Dataset Information

Mechanisms of cross-modal plasticity in early-blind subjects.

ABSTRACT: A variety of studies have demonstrated enhanced blood oxygenation level dependent responses to auditory and tactile stimuli within occipital cortex as a result of early blindness. However, little is known about the organizational principles that drive this cross-modal plasticity. We compared BOLD responses to a wide variety of auditory and tactile tasks (vs. rest) in early-blind and sighted subjects. As expected, cross-modal responses were larger in blind than in sighted subjects in occipital cortex for all tasks (cross-modal plasticity). Within both blind and sighted subject groups, we found patterns of cross-modal activity that were remarkably similar across tasks: a large proportion of cross-modal responses within occipital cortex are neither task nor stimulus specific. We next examined the mechanisms underlying enhanced BOLD responses within early-blind subjects. We found that the enhancement of cross-modal responses due to early blindness was best described as an additive shift, suggesting that cross-modal plasticity within blind subjects does not originate from either a scaling or unmasking of cross-modal responsivities found in sighted subjects.

SUBMITTER: Lewis LB

PROVIDER: S-EPMC3007643 | biostudies-literature | 2010 Dec

REPOSITORIES: biostudies-literature

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Mechanisms of cross-modal plasticity in early-blind subjects.

Lewis Lindsay B LB Saenz Melissa M Fine Ione I

Journal of neurophysiology 20100728 6

A variety of studies have demonstrated enhanced blood oxygenation level dependent responses to auditory and tactile stimuli within occipital cortex as a result of early blindness. However, little is known about the organizational principles that drive this cross-modal plasticity. We compared BOLD responses to a wide variety of auditory and tactile tasks (vs. rest) in early-blind and sighted subjects. As expected, cross-modal responses were larger in blind than in sighted subjects in occipital co ...[more]

PMID: 20668272

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Project description:Sensory deprivation prompts extensive structural and functional reorganizations of the cortex resulting in the occupation of space for the lost sense by the intact sensory systems. This process, known as cross-modal plasticity, has been widely studied in individuals with vision or hearing loss. However, little is known on the neuroplastic changes in restoring the deprived sense. Some reports consider the cross-modal functionality maladaptive to the return of the original sense, and others view this as a critical process in maintaining the neurons of the deprived sense active and operational. These controversial views have been challenged in both auditory and vision restoration reports for decades. Recently with the approval of Luxturna as the first retinal gene therapy (GT) drug to reverse blindness, there is a renewed interest for the crucial role of cross-modal plasticity on sight restoration. Employing a battery of task and resting state functional magnetic resonance imaging (rsfMRI), in comparison to a group of sighted controls, we tracked the functional changes in response to auditory and visual stimuli and at rest, in a group of patients with biallelic mutations in the RPE65 gene ("RPE65 patients") before and 3 years after GT. While the sighted controls did not present any evidence for auditory cross-modal plasticity, robust responses to the auditory stimuli were found in occipital cortex of the RPE65 patients overlapping visual responses and significantly elevated 3 years after GT. The rsfMRI results showed significant connectivity between the auditory and visual areas for both groups albeit attenuated in patients at baseline but enhanced 3 years after GT. Taken together, these findings demonstrate that (1) RPE65 patients present with an auditory cross-modal component; (2) visual and non-visual responses of the visual cortex are considerably enhanced after vision restoration; and (3) auditory cross-modal functions did not adversely affect the success of vision restitution. We hypothesize that following GT, to meet the demand for the newly established retinal signals, remaining or dormant visual neurons are revived or unmasked for greater participation. These neurons or a subset of these neurons respond to both the visual and non-visual demands and further strengthen connectivity between the auditory and visual cortices.

Project description:Sensory loss induces cross-modal plasticity, often resulting in altered performance in remaining sensory modalities. Whereas much is known about the macroscopic mechanisms underlying cross-modal plasticity, only scant information exists about its cellular and molecular underpinnings. We found that Caenorhabditis elegans nematodes deprived of a sense of body touch exhibit various changes in behavior, associated with other unimpaired senses. We focused on one such behavioral alteration, enhanced odor sensation, and sought to reveal the neuronal and molecular mechanisms that translate mechanosensory loss into improved olfactory acuity. To this end, we analyzed in mechanosensory mutants food-dependent locomotion patterns that are associated with olfactory responses and found changes that are consistent with enhanced olfaction. The altered locomotion could be reversed in adults by optogenetic stimulation of the touch receptor (mechanosensory) neurons. Furthermore, we revealed that the enhanced odor response is related to a strengthening of inhibitory AWC→AIY synaptic transmission in the olfactory circuit. Consistently, inserting in this circuit an engineered electrical synapse that diminishes AWC inhibition of AIY counteracted the locomotion changes in touch-deficient mutants. We found that this cross-modal signaling between the mechanosensory and olfactory circuits is mediated by neuropeptides, one of which we identified as FLP-20. Our results indicate that under normal function, ongoing touch receptor neuron activation evokes FLP-20 release, suppressing synaptic communication and thus dampening odor sensation. In contrast, in the absence of mechanosensory input, FLP-20 signaling is reduced, synaptic suppression is released, and this enables enhanced olfactory acuity; these changes are long lasting and do not represent ongoing modulation, as revealed by optogenetic experiments. Our work adds to a growing literature on the roles of neuropeptides in cross-modal signaling, by showing how activity-dependent neuropeptide signaling leads to specific cross-modal plastic changes in neural circuit connectivity, enhancing sensory performance.

Dataset Information

Mechanisms of cross-modal plasticity in early-blind subjects.

Publications

Mechanisms of cross-modal plasticity in early-blind subjects.

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