Organization and Reorganization of Sensory-Deprived Cortex
2012; Elsevier BV; Volume: 22; Issue: 5 Linguagem: Inglês
10.1016/j.cub.2012.01.030
ISSN1879-0445
AutoresPatrice Voss, Robert J. Zatorre,
Tópico(s)Neural dynamics and brain function
ResumoThe scientific literature has grown rich in research illustrating the remarkable ability of the brain to reorganize itself following sensory loss. In particular, visually deafferented regions within the occipital cortex of early blind individuals have been repeatedly shown to be functionally recruited to carry out a wide variety of nonvisual tasks. While the novelty of such a finding might be wearing off, more recent research has begun to examine whether this crossmodal takeover of the occipital cortex in blindness follows some sort of organizational principle. Here we first review the most recent evidence from neuroimaging studies that illustrate how the pre-existing functional specialization of cortical sub-regions appears to be preserved following sensory deprivation. We discuss and compare work on visual and auditory deprivation, as well as research on individuals with intact sensory systems. We suggest avenues for future exploration of these issues, such as identifying the neuroanatomical markers of crossmodal plasticity and elucidating the behavioral relevance of observed changes. The scientific literature has grown rich in research illustrating the remarkable ability of the brain to reorganize itself following sensory loss. In particular, visually deafferented regions within the occipital cortex of early blind individuals have been repeatedly shown to be functionally recruited to carry out a wide variety of nonvisual tasks. While the novelty of such a finding might be wearing off, more recent research has begun to examine whether this crossmodal takeover of the occipital cortex in blindness follows some sort of organizational principle. Here we first review the most recent evidence from neuroimaging studies that illustrate how the pre-existing functional specialization of cortical sub-regions appears to be preserved following sensory deprivation. We discuss and compare work on visual and auditory deprivation, as well as research on individuals with intact sensory systems. We suggest avenues for future exploration of these issues, such as identifying the neuroanatomical markers of crossmodal plasticity and elucidating the behavioral relevance of observed changes. A longstanding debate about brain organization has revolved around the question of modularity: whether there exist focal brain areas that are functionally specialized in the processing of specific inputs/features provided by the external world, or if such processing is distributed across regions that respond to non-specific inputs (see [1Barrett H.C. Kurzban R. Modularity in cognition: framing the debate.Psychol. Rev. 2006; 113: 628-647Crossref PubMed Scopus (466) Google Scholar]). A related debate concerns the modal nature of specific sensory brain regions. It was originally thought that sensory cortices are inherently unimodal and respond to only one type of predetermined sensory input. Studies of sensory deprivation, however, have challenged this view. Indeed, there is now abundant evidence that brain areas known to underlie visual processing can be recruited, under certain circumstances, to carry out a wide range of non-visual tasks in individuals deprived of vision. These findings have been reviewed extensively [2Merabet L.B. Pascual-Leone A. Neural reorganization following sensory loss: the opportunity of change.Nat. Rev. Neurosci. 2010; 11: 44-52Crossref PubMed Scopus (462) Google Scholar, 3Voss P. Collignon O. Lassonde M. Lepore F. Adaptation to sensory loss.Wiley Int. Rev. Cog. Sci. 2010; 1: 308-328Crossref Scopus (48) Google Scholar], so here we rather illustrate how some more recent findings suggest that this crossmodal plasticity appears to follow a specific and innate functional organization of the affected areas. An important question to address first relates to whether or not the crossmodal recruitment of normally visual areas in the blind follows a pattern of modular organization — that is, do specific types of processing elicit the crossmodal recruitment of specific areas? There are currently several lines of evidence suggesting the existence of modularity in the visual cortex of the blind. Studies of auditory spatial processing, for instance, tend to show specific recruitment of dorsal occipital regions and the right middle occipital gyrus in particular [4Collignon O. Vandewalle G. Voss P. Albouy G. Charbonneau G. Lassonde M. Lepore F. Functional specialization for auditory-spatial processing in the occipital cortex of congenitally blind humans.Proc. Natl. Acad. Sci. USA. 2011; 108: 4435-4440Crossref PubMed Scopus (222) Google Scholar, 5Renier L.A. Anurova I. De Volder A.G. Carlson S. VanMeter J. Rauschecker J.P. Preserved functional specialization for spatial processing in the middle occipital gyrus of the early blind.Neuron. 2010; 68: 138-148Abstract Full Text Full Text PDF PubMed Scopus (211) Google Scholar], whereas sound motion preferentially activates areas in the middle temporal area [6Poirier C. Collignon O. De Volder A.G. Renier L. Vanlierde A. Tranduy D. Scheiber C. Specific activation of V5 brain area by auditory motion processing: an fMRI study.Brain Res. Cog. Brain Res. 2005; 25: 650-658Crossref PubMed Scopus (121) Google Scholar]. Although the primary visual cortex (V1) appears to be an exception to this rule, as it appears often to be unselectively recruited by various tasks and inputs (see below for a more detailed discussion on the possible role of V1 after blindness), the crossmodal recruitment of visual areas outside of V1 appears to follow some form of modular organization. The following sections will discuss how this modularity relates to the preexisting functional specialization of subregions observed in the intact visual system. One of the most well-known features of the visual system is its segregation into two streams, a dorsal one and a ventral one [7Ungerleider L. Mishkin M. Two cortical visual systems.in: Ingle D.J. Goodale M.A. Mansfield R.J.W. Analysis of Visual Behavior. MIT Press, Cambridge, MA1982: 549-586Google Scholar]. The dorsal one has been commonly characterized as playing a role in the processing of spatial information, whereas the ventral stream has been associated with specialization in the processing of various features relevant to stimulus identity. A number of reports have suggested that the functional nature of these streams is maintained in blindness for the processing of non-visual spatial [8Collignon O. Voss P. Lassonde M. Lepore F. Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects.Exp. Brain Res. 2009; 192: 343-358Crossref PubMed Scopus (195) Google Scholar] and non-spatial [9Amedi A. Stern W.M. Camprodon J.A. Bermpohl F. Merabet L. Rotman S. Hemond C. Meijer P. Pascual-Leone A. Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex.Nat. Neurosci. 2007; 10: 687-689Crossref PubMed Scopus (298) Google Scholar, 10Pietrini P. Furey M.L. Ricciardi E. Gobbini M.I. Wu W.H. Cohen L. Guazzelli M. Haxby J.V. Beyond sensory images: Object-based representation in the human ventral pathway.Proc. Natl. Acad. Sci. USA. 2004; 101: 5658-5663Crossref PubMed Scopus (345) Google Scholar] information. Until recently, however, no study had attempted to truly dissociate both processing streams in the blind. Recent publications by Collignon et al. [4Collignon O. Vandewalle G. Voss P. Albouy G. Charbonneau G. Lassonde M. Lepore F. Functional specialization for auditory-spatial processing in the occipital cortex of congenitally blind humans.Proc. Natl. Acad. Sci. USA. 2011; 108: 4435-4440Crossref PubMed Scopus (222) Google Scholar] and Renier et al. [5Renier L.A. Anurova I. De Volder A.G. Carlson S. VanMeter J. Rauschecker J.P. Preserved functional specialization for spatial processing in the middle occipital gyrus of the early blind.Neuron. 2010; 68: 138-148Abstract Full Text Full Text PDF PubMed Scopus (211) Google Scholar] are among the first to attempt to address this issue. The primary goal of both studies was to contrast fMRI activations elicited by non-visual spatial processing with those of non-visual non-spatial processing (frequency discrimination) in the auditory (pitch) [4Collignon O. Vandewalle G. Voss P. Albouy G. Charbonneau G. Lassonde M. Lepore F. Functional specialization for auditory-spatial processing in the occipital cortex of congenitally blind humans.Proc. Natl. Acad. Sci. USA. 2011; 108: 4435-4440Crossref PubMed Scopus (222) Google Scholar, 5Renier L.A. Anurova I. De Volder A.G. Carlson S. VanMeter J. Rauschecker J.P. Preserved functional specialization for spatial processing in the middle occipital gyrus of the early blind.Neuron. 2010; 68: 138-148Abstract Full Text Full Text PDF PubMed Scopus (211) Google Scholar] and the tactile (vibrotactile) [5Renier L.A. Anurova I. De Volder A.G. Carlson S. VanMeter J. Rauschecker J.P. Preserved functional specialization for spatial processing in the middle occipital gyrus of the early blind.Neuron. 2010; 68: 138-148Abstract Full Text Full Text PDF PubMed Scopus (211) Google Scholar] modalities. Both found that dorsal occipital areas, in particular the right middle occipital gyrus (MOG), showed a strong preference for spatial processing. Renier et al. [5Renier L.A. Anurova I. De Volder A.G. Carlson S. VanMeter J. Rauschecker J.P. Preserved functional specialization for spatial processing in the middle occipital gyrus of the early blind.Neuron. 2010; 68: 138-148Abstract Full Text Full Text PDF PubMed Scopus (211) Google Scholar], moreover, obtained support for the idea of a preserved functional specialization of occipital areas in blindness via a control experiment in which they showed that the same area of MOG recruited in the blind is also activated in the sighted during a visual spatial task. Collignon et al. [4Collignon O. Vandewalle G. Voss P. Albouy G. Charbonneau G. Lassonde M. Lepore F. Functional specialization for auditory-spatial processing in the occipital cortex of congenitally blind humans.Proc. Natl. Acad. Sci. USA. 2011; 108: 4435-4440Crossref PubMed Scopus (222) Google Scholar] performed functional connectivity analyses and showed that the MOG is functionally connected to the intraparietal sulcus and the superior frontal gyrus, areas traditionally considered important for spatial attention and awareness, again highlighting this region's preserved functional specialization. Perhaps surprisingly, however, neither of these two studies found occipital regions that preferentially responded to the pitch discrimination versus the localization task. Collignon et al. [4Collignon O. Vandewalle G. Voss P. Albouy G. Charbonneau G. Lassonde M. Lepore F. Functional specialization for auditory-spatial processing in the occipital cortex of congenitally blind humans.Proc. Natl. Acad. Sci. USA. 2011; 108: 4435-4440Crossref PubMed Scopus (222) Google Scholar] proposed that this is likely due to the fact that pitch processing is a purely auditory process, whereas spatial localization is shared both by vision and audition, thus facilitating the crossmodal processing of auditory input for spatial tasks. Indeed, this is in line with the recent proposition of Lomber et al. [11Lomber S.G. Meredith M.A. Kral A. Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf.Nat. Neurosci. 2010; 13: 1421-1427Crossref PubMed Scopus (323) Google Scholar], who suggested that ‘supramodal’ functions or attributes that are shared across senses are those that have a greater potential to engage specific crossmodal recruitment. This is also in line with recent findings of Striem-Amit et al. [12Striem-Amit E. Dakwar O. Reich L. Amedi A. The large-scale organization of “visual” streams emerges without visual experience.Cereb. Cortex. 2011; https://doi.org/10.1093/cercor/bhr253Crossref Scopus (91) Google Scholar] which provide additional support for the preservation of the two visual streams in blindness. Following brief training on a visual-to-auditory sensory substitution device, blind subjects were shown to preferentially recruit the dorsal areas when performing object location tasks, and to preferentially recruit ventral areas when performing form identification tasks using visual stimuli (coded into auditory input via specific algorithms), thus providing a first and compelling double dissociation in the functional division of labor of the visual streams in blind individuals. While the division of cortical visual processing into distinct dorsal and ventral streams is a key framework that has guided visual neuroscience for decades, the characterization of the streams is not without controversy. One current viewpoint suggests that the dorsal stream, originally proposed as mediating spatial perception (‘where'), primarily serves non-conscious visually guided action [13Goodale M. Action without perception in human vision.Cogn. Neuropsychol. 2008; 25: 891-919Crossref PubMed Scopus (100) Google Scholar]. Moreover, recent evidence suggests that the dorsal stream can be segregated into multiple individual pathways from the parietal cortex onwards [14Kravitz D.J. Saleem K.S. Baker C.I. Mishkin M. A new neural framework for visuospatial processing.Nat. Neurosci. Rev. 2011; 12: 217-230Crossref PubMed Scopus (843) Google Scholar], suggesting that this stream may subserve multiple distinct processes. Consequently, limiting ourselves to the global processing of the two popular streams is probably insufficient to determine whether the functional specificity of particular brain areas is preserved in blindness. A more prudent approach would be to identify the functional nature of sensory cortex by studying its properties in sensory deprivation. One area well known for its functional specialization is the lateral-occipital complex (LOC), notably involved in object/form recognition processes. Amedi and colleagues have shown on several occasions that the LOC is responsive to non-visual form processing in the blind, first using a visual-to-auditory sensory substitution device [9Amedi A. Stern W.M. Camprodon J.A. Bermpohl F. Merabet L. Rotman S. Hemond C. Meijer P. Pascual-Leone A. Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex.Nat. Neurosci. 2007; 10: 687-689Crossref PubMed Scopus (298) Google Scholar], and second when subjects performed tactile object recognition tasks [15Amedi A. Raz N. Azulay H. Malach R. Zohary E. Cortical activity during tactile exploration of objects in blind and sighted humans.Restor. Neurol. Neurosci. 2010; 28: 143-156PubMed Google Scholar]. Furthermore, Pietrini and colleagues [10Pietrini P. Furey M.L. Ricciardi E. Gobbini M.I. Wu W.H. Cohen L. Guazzelli M. Haxby J.V. Beyond sensory images: Object-based representation in the human ventral pathway.Proc. Natl. Acad. Sci. USA. 2004; 101: 5658-5663Crossref PubMed Scopus (345) Google Scholar] had previously shown that the tactile exploration of faces activated different regions than those elicited by the exploration of objects in the blind, suggesting that the development of topographically organized, category-related representations in extrastriate visual cortex does not require visual experience. Similarly, it was recently demonstrated [16Mahon B.Z. Anzellotti S. Schwarzbach J. Zampini M. Caramazza A. Category-specific organization in the human brain does not require visual experience.Neuron. 2009; 63: 397-405Abstract Full Text Full Text PDF PubMed Scopus (239) Google Scholar] in blind individuals that distinct regions within the ventral visual pathway show neural specialization for nonliving and living stimuli in the auditory modality, suggesting that the conceptual domain organization in the ventral visual pathway does not require visual experience to develop. Additional evidence supporting a preservation of functional specialization of extrastriate ‘visual’ cortex has been provided by Reich and colleagues [17Reich L. Szwed M. Cohen L. Amedi A. A ventral visual stream reading center independent of visual experience.Curr. Biol. 2011; 21: 363-368Abstract Full Text Full Text PDF PubMed Scopus (192) Google Scholar]. The authors showed that the visual word form area, which, as its name indicates, responds well to the visual presentation of words, is highly responsive to tactually presented Braille words in blind subjects. Lastly, another well known area for its functional specialization is the human extrastriate cortical region known as the middle temporal complex (hMT+), which is highly responsive to visual motion; several studies have shown that this region in blind individuals becomes responsive to tactile motion on the fingers [18Ricciardi E. Vanello N. Sani L. Gentilli C. Scilingo E.P. Landini L. Guazelli M. Bicchi A. Haxby J.V. Pietrini P. The effect of visual experience on functional architecture in hMT+.Cereb. Cortex. 2007; 17: 2933-2939Crossref PubMed Scopus (137) Google Scholar], as well as to auditory motion input [6Poirier C. Collignon O. De Volder A.G. Renier L. Vanlierde A. Tranduy D. Scheiber C. Specific activation of V5 brain area by auditory motion processing: an fMRI study.Brain Res. Cog. Brain Res. 2005; 25: 650-658Crossref PubMed Scopus (121) Google Scholar]. Taken together, these findings provide compelling evidence that visual deprivation does not alter the specialized modular organization of the visually deafferented occipital/occipitotemporal areas of the brain, and that the operations subserved by each region need not depend on visual input to be solicited by a given task. Indeed the brain appears to possess a default modular organization that is independent of visual experience and that is highly metamodal in nature (Figure 1). Like blindness, deafness has been shown to lead to crossmodal plastic phenomena. To date, adaptive plasticity has been largely shown only under circumstances where visual attention and/or processing of the peripheral visual field are manipulated (see [19Bavelier D. Dye M.W. Hauser P.C. Do deaf individuals see better?.Trends Cogn. Sci. 2006; 10: 512-518Abstract Full Text Full Text PDF PubMed Scopus (353) Google Scholar]). This phenomenon may be related to the connections existing between visual and auditory cortices, as evidenced in the primate, which involve primarily portions of visual cortex representing the periphery of the visual field [20Falchier A. Schroeder C.E. Hackett T.A. Lakatos P. Nascimento-Silva S. Ulbert I. Karmos G. Smiley J.F. Projection from visual areas V2 and prostriata to caudal auditory cortex in the monkey.Cereb. Cortex. 2010; 20: 1529-1538Crossref PubMed Scopus (89) Google Scholar]. Similarly, crossmodal recruitment of auditory cortices appears to be more specific to particular stimulation paradigms such as visual motion [21Finney E.M. Fine I. Dobkins K.R. Visual stimuli activate auditory cortex in the deaf.Nat. Neurosci. 2001; 4: 1171-1173Crossref PubMed Scopus (450) Google Scholar] and sign language [22Petitto L.A. Zatorre R.J. Gauna K. Nikelski E.J. Dostie D. Evans A.C. Speech-like cerebral activity in profoundly deaf people processing signed languages: implications for the neural basis of human language.Poc. Natl. Acad. Sci. USA. 2000; 97: 13961-13966Crossref PubMed Scopus (372) Google Scholar]. It is of interest to note that visual stimuli which are most effective at eliciting activation in typically auditory cortex are dynamic in nature, perhaps reflecting the well-known capacity of auditory cortex to process temporal cues. There has been little evidence, until very recently, for preservation of the functional specialization of the aurally deafferented regions; however, some evidence for this has come from a recent study [23Meredith M.A. Kryklywy J. McMillan A.J. Malhotra S. Lum-Tai R. Lomber S.G. Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex.Proc. Natl. Acad. Sci. USA. 2011; 108: 8856-8861Crossref PubMed Scopus (103) Google Scholar] with deafened cats. In normal hearing cats, the unilateral deactivation of the auditory field of the anterior ectosylvian sulcus (FAES) results in profound contralateral acoustic orienting deficits. Meredith et al. [23Meredith M.A. Kryklywy J. McMillan A.J. Malhotra S. Lum-Tai R. Lomber S.G. Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex.Proc. Natl. Acad. Sci. USA. 2011; 108: 8856-8861Crossref PubMed Scopus (103) Google Scholar] were able to show using cooling loops that the deactivation of the same region in deaf cats produced substantial contralateral visual orienting deficits, thus demonstrating that the crossmodal substitution of inputs following deafness appears to drive the established output circuitry to preserve the region's behavioral role. Further work is required to determine if other crossmodal correspondences can be demonstrated in other regions of deafened auditory cortex as previously shown by Lomber et al. [11Lomber S.G. Meredith M.A. Kral A. Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf.Nat. Neurosci. 2010; 13: 1421-1427Crossref PubMed Scopus (323) Google Scholar]. However, this might not be as straightforward as with blindness, as many functions of the auditory cortices, such as processing of speech or musical tones, do not appear to have an evident visual analogue and are more difficult to study in animal models. An important distinction to make is between what is considered a metamodal area and what is considered a multisensory integration area. The former, as depicted here, is one that carries out similar operations regardless of the modality of the sensory input, whereas the latter is dedicated to the integration of multimodal inputs to allow the formation of a coherent percept. Multimodal integration areas will not be further discussed herein, as their function, anatomical location and how they influence other areas has been extensively reviewed elsewhere [24Ghazanfar A.A. Schroeder C.E. Is neocortex essentially multisensory?.Trends Cogn. Sci. 2006; 10: 278-285Abstract Full Text Full Text PDF PubMed Scopus (991) Google Scholar, 25Macaluso E. Multisensory processing in sensory-specific cortical areas.Neuroscientist. 2006; 12: 327-338Crossref PubMed Scopus (99) Google Scholar]. The idea that the visual cortex might be metamodal, or at least not as unimodal as once thought, has been floating around for some time now. One of the first convincing pieces of evidence stems from work showing that the temporary blindfolding of sighted subjects for five days enabled strong crossmodal recruitment of occipital areas for both tactile and auditory tasks that also quickly disappeared following removal of the blindfold [26Pascual-Leone A. Hamilton R. The metamodal organization of the brain. Prog.Brain Res. 2001; 134: 427-445Crossref Scopus (406) Google Scholar]. There are, however, multiple lines of evidence suggesting that sensory deprivation, temporary or not, may not be required for crossmodal influences within ‘unisensory’ cortices. One comes from the activation of auditory cortical regions in response to the visual component of typical audiovisual tasks such as lipreading [27Calvert G.A. Crossmodal processing in the human brain: Insights from functional neuroimaging studies.Cereb. Cortex. 2001; 11: 1110-1123Crossref PubMed Scopus (788) Google Scholar]. Similarly, it was recently shown that occipital regions in sighted individuals became responsive to auditory input following very brief exposures to audiovisual stimuli that were spatially and temporally congruent [28Zangenehpour S. Zatorre R.J. Crossmodal recruitment of primary visual cortex following brief exposure to bimodal audiovisual stimuli.Neuropsychologia. 2010; 48: 591-600Crossref PubMed Scopus (43) Google Scholar]. These findings highlight the experience-dependent nature of the rapid crossmodal recruitment of primary sensory cortices in normal individuals. Indeed, there is now strong reason to believe that blindness may not be a prerequisite for crossmodal takeover of visually deafferented brain regions, but that it may simply facilitate it by removing competitive visual input. Several studies have now provided evidence that the auditory and tactile crossmodal recruitment observed in normal individuals also follows the already existing functional specialization of the occipital cortex. For instance, several groups have shown that the LOC is highly responsive when processing the shape of tactually presented objects [10Pietrini P. Furey M.L. Ricciardi E. Gobbini M.I. Wu W.H. Cohen L. Guazzelli M. Haxby J.V. Beyond sensory images: Object-based representation in the human ventral pathway.Proc. Natl. Acad. Sci. USA. 2004; 101: 5658-5663Crossref PubMed Scopus (345) Google Scholar, 14Kravitz D.J. Saleem K.S. Baker C.I. Mishkin M. A new neural framework for visuospatial processing.Nat. Neurosci. Rev. 2011; 12: 217-230Crossref PubMed Scopus (843) Google Scholar, 29Amedi A. Malach R. Hendler T. Peled S. Zohary E. Visuo-haptic object-related activation in the ventral visual pathway.Nat. Neurosci. 2001; 4: 324-330Crossref PubMed Scopus (507) Google Scholar]. One explanation suggests that regions like the LOC are important for object form processing and recognition, abilities that are shared both by the visual and tactile modalities. This conclusion is consistent with a recent study [30Kim J.K. Zatorre R.J. Tactile-auditory shape learning engages the lateral occipital complex.J. Neurosci. 2011; 31: 7848-7856Crossref PubMed Scopus (44) Google Scholar] showing that auditory input may also activate LOC when it conveys shape information, when sighted subjects were trained to learn the relationship between raised tactile abstract shapes and their corresponding shape-coded sounds. Importantly, LOC activation was detected to tactile shapes even with minimal exposure, but after extensive training, the functional connectivity between auditory cortex and LOC increased, highlighting the fact that the LOC appears to be available to many different sensory systems for shape processing, and that efficient training can lead to a more direct access to this site by the auditory system. Similarly, hMT+ has been shown to be active for both auditory [31Poirier C. Collignon O. Scheiber C. Renier L. Vanlierde A. Tranduy D. Veraart C. De Volder A.G. Auditory motion perception activates visual motion areas in early blind subjects.NeuroImage. 2006; 31: 279-285Crossref PubMed Scopus (171) Google Scholar] and tactile [18Ricciardi E. Vanello N. Sani L. Gentilli C. Scilingo E.P. Landini L. Guazelli M. Bicchi A. Haxby J.V. Pietrini P. The effect of visual experience on functional architecture in hMT+.Cereb. Cortex. 2007; 17: 2933-2939Crossref PubMed Scopus (137) Google Scholar, 32Matteau I. Kupers R. Ricciardi E. Pietrini P. Ptito M. Beyond visual, aural and haptic movement perception: hMT+ is activated by electrotactile motion stimulation of the tongue in sighted and in congenitally blind individuals.Brain Res. Bull. 2010; 30: 264-270Crossref Scopus (109) Google Scholar] motion in non-sensory deprived individuals. Such findings underscore the preexisting multimodal nature of these occipital areas. One important question that remains unanswered is how auditory and tactile information reaches the occipital cortex. Regarding auditory input, there are several possibilities, including a direct thalamocortical input from the medial geniculate (auditory relay) and/or the ventral posterior nucleus (somatosensory relay), a direct corticocortical pathway from unisensory cortices to the occipital cortex, or a corticocortical pathway from multisensory cortices [33Bavelier D. Neville H.J. Cross-modal plasticity: where and how?.Nat. Rev. Neurosci. 2002; 2: 443-452Crossref Scopus (717) Google Scholar]. The animal literature in particular is quite rich with demonstrations of potential pathways that could mediate crossmodal processing in typical unisensory areas (for reviews see [34Cappe C. Rouiller E.M. Barone P. Multisensory anatomical pathways.Hear. Res. 2009; 258: 28-36Crossref PubMed Scopus (141) Google Scholar, 35Schroeder C.E. Smiley J. Fu K.G. McGinnis T. O'Connell M.N. Hackett T.A. Anatomical mechanisms and functional implications of multisensory convergence in early cortical processing.Int. J. Psychophysiol. 2003; 50: 5-17Crossref PubMed Scopus (147) Google Scholar]); however, most projections described to date involve at least one higher-order sensory area, with little evidence for direct connections between primary sensory cortices. Important studies in the non-human primate deserve specific mention, as they have shown the existence of direct corticortico connections between unisensory areas. Bidirectional connections involving caudal auditory areas have been demonstrated, both going to peripheral V1 and V2 [36Falchier A. Clavagnier S. Barone P. Kennedy H. Anatomical evidence of multimodal integration in primate striate cortex.J. Neurosci. 2002; 22: 5749-5759Crossref PubMed Google Scholar, 37Rockland K.S. Ojima H. Multisensory convergence in calcarine visual areas in macaque monkey.Int. J. Psychophysiol. 2003; 50: 19-26Crossref PubMed Scopus (438) Google Scholar] and originating from peripheral V2 [20Falchier A. Schroeder C.E. Hackett T.A. Lakatos P. Nascimento-Silva S. Ulbert I. Karmos G. Smiley J.F. Projection from visual areas V2 and prostriata to caudal auditory cortex in the monkey.Cereb. Cortex. 2010; 20: 1529-1538Crossref PubMed Scopus (89) Google Scholar], which could potentially subserve the crossmodal recruitment observed in both deaf and blind individuals, respectively. In humans, evidence for the existence of such pathways is somewhat limited. Recently, however, a DTI tractography study [38Beer A.L. Plank T. Greenlee M.W. Diffusion tensor imaging shows white matter tracts between human auditory and visual cortex.Exp. Brain Res. 2011; 213: 299-308Crossref PubMed Scopus (89) Google Scholar] in normal humans has revealed the existence of corticocortical connections between Heschl's region and the calcarine sulcus. Whether this pathway is different in blind individuals has, however, yet to be established, although a recent report [39Klinge C. Eippert F. Röder B. Büchel C. Corticocortical connections mediate primary visual cortex responses to auditory stimulation in the blind.J. Neurosci. 2010; 30: 12798-12805Crossref PubMed Scopus (104) Google Scholar] has shown that the functional connectivity between primary auditory and primary visual areas is increased in blind subjects relative to sighted ones, suggesting that the anatomical connection may also be stronger in the blind. Support for parietal-occipital pathway in humans is provided by a transcranial magnetic stimulation (TMS) study [40Wittenberg G.F. Werhahn K.J. Wassermann E.M. Herscovitch P. Cohen L.G. Functional connectivity between somatosensory and visual cortex in early blind humans.Eur. J. Neurosci. 2004; 20: 1923-1927Crossref PubMed Scopus (127) Google Scholar] which showed that stimulating the primary somatosensory cortex in blind subjects activates the occipital cortex, consistent with the hypothesis that tactile information may reach occipital areas via corticocortical pathways. Notably, as the activity elicited in the blind was not significantly greater than in the sighted, it could also be argued that a similar pathway also exists in the sighted. Future work is required to determine whether such pathways do indeed mediate the crossmodal recruitment of deafferented cortices. Although there is a growing body of evidence supporting the idea that the crossmodal recruitment of occipital regions follows a preexisting functional specialization, it is still not known whether the primary visual cortex (V1) has a specific role following visual deprivation. Evaluating the functional specialization of V1 is not straightforward, as in sighted individuals it is a low-level processing node in the hierarchical visual system that is involved in the coding of local contrasts, whereas in the blind V1 has been shown to be significantly activated during a wide variety of auditory and tactile tasks [2Merabet L.B. Pascual-Leone A. Neural reorganization following sensory loss: the opportunity of change.Nat. Rev. Neurosci. 2010; 11: 44-52Crossref PubMed Scopus (462) Google Scholar, 3Voss P. Collignon O. Lassonde M. Lepore F. Adaptation to sensory loss.Wiley Int. Rev. Cog. Sci. 2010; 1: 308-328Crossref Scopus (48) Google Scholar]. Perhaps even more astonishing is the finding that higher-order cognitive functions such as memory [41Amedi A. Raz N. Pianka P. Malach R. Zohary E. Early ‘visual’ cortex activation correlates with superior verbal memory in the blind.Nat. Neurosci. 2003; 6: 758-766Crossref PubMed Scopus (441) Google Scholar] and language [42Röder B. Stock O. Bien S. Neville H.J. Rosler F. Speech processing activates visual cortex in congenitally blind humans.Eur. J. Neurosci. 2002; 16: 930-936Crossref PubMed Scopus (268) Google Scholar] can evoke activity in V1. Despite the apparent unspecific nature of V1's participation in multimodal functions, there is, however, some evidence that it may follow some of the brain's known functional specialization for particular types of inputs. For instance, several groups investigating language processing in the blind have shown the occipital cortex to be more responsive in the left hemisphere, in agreement with the left lateralization of language [41Amedi A. Raz N. Pianka P. Malach R. Zohary E. Early ‘visual’ cortex activation correlates with superior verbal memory in the blind.Nat. Neurosci. 2003; 6: 758-766Crossref PubMed Scopus (441) Google Scholar, 42Röder B. Stock O. Bien S. Neville H.J. Rosler F. Speech processing activates visual cortex in congenitally blind humans.Eur. J. Neurosci. 2002; 16: 930-936Crossref PubMed Scopus (268) Google Scholar]. 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Brain Res. 2008; 187: 41-49Crossref PubMed Scopus (158) Google Scholar] with their apparent functional recruitment. Although recent functional connectivity analyses have shown the co-existence of functional connectivity decreases and increases involving the occipital cortices in the blind [46Liu Y. Yu C. Liang M. Li J. Tian L. Zhou Y. Qin W. Li K. Jiang T. Whole brain functional connectivity in the early blind.Brain. 2007; 130: 2085-2096Crossref PubMed Scopus (198) Google Scholar], which may in turn be related to functional losses and gains; but it is still unclear how this is reflected in the neuroanatomy of visual structures. It will hence be necessary to dissociate both at macro and micro levels anatomical changes related to deprivation from those related to reorganization. A first step in this direction was taken in a recent study [47Voss P. Zatorre R.J. Occipital cortical thickness predicts performance on pitch and musical tasks in blind individuals.Cereb. Cortex. 2011; https://doi.org/10.1093/cercor/bhr311Crossref Scopus (63) Google Scholar] in which we tested whether the previously reported increase in occipital cortical thickness in the blind actually reflects adaptive compensatory changes in the auditory modality. By inputting performance scores obtained in various auditory tasks (on which the blind had shown superior abilities) along with cortical thickness measures into a regression analysis, we showed that the cortical thickness in occipital areas was most predictive of behavioral enhancements, more so than the thickness of any other cortical area. Hence, this finding constitutes a clear dissociation between anatomical changes that are related to compensation, and those related to sensory deprivation and consequent atrophy [44Noppeney U. Friston K.J. Ashburner J. Frackowiak R. Price C.J. Early visual deprivation induces structural plasticity in gray and white matter.Curr. Biol. 2005; 15: R488-490Abstract Full Text Full Text PDF PubMed Scopus (148) Google Scholar, 45Ptito M. Schneider F.C. Paulson O.B. Kupers R. Alterations of the visual pathways in congenital blindness.Exp. Brain Res. 2008; 187: 41-49Crossref PubMed Scopus (158) Google Scholar]. Importantly, this finding demonstrates that crossmodal reorganization leads to measurable anatomical changes within occipital cortex, opening the door to understanding at a finer grain of detail the nature of such changes in cortical structure. Using a different technique, magnetization transfer imaging, we have been able to show in a preliminary dataset another type of relationship between a neuroanatomical change in the blind and behavioral adaptation. Magnetization transfer imaging is a powerful tool that provides an indirect measure of myelin content throughout the entire brain volume via the magnetization transfer ratio (MTR) [48Giacomini P.S. Levesque I.R. Ribeiro L. Narayanan S. Francis S.J. Pike G.B. Arnold D.L. Measuring demyelination and remyelination in acute multiple sclerosis lesion voxels.Arch. Neurol. 2009; 66 (375–81)Crossref Scopus (46) Google Scholar]. In our dataset of early blind and sighted individuals, we observed an increase in MTR in lateral extrastriate occipital areas in the early blind (Figure 2). Furthermore, we observed that the MTR in these regions strongly correlates with pitch discrimination scores in the blind, the same task which also correlated with increases in cortical thickness. This finding provides further evidence for anatomical reorganization, beyond the cortical thickness finding, and also suggests that one mechanism for this reorganization may be related to increased myelination of intracortical neurons, or perhaps of fibers conveying information to and from remote locations. Future work would definitely benefit from further exploring the neuroanatomical changes that occur in sensory deprivation and how these changes may facilitate the crossmodal takeover of deafferented sensory cortex. Much of the work we have reviewed has identified important specializations of function for reorganized cortical regions, but not all studies have specifically demonstrated the behavioral relevance of the specialization. Without some link to behavior, the nature of the reorganization — whether adaptive, maladaptive, or epiphenomenal — will remain difficult to establish. Studies focusing on this goal will be important, with procedures allowing functional perturbation of particular relevance to establish causality [23Meredith M.A. Kryklywy J. McMillan A.J. Malhotra S. Lum-Tai R. Lomber S.G. Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex.Proc. Natl. Acad. Sci. USA. 2011; 108: 8856-8861Crossref PubMed Scopus (103) Google Scholar]. This issue is especially relevant in terms of understanding individual differences, which have sometimes been ignored in both human and animal studies. It is clear that not all individuals necessarily show the same degree of functional or structural reorganization, nor the same degree of behavioral adaptation. For example, only about half of congenitally blind individuals excel at monaural auditory localization, but in those who do, it is linked to enhanced recruitment of visual cortex [49Gougoux F. Lepore F. Lassonde M. Voss P. Zatorre R.J. A functional neuroimaging study of sound localization: visual cortex activity predicts performance in early-blind individuals.PLoS Biol. 2005; 3: 324-333Crossref Scopus (455) Google Scholar]. Establishing the behavioral-functional relationship is thus critical to address this source of variance. A further related question which has yet to be adequately addressed is to understand how and why individual differences may come about. It is not clear to what extent environmental factors may play a role in establishing functional reorganization to a greater or lesser extent across individuals, as opposed to genetic, epigenetic, or maturational factors which might also differ across individuals. In humans, social or even personality factors are also likely to be at play, insofar as they might influence an individual's access to, or willingness to engage in, activities that might promote reorganization. It is also likely that all these factors interact in complex ways. Animal studies could be useful in addressing some of these points as environmental variables at least could be better controlled than in human studies; however, to date, animal studies on sensory deprivation have with few exceptions [50Piché M. Robert S. Miceli D. Bronchti G. Environmental enrichment enhances auditory takeover of the occipital cortex in anophthalmic mice.Eur. J. Neurosci. 2004; 20: 3463-3472Crossref PubMed Scopus (44) Google Scholar] not been set up in such a way as to promote cross-modal reorganization comparable to what happens in humans (for instance, by providing an enriched environment in the nondeprived modality, or via formal training paradigms, or by testing after sufficiently prolonged time periods). Answering these questions could have important repercussions for training and rehabilitation of the blind. Finally, all of these points can also be brought to bear on issues related to anatomical changes, in order to better understand how the structural features of the brain pertain to loss vs enhancement of sensory function. We thank the anonymous reviewers for their helpful comments and suggestions that significantly helped to improve the quality of the manuscript.
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