Dynamic Recruitment of the Feedforward and Recurrent Mechanism for Black–White Asymmetry in the Primary Visual Cortex

Abstract

Black and white information is asymmetrically distributed in natural scenes, evokes asymmetric neuronal responses, and causes asymmetric perceptions. Recognizing the universality and essentiality of black–white asymmetry in visual information processing, the neural substrates for black–white asymmetry remain unclear. To disentangle the role of the feedforward and recurrent mechanisms in the generation of cortical black–white asymmetry, we recorded the V1 laminar responses and LGN responses of anesthetized cats of both sexes. In a cortical column, we found that black–white asymmetry starts at the input layer and becomes more pronounced in the output layer. We also found distinct dynamics of black–white asymmetry between the output layer and the input layer. Specifically, black responses dominate in all layers after stimulus onset. After stimulus offset, black and white responses are balanced in the input layer, but black responses still dominate in the output layer. Compared with that in the input layer, the rebound response in the output layer is significantly suppressed. The relative suppression strength evoked by white stimuli is notably stronger and depends on the location within the ON-OFF cortical map. A model with delayed and polarity-selective cortical suppression explains black–white asymmetry in the output layer, within which prominent recurrent connections are identified by Granger causality analysis. In addition to black–white asymmetry in response strength, the interlaminar differences in spatial receptive field varied dynamically. Our findings suggest that the feedforward and recurrent mechanisms are dynamically recruited for the generation of black–white asymmetry in V1.SIGNIFICANCE STATEMENTBlack–white asymmetry is universal and essential in visual information processing, yet the neural substrates for cortical black–white asymmetry remain unknown. Leveraging V1 laminar recordings, we provided the first laminar pattern of black–white asymmetry in cat V1 and found distinct dynamics of black–white asymmetry between the output layer and the input layer. Comparing black–white asymmetry across three visual hierarchies, the LGN, V1 input layer, and V1 output layer, we demonstrated that the feedforward and recurrent mechanisms are dynamically recruited for the generation of cortical black–white asymmetry. Our findings not only enhance our understanding of laminar processing within a cortical column but also elucidate how feedforward connections and recurrent connections interact to shape neuronal response properties.