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.blindness | cross-modal plasticity | ventral-dorsal auditory streams | modularity W hen the brain is deprived of its natural sensory inputs, it can rewire itself, showing an impressive range of plastic changes (1). Early visual deprivation thus provides an exceptional model to explore the role of sensory experience in shaping the functional architecture of the brain. Based on a number of studies comparing brain activity of congenitally blind (CB) and sighted individuals (SI), the current prevailing view is that visual deafferentation results in a reliable recruitment of the occipital cortex for nonvisual sensory processing to compensate for the challenging condition that is visual deprivation (2).Although such findings highlight the brain's remarkable ability to rewire its components, questions remain about the functional organization of the occipital cortex in CB. An important characteristic of the visual cortex in SI is domain specialization wherein specific functional activity has been found in anatomically identifiable regions (3, 4). Our main question was, therefore: does the occipital cortex of CB process the colonizing nonvisual stimuli in a global manner or does it do so using some functional modularity similar to what is observed in SI, with precise regions involved in specific cognitive functions?Several studies have reported that the occipital cortex of CB responds quite indifferently to a variety of cogn...

The Effect of Early Visual Deprivation on the Neural Bases of Auditory Processing

“…The maximum volume level of the auditory stimuli was adjusted so that their intensity was the same across conditions. In addition, the intensity of the auditory stimuli was individually adjusted inside the scanner and before testing to equalize the perceived loudness across participants (Collignon et al, 2011Moerel et al, 2012Moerel et al, , 2013. This was done by increasing or decreasing the intensity of the auditory stimuli until a hearing level was reached that was both audible and comfortable for each participant.…”

Shape-specific activation of occipital cortex in an early blind echolocation expert

“…The right dorsal occipital lobe in particular is known to be prominently active when blind but not sighted individuals localize sounds (Collignon, Lassonde, Lepore, Bastien, & Veraart, 2007;Collignon, Vandewalle et al, 2011;Renier et al, 2010;Weeks et al, 2000), and it is interesting to note that both EB and LB showed strong activation of this region when lateralized objects were being discerned through echoes (Figures 5 and S4), but that this area was not activated by either EB or CB when there was no variation in object location (i.e., the Shape and Material task of Experiment 1).…”

“…A secondary question that the topic of feature-specific activation in the blind raises relates to the broader issue in sensory substitution literature concerning how the occipital lobe is colonized by non-visual sensory input, once it is deprived of visual input as occurs in the blind (c.f., Collignon, Vandewalle et al, 2011). Converging evidence indicates that the age of onset of visual deprivation affects the degree of functional as well as structural brain reorganization that occurs within occipital cortex, with the largest amount of reorganization occurring when sight loss coincides with sensitive periods of neurodevelopment (for a review, see Noppeney, 2007).…”

Altered Intrinsic Neuronal Interactions in the Visual Cortex of the Blind

“…The metabolic demand of the occipital cortical areas of blind humans is elevated compared with sighted humans (Wanet-Defalque et al, 1988;Veraart et al, 1990;De Volder et al, 1997). Moreover, the neural activity levels that are present in these regions are modulated by other sensory modalities and are proposed to contribute to higher cognitive capacities such as language and episodic memory (Sadato et al, 1996;Cohen et al, 1997;Büchel et al, 1998;Röder et al, 1999Röder et al, , 2002Bavelier and Neville, 2002;Amedi et al, , 2004Burton, 2003;Gougoux et al, 2005;Raz et al, 2005;Collignon et al, 2009Collignon et al, , 2011Merabet and Pascual-Leone, 2010;Bedny et al, 2011;Schepers et al, 2012).…”