occipital fasciculus” have led to the actual FOF being misnamed post hoc as the “superior fronto-occipital fasciculus.”

It took considerable effort to disentangle the cingulum bundle and the arcuate fasciculus/superior longitudinal fasciculus from confusion with these other fiber pathways. Even straightforward issues such as distinguishing the ependymal lining of the ventricle from the subcallosal fasciculus met with mixed results.

Investigators using contemporary DT-MRI methodology have inadvertently incorporated some of the earlier imprecise concepts and terminologies in the belief that the classical neuroanatomy was established and incontrovertible. The foregoing account details the limitations inherent in the earlier discussions. In the present investigation, we have attempted to resolve the question as to whether the two bundles (FOF and Muratoff) are one and the same, or whether they are separate.

Results of the Present Investigation

Our observations in the monkey confirm the existence of the FOF where Dejerine located it in the human, and provide compelling evidence that it is a true association fasciculus linking parieto-occipital regions with the dorsolateral premotor and prefrontal areas. Moreover, the present study also adds detail to the understanding of its location and to the origin and termination of its fibers.

The FOF is a triangular bundle bounded laterally by the corona radiata and medially and superiorly by the corpus callosum; ventrally its base rests on the subcallosal fasciculus of Muratoff that separates the FOF from the body and head of the caudate nucleus. The FOF is formed by fibers that coalesce at a level just anterior to the atrium of the lateral ventricle, and the fasciculus continues rostrally into the frontal lobe until the frontal horn of the lateral ventricle (figure 19-2).

Rostrally directed fibers in the FOF are derived from the medial preoccipital area PO, lateral-dorsal preoccipital area DP, medial parietal area PGm, caudal cingulate gyrus, and area PG/Opt in the caudal inferior parietal lobule. The fibers of the FOF terminate in the frontal lobe in dorsolateral area 6, area 8Ad, area 8B, caudal area 46 dorsally, and area 9. Some fibers from the inferior parietal lobule pass through the SLF II before entering the FOF, where they travel rostrally into the frontal lobe.

Like the other long association fiber systems, the FOF also conveys reciprocal fibers from the frontal lobe into caudal sectors of the hemisphere. The caudal parts of the dorsolateral prefrontal cortex (area 8Ad and dorsal area 46) contribute fibers to the FOF that terminate caudally in area PGm and possibly also in area PO along with fibers from the SLF I, and in area PG/Opt along with fibers from the SLF II.

Our findings indicate that the FOF and the subcallosal fasciculus of Muratoff (Muratoff bundle) are two separate entities. The Muratoff bundle is a compact and distinct fiber tract that carries fibers from the occipital lobe, parietal lobe, cingulate gyrus, and temporal lobe, (p.467)

                         Fronto-Occipital Fasciculus

Figure 19-2 Summary diagrams of the course and composition of the FOF in the rhesus monkey. A, The lateral view of the cerebral hemisphere (lower diagram) shows the trajectory of the FOF and the cortical areas that are linked in a bidirectional manner by the fibers in this pathway. The medial view of the hemisphere (above) is shown to represent other cortical areas that contribute to this fiber pathway. B, Schematic diagrams from rostral to caudal coronal sections through the FOF extracted from the composite views of the hemisphere shown in chapter 27. The numbers refer to the sections of the template brain from which these images of the FOF are derived. The areas of origin of the fibers within the FOF are color-coded according to the legend above right. Bar = 2 mm.

(p.468) as well as the frontal lobe, and these fibers terminate in the head, body, genu, and tail of the caudate nucleus. The Muratoff bundle is therefore strictly a corticostriatal bundle (see chapter 20). The FOF, in contrast, is an association bundle, although it does contribute some fibers to the Muratoff bundle, which then terminate in the striatum.

Functional Notions

The cortical regions from which the FOF originates (medial preoccipital area PO, lateral-dorsal preoccipital area DP, medial parietal area PGm, caudal cingulate gyrus, and caudal inferior parietal lobule area PG/Opt) are involved in the processing of visual information regarding the peripheral visual field. The FOF conveys this information predominantly to the dorsal premotor (area 6) and dorsal prefrontal (areas 8Ad, 8B, dorsal area 46, and area 9) cortices concerned with higher-order aspects of motor behavior and attention.

Ungerleider and Mishkin’s (1982) concept of the dorsal visual stream (occipitoparietal cortices subserving spatial perception and projecting to dorsal regions of the frontal lobe) has been further subdivided (Rizzolatti and Matelli, 2003) into two components. This approach has relevance for the discussion of the putative functional properties of the FOF. In this view, the parietal lobe comprises two systems. The dorsal—dorsal stream is formed by areas V6, V6A, and MIP of the superior parietal lobule. Its major functional role is the control of actions “on line,” and damage to these parietal areas leads to optic ataxia. The ventral–dorsal stream, in contrast, is formed by area MT and visual areas of the inferior parietal lobule; it is responsible for action organization and plays a crucial role in space perception and action understanding.

The FOF may be the fiber system of the dorsal—dorsal component of the dorsal visual stream. If the dorsal parieto-occipital and medial parietal areas, including area PO or V6, are engaged in the control of actions (Rizzolatti and Matelli, 2003), then their projection to motor-related regions via the FOF suggests a role of the FOF in the awareness and use of visual information for the purpose of guiding movements and in the preparation and release of reaching—grasping arm movements (Rizzolatti et al., 1990). Further, the FOF-mediated projections in dorsal frontal areas, including the supplementary eye field in area 9 (Schlag and Schlag-Rey, 1987), as well as in areas 6 and 8, which have been shown to be necessary to maintain vigilance (Rizzolatti et al., 1983), may be relevant for spatial aspects of attention.

The FOF also conveys reciprocal connections from dorsolateral prefrontal regions back to the parieto-occipital areas, and it is therefore the conduit by which the posterior dorsal prefrontal cortex (mainly area 8) may influence visual spatial processing within the occipital and caudal parietal cortices.

Thus, the FOF is the long association fiber pathway of the dorsomedial aspects of the dorsal visual stream, and it appears to be an important component of the anatomical substrates involved in peripheral vision and the processing of visual spatial information. It is distinguished from the SLF II, which subserves the ventral—dorsal component of the dorsal visual stream. It also stands in contrast to the ILF, the long association pathway of the ventral stream, which arises in part from the ventrolateral part of the extrastriate visual area and is engaged in processes subserving feature detection and object knowledge and memory.

Notes:

(1.) Onufrowicz obtained the brain of a patient with callosal agenesis (Onufrowicz, 1887, p. 305) “through the courtesy of my previous employer, Dr. Moore, who was the previous director of the mental institution in Rheinau (Kanton Zürich), where this brain was stored.” Onufrowicz stated that he was (p. 305):

indebted to Professor Dr. Forel for letting me use his library, and for his willingness to guide me through this work and for teaching me how to interpret the brain and its parts, and for making the illustrations in this article…. Although many cases of agenesis of the corpus callosum have been described in the human brain, we are in a position to make a small contribution to the knowledge of the anatomy of this condition with this case. Further, we are able to make a contribution to brain anatomy in general that should be valuable, because, to our knowledge, cross sections were performed only in the most recently described case of Anton. In that case of a fetal brain, myelinated fiber systems were not yet developed. That previously described case did not produce any further insights into the internal structural changes of the brain because no cross sections were taken. In the current case we performed coronal sections of the left half of the brain, and stored the other half in the collection of the Burghölzli institution.

(2.) Page 313:

Description of our case. Gottlieb Hoffman von Seen (Kanton Zürich). Born in 1842, died in Rheinau Feb. 22, 1879 from pneumonia. Thanks to the priest Meister in Seen I received the following valuable remarks about Hoffman. “One could see even in the cradle, he was completely stupid and without all sense. As a young boy, he walked around the house with pitiful screaming. He was even unable to learn how to eat. He either tried to stuff a whole slice of bread into his mouth or he made little pieces and crumbled them on the floor. His father was a farmer and weaver, and Hoffman used the basket cane to vandalize mirrors and the glass in windows. The only sign of intelligence (p.602) was that he would return to his parents’ house in response to a particular whistle. The behavior of Hoffman during his stay in Rheinau is as follows. He sat in a chair that was specially constructed for him. He would walk close to walls. He was filthy and had to be fed since he put food all over himself and as described above, he tried to stuff food in big pieces in his mouth. From time to time he made inarticulate noises. His sensory organs were unfortunately not examined, but he was able to see, he was able to feel, and it appears he was able to hear. Furthermore, he had deformed hands and feet. This was the reason he could not walk.” A detailed history of his illness is unfortunately not available, and the very poorly performed autopsy is as follows. He had scoliosis of the spine, severe stiffness [after death], he had stains in dependent areas and he was very cachectic. He had a small round and pointed skull, slightly asymmetric, somewhat thickened in the midline, and tethered to the pia, which was injected. The gyri were very flattened because of compression, and the sulci were flat due to poor preservation. The olfactory nerves were absent and the pia was difficult to detach from the skull. (Autopsy on Feb 24th 1879.)

(3.) Page 313:

When the brain was taken out it immediately fell apart in 2 pieces and it became apparent at once that the corpus callosum and the olfactory bulb were missing. The brain in our descriptions is depicted as normal size, was put in a solution of potassium bichromate, but unfortunately became foul. It was subsequently immersed in cognac, and as a consequence of this treatment, the surface of the brain became very fragile. The gyri at the base, in particular, were compressed, so that no clear interpretation of those could be done.

(4.) Dejerine, 1895 (pp. 760–761):

This fascicle that we call in our serial sections, occipital frontal fascicle, is in fact the fascicle that was described by Meynert under the name of corona radiata of the caudate nucleus, and by Wernicke under the name of fascicle of the corpus callosum traveling to the internal capsule. According to Meynert the corona radiata of the caudate nucleus is formed by numerous fibers that originate in the caudate nucleus, merge along the angle of the superior and external aspect of the caudate nucleus and radiate within the convolutions of the superior aspect of the hemisphere. Wernicke has shown that these fibers have no connection with the caudate nucleus, and when we examine serial sections we do not see any fiber terminating in the caudate nucleus.

According to Wernicke these fibers form a fascicle of callosal fibers reaching the internal capsule. They originate from the anterior wall of the frontal horn, that is, from the genu of the corpus callosum and from the white matter of the frontal lobe. They then unite in one compact fascicle 1.5 centimeters thick, and run along the superior and external edge of the caudate nucleus. The fibers enter the internal capsule between the caudate nucleus and the superior edge of the putamen at the level of the middle part of the thalamus. This fascicle is not part of the anterior segment of the internal capsule.

From the examination of serial sections, whether coronal sections or horizontal or sagittal sections, we have been able to reach the conclusion that none of these fibers make contact with the caudate nucleus.

(5.) Dejerine, 1895 (p. 761):

Because we have no anatomical-pathological or experimental data supporting the previous idea of Gratiolet and of Foville, an idea that has been supported by Wernicke regarding the existence of callosal fibers traveling within the internal capsule, we believe we can identify this fascicle as the occipital-frontal fascicle described by Forel and Onufrowicz when they discuss agenesis of the corpus callosum.

Page 765:

These observations made in the human are consistent with the lessons learned from experimental pathology. Experimental work by Muratoff that is being performed in the dog indicates that the occipito-frontal fascicle of Forel and Onufrowicz (subcallosal fasciculus of Muratoff), partially degenerates following ablation of the motor sphere, or the destruction of frontal or occipital convolutions.

(6.) Dejerine, 1895 (p. 758):

Forel and Onufrowicz demonstrated, and this has been confirmed by Kaufmann and Hochhaus, that in the case of complete agenesis of the corpus callosum the arrest of development concerns mainly the corpus callosum, the forceps and the commissural system of the cerebral trigone (David’s Lyre). The tapetum, in contrast, which corresponds to the layer of fibers that cover the external wall of the temporal and occipital horns, develops normally and continues rostrally with a fascicle that is directed sagittally, located medial to the corona radiata and lateral to the body of the trigone with which it is intimately united. These facts demonstrate that the tapetum does not belong to the corpus callosum, but belongs to the intra-hemispheric association fascicle that Forel and Onufrowicz termed the occipital-frontal fascicle … In the temporo-occipital lobe, after it forms the tapetum, the occipito-frontal fascicle radiates in the convolutions of the external aspect and the inferior external aspect of the lobe.

(7.) Schröder, 1901 (pp. 94–95):

The assumption of Onufrowicz … was no doubt a conclusion per exclusionem. The corpus callosum, i.e., the horizontal connecting bridge between both hemispheres, was missing, the bundle could not easily be regarded as belonging to the corona radiata and therefore the only remaining option was the interpretation that it is an association system. The first and only one who doubted this interpretation was H. Sachs. Sachs said that in the described cases of callosal agenesis the callosal fibers were not missing, but present, and that the trunk of the corpus callosum did not connect both hemispheres but the poles of the same hemisphere. What Onufrowicz thought to be the fronto-occipital bundle was this trunk portion of the corpus callosum. This attempt at an explanation has not been very popular. Vogt called it untenable and not viable. Dejerine likewise had his doubts. On first inspection this explanation does indeed appear surprising.

Onufrowicz saw that the corpus callosum was missing and concluded without any reasoning that the entire callosal fiber system was missing completely (agenesis). He did not even try to search for possible remnants of the corpus callosum. He found an exceptional fiber tract but did not consider the possibility that it could possibly have something to do with the corpus callosum.

Sachs now postulates that the normally developed callosal fibers have grown from the cortex until they reach their gathering place in proximity to the lateral ventricle. Here they are prevented by an unknown circumstance from crossing the midline, they have therefore curved posteriorly and anteriorly and made connections to cortical areas of the same, instead of the contralateral, hemispheres (heterotopia of the corpus callosum).

Sachs’ assumption is just a hypothesis, but a hypothesis that facilitates the understanding of certain teratological cases much more than the forced interpretation by Onufrowicz. One thing has to be mentioned: according to Sachs the controversial fiber tract also represents an association bundle in cases lacking the corpus callosum, i.e., a system that connects cortical areas of the same hemisphere with each other and since it can be traced from the frontal lobe to the occipital pole, one could not argue with its name “fronto-occipital bundle.” But, and this is the core message, this fronto-occipital bundle does not have an analogue in the normal brain, such as the superior longitudinal fascicle or another of the known fiber tracts. It has formed in an abnormal manner from the corpus callosum that was prevented from crossing the midline. The finding of such a fiber tract in the normal brain is therefore excluded from the outset since this bundle only forms under certain pathological conditions and forms a replacement for the missing corpus callosum. It contains fibers that were meant to connect with cortical areas of the contralateral hemisphere, but since they were prevented from doing so, have made a connection with the corresponding cortical areas of the same hemisphere. If they did not find the connection to adequate cortical territories they would have perished, as we know from experience.

How the axis cylindrical processes of callosal cells form such unusual connections is impossible to explain. But according to the current status of our knowledge on the embryological mechanisms in the brain it is equally difficult to explain how each cell finds its partner in the other hemisphere under normal circumstances.

If one familiarizes oneself with the thought that a heterotopia in the sense of Sachs is possible, the illustrations by Kaufmann and Onufrowicz are in fact evidence of such heterotopia. What is designated as fronto-occipital bundle assumes the position of the trunk of the normal corpus callosum, but the connecting bridge between both hemispheres is missing. In the anterior horn, the fiber layer lies like the normal corpus callosum medial to the ventricle and not at its lateral edge where the authors are searching for the fronto-occipital bundle. Posteriorly it moves gradually laterally like the normal corpus callosum, and finally sends the main portion of its fibers on the lateral side of the posterior horn as the tapetum in the occipital direction. (At the time of Onufrowicz’s work everyone considered that the tapetum contained only callosal fibers. If he had concluded more correctly: my bundle continues posteriorly directly into the tapetum which we know represents callosal fibers, consequently my bundle has to do with the corpus callosum, if he had concluded this, the currently favored but entirely unfruitful tapetum question would not have arisen).

(8.) Schröder, 1901 (pp. 84–86):

On coronal section through the area of the central gyri (Taf II, Fig. 1-The image is from the same preparation as in Wernicke’s Atlas des Gehirns, Part 1) we see the lateral angle of the lateral ventricle surrounded by a brighter fiber-mass (fnc), which sits broadly on the caudate nucleus and reaches the corpus callosum superiorly. Its medial lower rim continues in a thin fiber layer that covers the caudate nucleus on its free surface, its medial superior rim reaches below the corpus callosum towards the midline. This bundle is remarkable because of the abundance of coarse vessels. A clearly defined direction of fibers cannot be recognized. Even under the microscope one sees only within the lateral part, a predominance of sagittal fibers by means of its slightly darker coloration. Sachs has called this bundle, fasciculus nuclei caudati (“Schwanzkernbündel”). We agree with his nomenclature.

In the frontal lobe, where the fasciculus nuclei caudati is best developed, it descends in front of the head of the caudate close to the base of the brain and one finds it therefore on coronal sections that lie in front of the tip of the anterior (p.604) horn (see Wernicke Atlas I, Taf. 2), where it lies encircled by the corpus callosum. In the most anterior portion of the anterior horn it forms a thick layer at its lateral wall; the head of the caudate, which pushes the bundle gradually into the superior and lateral corner of the ventricle, appears on adjacent cuts. Here, one can track it posteriorly up to the area of the pulvinar.

Laterally, a sharply demarcated area of thick, dark and convoluted fiber bundles borders the fasciculus nuclei caudati (r). The formation of this bundle is subject to individual variability. In more anterior planes, the space it takes up is larger and its formation is therefore different, as it has a characteristic net-like appearance, i.e., dark fiber bundles form a meshwork in which the mesh is filled by bright oblique bundles (compare Wernicke Atlas I, Taf. 7-12). H. Sachs has introduced these bundles as corona radiata bundles that ascend from the internal capsule initially for a stretch along the caudate before they run towards the cortex. He called this the net-like or reticulated corona radiata area (“reticulirtes Stabkranzfeld”), we simply refer to as “area r.” It descends like the fasciculus nuclei caudati in front of the caudate towards the base and it runs posteriorly. The further one gets posteriorly, the more the bright, gap-filling fiber mass diminishes and the closer the darker bundles move together. One constantly finds here, however, a thin layer of bright fibers on the lateral side of the area. From the description of area r it becomes immediately apparent that it is not a bundle in the strong anatomical sense, but that it is formed by fibers that run in only a portion of it; this also explains its changing characteristics in different brains and in different parts of the same brain. The position of area r is always lateral to the fasciculus nuclei caudati within the area of the corona radiata radiations (cr), i.e., close to their exit from the internal capsule, i.e., close above a line that connects the superior edge of the caudate and the putamen.

Area r consists superiorly only of a few crowded bundles. It moves superiorly between the caudate bundle and the corpus callosum and sits with its base on the remaining corona radiata fibers. In the lower horn, we find it in corresponding formation: the basis is directed superiorly at the corona radiata, the tip wedged between the fasciculus nuclei caudati and the tapetum. On fortuitous coronal sections one can see the descending part of this bundle in considerable length. We see therefore that the formation of the area r is not limited to the area of the parietal and frontal lobe as Sachs stated, but can also be clearly recognized in the temporal lobe. Neither area r nor the caudate bundle continues into the occipital lobe.

(9.) Schröder, 1901 (pp. 91–93):

Dejerine addresses the fronto-occipital bundle in detail in his great work. At the outset it should be mentioned that Dejerine calls what Sachs designated fasciculus nuclei caudati “substance grise sous-ependymaire”; we will not elaborate upon whether this name is justified. Sachs has already pointed out that nerve cells can not be found in it, so that one can not talk of a ‘gray [area]’…. Dejerine begins also with the cases of callosal agenesis (Onufrowicz, Kaufmann, Hochhaus). He is convinced that the fronto-occipital bundle of these authors cannot be identified with the superior longitudinal fascicle of Burdach. He then describes a fiber tract in great detail that he considers to be the analogue of Onufrowicz’s bundle in the normal brain. He describes it as a fiber tract that on anterior cross section is shaped like a pyramid and about 0.5 cm thick, separated from the ventricle by the gris sous-ependymaire, lateral to the corona radiata, superior to the corpus callosum, inferiorly abutting the caudate nucleus. This is nothing other than Sachs’ reticulated corona radiata area (“reticulirtes Stabkranzfeld”) our area r (see above). Further posteriorly the bundle is said to curve inferiorly and anteriorly and to form the tapetum together with the callosal fibers from the forceps major. This precise [feature] cannot be seen on Dejerine’s images.

Dejerine’s figures (figs 281-287 and 301-302) do not show an indication of the border between the fiber-complex he designates as a fronto-occipital bundle and the base of the corona radiata; the naïve viewer could rather see evidence for an affiliation of this bundle with the corona radiata in these illustrations. Further, Dejerine discusses in detail fiber tracts that he believes run from the frontal portion of the bundle to the cortex. He distinguishes on the horizontal cut (page 570, fig 295) three groups of such fibers. The first runs from the main bundle anteriorly and is embedded into the lateral part of the substance grise sous-ependymaire, crosses the corpus callosum and radiates into the frontal gyri. According to my preparations, this fiber tract appears to me to be an artificial construct. It was previously mentioned above that the lateral portion of the fasciculus nuclei caudati (Dejerine’s substance grise sous-ependymaire) contains darker fibers than the medial portion. There is no relationship of these fibers to the formation that Dejerine designates as fronto-occipital bundle (our area r). Furthermore, like the fasciculus nuclei caudati, this dark bundle generally has its border on the posterior edge of the corpus callosum. What not infrequently impresses one as its anterior-bound continuation through the corpus callosum, is a bundle of rectangular callosal fibers, described above, that frequently come off here. It should not be denied that a part of the delicate fibers of the fasciculus nuclei caudati is also interspersed with the corpus callosum. However, I have never seen a compact fiber tract such as Dejerine has illustrated. On the contrary, I almost always saw a callosal bundle that comes off right in this location (compare Wernicke Atlas II (4B) Text p. 13 and Taf. 9).

(p.605)

As a second group of fibers, Dejerine describes those that run medially from the corona radiata together with the corona radiata fibers to the medial surface of the hemisphere. These fibers can easily be identified and construed (see Taf. II, Fig 2, r2), if one recognizes that Dejerine’s fronto-occipital bundle is a corona radiata region: those fibers are corona radiata fibers from this region that join the remaining corona radiata fibers.

As a third grand group of fibers, Dejerine finally mentions fibers that run from his fronto-occipital bundle laterally and inferiorly through the base of the corona radiata to the external capsule. Those are obviously the same fibers that Sachs considers to be fibers moving into the fasciculus nuclei caudati, and they are also mentioned by other authors. According to my preparations, these are largely callosal radiations; it is very probable that the fasciculus nuclei caudati also sends fibers to the cortex here, but these are not the easily recognizable, markedly firm, straight-running fibers that remain visible even when the preparations are so far differentiated that the caudate nucleus bundle that easily decolorizes has lost its colored fibers. One will understand the relationship of these fibers with the corpus callosum if one considers what was said about the callosal radiation above. (Footnote—Much more noticeable is a tract of fine fibers that leaves the fasciculus nuclei caudati posteriorly, as can be seen on horizontal cuts, and which can be tracked to the base of the corona radiata and the internal capsule, but not through them [see Wernicke Atlas II, Taf.6-8]).

The cited literature lets us sufficiently recognize a fact that will need to be emphasized next: What different authors describe as a fronto-occipital bundle in the normal brain, is by no means a uniform structure. All consider the tapetum to be its occipital portion, either as a whole or in part. For the frontal portion however, at least two different tracts come into consideration, the fasciculus nuclei caudati and the area r, according to our description above. von Monakow is probably the only one who still adheres, together with Onufrowicz, to the identification of the fronto-occipital bundle as the superior longitudinal fasciculus. It appears therefore obvious that it is unacceptable to talk of a “fronto-occipital bundle” in pathologic-anatomical descriptions.

As concerns the area r, in which Dejerine in particular sees a fronto-occipital association system, as mentioned above one can recognize most easily on sagittal cuts that it belongs to the corona radiata.

(10.) Obersteiner and Redlich (1902, p. 301) found it “completely inadmissible to draw conclusions regarding normal anatomy from findings in brains with hereditary agenesis of the corpus callosum” and they (pp. 302–306):

agree with those authors (Sachs, Marchand, Roemer, Probst, Bischoff and others) who assume that the so-called fronto-occipital fascicle in the brain with corpus callosum agenesis consists of callosal fibers…. First of all we would like to emphasize that a bundle characterized by the location and size of the so-called fronto-occipital fasciculus [seen] in the brain without a corpus callosum does not exist in the normal human brain. If we admit the assumption, that due to the missing callosal fibers the fasciculus fronto-occipitalis could have changed its location and emerged more visibly, by all means we would have to find evidence for such a bundle in the normal brain. But that is not the case. If we follow, for example, Dejerine’s description and illustrations, which we can compare especially well in frontal and basal cuts of brains of young children, we have to admit that a fiber system exists in the area of the caudate nucleus that is set apart moderately well in certain areas of the brain. However, it is located lateral to the caudate nucleus, as Schröder has already mentioned, and not medially as is the case with the fronto-occipital fasciculus of Onufrowicz.

If we try to clarify the course of this bundle on frontal and basal cuts, we have to state that it appears in front of the caudate nucleus in the form of a few bundles of coarse fibers that appear to emerge from the posterior layer of the corpus callosum (“rückläufigen Balkenschichte,” Sachs). Those fibers then form an arc that runs dorsally and remains lateral to the caudate nucleus. New fibers from the frontal and dorsal areas of the brain enter the tract, because on frontal cuts of the white matter we see a few of those fibers appearing, arranged in thin bundles, breaking into the callosal fibers and running to the lateral part of the caudate nucleus and—as we learn from horizontal sections—they turn dorsally. This is the reason that the fiber bundle becomes more bulky dorsally. The bulkiest portion is in the plane in which the caudate nucleus has just been capped (“gekappt”). But even here (Fig. 4) the bundle is not impressive and by no means comparable to the massive bundles described in brains without a corpus callosum. Furthermore it cannot be traced much further in the caudal direction, even along the entire dimensions of the caudate nucleus. Its rostral and dorsal aspect that has a fuzzy (indistinct) border with the corona radiata becomes progressively more washed-out and it essentially dissolves in it. If anything, this bundle can be separated best [from the corona radiata] in young children due to the slightly different caliber and color of its fibers. One can almost always easily separate this bundle from the callosal fibers (due to the bigger caliber of the fibers). Again, a combination of frontal and basal cuts teaches us that a very small tract of this bundle can be traced backwards where it runs apparently along the tail of the caudate nucleus to the lower horn in a dorsally-convex arc (Fig. 5), slightly lateral to the stratum subcallosum. But it is necessary to re-emphasize the fact (p.606) that these bundles are minute and can only be seen in certain cuts.

Another detail has to be added. The thick fibers that belong to this bundle are, as more rostrally-made frontal cuts illustrate, arranged in small bundles that become interwoven and dissolve towards the caudate nucleus. The coarse fibers that constitute the bundles are braided around the fibers that build a thick meshwork (also in Schröder and Fig. 1). Further back, the fine braided fibers disappear again, and only bundles of coarse fibers remain. The fine fibers become myelinated later than the coarse ones.

In the animal we find very different circumstances. A sharply delineated fiber system that would correspond to the one that we have just described in the human cannot be found. At most, we see a few bundles that maintain the same direction as the bundles just discussed in the monkey and in martens, which cannot be separated from the corona radiata in any way.

We believe that these few remarks justify the claim that the normal bundle cannot be identified as the fronto-occipital bundle of Onufrowicz. We can exclude the possibility that the former contains association fibers based on what we have said (see also Probst). Therefore the assumptions of certain authors who previously ascribed certain physiological roles to the system are invalid (for example Kirchhoff). Its origin in the frontal brain seems to be certain, but we cannot trace it to the occipital lobe. The assumption by Sachs, who agrees with Schröder, that this system contains corona radiata fibers, seems quite plausible. Also Flechsig, Romer and Probst ascribe the fasciculus fronto-occipitalis of Dejerine to the projection fibers. The latter designates this fiber area in the second volume of his Anatomie des Centres nerveux as OF+P, “faisceau complexe contenant a la fois des fibres du faisceau occipito-frontal et des fibres de projections.” The designation by Sachs “reticulated corona radiata field” (“reticulirtes Stabkranzfeld”) is quite correct. In considering the intimate spatial relationship of this bundle to the caudate nucleus—we refer among other things to the part following the tail of the caudate—it appears quite likely that this bundle, that stands out from the remaining projection fibers to a certain degree, contains fibers that run directly from the cortex to the caudate nucleus, so that we would suggest the designation reticulated cortico-caudal bundle. It would not be impossible that the fibers that constitute the coarse bundle dissolve into the fine braided fibers and from here transition into their terminal station, the caudate nucleus. A definite conclusion will only be possible after examining circumscribed fresh cortical foci that have been prepared according to the method of Marchi. An experimental-anatomical examination is excluded since the bundle cannot be separated sufficiently in the animal.

(11.) As Muratoff wrote in 1893 (1893a, p. 724): “The tapetum, the posterior end of the subcallosal fasciculus, is … not affected by a transection of the corpus callosum.” Page 725:

In experiment 24, during the transection of the corpus callosum, I injured the subcallosal fasciculus and this resulted in degeneration of large numbers of its fibers. The degeneration was much more severe than following destruction of various parts of the cortex. I could not follow the degenerated fibers throughout the entire course of the system. After a long course in the sagittal direction they curve upwards and disappear in the cortex after the curvature around the corpus callosum. Therefore the subcallosal fasciculus and the tapetum of the corpus callosum represent one and the same fiber system. Both are long tracts that connect different areas in the cortex of one hemisphere with each other, and therefore they are association fibers in the sense of Meynert. This is a complicated system. All its fibers have the same physiological characteristics but their terminations in the cortex are different. Based on the results of my experiments, one can assume that all fibers of the system originate and terminate in the cortex.

(12.) In Schröder (1901, p. 90), von Monakow (1892) is quoted as follows: “The fibers of the so-called tapetum of the corpus callosum (‘Balkentapete’) … I consider as association fibers that connect the occipital lobe partly with the parietal and partly with the frontal lobe (fasciculus longitudinalis superior). In normal brains one sees that these fiber bundles cease to be a cohesive fiber tract in the area of the posterior central gyrus and start to scatter from here.” In a later work, von Monakow (1899) argues in a similar manner, except that he modifies his opinion concerning the tapetum, which he regards as consisting largely of callosal fibers, and then he says: “The parts of the tapetum that enter the superior longitudinalis fasciculus curve initially in an upward direction and disperse with numerous fascicles through the … splenium-portions of the callosum, and only gather again in the area of the posterior thalamus, in fact in a portion that lies between the internal capsule, the tail of the striate and the hemispheric myelin substance.”

(13.) Obersteiner and Redlich, 1902(p. 286):

Schröder can take credit for pointing out the confusion and its causes surrounding the “Tapetum-question” in two recently published essays. While on the one hand, the tapetum is considered a part of the corpus callosum, on the other hand—especially based on findings on brains lacking the corpus callosum—the callosal nature of the tapetum has been denied, and [instead] it has been allocated to a long association bundle (fasciculus fronto-occipitalis), which itself has been identified respectively as the fasciculus nuclei caudati (Sachs) and the fasciculus subcallosus (Muratoff). Schröder has correctly pointed out that things were brought (p.607) in parallel here whose relationship cannot be proven. Schröder now argues that this fasciculus subcallosus does not represent the tapetum in a strict sense; he also doubts, that it contains exclusively association fibers. Herewith, Schröder returns with Sachs to the original assumption, that the tapetum exclusively contains callosal fibers. We have previously mentioned that on the one hand people adhere to the callosal nature of the tapetum, while on the other hand it has been assigned to the fasciculus fronto-occipitalis either in whole or in part (for example by Dejerine, Edinger, Monakow, Gianelli, Zingerle). From the fronto-occipital fasciculus we could only track a very small and thin bundle to the lower horn, otherwise it is not in consideration here. The statement by Bianchi, that after ablating the frontal lobe in the monkey, a degeneration of the fronto-occipital association-system according to Marchi cannot be traced to the tapetum may be mentioned here.

(14.) Muratoff, 1893b (p. 98):

Through faradic excitation, I determined the center of this or that extremity, of the facial muscles and the center of the entire motor area. Afterwards, I removed the corresponding area with a sharp spoon…. The operated animals were kept alive for two weeks up to one month … The anatomical examination was identical in all cases. I used a new method that was introduced by Marchi.

In his experiment 5 he removed the entire motor area:

The defect in the left hemisphere covers almost the entire area of the motor cortex. The superior border of the defect reaches almost the medial edge of the hemisphere…. The lesion is exclusively bordered by cortical substance and only the most superficial layer of the corona radiata fibers is here and there affected. The lesion produced motor weakness of both extremities, inversion of the right-sided paws when walking, and all modalities of sensation were affected on the right side.

(15.) Muratoff, 1893b (p. 98):

In our material, only its broadened angulated mid-portion is degenerated, [comprising] in fact, the majority of fibers. The medial and inferior portions, which face the corpus callosum and the caudate, are normal. (Fig I and Fig II) … [T]he degeneration within this system is always localized to a certain portion, i.e., an expanded protrusion situated above the body of the caudate. On sagittal section one can recognize long degenerated fibers within this bundle; the number of the degenerated fibers depends again on the size of the lesion. On some cuts one can see how the fibers from the cortex run into the subcallosal fascicle. Its degeneration is always on the same side as the lesion. Within this system, the fibers have the following order: from the lesioned area of the cortex they descend downwards, run around the corpus callosum and enter the subcallosal fascicle. Here they run a longer or shorter distance sagittally, and terminate in the cortex of the frontal or occipital lobe. These are the long bow-like fibers that run below the corpus callosum. The fact that the degeneration is always limited to the expanded mid-portion of the bundle is noteworthy.

(16.) Muratoff provided further detail in his description of the subcallosal fasciculus (1893a, pp. 721–722):

On sagittal cuts this fiber system is longitudinally oriented. As a consequence of the increase in caliber of the descending part, the thickness of this bundle is different on the various cuts—some taken from the medial border of the hemisphere and others from the lateral. On sections from the medial border of the hemisphere, it looks like a small fiber bundle in the form of a flat arc, corresponding to the curvature of the corpus callosum. On sections taken 0.5 cm further laterally, the subcallosal bundle is much thicker, equal in size to approximately half of the corpus callosum. One can follow the subcallosal fasciculus through the entire length of the corpus callosum. The lower surface is covered by ependyma. Posteriorly, below the splenium of the corpus callosum, this lower border becomes unclear, and merges together with the fornix in one structure. At high magnification, one can convince oneself that here, two leaves of ependyma touch each other. The superior leaf covers the surface of the subcallosal fasciculus, and the inferior leaf is on the upper surface of the fornix. Following the corpus callosum, the subcallosal fasciculus makes two flat curves—a posterior curve below the splenium of the corpus callosum, and an anterior curve below the genu of the corpus callosum. Here the fasciculus becomes much thicker, and without sharp delimitation it becomes a layer of fibers that covers the caudate body. These two fiber categories form, so to speak, an anatomically indivisible bundle at the anterior end of the genu. Further back, one again sees two layers of ependyma that cover the subcallosal fasciculus and the caudate body.

Therefore the parts in the above-mentioned areas have the following relation to one another. 1: corpus callosum; 2: subcallosal fasciculus; 3: superior ependymal layer; 4: the anterior end of the caudate body and the posterior end of the fornix. We provide this detailed topographical and anatomical description of the system because in textbooks it is mostly not described. On reviewing the literature in this regard we find multiple previous reports of this system. As far as I can ascertain, it was described first by Onufrowitz … [and subsequently] … Kauffman described this in more detail in a brain with agenesis of the corpus callosum…. If we imagine that in our cases the corpus callosum was missing, the anatomical position of our subcallosal fasciculus would be the same as the (p.608) fronto-occipital bundle described by Onufrowitz and Kauffman…. Both authors equate their system with Burdach’s arcuate fasciculus. “The genius Burdach recognized this fiber tract, or probably guessed it” (Onufrowicz, p. 322). Reading the original text, one can have doubts about this assumption. Burdach certainly described a bundle that connects the frontal and occipital lobes, but he localized it lateral to the corona radiata at the level of the corpus callosum. Sachs emphasizes this inconsistency. Indeed, our system is positioned as a compact bundle medial to the corona radiata and below the corpus callosum. Without denying the priority of the discovery of the system by Onufrowicz and Kaufmann, I would like to insist on the term “subcallosal fasciculus.” As we will see further below, this bundle does not exclusively represent a frontal occipital association tract. In his recent book, Sachs described this system as the fasciculus of the caudate nucleus. Miraculously, Schnopfhagen did not recognize the neuronal nature of this structure, and concluded instead that it was an ependymal layer.

(17.) Muratoff, 1893 (p. 724):

The subcallosal fasciculus degenerates with destruction of the frontal or occipital gyri. In the latter case, degeneration is not limited to the descending part, but is more diffuse and involves the entire system. From a number of frontal cuts, one can convince oneself that the degenerated fibers do not traverse the entire system. In other words, the subcallosal fasciculus does not carry direct frontal occipital communication tracts. (von Monakow had the same opinion regarding the probable structure of the frontal occipital bundle when he referred to pathological anatomical examinations.) Fibers from the anterior sigmoid gyrus travel a short distance within this bundle anteriorly and posteriorly and then enter the cortex of more distant parts of the hemisphere. This seminal picture is evident from examination of sagittal cuts, regardless of whether the lesion is in the frontal or the occipital lobes.

(18.) Sachs (1893, pp. 78–79) chose the designation “fasciculus nuclei caudati” because of the:

intimate relationship of the so-called fiber layer to the caudate nucleus…. [T]he bundle, which connects the striatum (“Streifenhuegel”) with the cortex, in particular with the cortex of the frontal and parietal lobe as well as the insula, and therefore contains association fibers of both parts of the brain, accompanies the caudate nucleus along its entire course lateral to the lateral ventricle. The cross section of this bundle becomes smaller posteriorly in relationship to the decrease in size of the caudate nucleus, so that only the outline of this bundle is present in the descending part of the caudate nucleus. With a thin tapering layer, like a capsule, this bundle covers also the free, ventricular surface of the nucleus. From this bundle, fibers continually enter the bulk of the caudate nucleus, to dissolve here in its fine fiber meshwork. Another contribution comes also from the external capsule.

(19.) Dejerine, 1895 (pp. 760 and 765):

This fascicle that we call in our serial sections, occipital frontal fascicle, is in fact the fascicle that was described by Meynert under the name of corona radiata of the caudate nucleus, and by Wernicke under the name of fascicle of the corpus callosum traveling to the internal capsule … Experimental work in the dog being performed by Muratoff indicates that the occipito-frontal fascicle of Forel and Onufrowicz (subcallosal fasciculus of Muratoff), is partially degenerated following ablation of the motor sphere, or destruction of the frontal or occipital convolutions.

(20.) Flechsig, 1896 (p. 3):

The “subcallosal fasciculus” (Muratoff) contains corona radiata bundles that exit from the internal capsule in the area that is situated in front of the mid-portion of the thalamus. Tracts of different lengths run adjacent to the caudate body, in part reach anteriorly to the genu of the corpus callosum, and join the corona radiata of the gyrus fornicatus and the anterior portion of my cortical sensory area (“Tastsphäre”). Some of these corona radiata bundles run almost through a third of the hemispheric length in sagittal direction. Callosal fibers join them and while some accompany them leading rostrally, others curve posteriorly leading to the parietal and occipital lobes. There are only very few bundles that join from the stratum zonale of the caudate nucleus.

(21.) According to Schröder (1901, p. 89), Oskar Vogt (1895) recognized that Muratoff had described a subcallosal fasciculus, but Vogt:

distinguished the subcallosal fascicle from a very narrow, darkly tinged fiber layer that covers the caudate nucleus on its dorsal and medial surface, [that he regarded as] an association system of the caudate nucleus. Vogt considered the subcallosal fascicle to be an association system of the cortex that has nothing to do with the caudate nucleus. In contrast to Muratoff, he assumed the predominance of long fibers, based only on the experience that association fibers within the brain are always longer when they lie more closely adjacent to the ventricle. He saw especially prominent dispersion of fibers to the cortex frontally and laterally through the external capsule towards the insula.

(22.) Schröder, 1901 (p. 93):

Experiments by Muratoff and O. Vogt who saw degenerations within this bundle after removal of cortical parts are (p.609) evidence that it has relationships to the cortex. Two facts however speak against considering this bundle as a pure association system of the cortex, i.e., to assume that its fibers come from the cortex and return to the cortex after a longer or shorter course. At first, the intimate positioning of this bundle to the caudate nucleus is remarkable, it accompanies it as we saw on its entire course and—this is also important—its cross section diameter is always proportional to that of the caudate. In the anterior horn at the head of the caudate nucleus, a massive fiber layer; along the tail of the caudate nucleus in the lower horn, a small and thin fiber layer underneath the ependyma. This seems to suggest with high probability that the caudate bundle and caudate nucleus have a close anatomical and physiological relationship to each other. The second point is the unusual position for a cortical association system in the deepest depth of the hemisphere, directly adjacent to the ventricular wall. It is inconceivable that association fibers from the cortex run so deep only to run back the same far distance, especially since these fibers, as Muratoff’s degeneration experiments revealed, are not long ones that connect distant cortical areas, but only run a very short distance in the sagittal direction within the bundle. That must be the reason why O. Vogt disagreed with the findings of Muratoff and made the a priori assumption of the predominance of long fibers within the bundle, because of the empirical evidence that association fibers within the brain seem to be longer the further away they are from the cortex. The formation of the fasciculus nuclei caudati, however, argues against the predominance of long sagittal fibers within it. Fibers that run for long stretches in the same direction tend to form compact bundles, whereas the fasciculus nuclei caudati has more the appearance of a meshwork.

(23.) Obersteiner and Redlich, 1902 (pp. 290–301):

One of us (Redlich, 1897) has seen degeneration of the subcallosal fasciculus after an extensive lesion of the frontal brain that was not limited to the cortex alone, but it was insignificant and could only be seen in short stretches. There is therefore no evidence that the above-mentioned bundle contains fibers directly from the frontal lobe to the occipital lobe. In those cases the lesion extended beyond the cortex, so that a direct relationship between cortex and the fasciculus cannot be alleged, although we can confirm Muratoff’s statement that the degeneration of this bundle is restricted to the same side…. [A]fter unilateral lesions of posterior parts of the brain, degeneration of the corpus callosum was seen above the lower horn on the other side, but medial to it, immediately adjacent to the ventricular ependyma, one can find a non-degenerated area. In contrast, the statement by Muratoff, that the subcallosal fascicle forms an anatomically indivisible bundle with the fiber layer that covers the caudate nucleus—he obviously means the stratum zonale of the caudate nucleus—is wrong. Moreover it is obvious that both fiber categories only have a spatial relationship—and this to only limited degree—but they are otherwise to be differentiated.

On frontal cuts of adult humans and also in most animals, the basal aspect of the subcallosal fascicle abuts the caudate nucleus and reaches along the medial plane of the caudate nucleus inferiorly, so that it appears that it merges with the thin layer of nerve fibers that wrap around the caudate nucleus on its dorsal and medial surface (Stratum zonale, nuclei caudati of Obersteiner). On closer view, the two layers can be separated from each other; whereas the fibers of the subcallosal fascicle have thin caliber, the fibers of the stratum zonale are a little thicker and represent an even thicker meshwork than the subcallosal fascicle…. Both fiber layers can also be separated by reference to their historical development. As Bechterew has described elsewhere, the fibers of the subcallosal fascicle myelinate relatively late; even in a child of several months (Fig. 1) we find the subcallosal fascicle unmyelinated, whereas the stratum zonale is fully developed and covers the caudate nucleus as a narrow and compact nerve fiber layer on its dorsal surface, reaching medially and downwards, separated from the ventricular surface by a thin and bright layer, the ependyma. Carmine preparations or other techniques that stain the cells permit the separation of the subcallosal fascicle from the stratum zonale by yet another means (here one can also convince himself of the correct statement by Sachs that the fasciculus nuclei caudati does not contain ganglia). On such preparations in humans one can easily convince oneself that nests of relatively large cells, which resemble ependymal cells, can be found between the caudate nucleus and the subcallosal fascicle. Here, the glia frequently tend to show a slight aggregation, corresponding to Weigert’s striped keel (“Kielstreifen”). These cells can also be found along the medial plane of the caudate nucleus between the ependyma and the stratum zonale, as well as on the outer plane of the caudate nucleus. They can also be seen on the dorsal surface of the subcallosal fascicle that trails dorsally along the corpus callosum, above the former. Not uncommonly one finds crosscut vessels or large lymphatic areas that create border zones. The aggregation of such cells is even more substantial between the subcallosal fascicle and the caudate nucleus in animals such as cats, dogs, horses, calves etc., where one can distinguish the subcallosal fascicle macroscopically. Our findings permit almost no other interpretation than that both formations are differentiated historically through development. The cells described must therefore be considered as remnants of further divisions that existed previously.

Whereas the subcallosal fascicle maintains an intimate spatial relationship to the caudate nucleus in humans so that Sachs suggested the term fascicle nuclei caudati, the situation (p.610) is profoundly different in animals. Here, the spatial relationship between the caudate nucleus and the subcallosal fascicle is only regional, i.e., it exists only in certain portions of this bundle, if we may be permitted to say it like that. Concerning this matter, however, many differences exist in various animals….

In the most anterior portion as well as posteriorly where it covers the lateral wall of the lower horn of the ventricle the fibers [of the subcallosal fasciculus] have a more parallel direction—at least in a few places—but here they follow a mostly dorso-ventral direction, not a fronto-occipital one, so that in the frontal cut the fibers are cut longitudinally and not transversely. This is in contrast to the assumption of Muratoff and Vogt that the subcallosal fascicle represents a fronto-occipital association system. Rather, the designation fasciculus subcallosus, as chosen by Muratoff, is more correct than the term fasciculus nuclei caudati (Sachs), particularly when considering the situation in animals. Whereas in the human the latter term may be right in that the aforementioned fiber system has a spatial relation to the caudate nucleus, this is not the case in animals as we have seen. But even in humans it is not entirely correct that the caudate nucleus and the subcallosal fascicle are proportional in size to each other. How much less this is true in animals—especially in those animals that have a well-developed bundle—we have previously described in detail. Here, we see a spatial relationship to the caudate nucleus only in certain stretches, but there is always very close attachment to the corpus callosum, which is why it is called subcallosus. It does not, however, represent a fascicle in the ordinary sense in which one understands it to contain fibers oriented in the same direction. Rather, it contains thickly woven fibers that have a great variety of directions. Therefore it seems that the term stratum subcallosum is possibly the best fitting one.

It appears quite difficult to comment on the significance of this fiber system, its origin and its terminations. I can state that the fibers contained in the stratum subcallosum do not originate within it, because, as mentioned earlier, the stratum subcallosum does not contain ganglion cells. Many authors count the subcallosal fascicle among the projection systems … Sachs also believes that his fasciculus nuclei caudati provides a connection between cortex and caudate nucleus …

An exclusive relation of the subcallosal fascicle to the caudate nucleus cannot be defended for we find the subcallosal fascicle particularly prominent in animals in which the caudate nucleus does not exist. However, a relation to the cortex does not appear to be implausible. On basal cuts in human one sees on extremely ventrally placed cuts, where the subcallosal fascicle is relatively poorly myelinated, more or less distinct bundles of fine fibers that run through its area and cross each other, apparently coming from the frontal cortex, according to what Dejerine designated as “bundle of the fronto-occipital fascicle to the third frontal gyrus.” Considering the small caliber of the fibers that are contained in the subcallosal fascicle it appears quite unlikely that those are long fibers, such as [one sees in] a long association system. We found no evidence for connections to the external capsule as has been assumed by several authors.

(24.) Riley (1960, p. 568) dismissed the existence of a “[f]asciculus cortico-caudalis reticulatus (Obersteiner-Redlich). This fasciculus is erroneously named and does not connect the cortex and caudate nucleus except for perhaps a few fibers. It is applied to the caudate nucleus laterally. Its fibers probably enter the internal capsule or the thalamic nuclei.”