Elsevier

NeuroImage

Volume 37, Issue 4, 1 October 2007, Pages 1100-1111
NeuroImage

The occipitofrontal fascicle in humans: A quantitative, in vivo, DT-MRI study

https://doi.org/10.1016/j.neuroimage.2007.05.042Get rights and content

Abstract

Since the existence of the occipitofrontal fascicle (OFF) in humans has remained controversial, we utilized diffusion tensor imaging (DT-MRI)-based segmentation and tractography to investigate its trajectory in vivo in the human. We found that the OFF is distinct from the subcallosal fasciculus or Muratoff's bundle (MB) and extends from the dorsal and medial parts of the occipital lobe as well as the dorsal, medial and inferior parietal lobules to the dorsal and medial part of the prefrontal and premotor regions. In most of its course, it remains parallel to the corpus callosum, the caudate nucleus and the lateral ventricle. In the coronal plane, the OFF is discerned in the core of the white matter medial to the corona radiata and the superior longitudinal fascicle II (SLF II) and lateral to MB and the corpus callosum. The volumetric measurements of the stem portion of the OFF indicate that the OFF is smaller than the SLF II and the cingulum bundle. Since DT-MRI allows the visualization of OFF fibers leading to the projection areas but not to the origin or termination of these fibers, this has been extrapolated from the experimental data in non-human primates. The OFF may have a role in visual spatial processing along with SLF II.

Introduction

Several cortical association fiber pathways have been described in the human brain using gross dissection and myelin staining techniques. One of these fiber tracts, the occipitofrontal fascicle (OFF), has elicited a great deal of debate regarding its trajectory, origin and termination. Forel and his student Onufrowicz, while studying a case of callosal agenesis attributed the name of occipitofrontal fascicle to an intrahemispheric association fiber pathway, which they observed running in the sagittal orientation lateral to the fornix and internal to the corona radiata (Onufrowicz, 1887). This conclusion was corroborated by Kaufmann (1888) and Hochhaus (1893). Forel and Onufrowitz also stated that the tapetum was part of the OFF and further suggested that the OFF is part of the superior longitudinal (SLF) or arcuate fascicle of Burdach. However, other authors such as Sachs (1893) suggested that the pathway that Forel and Onufrowicz described was just aberrant fibers of the corpus callosum that failed to cross to the opposite hemisphere. Subsequently, this view was confirmed by Probst, 1901a, Probst, 1901b. Dejerine (1895), while describing different association fiber pathways, gave a detailed description of this fiber bundle as well. Dejerine identified the OFF in the normal human brain as a distinct fiber bundle, located medial to the corona radiata and SLF. However, he attributed the original discovery of the OFF to Forel and Onufrowicz and, like those investigators, considered the tapetum to be part of the OFF. Although in his monograph Dejerine illustrated the subcallosal fasciculus or Muratoff's bundle (MB) and the OFF as two separate entities, in his textual description he considered them as equivalent. Since then several authors have considered these two fiber bundles as one and the same. Rosett (1933), using the gross dissection method, interpreted the OFF as contributing thalamo-cortical and cortico-pontine fibers to the cerebral peduncle. Yakovlev and Locke (1961) and Mufson and Pandya (1984) described Muratoff's bundle in the macaque monkey as a separate entity that carries corticostriatal fibers. Recently, the fiber trajectory of the OFF has been outlined in the macaque monkey using the anterograde tracing technique (Schmahmann and Pandya, 2006; Yeterian and Pandya, unpublished data, 2007). According to these authors the OFF fibers originate from the dorsal and medial preoccipital areas and from the inferior parietal lobule and medial parietal region. Petrides and Pandya (2006) have shown that fibers from the caudal dorsolateral prefrontal areas and from the premotor regions project to the inferior and medial parietal as well as the medial occipital cortices. They have designated these fibers as the fronto-occipital fascicle-FOF (Petrides and Pandya, 2006).

With the availability of more refined neuroimaging techniques, several studies in recent years have described the location and course of the OFF in humans in vivo using diffusion tensor MRI (DT-MRI) (Makris et al., 1997, Catani et al., 2002, Mori, 2002). Although the available descriptions of this fiber bundle provide some basic anatomical information, two issues need to be addressed for a better understanding of this fiber system. The first issue is the relationship of the occipitofrontal fascicle with the nearby subcallosal fascicle or MB. So far, no attempt has been done to differentiate the OFF from the MB in the human. These two fiber bundles have been co-equated using DT-MRI (Catani et al., 2002, Mori, 2002). As noted earlier, the OFF and the MB have been identified as two separate entities in non-human primates (Schmahmann and Pandya, 2006; Yeterian and Pandya, unpublished data, 2007). The second issue regards the delineation of the precise origin and terminations of the OFF in humans. In non-human primates, the OFF has been described in terms of its trajectory, origin and terminations (Petrides and Pandya, 2006, Schmahmann and Pandya, 2006; Yeterian and Pandya, unpublished data, 2007) and its relation with MB has been clarified. Using this information derived from non-human primates, one can extrapolate and suggest the possible origin and termination of this fiber pathway on the basis of data obtained with DT-MRI in humans in vivo. The use of DT-MRI tractography along with cortical parcellation of the human brain allows a better delineation of the trajectory of fiber pathways (Makris et al., 2005).

We found that the OFF is present in the human brain as a distinct entity and is separate from the subcallosal fascicle or MB as has been shown in non-human primates. The trajectory and volume of the OFF in normal human subjects were determined in vivo using the tractographic and segmentation DT-MRI methods. We also have extrapolated the experimental findings for the OFF in non-human primates to the human OFF to provide the trajectory of this fiber pathway in terms of its origin and terminations. Detailed information regarding the trajectory and quantification of this fiber system would facilitate more precise anatomical–functional correlational studies as well as better evaluation of white matter structures in clinical conditions.

Section snippets

Methods

We used magnetic resonance imaging (MRI) to quantify the stem portions of the OFF and delineate their trajectories in six normal adult (age range 23 to 33 years) right-handed human subjects (5 males and 1 female). We combined two different DT-MRI-based techniques, specifically fiber tract segmentation and tractography and a T1-based technique for cortical parcellation of the human brain (Caviness et al., 1996). Additionally, in a second ‘illustrative’ experiment, we performed a tractographic

Results

The term occipitofrontal fascicle requires clarification. The designation of a fascicle as occipito-frontal implies that fibers course from the occipital lobe towards the frontal lobe. In experimental animals, however, the OFF region has been shown to contain fibers directed from the frontal to the occipital lobe as well (Petrides and Pandya, 2006). These fibers have been designated as the fronto-occipital fascicle. The term occipitofrontal fascicle has been used interchangeably with

Discussion

As mentioned above the occipitofrontal fascicle (OFF) is a controversial cortico-cortical association fiber pathway. The term occipitofrontal fascicle was originally coined by Forel and Onufrowicz; however, they considered the tapetum to be part of the OFF (Onufrowicz, 1887). To designate the aberrant fibers as the occipitofrontal fascicle was inaccurate, as was pointed out by Sachs (1892), Wernicke (1897), Schröder (1901) and Probst, 1901a, Probst, 1901b (for detailed historical discussion,

Acknowledgments

Preparation of this article was supported in part by grants from: the National Association for Research in Schizophrenia and Depression (NARSAD) and the National Institutes of Health National Center for Complementary and Alternative Medicine (NCCAM) to Dr. Nikos Makris; NS34189 and the Fairway Trust to Dr. David Kennedy. The authors gratefully acknowledge Dr. Edward H. Yeterian, Dr. Larry Seidman, Dr. Andre van der Kouwe, Rudolph Pienaar, Steven Hodge and Ruopeng Wang for their valuable

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