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Crossmodal Reorganization in the Early Deaf Switches Sensory, but Not Behavioral Roles of Auditory Cortex

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Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex M. Alex Mereditha,1, James Kryklywyb, Amee J. McMillanb, Shveta Malhotrab, Ryan Lum-Taib, and Stephen G. Lomberb aDepartment of Anatomy and Neurobiology, Virginia Commonwealth University School of Medicine, Richmond, VA 23298; and bCentre for Brain and Mind, Department of Physiology and Pharmacology and Department of Psychology, University of Western Ontario, London, ON Canada N6A 5C2 Edited* by Jon H. Kaas, Vanderbilt University, Nashville, TN, and approved April 13, 2011 (received for review December 9, 2010) It is well known that early disruption of sensory input from one innervate (17) the primary auditory cortex. In contrast, early modality can induce crossmodal reorganization of a deprived deafness induces visual reorganization of the posterior auditory cortical area, resulting in compensatory abilities in the remaining field and the dorsal auditory zone (11). The factors that select senses. Compensatory effects, however, occur in selected cortical a deprived region for reorganization, and the specific sensory regions and it is not known whether such compensatory phenom- modalities to be involved, are unknown. One clue might be the ena have any relation to the original function of the reorganized observation that the posterior auditory field of hearing animals is area. In the cortex of hearing cats, the auditory field of the involved in auditory localization (18) whereas the same region in anterior ectosylvian sulcus (FAES) is largely responsive to acoustic congenitally deaf animals underlies their improvement in visual stimulation and its unilateral deactivation results in profound localization of peripheral targets (11). Similarly, following early contralateral acoustic orienting deficits. Given these functional blindness, the lexigraphic components of Braille reading provide and behavioral roles, the FAES was studied in early-deafened cats activation of visual cortex (19). Therefore, it seems possible that to examine its crossmodal sensory properties as well as to assess the behavioral role of a crossmodally reorganized area is related the behavioral role of that reorganization. Recordings in the FAES to its role in hearing/sighted individuals. This hypothesis was ex- of early-deafened adults revealed robust responses to visual amined in the present study. stimulation as well as receptive fields that collectively represented The auditory field of the anterior ectosylvian sulcus (FAES) of the contralateral visual field. A second group of early-deafened the cat is a higher-level component of auditory cortex (20) that cats was trained to localize visual targets in a perimetry array. In has extensive connections with the orienting centers of the these animals, cooling loops were surgically placed on the FAES to brainstem (20, 21). Unilateral cooling deactivation of the FAES reversibly deactivate the region, which resulted in substantial results in severe acoustic localization deficits in the contralateral contralateral visual orienting deficits. These results demonstrate field (18), and its neurons show sensitivity to sound location (22). that crossmodal plasticity can substitute one sensory modality for The region also contains a subset of auditory neurons whose another while maintaining the functional repertoire of the reor- activity can be modulated by the presence of visual (23) or so- ganized region. matosensory (24) stimulation, as well as bimodal visual–auditory neurons (25, 26). These multisensory properties suggest that vision | single-unit electrophysiology | orienting behavior | a substrate is present for crossmodal reorganization should au- cooling deactivation ditory inputs be damaged or lost. The present experiment sought to determine whether neurons in FAES of early-deafened cats remarkable property of the brain is its capacity to respond to become crossmodally reorganized and whether deactivation of fi Achange. This neuroplastic process endows the nervous sys- the reorganized area results in behavioral localization de cits tem with the ability to adjust itself to the loss of an entire set of mediated by the replacement modality. sensory inputs or even two (1). Under these conditions, it is Results clearly adaptive for inputs from an intact modality to substitute for those that have been lost, such as auditory navigation in the Sensory Activity of Deafened FAES Cortex. Single-unit recordings blind. Crossmodal plasticity can also enhance perceptual per- made from the FAES of early-deafened cats (n = 3), summa- rized in Fig. 1, revealed physiologically active neurons (n = 415), formance within the remaining sensory modalities. Numerous ± reports document improvement over sighted subjects in auditory the majority of which (67.7% 7.6 SD) were responsive to visual stimulation. By contrast, similar recordings from the FAES in and somatosensory tasks in blind individuals (2–7), as well as adult hearing cats (n = 3) in this and in previous studies (2, 22, enhanced performance in visual and tactile behaviors in the deaf 23, 25–28) showed a strong preference auditory responsivity, (8–11). However, with the accumulation of studies examining although a small proportion of nonauditory responses also oc- such compensatory effects following early sensory loss, it is be- curred (Fig. 1). In early-deafened FAES, responses were detec- coming evident that not all features of the replacement sensory ted using either manually presented visual cues or, as in Fig. 1C, modalities are equally represented. For example, early-deaf by repeatable, electronically gated visual stimuli. When stimu- subjects exhibit supranormal abilities for visual localization (10) lating with the latter, it was clear that responses to visual stimuli and visual motion detection (11, 12), but not visual brightness were robust and reliable. Most visually responsive neurons were discrimination (13), contrast sensitivity (14), visual shape detec- sensitive to movement direction and preferred high-velocity tion (15), grating acuity, vernier acuity, orientation discrimina- movement (e.g., >100°/s), thus demonstrating response proper- tion, motion direction, or velocity discrimination (11). Thus, rather than a generalized overall improvement, it seems that only fi speci c features of the replacement modality are affected by Author contributions: M.A.M. and S.G.L. designed research; M.A.M., J.K., A.J.M., S.M., crossmodal plasticity. R.L.-T., and S.G.L. performed research; M.A.M., S.M., and S.G.L. analyzed data; and Crossmodal plasticity itself does not appear to be a uniformly M.A.M. and S.G.L. wrote the paper. distributed effect. Although it seems plausible that the entire The authors declare no conflict of interest. territory vacated by a damaged sensory modality might be avail- *This Direct Submission article had a prearranged editor. able for crossmodal innervation, this assumption is not supported 1To whom correspondence should be addressed. E-mail: [email protected]. by evidence from studies of early deafness. Following early deaf- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. ness, crossmodal inputs appear to avoid (5, 16) or only partially 1073/pnas.1018519108/-/DCSupplemental. 8856–8861 | PNAS | May 24, 2011 | vol. 108 | no. 21 www.pnas.org/cgi/doi/10.1073/pnas.1018519108 Downloaded by guest on September 29, 2021 Fig. 1. (A) On the lateral view of the cat brain, the arrow indicates the anterior ectosylvian sulcus (AES) and the plane of section corresponds with the coronal sections displayed in B.(B) Portions of serially arranged coronal sections containing the AES (large arrows) and the field of the anterior ectosylvian sulcus (FAES; shaded). Representative recording penetrations are shown traversing the FAES. Unlike hearing animals, where the FAES is largely auditory, recordings from adults that were postnatally deafened revealed responses driven primarily by visual stimulation (labeled V; also somatosensory, S; unresponsive, U). (C) Typical single-unit neuronal responses (raster dot = 1 spike; row = 1 presentation; histogram is 10-ms time bin) to visual stimulation showed vigorousand reliable activation by a moving bar of light (ramp labeled V). For neurons histologically verified in the FAES, D summarizes the sensory modality patterns found in postnatally deafened (solid bars; three cats, n = 415 neurons) and in hearing (shaded bars; three cats, n = 205 neurons) cats. These data indicate that the FAES is crossmodally reorganized from the auditory to visual modality in early-deafened animals. ties characteristic of visual cortical neurons. As illustrated in receptive fields included a representation of central visual space Fig. 2A, these visually responsive neurons exhibited receptive and were quite large, averaging 63.9° (±18 SD) in diameter. fields that were collectively distributed across the contralateral Visual receptive fields of hearing animals exhibited similar size visual hemifield, sparing only the most superior and inferior and position distributions to those of deafened FAES animals extremes, although no clear retinotopy was observed. In addi- (Fig. 2B), but were far fewer in occurrence. tion, the majority (89%) of visual receptive fields extended into Early-deafened animals also revealed a small proportion of the ipsilateral visual field (average 12.7° ± 10.4 SD). Thus, most FAES neurons responsive to somatosensory stimulation (33.5% ± NEUROSCIENCE Fig. 2. (A) On a representation of the visual field, visual
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