Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf

Lomber, Stephen G.; Meredith, M. Alex; Kral, Andrej

doi:10.1038/nn.2653

Cited by 432 publications

(412 citation statements)

References 49 publications

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“…The fact that no occipital regions showed preferential activations for the processing of pitch in CB is not so surprising in light of the results of a recent study carried out in deaf cats (39). The authors propose that "supramodal" functions, or attributes that are shared across senses, have a greater potential to engage specific cross-modal plasticity mechanisms after the loss of a sensory input.…”

Section: Functional Specialization In the Occipital Cortex Of Cb For mentioning

confidence: 94%

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

Collignon

Vandewalle

Voss

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

295

243

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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...

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Section: Functional Specialization In the Occipital Cortex Of Cb For mentioning

confidence: 94%

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

Collignon

Vandewalle

Voss

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

295

243

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“…Crossmodal plasticity can also enhance perceptual performance within the remaining sensory modalities. Numerous reports document improvement over sighted subjects in auditory and somatosensory tasks in blind individuals (2-7), as well as enhanced performance in visual and tactile behaviors in the deaf (8)(9)(10)(11). However, with the accumulation of studies examining such compensatory effects following early sensory loss, it is becoming evident that not all features of the replacement sensory modalities are equally represented.…”

mentioning

confidence: 99%

“…However, with the accumulation of studies examining such compensatory effects following early sensory loss, it is becoming evident that not all features of the replacement sensory modalities are equally represented. For example, early-deaf subjects exhibit supranormal abilities for visual localization (10) and visual motion detection (11,12), but not visual brightness discrimination (13), contrast sensitivity (14), visual shape detection (15), grating acuity, vernier acuity, orientation discrimination, motion direction, or velocity discrimination (11). Thus, rather than a generalized overall improvement, it seems that only specific features of the replacement modality are affected by crossmodal plasticity.…”

mentioning

confidence: 99%

“…Following early deafness, crossmodal inputs appear to avoid (5, 16) or only partially innervate (17) the primary auditory cortex. In contrast, early deafness induces visual reorganization of the posterior auditory field and the dorsal auditory zone (11). The factors that select a deprived region for reorganization, and the specific sensory modalities to be involved, are unknown.…”

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confidence: 99%

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Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex

Meredith

Kryklywy²,

McMillan³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

126

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It is well known that early disruption of sensory input from one modality can induce crossmodal reorganization of a deprived cortical area, resulting in compensatory abilities in the remaining senses. Compensatory effects, however, occur in selected cortical regions and it is not known whether such compensatory phenomena have any relation to the original function of the reorganized area. In the cortex of hearing cats, the auditory field of the anterior ectosylvian sulcus (FAES) is largely responsive to acoustic stimulation and its unilateral deactivation results in profound contralateral acoustic orienting deficits. Given these functional and behavioral roles, the FAES was studied in early-deafened cats to examine its crossmodal sensory properties as well as to assess the behavioral role of that reorganization. Recordings in the FAES of early-deafened adults revealed robust responses to visual stimulation as well as receptive fields that collectively represented the contralateral visual field. A second group of early-deafened cats was trained to localize visual targets in a perimetry array. In these animals, cooling loops were surgically placed on the FAES to reversibly deactivate the region, which resulted in substantial contralateral visual orienting deficits. These results demonstrate that crossmodal plasticity can substitute one sensory modality for another while maintaining the functional repertoire of the reorganized region.vision | single-unit electrophysiology | orienting behavior | cooling deactivation A remarkable property of the brain is its capacity to respond to change. This neuroplastic process endows the nervous system with the ability to adjust itself to the loss of an entire set of sensory inputs or even two (1). Under these conditions, it is clearly adaptive for inputs from an intact modality to substitute for those that have been lost, such as auditory navigation in the blind. Crossmodal plasticity can also enhance perceptual performance within the remaining sensory modalities. Numerous reports document improvement over sighted subjects in auditory and somatosensory tasks in blind individuals (2-7), as well as enhanced performance in visual and tactile behaviors in the deaf (8-11). However, with the accumulation of studies examining such compensatory effects following early sensory loss, it is becoming evident that not all features of the replacement sensory modalities are equally represented. For example, early-deaf subjects exhibit supranormal abilities for visual localization (10) and visual motion detection (11, 12), but not visual brightness discrimination (13), contrast sensitivity (14), visual shape detection (15), grating acuity, vernier acuity, orientation discrimination, motion direction, or velocity discrimination (11). Thus, rather than a generalized overall improvement, it seems that only specific features of the replacement modality are affected by crossmodal plasticity.Crossmodal plasticity itself does not appear to be a uniformly distributed effect. Although it seems plausible ...

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“…hearing), but only if the functions of the two are homologous. For example, spatial hearing functions are improved but not tone discrimination [18]. If the auditory cortex is deafferented as in the deaf, then visual spatial discrimination is improved, but not colour functions.…”

Section: The Developments In Clinical and Experimental Neurologymentioning

confidence: 97%

The role of epigenetic-related codes in neurocomputation: dynamic hardware in the brain

Edelstein

Smythies

2014

Phil. Trans. R. Soc. B

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This paper presents a review of recent work on the role that two epigeneticrelated systems may play in information processing mechanisms in the brain. The first consists of exosomes that transport epigenetic-related molecules between neurons. The second consists of homeoproteins like Otx2 that carry information from sense organs to primary sensory cortex. There is developing evidence that presynaptic neurons may be able to modulate the fine microanatomical structure in the postsynaptic neuron. This may be conducted by three mechanisms, of which the first is well established and the latter two are novel. (i) By the well-established activation of receptors that trigger a chain of signalling molecules (second messengers) that result in the upregulation and/or activation of a transcription factor. The two novel systems are the exosome system and homeoproteins. (ii) Exosomes are small vesicles that are released upon activation of the axon terminal, traverse the synaptic cleft, probably via astrocytes and are taken up by the postsynaptic neuron. They carry a load of signalling proteins and a variety of forms of RNA. These loads may then be transported widely throughout the postsynaptic neuron and engineer modulations in the fine structure of computational machinery by epigenetic-related processes. (iii) Otx2 is a transcription factor that, inter alia, controls the development and survival of PVþ GABAergic interneurons (PV cells) in the primary visual cortex. It is synthesized in the retina and is transported to the cortex by a presently unknown mechanism that probably includes direct cell-to-cell transfer, and may, or may not, include transfer by the dynein and exosome systems in addition. These three mechanisms explain a quantity of data from the field of de-and reafferentation plasticity. These data show that the modality of the presynaptic neuron controls to a large extent the modality of the postsynaptic neuron. However, the mechanism that effects this is currently unknown. The exosome and the homeoprotein hypotheses provide novel explanations to add to the well-established earlier mechanism described above.

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Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf

Cited by 432 publications

References 49 publications

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

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

Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex

The role of epigenetic-related codes in neurocomputation: dynamic hardware in the brain

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