The anatomy of fronto-occipital connections from early blunt dissections to contemporary tractography

Abstract

The occipital and frontal lobes are anatomically distant yet functionally highly integrated to generate some of the most complex behaviour. A series of long associative fibres, such as the fronto-occipital networks, mediate this integration via rapid feed-forward propagation of visual input to anterior frontal regions and direct top-down modulation of early visual processing. Despite the vast number of anatomical investigations a general consensus on the anatomy of fronto-occipital connections is not forthcoming. For example, in the monkey the existence of a human equivalent of the 'inferior fronto-occipital fasciculus' (iFOF) has not been demonstrated. Conversely, a 'superior fronto-occipital fasciculus' (sFOF), also referred to as 'subcallosal bundle' by some authors, is reported in monkey axonal tracing studies but not in human dissections. In this study our aim is twofold. First, we use diffusion tractography to delineate the in vivo anatomy of the sFOF and the iFOF in 30 healthy subjects and three acallosal brains. Second, we provide a comprehensive review of the post-mortem and neuroimaging studies of the fronto-occipital connections published over the last two centuries, together with the first integral translation of Onufrowicz's original description of a human fronto-occipital fasciculus (1887) and Muratoff's report of the 'subcallosal bundle' in animals (1893). Our tractography dissections suggest that in the human brain (i) the iFOF is a bilateral association pathway connecting ventro-medial occipital cortex to orbital and polar frontal cortex, (ii) the sFOF overlaps with branches of the superior longitudinal fasciculus (SLF) and probably represents an 'occipital extension' of the SLF, (iii) the subcallosal bundle of Muratoff is probably a complex tract encompassing ascending thalamo-frontal and descending fronto-caudate connections and is therefore a projection rather than an associative tract. In conclusion, our experimental findings and review of the literature suggest that a ventral pathway in humans, namely the iFOF, mediates a direct communication between occipital and frontal lobes. Whether the iFOF represents a unique human pathway awaits further ad hoc investigations in animals.

Occipital Cortex of Blind Individuals Is Functionally Coupled with Executive Control Areas of Frontal Cortex

“…However, prior diffusion tensor imaging studies with blind individuals argue against this possibility. The frontal and occipital lobes are connected by the inferior fronto-occipital fasciculus and by a portion of the superior longitudinal fasciculus extending into the occipital lobe (Forkel et al, 2014). Contrary to the hypothesis of increased anatomical connectivity, inferior fronto-occipital fasciculus shows reduced white matter integrity in blindness (Shu, Liu, et al, 2009).…”

Transport for language south of the Sylvian fissure: The routes and history of the main tracts and stations in the ventral language network

“…While both the UF and ILF have relatively long histories, the MdLF has been scarcely considered until very recently and its potential function remains poorly understood. Additionally, the IFOF has become increasingly popular in the current literature but it is riddled with a debate over its very existence, as is ILF (Forkel et al, 2014;Schmahmann & Pandya, 2007;Tusa & Ungerleider, 1985). There is also considerable controversy over tract origins, terminations and routes.…”

“…Although many studies have documented the presence of this pathway using both gross dissection and tractography methods (Axer et al, 2012;Catani et al, 2002;Forkel et al, 2014;Martino, Brogna, et al, 2010;Sarubbo et al, 2013), based on its absence in primate tracer studies, some researchers have argued that the IFOF is not a true tract but a misidentification of other ventral pathways Saur et al, 2008;Schmahmann & Pandya, 2007). However, while there has been no evidence for the existence of the IFOF in primates (Schmahmann & Pandya, 2007), studies have described a primate EmC which tracks from the frontal lobe to posterior regions in the superior temporal sulcus, following a course similar to the IFOF (Schmahmann & Pandya, 2009).…”

Remission of lifelong episodic dyscontrol after bilateral dorsolateral temporal lobe damage

“…Bauer's patient suffered a bilateral occipitotemporal traumatic hemorrhage, while Habib's patient suffered a right occipitotemporal infarction. The authors concluded that the visual hypoemotionality resulted from the interruption of the fiber systems that connect the visual association cortices with the anterior temporal lobes 1 (Forkel et al, 2014;Tusa & Ungerleider, 1985).…”

“…The other system is direct and composed of fast conducting long association fibers that connect the ventromedial extrastriate occipital cortex with (a) the anterior lateral and medial temporal cortices, and (b) the orbitofrontal and frontopolar cortices. This system has long been known as the inferior fronto-occipital fascicle (Forkel et al, 2014). The projections of both fiber systems are reciprocal.…”