Modified Origins of Cortical Projections to the Superior Colliculus in the Deaf: Dispersion of Auditory Efferents

Abstract

Following the loss of a sensory modality, such as deafness or blindness, crossmodal plasticity is commonly identified in regions of the cerebrum that normally process the deprived modality. It has been hypothesized that significant changes in the patterns of cortical afferent and efferent projections may underlie these functional crossmodal changes. However, studies of thalamocortical and corticocortical connections have refuted this hypothesis, instead revealing a profound resilience of cortical afferent projections following deafness and blindness. This report is the first study of cortical outputs following sensory deprivation, characterizing cortical projections to the superior colliculus in mature cats ( = 5, 3 female) with perinatal-onset deafness. The superior colliculus was exposed to a retrograde pathway tracer, and subsequently labeled cells throughout the cerebrum were identified and quantified. Overall, the percentage of cortical projections arising from auditory cortex was substantially increased, not decreased, in early-deaf cats compared with intact animals. Furthermore, the distribution of labeled cortical neurons was no longer localized to a particular cortical subregion of auditory cortex but dispersed across auditory cortical regions. Collectively, these results demonstrate that, although patterns of cortical afferents are stable following perinatal deafness, the patterns of cortical efferents to the superior colliculus are highly mutable. When a sense is lost, the remaining senses are functionally enhanced through compensatory crossmodal plasticity. In deafness, brain regions that normally process sound contribute to enhanced visual and somatosensory perception. We demonstrate that hearing loss alters connectivity between sensory cortex and the superior colliculus, a midbrain region that integrates sensory representations to guide orientation behavior. Contrasting expectation, the proportion of projections from auditory cortex increased in deaf animals compared with normal hearing, with a broad distribution across auditory fields. This is the first description of changes in cortical efferents following sensory loss and provides support for models predicting an inability to form a coherent, multisensory percept of the environment following periods of abnormal development.

The way of the light: how visual information reaches the auditory cortex in congenitally deaf adults

“…Extant human and non-human studies on structural connectivity, volumetry, and anterograde tracing show that there are neuroplastic changes in (i) the colliculi (Amaral et al, 2016); (ii) the thalamus (Amaral et al, 2016; Kok & Lomber, 2017; Butler et al, 2018); and (iii) cortical regions (Beer et al, 2011; Amaral et al, 2016). For instance, Amaral and colleagues (2016) proposed that volumetric changes in subcortical structures in deaf individuals that mimic the kinds of volumetric and functional asymmetries found in the auditory cortex of those same individuals could be related to information rerouting from visual to auditory streams.…”

“…Tracing results on deaf cats also suggest that subcortical structures, and specifically the superior colliculi, may be partially involved in the passage of visual information to the auditory cortex under deafness (Butler et al, 2018). Retrograde tracers injected into the superior colliculus led to labelling in the auditory cortex (Butler et al, 2018).…”

“…Tracing results on deaf cats also suggest that subcortical structures, and specifically the superior colliculi, may be partially involved in the passage of visual information to the auditory cortex under deafness (Butler et al, 2018). Retrograde tracers injected into the superior colliculus led to labelling in the auditory cortex (Butler et al, 2018). Although the results from Butler and colleagues (2018) suggest projections from the auditory cortex to subcortical structures, their results clearly show that the superior colliculi are connected to the auditory cortex in early deaf animals.…”

“…Retrograde tracers injected into the superior colliculus led to labelling in the auditory cortex (Butler et al, 2018). Although the results from Butler and colleagues (2018) suggest projections from the auditory cortex to subcortical structures, their results clearly show that the superior colliculi are connected to the auditory cortex in early deaf animals. Moreover, Kok and Lomber (2017) showed that the pattern of connections from the thalamus to the dorsal zone of the auditory cortex of early and late deaf cats remains similar to the pattern of connections of hearing cats.…”

Optimizing Speech Recognition Using a Computational Model of Human Hearing: Effect of Noise Type and Efferent Time Constants

“…Computational modeling of the auditory system provides a useful means of understanding the mechanisms contributing to improved speech recognition in noise. Modeling the auditory neural pathways has been informative with regards to understanding peripheral and central auditory processing [8], top-down cognitive and linguistic processing [9], changes in cortical projections due to deafness [10], and speechrecognition performance in noise [11].…”