What and How the Deaf Brain Sees

Over the past decade, there has been an unprecedented level of interest and progress into understanding visual processing in the brain of the deaf. Specifically, when the brain is deprived of input from one sensory modality (such as hearing), it often compensates with supranormal performance in one or more of the intact sensory systems (such as vision). Recent psychophysical, functional imaging, and reversible deactivation studies have converged to define the specific visual abilities that are enhanced in the deaf, as well as the cortical loci that undergo crossmodal plasticity in the deaf and are responsible for mediating these superior visual functions. Examination of these investigations reveals that central visual functions, such as object and facial discrimination, and peripheral visual functions, such as motion detection, visual localization, visuomotor synchronization, and Vernier acuity (measured in the periphery), are specifically enhanced in the deaf, compared with hearing participants. Furthermore, the cortical loci identified to mediate these functions reside in deaf auditory cortex: BA 41, BA 42, and BA 22, in addition to the rostral area, planum temporale, Te3, and temporal voice area in humans; primary auditory cortex, anterior auditory field, dorsal zone of auditory cortex, auditory field of the anterior ectosylvian sulcus, and posterior auditory field in cats; and primary auditory cortex and anterior auditory field in both ferrets and mice. Overall, the findings from these studies show that crossmodal reorganization in auditory cortex of the deaf is responsible for the superior visual abilities of the deaf.

A multimodal pathway including the basal ganglia in the feline brain

The purpose of this paper is to give an overview of our present knowledge about the feline tecto-thalamo-basal ganglia cortical sensory pathway. We reviewed morphological and electrophysiological studies of the cortical areas, located in ventral bank of the anterior ectosylvian sulcus as well as the region of the insular cortex, the suprageniculate nucleus of the thalamus, caudate nucleus, and the substantia nigra. Microelectrode studies revealed common receptive field properties in all these structures. The receptive fields were extremely large and multisensory, with pronounced sensitivity to motion of visual stimuli. They often demonstrated directional and velocity selectivity. Preference for small visual stimuli was also a frequent finding. However, orientation sensitivity was absent. It became obvious that the structures of the investigated sensory loop exhibit a unique kind of information processing, not found anywhere else in the feline visual system.

Do the Different Sensory Areas Within the Cat Anterior Ectosylvian Sulcal Cortex Collectively Represent a Network Multisensory Hub?

Current theory supports that the numerous functional areas of the cerebral cortex are organized and function as a network. Using connectional databases and computational approaches, the cerebral network has been demonstrated to exhibit a hierarchical structure composed of areas, clusters and, ultimately, hubs. Hubs are highly connected, higher-order regions that also facilitate communication between different sensory modalities. One computationally identified network hub is the visual area of the Anterior Ectosylvian Sulcal cortex (AESc) of the cat. The Anterior Ectosylvian Visual area (AEV) is but one component of the AESc since the latter also includes the auditory (Field of the Anterior Ectosylvian Sulcus — FAES) and somatosensory (Fourth somatosensory representation — SIV) areas. To better understand the nature of cortical network hubs, the present report reviews the biological features of the AESc. Within the AESc, each area has extensive external cortical connections as well as among one another. Each of these core representations is separated by a transition zone characterized by bimodal neurons that share sensory properties of both adjoining core areas. Finally, core and transition zones are underlain by a continuous sheet of layer 5 neurons that project to common output structures. Altogether, these shared properties suggest that the collective AESc region represents a multiple sensory/multisensory cortical network hub. Ultimately, such an interconnected, composite structure adds complexity and biological detail to the understanding of cortical network hubs and their function in cortical processing.

Development and Plasticity of Intra- and Intersensory Information Processing

The functional architecture of sensory brain regions reflects an ingenious biological solution to the competing demands of a continually changing sensory environment. While they are malleable, they have the constancy necessary to support a stable sensory percept. How does the functional organization of sensory brain regions contend with these antithetical demands? Here we describe the functional organization of auditory and multisensory (i.e., auditory-visual) information processing in three sensory brain structures: (1) a low-level unisensory cortical region, the primary auditory cortex (A1); (2) a higher-order multisensory cortical region, the anterior ectosylvian sulcus (AES); and (3) a multisensory subcortical structure, the superior colliculus (SC). We then present a body of work that characterizes the ontogenic expression of experience-dependent influences on the operations performed by the functional circuits contained within these regions. We will present data to support the hypothesis that the competing demands for plasticity and stability are addressed through a developmental transition in operational properties of functional circuits from an initially labile mode in the early stages of postnatal development to a more stable mode in the mature brain that retains the capacity for plasticity under specific experiential conditions. Finally, we discuss parallels between the central tenets of functional organization and plasticity of sensory brain structures drawn from animal studies and a growing literature on human brain plasticity and the potential applicability of these principles to the audiology clinic.

Spatial Heterogeneity of Cortical Receptive Fields and Its Impact on Multisensory Interactions

Investigations of multisensory processing at the level of the single neuron have illustrated the importance of the spatial and temporal relationship of the paired stimuli and their relative effectiveness in determining the product of the resultant interaction. Although these principles provide a good first-order description of the interactive process, they were derived by treating space, time, and effectiveness as independent factors. In the anterior ectosylvian sulcus (AES) of the cat, previous work hinted that the spatial receptive field (SRF) architecture of multisensory neurons might play an important role in multisensory processing due to differences in the vigor of responses to identical stimuli placed at different locations within the SRF. In this study the impact of SRF architecture on cortical multisensory processing was investigated using semichronic single-unit electrophysiological experiments targeting a multisensory domain of the cat AES. The visual and auditory SRFs of AES multisensory neurons exhibited striking response heterogeneity, with SRF architecture appearing to play a major role in the multisensory interactions. The deterministic role of SRF architecture was tightly coupled to the manner in which stimulus location modulated the responsiveness of the neuron. Thus multisensory stimulus combinations at weakly effective locations within the SRF resulted in large (often superadditive) response enhancements, whereas combinations at more effective spatial locations resulted in smaller (additive/subadditive) interactions. These results provide important insights into the spatial organization and processing capabilities of cortical multisensory neurons, features that may provide important clues as to the functional roles played by this area in spatially directed perceptual processes.

Sound Localization Deficits During Reversible Deactivation of Primary Auditory Cortex and/or the Dorsal Zone

We examined the contributions of primary auditory cortex (A1) and the dorsal zone of auditory cortex (DZ) to sound localization behavior during separate and combined unilateral and bilateral deactivation. From a central visual fixation point, cats learned to make an orienting response (head movement and approach) to a 100-ms broadband noise burst emitted from a central speaker or one of 12 peripheral sites (located in front of the animal, from left 90° to right 90°, at 15° intervals) along the horizontal plane. Following training, each cat was implanted with separate cryoloops over A1 and DZ bilaterally. Unilateral deactivation of A1 or DZ or simultaneous unilateral deactivation of A1 and DZ (A1/DZ) resulted in spatial localization deficits confined to the contralateral hemifield, whereas sound localization to positions in the ipsilateral hemifield remained unaffected. Simultaneous bilateral deactivation of both A1 and DZ resulted in sound localization performance dropping from near-perfect to chance (7.7% correct) across the entire field. Errors made during bilateral deactivation of A1/DZ tended to be confined to the same hemifield as the target. However, unlike the profound sound localization deficit that occurs when A1 and DZ are deactivated together, deactivation of either A1 or DZ alone produced partial and field-specific deficits. For A1, bilateral deactivation resulted in higher error rates (performance dropping to ∼45%) but relatively small errors (mostly within 30° of the target). In contrast, bilateral deactivation of DZ produced somewhat fewer errors (performance dropping to only ∼60% correct), but the errors tended to be larger, often into the incorrect hemifield. Therefore individual deactivation of either A1 or DZ produced specific and unique sound localization deficits. The results of the present study reveal that DZ plays a role in sound localization. Along with previous anatomical and physiological data, these behavioral data support the view that A1 and DZ are distinct cortical areas. Finally, the findings that deactivation of either A1 or DZ alone produces partial sound localization deficits, whereas deactivation of either posterior auditory field (PAF) or anterior ectosylvian sulcus (AES) produces profound sound localization deficits, suggests that PAF and AES make more significant contributions to sound localization than either A1 or DZ.

Visual Deprivation Alters the Development of Cortical Multisensory Integration

It has recently been demonstrated that the maturation of normal multisensory circuits in the cortex of the cat takes place over an extended period of postnatal life. Such a finding suggests that the sensory experiences received during this time may play an important role in this developmental process. To test the necessity of sensory experience for normal cortical multisensory development, cats were raised in the absence of visual experience from birth until adulthood, effectively precluding all visual and visual–nonvisual multisensory experiences. As adults, semichronic single-unit recording experiments targeting the anterior ectosylvian sulcus (AES), a well-defined multisensory cortical area in the cat, were initiated and continued at weekly intervals in anesthetized animals. Despite having very little impact on the overall sensory representations in AES, dark-rearing had a substantial impact on the integrative capabilities of multisensory AES neurons. A significant increase was seen in the proportion of multisensory neurons that were modulated by, rather than driven by, a second sensory modality. More important, perhaps, there was a dramatic shift in the percentage of these modulated neurons in which the pairing of weakly effective and spatially and temporally coincident stimuli resulted in response depressions. In normally reared animals such combinations typically give rise to robust response enhancements. These results illustrate the important role sensory experience plays in shaping the development of mature multisensory cortical circuits and suggest that dark-rearing shifts the relative balance of excitation and inhibition in these circuits.