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

Abstract

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 ...

Task-specific reorganization of the auditory cortex in deaf humans

“…In deaf cats, cross-modal activations are spatially specific: They are found in high-level auditory areas and usually do not extend to the primary auditory cortex (20,21,37). To test directly if this specificity is shown in our data, we applied anatomically guided region-of-interest (ROI) analysis of the highlevel auditory cortex (area Te 3) and the primary auditory cortex (the combined areas Te 1.0, Te 1.1, and Te 1.2) (Methods, fMRI Data Analysis) (34,35,38).…”

“…Several areas in the auditory cortex are known to be recruited for visual and tactile input in the deaf (18)(19)(20)(21)(22). However, the only clear case of task-specific reorganization of the auditory cortex has been demonstrated in deaf cats.…”

“…Particularly, Lomber et al (20) showed that distinct auditory regions support peripheral visual localization and visual motion detection in deaf cats, and that the same auditory regions support auditory localization and motion detection in hearing cats. Following their line of work, using cooling-loop cortex deactivation, Meredith et al (21) demonstrated that a specific auditory region, the auditory field of the anterior ectosylvian sulcus, is critical for visual orientation in deaf cats and for auditory orientation in hearing cats. In deaf cats, recruitment of the auditory cortex for visual orientation was spatially specific, because deactivation of the primary auditory cortex did not produce deficits in this visual function.…”

Whether the hearing brain hears it or the deaf brain sees it, it’s just the same

“…True, task-specific reorganization of the auditory cortex has been demonstrated in deaf cats. Impressive experiments, some of them involving reversible inactivation of auditory cortex with cooling loops, have shown that a distinct auditory area supports peripheral visual localization and visual motion detection in deaf cats, and that the same region supports these functions in the auditory modality in hearing cats (11,12). However, human evidence, in contrast, has been relatively scarce (13).…”

Cross-modal connectivity of the secondary auditory cortex with higher visual area in the congenitally deaf—A case study

“…Numerous studies have reported auditory-visual crossmodal reorganization in deaf [1][2][3][4][5][6][7][8][9][10][11][12]. Furthermore, changes in auditory-visual connections and cortical responses to visual stimuli such as the neonatal diversion of retinal axons to the auditory thalamus (cross-modal reorganization) results in the development of a primary auditory cortex that resembles visual cortex in its response properties and topography [1].…”