Functional Anatomy of the Inferior Longitudinal Fasciculus: From Historical Reports to Current Hypotheses

Abstract

The inferior longitudinal fasciculus (ILF) is a long-range, associative white matter pathway that connects the occipital and temporal-occipital areas of the brain to the anterior temporal areas. In view of the ILF's anatomic connections, it has been suggested that this pathway has a major role in a relatively large array of brain functions. Until recently, however, the literature data on these potential functions were scarce. Here, we review the key findings of recent anatomic, neuromodulation, and neuropsychological studies. We also summarize reports on how this tract is disrupted in a wide range of brain disorders, including psychopathologic, neurodevelopmental, and neurologic diseases. Our review reveals that the ILF is a multilayered, bidirectional tract involved in processing and modulating visual cues and thus in visually guided decisions and behaviors. Accordingly, sudden disruption of the ILF by neurologic insult is mainly associated with neuropsychological impairments of visual cognition (e.g., visual agnosia, prosopagnosia, and alexia). Furthermore, disruption of the ILF may constitute the pathophysiologic basis for visual hallucinations and socio-emotional impairments in schizophrenia, as well as emotional difficulties in autism spectrum disorder. Degeneration of the ILF in neurodegenerative diseases affecting the temporal lobe may explain (at least in part) the gradual onset of semantic and lexical access difficulties. Although some of the functions mediated by the ILF appear to be relatively lateralized, observations from neurosurgery suggest that disruption of the tract's anterior portion can be dynamically compensated for by the contralateral portion. This might explain why bilateral disruption of the ILF in either acute or progressive disease is highly detrimental in neuropsychological terms.

Keywords: emotion recognition; inferior longitudinal fasciculus; lexical retrieval; prosopagnosia; reading; semantics; ventral pathway; visual agnosia.

FIGURE 1

Historical and recent anatomic descriptions of the ILF. (A) A drawing of a coronal section passing through the ventricular atrium posterior to the caudate nucleus, showing the inferior longitudinal fasciculus (Fli) surrounding the optic radiations (RTh), the tapetum fibers (Tap), and the lateral ventricle (Vl). From Dejerine’s and Dejerine-Klumpke’s book “Anatomiedes Centres Nerveux,” 1895. Figure 383. (B) Reconstructions of autoradiographic observations. Injection sites and cortical projections in three monkeys are illustrated. Top left panel: injection (in black) into the striate cortex (V1), showing projection to V2 via U fibers and labeled fibers in the internal sagittal stratum that terminate subcortically in more rostral sections. Top right panel: injection into V2, showing projection to V4 via U fibers, labeled fibers in the internal sagittal stratum that terminate subcortically in more rostral sections, and labeled fibers in the tapetum that cross to the contralateral hemisphere. Bottom panel: injection into V4, showing projection to inferior temporal (IT) cortex via U fibers, labeled fibers in the internal sagittal stratum that terminate subcortically, and labeled fibers in the tapetum that cross to the contralateral hemisphere via the corpus callosum. Tusa and Ungerleider (1985) concluded that the ILF does not have long association fibers. (C) The ILF (in green) and the U-shaped fibers (in red) of the right hemisphere in a single brain dataset. The U-shaped fibers are located laterally to the ILF, and connect the adjacent gyri of the lateral occipitotemporal cortices to form the occipital-temporal projection system from Catani et al. (2003) (D) Subcomponents of the ILF. Top and middle rows: Diffusion tensor tractography of ILF subcomponents in an individual. Top row: a coronal view of the whole course of each segment (from the occipital terminations). Middle row: a sagittal view of a tractographic reconstruction of the four ILF subcomponents on the right side and only three segments on the left side. Bottom row: White matter dissection of the lateral aspect of a left hemisphere, showing the dorsolateral occipital segment (left panel) and the cuneal segment (right panel). Permission to reproduce the figures has been granted. A, anterior; AF, arcuate fasciculus; COp, central operculum; Cu, cuneal segment (blue); DL, dorsolateral occipital segment (turquoise); DLOC, dorsolateral occipital segment; Fu, fusiform segment (orange); hSLF, horizontal segment of the superior longitudinal fasciculus; L, left; Li, lingual segment (green); P, posterior; POS, parieto-occipital sulcus; R, right; SSS, sagittal stratum; STG, superior temporal gyrus.

FIGURE 2

Putative functional pathways supported by the short and long fibers of the ILF. This schematic summary is derived from the recent literature data (mainly neuropsychological studies) on the ILF’s functions. Functional pathways that are biased toward a particular hemisphere are represented by thicker lines and larger circles. The neuropsychological syndromes in the event of disruption are as follows: (1) pure alexia; (2) reading comprehension; (3) apperceptive prosopagnosia; (4) associative prosopagnosia; (5) impairments in emotion recognition or hypoemotionality; (6) scene perception impairments; (7) visual memory impairments; (8) semantic and/or lexical retrieval impairments; and (9) visual agnosia. AMG: amygdala; ATL: anterior temporal lobe; FFA: fusiform face area; Hip: hippocampus; LOC, lateral occipital cortex; OFA: occipital face area; pITG: posterior inferior temporal gyrus; PPA, parahippocampal place area; vWFA, visual word form area.