Top-down influence affects the response adaptation of V1 neurons in cats

Abstract The visual system lowers its perceptual sensitivity to a prolonged presentation of the same visual signal. This brain plasticity, called visual adaptation, is generally attributed to the response adaptation of neurons in the visual cortex. Although well-studied in the neurons of the primary visual cortex (V1), the contribution of high-level visual cortical regions to the response adaptation of V1 neurons is unclear. In the present study, we measured the response adaptation strength of V1 neurons before and after the top-down influence of the area 21a (A21a), a higher-order visual cortex homologous to the primate V4 area, was modulated with a noninvasive tool of transcranial direct current stimulation (tDCS). Our results showed that the response adaptation of V1 neurons enhanced significantly after applying anode (a-) tDCS in A21a when compared with that before a-tDCS, whereas the response adaptation of V1 neurons weakened after cathode (c-) tDCS relative to before c-tDCS in A21a. By contrast, sham (s-) tDCS in A21a had no significant impact on the response adaptation of V1 neurons. Further analysis indicated that a-tDCS in A21a significantly increased both the initial response (IR) of V1 neurons to the first several (five) trails of visual stimulation and the plateau response (PR) to the prolonged visual stimulation; the increase in PR was lower than in IR, which caused an enhancement in response adaptation. Conversely, c-tDCS significantly decreased both IR and PR of V1 neurons; the reduction in PR was smaller than in IR, which resulted in a weakness in response adaptation. Furthermore, the tDCS-induced changes of V1 neurons in response and response adaptation could recover after tDCS effect vanished, but did not occur after the neuronal activity in A21a was silenced by electrolytic lesions. These results suggest that the top-down influence of A21a may alter the response adaptation of V1 neurons through activation of local inhibitory circuitry, which enhances network inhibition in the V1 area upon an increased top-down input, weakens inhibition upon a decreased top-down input, and thus maintains homeostasis of V1 neurons in response to the long-presenting visual signals.