Visual deprivation independent shift of ocular dominance induced by cross-modal plasticity.

Manuel Teichert,Konrad Lehmann,Franziska Wieske,Christian A Hübner,Marcel Isstas,Jürgen Bolz,Lutz Liebmann,Christine Winter,Benjamin Thompson

doi:10.1371/journal.pone.0213616

Manuel Teichert, Konrad Lehmann + Show 7 more

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https://doi.org/10.1371/journal.pone.0213616

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Abstract

There is convincing evidence that the deprivation of one sense can lead to adaptive neuronal changes in spared primary sensory cortices. However, the repercussions of late-onset sensory deprivations on functionality of the remaining sensory cortices are poorly understood. Using repeated intrinsic signal imaging we investigated the effects of whisker or auditory deprivation (WD or AD, respectively) on responsiveness of the binocular primary visual cortex (V1) in fully adult mice. The binocular zone of mice is innervated by both eyes, with the contralateral eye always dominating V1 input over ipsilateral eye input, the normal ocular dominance (OD) ratio. Strikingly, we found that 3 days of WD or AD induced a transient shift of OD, which was mediated by a potentiation of V1 input through the ipsilateral eye. This cross-modal effect was accompanied by strengthening of layer 4 synapses in V1, required visual experience through the ipsilateral eye and was mediated by an increase of the excitation/inhibition ratio in V1. Finally, we demonstrate that both WD and AD induced a long-lasting improvement of visual performance. Our data provide evidence that the deprivation of a non-visual sensory modality cross-modally induces experience dependent V1 plasticity and improves visual behavior, even in adult mice.

Highlights

It has been demonstrated that the loss or deprivation of one sensory modality can have profound effects on the remaining senses
In the present study we investigated the cross-modal effects of whisker deprivation (WD) and auditory deprivation (AD) on visually evoked V1 responses and visually mediated behavior in fully adult mice
These results indicate that the late-onset loss of a non-visual sensory modality dramatically alters neuronal processing at different stages of the visual pathway of adult mice, which in turn improves visually dependent behavior

Summary

Introduction

It has been demonstrated that the loss or deprivation of one sensory modality can have profound effects on the remaining senses. Such changes are broadly referred to as “cross-modal plasticity” and can improve the functionality of the intact senses [1,2,3,4,5,6]. Earlier studies suggested that these compensatory enhancements arise because the deprived cortex becomes driven by the spared sensory modalities, broadly referred to as “cross-modal recruitment” [1, 2, 6, 7]. There is increasing evidence that functional improvements of the remaining senses can be attributed to rapid or long-term adaptive changes in the spared sensory cortices. We could recently show that auditory deprivation (AD) leads to a rapid

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