Segregated encoding of spatiotemporal features in the mouse visual cortex

Abstract

Visual processing and behavior depend on specialized neural representations and information channels that encode distinct visual information and enable distinct computations. Our understanding of the neural substrate, however, remain severely limited by sparse recordings and the restricted range of visual areas and visual stimuli considered. We characterized in the mouse the multidimensional spatiotemporal tuning properties of > 30,000 layer 2/3 pyramidal neurons across seven areas of the cortex. The dataset reveals population specialized for processing of oriented and non-oriented contrast, spatiotemporal frequency, and motion speed. Areal analysis reveals profound functional diversity and specificity as well as highly specific representations of visual processing channels in distinct visual areas. Clustering analysis shows a branching of visual representations along the posterior to anterior axis, and between lateral and dorsal areas. Overall, this dataset provides a cellular-resolution atlas for understanding organizing principles underlying sensory representations across the cortex. SummaryVisual representations and visual channels are the cornerstones of mammalian visual processing and critical for a range of life sustaining behaviors. However, the lack of data sets spanning multiple visual areas preclude unambiguous identification of visual processing streams and the sparse, singular recording data sets obtained thus far are insufficient to reveal the functional diversity of visual areas and to study visual information channels. We characterized the tunings of over 30,000 cortical excitatory neurons from 7 visual areas to a broad array of stimuli and studied their responses in terms of their ability to encode orientation, spatiotemporal contrast and visual motion speed. We found all mouse visual cortical areas convey diverse information but show distinct biases in terms of numbers of neurons tuned to particular spatiotemporal features. Neurons in visual areas differ in their spatiotemporal tuning but also in their relative response to oriented and unoriented contrast. We uncovered a population that preferentially responds to unoriented contrast and shows only weak responses to oriented stimuli. This population is strongly overrepresented in certain areas (V1, LM and LI) and underrepresented in others (AL, RL, AM, and PM). Spatiotemporal tunings are broadly distributed in all visual areas indicating that all areas have access to broad spatiotemporal information. However, individual areas show specific biases. While V1 is heavily biased in favor of low spatial and temporal frequencies, area LM responds more strongly to mid-range frequencies. Areas PM and LI are biased in favor of slowly-varying high-resolution signals. By comparison, anterior areas AL, RL and AM are heavily biased in favor of fast-varying, low to mid spatial frequency signals. Critically, theses biases express themselves in vastly different number of cells tuned to particular features, suggesting differential sampling of visual processing channels across areas. Comparing across areas, we found divergent visual representations between anterior and posterior areas, and between lateral and dorsal areas, suggesting the segregated organization of cortical streams for distinct information processing.