Functional specialization for auditory-spatial processing in the occipital cortex of congenitally blind humans

Abstract

The study of the congenitally blind (CB) represents a unique opportunity to explore experience-dependant plasticity in a sensory region deprived of its natural inputs since birth. Although several studies have shown occipital regions of CB to be involved in nonvisual processing, whether the functional organization of the visual cortex observed in sighted individuals (SI) is maintained in the rewired occipital regions of the blind has only been recently investigated. In the present functional MRI study, we compared the brain activity of CB and SI processing either the spatial or the pitch properties of sounds carrying information in both domains (i.e., the same sounds were used in both tasks), using an adaptive procedure specifically designed to adjust for performance level. In addition to showing a substantial recruitment of the occipital cortex for sound processing in CB, we also demonstrate that auditory-spatial processing mainly recruits the right cuneus and the right middle occipital gyrus, two regions of the dorsal occipital stream known to be involved in visuospatial/motion processing in SI. Moreover, functional connectivity analyses revealed that these reorganized occipital regions are part of an extensive brain network including regions known to underlie audiovisual spatial abilities (i.e., intraparietal sulcus, superior frontal gyrus). We conclude that some regions of the right dorsal occipital stream do not require visual experience to develop a specialization for the processing of spatial information and to be functionally integrated in a preexisting brain network dedicated to this ability.

Fig. 1.

Ventral–dorsal auditory streams. Activations obtained in a conjunction analysis characterizing brain areas jointly activated in both groups (SI and CB) in the [Pitch > Spatial] (blue) and in the [Spatial > Pitch] (red) contrasts are overlaid at P_uncorrected < 0.001 on a 3D render.

Fig. 2.

Auditory cross-modal plasticity in the blind. Upper: Activations obtained from contrasts testing the main effects of group independently of condition [Blind > Sighted] × [Spatial + Pitch]. Functional data are displayed (P_uncorrected < 0.001) over a horizontal, a coronal, and a sagittal section of the mean structural image of all subjects normalized to the same stereotactic space. Lower: Mean activity estimates (arbitrary unit ± SEM) associated with sound processing (Spatial + Pitch) in the sighted (blue) and blind (red) groups for the three main activity peaks obtained with this contrast.

Fig. 3.

Network for the spatial processing of sounds in CB subjects. (Left) Activations obtained from the contrast testing which regions are specifically dedicated to the spatial processing of sounds in blind subjects: [Blind > Sighted] × [Spatial > Pitch]. Functional data are overlaid (P_uncorrected < 0.001) over a 3D render of the brain and over sagittal sections of the mean structural image of all blind subjects normalized to the same stereotactic space. (Lower) Mean parameter estimates (arbitrary unit ± SEM) associated with the processing of pitch (blue) or spatial (red) attributes of sounds in the sighted and the blind groups for the four main activity peaks. (A) The right cuneus. (B) The right middle occipital gyrus. (C) The right middle occipito-temporal gyrus. (D) The right lingual gyrus. Right: Psychophysiological interaction results using the four activity peaks as seed areas.