Date Published: March 11, 2019
Publisher: Public Library of Science
Author(s): Manuel Teichert, Marcel Isstas, Lutz Liebmann, Christian A. Hübner, Franziska Wieske, Christine Winter, Konrad Lehmann, Jürgen Bolz, Benjamin Thompson.
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.
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 [1–6]. 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]. However, there is increasing evidence that functional improvements of the remaining senses can be also attributed to rapid or long-term adaptive changes in the spared sensory cortices. For instance, we could recently show that auditory deprivation (AD) leads to a rapid increase of visually evoked responses in the spared V1 which was accompanied by improvements of V1 spatial frequency and contrast tuning [4, 8]. While these changes appeared most likely due to a rapid disinhibitory effect , previous studies demonstrated that more prolonged sensory deprivations lead to plastic alterations in spared primary sensory cortices . For example, a few days of visual deprivation in juvenile mice selectively strengthened layer 4-2/3 synapses in the somatosensory barrel cortex and sharpened the functional whisker-barrel map in layers 2/3 . Similarly, one week of visual deprivation was shown to strengthen thalamo-cortical synapses in the spared primary auditory cortex (A1) of juvenile but also adult mice . These plastic changes were accompanied by increased contrast sensitivity and frequency tuning of A1 neurons . Moreover, in a recent study we could demonstrate that one to two weeks of whisker deprivation (WD) in fully adult mice massively enhanced spatial frequency and contrast tuning of the primary visual cortex (V1) and even markedly improved visually driven behavior . These studies suggest that the ability of sensory cortices to undergo cross-modal plasticity is not restricted to sensory critical periods of early postnatal development, but can also take place in adults, although cortical plasticity levels decline with aging [11–13].
In the present study we investigated the cross-modal effects of WD and AD on visually evoked V1 responses and visually mediated behavior in fully adult mice. Strikingly, we found that both WD and AD transiently shifted the OD in V1 towards the input through the ipsilateral eye. These changes required patterned vision through the ipsilateral eye and were accompanied by an increase of the E/I ratio in V1, suggesting a cross-modal restoration of V1 plasticity. Moreover, the observed changes in V1 activity partially mediated potentiation of the OKR, a visual behavior predominantly mediated by subcortical structures. 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.