V1-Origin Bidirectional Plasticity in Visual Thalamo-Ventral Pathway and Its Contribution to Saliency Detection of Dynamic Visual Inputs

J Neurosci. 2022 Aug 17;42(33):6359-6379. doi: 10.1523/JNEUROSCI.0539-22.2022.

Abstract

Visual neural plasticity and V1 saliency detection are vital for efficient coding of dynamically changing visual inputs. However, how does neural plasticity contribute to saliency detection of temporal statistically distributed visual stream remains unclear. Therefore, we adopted randomly presented but unevenly distributed stimuli with multiple orientations and examined the single-unit responses evoked by this biased orientation-adaptation protocol by single-unit recordings in the visual thalamo-ventral pathway of cats (of either sex). We found neuronal responses potentiated when the probability of biased orientation was slightly higher than other nonbiased ones and suppressed when the probability became much higher. This single neuronal short-term bidirectional plasticity is selectively induced by optimal stimuli but is interocularly transferable. It is inducible in LGN, Area 17, and Area 21a with distinct and hierarchically progressive patterns. With the results of latency analysis, receptive field structural test, cortical lesion, and simulations, we suggest this bidirectional plasticity may principally originate from the adaptation competition between excitatory and inhibitory components of V1 neuronal receptive field. In our simulation, above bidirectional plasticity could achieve saliency detection of dynamic visual inputs. These findings demonstrate a rapid probability dependent plasticity on the neural coding of visual stream and suggest its functional role in the efficient coding and saliency detection of dynamic environment.SIGNIFICANCE STATEMENT Novel elements within a dynamic visual stream can pop up from the context, which is vital for rapid response to a dynamically changing world. Saliency detection is a promising bottom-up mechanism contributing to efficient selection of visual inputs, wherein visual adaptation also plays a significant role. However, the saliency detection of dynamic visual stream is poorly understood. Here, we found a novel form of visual short-term bidirectional plasticity in multistages of the visual system that contributes to saliency detection of dynamic visual inputs. This bidirectional plasticity may principally originate from the local balance of excitation inhibition in primary visual cortex and propagates to lower and higher visual areas with progressive pattern change. Our findings suggest the excitation-inhibition balance within the visual system contributes to visual efficient coding.

Keywords: Area 21a; LGN; plasticity; primary visual cortex; saliency detection; visual adaptation.