Nicole Chabot

Cross-modal reorganization of cortical afferents to dorsal auditory cortex following early- and late-onset deafness

Cat auditory cortex is known to undergo cross‐modal reorganization following deafness, such that behavioral advantages in visual motion detection are abolished when a specific region of deaf auditory cortex, the dorsal zone (DZ), is deactivated. The purpose of the present investigation was to examine the connectional adaptations that might subserve this plasticity. We deposited biotinylated dextran amine (BDA; 3,000 MW), a retrograde tracer, unilaterally into the posterior portion of the suprasylvian fringe, corresponding to area DZ of hearing, early‐deafened (onset <1 month), and late‐deafened (onset >3 months) cats to reveal cortical afferent projections. Overall, the pattern of cortical projections to DZ was similar in both hearing and deafened animals. However, there was a progressive increase in projection strength among hearing and late‐ and early‐deafened cats from an extrastriate visual cortical region known to be involved in the processing of visual motion, the posterolateral lateral suprasylvian area (PLLS). Additionally, although no such change was documented for the posteromedial lateral suprasylvian area (PMLS), labeled neurons were present within a subregion of PMLS devoted to foveal vision in both late‐ and early‐deafened animals but not in hearing controls. PMLS is also an extrastriate visual motion processing area and is widely considered to be the homolog of primate middle temporal area. No changes in auditory cortical connectivity were observed among groups. These observations suggest that amplified cortical projections from extrastriate visual areas involved in visual motion processing to DZ may contribute to the cross‐modal reorganization that functionally manifests as superior visual motion detection ability in the deaf animal. J. Comp. Neurol. 522:654–675, 2014.

Modified Areal Cartography in Auditory Cortex Following Early- and Late-Onset Deafness

Cross-modal plasticity following peripheral sensory loss enables deprived cortex to provide enhanced abilities in remaining sensory systems. These functional adaptations have been demonstrated in cat auditory cortex following early-onset deafness in electrophysiological and psychophysical studies. However, little information is available concerning any accompanying structural compensations. To examine the influence of sound experience on areal cartography, auditory cytoarchitecture was examined in hearing cats, early-deaf cats, and cats with late-onset deafness. Cats were deafened shortly after hearing onset or in adulthood. Cerebral cytoarchitecture was revealed immunohistochemically using SMI-32, a monoclonal antibody used to distinguish auditory areas in many species. Auditory areas were delineated in coronal sections and their volumes measured. Staining profiles observed in hearing cats were conserved in early- and late-deaf cats. In all deaf cats, dorsal auditory areas were the most mutable. Early-deaf cats showed further modifications, with significant expansions in second auditory cortex and ventral auditory field. Borders between dorsal auditory areas and adjacent visual and somatosensory areas were shifted ventrally, suggesting expanded visual and somatosensory cortical representation. Overall, this study shows the influence of acoustic experience in cortical development, and suggests that the age of auditory deprivation may significantly affect auditory areal cartography.

Amplified somatosensory and visual cortical projections to a core auditory area, the anterior auditory field, following early- and late-onset deafness

Cross‐modal reorganization following the loss of input from a sensory modality can recruit sensory‐deprived cortical areas to process information from the remaining senses. Specifically, in early‐deaf cats, the anterior auditory field (AAF) is unresponsive to auditory stimuli but can be activated by somatosensory and visual stimuli. Similarly, AAF neurons respond to tactile input in adult‐deafened animals. To examine anatomical changes that may underlie this functional adaptation following early or late deafness, afferent projections to AAF were examined in hearing cats, and cats with early‐ or adult‐onset deafness. Unilateral deposits of biotinylated dextran amine were made in AAF to retrogradely label cortical and thalamic afferents to AAF. In early‐deaf cats, ipsilateral neuronal labeling in visual and somatosensory cortices increased by 329% and 101%, respectively. The largest increases arose from the anterior ectosylvian visual area and the anterolateral lateral suprasylvian visual area, as well as somatosensory areas S2 and S4. Consequently, labeling in auditory areas was reduced by 36%. The age of deafness onset appeared to influence afferent connectivity, with less marked differences observed in late‐deaf cats. Profound changes to visual and somatosensory afferent connectivity following deafness may reflect corticocortical rewiring affording acoustically deprived AAF with cross‐modal functionality. J. Comp. Neurol. 523:1925–1947, 2015

Differential modification of cortical and thalamic projections to cat primary auditory cortex following early‐ and late‐onset deafness

Following sensory deprivation, primary somatosensory and visual cortices undergo crossmodal plasticity, which subserves the remaining modalities. However, controversy remains regarding the neuroplastic potential of primary auditory cortex (A1). To examine this, we identified cortical and thalamic projections to A1 in hearing cats and those with early‐ and late‐onset deafness. Following early deafness, inputs from second auditory cortex (A2) are amplified, whereas the number originating in the dorsal zone (DZ) decreases. In addition, inputs from the dorsal medial geniculate nucleus (dMGN) increase, whereas those from the ventral division (vMGN) are reduced. In late‐deaf cats, projections from the anterior auditory field (AAF) are amplified, whereas those from the DZ decrease. Additionally, in a subset of early‐ and late‐deaf cats, area 17 and the lateral posterior nucleus (LP) of the visual thalamus project concurrently to A1. These results demonstrate that patterns of projections to A1 are modified following deafness, with statistically significant changes occurring within the auditory thalamus and some cortical areas. Moreover, we provide anatomical evidence for small‐scale crossmodal changes in projections to A1 that differ between early‐ and late‐onset deaf animals, suggesting that potential crossmodal activation of primary auditory cortex differs depending on the age of deafness onset. J. Comp. Neurol. 523:2297–2320, 2015.

Quantifying and comparing the pattern of thalamic and cortical projections to the posterior auditory field in hearing and deaf cats

Following sensory loss, compensatory crossmodal reorganization occurs such that the remaining modalities are functionally enhanced. For example, behavioral evidence suggests that peripheral visual localization is better in deaf than in normal hearing animals, and that this enhancement is mediated by recruitment of the posterior auditory field (PAF), an area that is typically involved in localization of sounds in normal hearing animals. To characterize the anatomical changes that underlie this phenomenon, we identified the thalamic and cortical projections to the PAF in hearing cats and those with early‐ and late‐onset deafness. The retrograde tracer biotinylated dextran amine was deposited in the PAF unilaterally, to label cortical and thalamic afferents. Following early deafness, there was a significant decrease in callosal projections from the contralateral PAF. Late‐deaf animals showed small‐scale changes in projections from one visual cortical area, the posterior ectosylvian field (EPp), and the multisensory zone (MZ). With the exception of these minor differences, connectivity to the PAF was largely similar between groups, with the principle projections arising from the primary auditory cortex (A1) and the ventral division of the medial geniculate body (MGBv). This absence of large‐scale connectional change suggests that the functional reorganization that follows sensory loss results from changes in synaptic strength and/or unmasking of subthreshold intermodal connections. J. Comp. Neurol. 524:3042–3063, 2016.

Cerebral origins of the auditory projection to the superior colliculus of the cat

The superior colliculus (SC) is critical for directing accurate head and eye movements to visual and acoustic targets. In visual cortex, areas involved in orienting of the head and eyes to a visual stimulus have direct projections to the SC. In auditory cortex of the cat, four areas have been identified to be critical for the accurate orienting of the head and body to an acoustic stimulus. These areas include primary auditory cortex (A1), the posterior auditory field (PAF), the dorsal zone of auditory cortex (DZ), and the auditory field of the anterior ectosylvian sulcus (fAES). Therefore, we hypothesized that these four regions of auditory cortex would have direct projections to the SC. To test this hypothesis, deposits of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) were made into the superficial and deep layers of the SC to label, by means of retrograde transport, the auditory cortical origins of the corticotectal pathway. Bilateral examination of auditory cortex revealed that the vast majority of the labeled cells were located in the hemisphere ipsilateral to the SC injection. In ipsilateral auditory cortex, nearly all the labeled neurons were found in the infragranular layers, predominately in layer V. The largest population of labeled cells was located in the fAES. Few labeled neurons were identified in A1, PAF, or DZ. Thus, in contrast to the visual system, only one of the auditory cortical areas involved in orienting to an acoustic stimulus has a strong direct projection to the SC. Sound localization signals processed in primary (A1) and other non-primary (PAF and DZ) auditory cortices may be transmitted to the SC via a multi-synaptic corticotectal network.

Origins of thalamic and cortical projections to the posterior auditory field in congenitally deaf cats.

ABSTRACT Crossmodal plasticity takes place following sensory loss, such that areas that normally process the missing modality are reorganized to provide compensatory function in the remaining sensory systems. For example, congenitally deaf cats outperform normal hearing animals on localization of visual stimuli presented in the periphery, and this advantage has been shown to be mediated by the posterior auditory field (PAF). In order to determine the nature of the anatomical differences that underlie this phenomenon, we injected a retrograde tracer into PAF of congenitally deaf animals and quantified the thalamic and cortical projections to this field. The pattern of projections from areas throughout the brain was determined to be qualitatively similar to that previously demonstrated in normal hearing animals, but with twice as many projections arising from non‐auditory cortical areas. In addition, small ectopic projections were observed from a number of fields in visual cortex, including areas 19, 20a, 20b, and 21b, and area 7 of parietal cortex. These areas did not show projections to PAF in cats deafened ototoxically near the onset of hearing, and provide a possible mechanism for crossmodal reorganization of PAF. These, along with the possible contributions of other mechanisms, are considered. HighlightsThe retrograde tracer BDA was injected into PAF of congenitally deaf cats.Neurons projecting to PAF were quantified throughout the brain.Non‐auditory projections to PAF more than doubled compared to hearing cats.Ectopic projections were observed from visual and parietal cortical areas.

Influence of Core Auditory Cortical Areas on Acoustically Evoked Activity in Contralateral Primary Auditory Cortex

In contrast to numerous studies of transcallosal communication in visual and somatosensory cortices, the functional properties of interhemispheric connections between auditory cortical fields have not been widely scrutinized. Therefore, the purpose of the present investigation was to measure the magnitude and type (inhibitory/excitatory) of modulatory properties of core auditory fields on contralateral primary auditory cortex (A1) activity. We combined single-unit neuronal recordings with reversible cooling deactivation techniques to measure variations in contralateral A1 response levels during A1, anterior auditory field (AAF), or simultaneous A1 and AAF neuronal discharge suppression epochs in cat auditory cortex. Cortical activity was evoked by presentation of pure tones, noise bursts, and frequency-modulated (FM) sweeps before, during, and after cortical deactivation periods. Comparisons of neuronal response changes before and during neuronal silencing revealed three major findings. First, deactivation of A1 and AAF-induced significant peak response reductions in contralateral A1 activity during simple (tonal) and complex (noise bursts and FM sweeps) acoustic exposure. Second, decreases in A1 neuronal activity appear to be in agreement with anatomical laminar termination patterns emanating from contralateral auditory cortex fields. Third, modulatory properties of core auditory areas lack hemispheric lateralization. These findings demonstrate that during periods of acoustic exposure, callosal projections emanating from core auditory areas modulate A1 neuronal activity via excitatory inputs.

A quantitative comparison of the hemispheric, areal, and laminar origins of sensory and motor cortical projections to the superior colliculus of the cat

The superior colliculus (SC) is a midbrain structure central to orienting behaviors. The organization of descending projections from sensory cortices to the SC has garnered much attention; however, rarely have projections from multiple modalities been quantified and contrasted, allowing for meaningful conclusions within a single species. Here, we examine corticotectal projections from visual, auditory, somatosensory, motor, and limbic cortices via retrograde pathway tracers injected throughout the superficial and deep layers of the cat SC. As anticipated, the majority of cortical inputs to the SC originate in the visual cortex. In fact, each field implicated in visual orienting behavior makes a substantial projection. Conversely, only one area of the auditory orienting system, the auditory field of the anterior ectosylvian sulcus (fAES), and no area involved in somatosensory orienting, shows significant corticotectal inputs. Although small relative to visual inputs, the projection from the fAES is of particular interest, as it represents the only bilateral cortical input to the SC. This detailed, quantitative study allows for comparison across modalities in an animal that serves as a useful model for both auditory and visual perception. Moreover, the differences in patterns of corticotectal projections between modalities inform the ways in which orienting systems are modulated by cortical feedback. J. Comp. Neurol. 524:2623–2642, 2016.

Amplified extrastriate visual cortical projections to the dorsal zone of auditory cortex following early- and late-onset deafness

Adaptive cross-modal plasticity refers to cortical reorganization that takes place across sensory modalities following the loss of a sensory system. This loss of one modality is often accompanied by a heightening of the remaining senses (Bavelier and Neville, 2002). Cat auditory cortex has been shown to undergo cross-modal reorganization following deafness, such that deaf animals are better able to detect visual motion than hearing controls, an advantage which can be localized to the dorsal zone (DZ) of auditory cortex (Lomber et al., 2010). However, because the structural adaptations that might subserve this plasticity remain largely unknown, the purpose of the present investigation was to examine modifications in anatomical connectivity following early- or late-onset deafness. We injected DZ of hearing, early- and late-deafened cats ( n = 5 per group) with biotinylated dextran amine (BDA). Immunohistochemistry was performed following perfusion to reveal the tracer. Overall, the pattern of cortical projections to DZ was similar in both early- and late-deafened cats and hearing controls. However, an increase in projection strength from visual areas involved in visual motion processing was observed in both early- and late-deafened animals compared to hearing controls. Our observations suggest that amplified cortical projections from visual motion processing regions to DZ may underlie the cross-modal reorganization that functionally manifests as superior visual motion detection abilities in the deaf animal. Furthermore, the degree to which this reorganization occurs is similar between early- and late-deafened animals, suggesting that structural compensations can occur regardless of duration of acoustic experience.