The occipitofrontal fascicle in humans: A quantitative, in vivo, DT-MRI study
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in the macaque monkey using the anterograde tracing technique (Schmahmann and Pandya, 2006; Yeterian and Pandya, unpublished data, 2007).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
References (49)
- et al.
Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI
J. Magn. Reson., Ser. B
(1996) - et al.
White matter fiber tracts of the human brain: three-dimensional mapping at microscopic resolution, topography and intersubject variability
NeuroImage
(2006) - et al.
Virtual in vivo interactive dissection of white matter fasciculi in the human brain
NeuroImage
(2002) - et al.
Cortical surface-based analysis. I. Segmentation and surface reconstruction
NeuroImage
(1999) - et al.
Cortical surface-based analysis: II. Inflation, flattening, and a surface-based coordinate system
NeuroImage
(1999) - et al.
Planum temporale asymmetry: reappraisal since Geschwind and Levitsky
Neuropsychologia
(1987) - et al.
Microstructure of temporo-parietal white matter as a basis for reading ability: evidence from diffusion tensor magnetic resonance imaging
Neuron
(2000) - et al.
MRI-based topographic parcellation of human cerebral white matter and nuclei II. Rationale and applications with systematics of cerebral connectivity
NeuroImage
(1999) Body schema disturbances: finger agnosia and right–left disorientation
- et al.
MRI-based parcellation of human neocortex: an anatomically specified method with estimate of reliability
J. Cogn. Neurosci.
(1996)
Comparative Correlative Neuroanatomy of the Vertebrate Telencephalon
Anatomie des Centres Nerveux, 1980
The young adult human brain: an MRI-based morphometric analysis
Cereb. Cortex
Fingeragnosie: cine umschriebene Storung der Orientierung am eigenen Korper
Wien. Klin. Wochenschr.
Syndrome of finger agnosia, disorientation for the right and left, agraphia, and acalculia
Arch. Neurol. Psych.
Problems of interception of disease and of impaired body territories with organic lesions
Arch. Neurol. Psych.
Some notes on the Gerstmann syndrome
Neurology
Ueber Balkenmangel im menschlichen Gehirn
Dtsch. Z. Nervenheilkd. (Leipzig)
Ueber Mangel des Balkens im menschlichen Gehirn
Arch. Psychiatr.
Neuropsychological Assessment
Diffusion tensor fiber tracking of human brain connectivity: acquisition methods, reliability analysis and biological results
NMR Biomed.
Morphometry of in vivo human white matter association pathways with diffusion-weighted magnetic resonance imaging
Ann. Neurol.
Quantitative DT-MRI investigations of the human cingulum bundle
Cent. Nerv. Syst. Spectr.
Diffusion tensor imaging
Cited by (84)
Deconstructing the Posterior Medial Episodic Network
2020, Trends in Cognitive SciencesEffects of unilateral cortical resection of the visual cortex on bilateral human white matter
2020, NeuroImageCitation Excerpt :In the ILF, abnormalities were evident in patients with either anterior or posterior resection, while in the IFOF, abnormalities were seen only in patients with posterior resections. This is unsurprising as the trajectory of the IFOF was more medial (Makris et al., 2007), while the anterior resections in the patients here were more lateral, thereby sparing the IFOF. Distal to the resection (either antero- or retrograde) in the ipsilesional tracts, the microstructural indices were normal compared to controls.
Does the superior fronto-occipital fascicle exist in the human brain? Fiber dissection and brain functional mapping in 90 patients with gliomas
2020, NeuroImage: ClinicalCitation Excerpt :It has been used extensively to reveal white matter fibers in vivo (Catani et al., 2002; Hagmann et al., 2003) and provides a powerful tool to demonstrate finer changes in white matter fibers (Tovar-Moll et al., 2007). Using this technique, some studies have delineated the SFOF in the human brain (Catani et al., 2002; Wakana et al., 2004; Makris et al., 2007). However, a recent study using more advanced fiber tractographies could not reveal its existence, location, and trajectory in the normal human brain (Forkel et al., 2014; Meola et al., 2015; Mori et al., 2002; Milian et al., 2014).
Depression Severity Over 27 Months in Adolescent Girls Is Predicted by Stress-Linked Cortical Morphology
2019, Biological PsychiatryCitation Excerpt :Premature activation by stress may alter developmental programming and increase vulnerability to develop psychopathology (10). The four stress-linked regions share physical connection via the occipitofrontal fasciculus (70), implicating maturation of this particular fiber pathway in vulnerability to stress (more so than other tracts for this cohort). In addition, these regions are part of functional connectivity networks that increase after trauma (71) and during recovery from experimentally induced social stress (72).
Neural Circuitry: Architecture and Function—A Fiber Dissection Study
2019, World NeurosurgeryCitation Excerpt :The inferior parietal lobule is known to play a role in spatial attention and visual awareness. Thus, the SLF-II provides the prefrontal cortex with information regarding the perception of visual space.9-11 The SLF-III connects the supramarginal gyrus to the ventral premotor and prefrontal cortex.