Visual Advantage in Deaf Adults Linked to Retinal Changes

The altered sensory experience of profound early onset deafness provokes sometimes large scale neural reorganisations. In particular, auditory-visual cross-modal plasticity occurs, wherein redundant auditory cortex becomes recruited to vision. However, the effect of human deafness on neural structures involved in visual processing prior to the visual cortex has never been investigated, either in humans or animals. We investigated neural changes at the retina and optic nerve head in profoundly deaf (N = 14) and hearing (N = 15) adults using Optical Coherence Tomography (OCT), an in-vivo light interference method of quantifying retinal micro-structure. We compared retinal changes with behavioural results from the same deaf and hearing adults, measuring sensitivity in the peripheral visual field using Goldmann perimetry. Deaf adults had significantly larger neural rim areas, within the optic nerve head in comparison to hearing controls suggesting greater retinal ganglion cell number. Deaf adults also demonstrated significantly larger visual field areas (indicating greater peripheral sensitivity) than controls. Furthermore, neural rim area was significantly correlated with visual field area in both deaf and hearing adults. Deaf adults also showed a significantly different pattern of retinal nerve fibre layer (RNFL) distribution compared to controls. Significant correlations between the depth of the RNFL at the inferior-nasal peripapillary retina and the corresponding far temporal and superior temporal visual field areas (sensitivity) were found. Our results show that cross-modal plasticity after early onset deafness may not be limited to the sensory cortices, noting specific retinal adaptations in early onset deaf adults which are significantly correlated with peripheral vision sensitivity

Metaplasticity framework for cross-modal synaptic plasticity in adults

Sensory loss leads to widespread adaptation of neural circuits to mediate cross-modal plasticity, which allows the organism to better utilize the remaining senses to guide behavior. While cross-modal interactions are often thought to engage multisensory areas, cross-modal plasticity is often prominently observed at the level of the primary sensory cortices. One dramatic example is from functional imaging studies in humans where cross-modal recruitment of the deprived primary sensory cortex has been observed during the processing of the spared senses. In addition, loss of a sensory modality can lead to enhancement and refinement of the spared senses, some of which have been attributed to compensatory plasticity of the spared sensory cortices. Cross-modal plasticity is not restricted to early sensory loss but is also observed in adults, which suggests that it engages or enables plasticity mechanisms available in the adult cortical circuit. Because adult cross-modal plasticity is observed without gross anatomical connectivity changes, it is thought to occur mainly through functional plasticity of pre-existing circuits. The underlying cellular and molecular mechanisms involve activity-dependent homeostatic and Hebbian mechanisms. A particularly attractive mechanism is the sliding threshold metaplasticity model because it innately allows neurons to dynamically optimize their feature selectivity. In this mini review, I will summarize the cellular and molecular mechanisms that mediate cross-modal plasticity in the adult primary sensory cortices and evaluate the metaplasticity model as an effective framework to understand the underlying mechanisms

Cross-Modal Re-Organization in Clinical Populations with Hearing Loss.

We review evidence for cross-modal cortical re-organization in clinical populations with hearing loss. Cross-modal plasticity refers to the ability for an intact sensory modality (e.g., vision or somatosensation) to recruit cortical brain regions from a deprived sensory modality (e.g., audition) to carry out sensory processing. We describe evidence for cross-modal changes in hearing loss across the age-spectrum and across different degrees of hearing impairment, including children with profound, bilateral deafness with cochlear implants, single-sided deafness before and after cochlear implantation, and adults with early-stage, mild-moderate, age-related hearing loss. Understanding cross-modal plasticity in the context of auditory deprivation, and the potential for reversal of these changes following intervention, may be vital in directing intervention and rehabilitation options for clinical populations with hearing loss

Experience-Dependent Loss of Cross-Modal Plasticity in Mouse Visual Cortex

We perceive the world through sensory experience. Sensory information is registered and processed by our brain in a modality specific fashion. Interestingly, studies have shown that the visual cortex of early but not late blind subjects is able to respond to touch or sound (Sadato et al., 1996; Buchel et al., 1998; Weeks et al., 2000; Gougoux et al., 2009). Here, we investigated whether sensory parcellation in adult cortex is innate or is acquired during early postnatal life in an experience-dependent manner. Furthermore, we studied the anatomical substrates and molecular pathways possibly involved in cross-modal activation and its plasticity. First, mice were reared from birth in total darkness until adulthood (DR) to replicate the human blind condition. Cross-modal activity and the underlying circuitry were analyzed. We found that DR visual cortex was strongly activated by sound stimulation using functional imaging, single-unit recording, and c-Fos immunohistochemistry. Functional analysis was followed by anatomical tracing studies, which showed ectopic projections from the auditory thalamus and auditory cortex into the secondary visual area in DR animals. The second half of our study looked at how visual experience affects cross-modal plasticity. We found that cross-modal activity and ectopic connectivity is present in normally reared young mice (25 postnatal days: P25). Normal sensory experience through the first two months of postnatal life was sufficient to decrease the number of ectopic inputs. Interestingly, exposing DR mice to visual experience as adults established transient functional sensory specificity in the visual cortex without eliminating the ectopic anatomical inputs. Lastly, we tested several molecular pathways that can potentially regulate cross-modal plasticity. We found that myelin signaling and cholinergic modulation controls the duration of cross-modal plasticity and consolidates sensory modularization. Overall, our work proposes a model of how cross-modal inputs into early sensory areas are pruned or retained depending on early life experience. This study provides insight into how the cortex develops functional specificity, and help approach disorders that exhibit abnormal sensory integration and disrupted neuronal connectivity such as Autism Spectrum Disorder

Structural reorganization of the early visual cortex following Braille training in sighted adults

Training can induce cross-modal plasticity in the human cortex. A well-known example of this phenomenon is the recruitment of visual areas for tactile and auditory processing. It remains unclear to what extent such plasticity is associated with changes in anatomy. Here we enrolled 29 sighted adults into a nine-month tactile Braille-reading training, and used voxel-based morphometry and diffusion tensor imaging to describe the resulting anatomical changes. In addition, we collected resting-state fMRI data to relate these changes to functional connectivity between visual and somatosensory-motor cortices. Following Braille-training, we observed substantial grey and white matter reorganization in the anterior part of early visual cortex (peripheral visual field). Moreover, relative to its posterior, foveal part, the peripheral representation of early visual cortex had stronger functional connections to somatosensory and motor cortices even before the onset of training. Previous studies show that the early visual cortex can be functionally recruited for tactile discrimination, including recognition of Braille characters. Our results demonstrate that reorganization in this region induced by tactile training can also be anatomical. This change most likely reflects a strengthening of existing connectivity between the peripheral visual cortex and somatosensory cortices, which suggests a putative mechanism for cross-modal recruitment of visual areas

Sensory Compensation in Children Following Vision Loss after Trauma and Disease

Sensory compensation or sensory substitution occurs when a sense organ, such as the eye, is lost due to trauma or disease. Individuals often experience phantom limb sensation or pain but research increasingly points towards some individuals developing a heightened level of functioning in their remaining senses, particularly in their remaining intact eye. Losing an eye at an early age can often result in “super functioning” in the remaining eye providing that no similar trauma or disease results. Cases include young children who have undergone enucleation because of diagnosed unilateral retinoblastoma and whose remaining eye is free from disease

Microstructural differences in the thalamus and thalamic radiations in the congenitally deaf

There is evidence of both crossmodal and intermodal plasticity in the deaf brain. Here, we investigated whether sub-cortical plasticity, specifically of the thalamus, contributed to this reorganisation. We contrasted diffusion weighted magnetic resonance imaging data from 13 congenitally deaf and 13 hearing participants, all of whom had learnt British Sign Language after 10 years of age. Connectivity based segmentation of the thalamus revealed changes to mean and radial diffusivity in occipital and frontal regions, which may be linked to enhanced peripheral visual acuity, and differences in how visual attention is deployed in the deaf group. Using probabilistic tractography, tracts were traced between the thalamus and its cortical targets, and microstructural measurements were extracted from these tracts. Group differences were found in microstructural measurements of occipital, frontal, somatosensory, motor and parietal thalamo-cortical tracts. Our findings suggest there is sub-cortical plasticity in the deaf brain, and that white matter alterations can be found throughout the deaf brain, rather than being restricted to, or focussed in auditory cortex