The segregation of figures from the background is an important step in visual perception. In primary visual cortex, figures evoke stronger activity than backgrounds during a delayed phase of the neuronal responses, but it is unknown how this figure-ground modulation (FGM) arises and whether it is necessary for perception. Here, we show, using optogenetic silencing in mice, that the delayed V1 response phase is necessary for figure-ground segregation. Neurons in higher visual areas also exhibit FGM and optogenetic silencing of higher areas reduced FGM in V1. In V1, figures elicited higher activity of vasoactive intestinal peptide–expressing (VIP) interneurons than the background, whereas figures suppressed somatostatin-positive interneurons, resulting in an increased activation of pyramidal cells. Optogenetic silencing of VIP neurons reduced FGM in V1, indicating that disinhibitory circuits contribute to FGM. Our results provide insight into how lower and higher areas of the visual cortex interact to shape visual perception.
The response of neurons to sensory stimuli depends on the context. In the mammalian primary visual cortex (V1), this is clear in the reduction in response to a stimulus when it is surrounded by a larger similar stimulus [1, 2, 3]. The source of this surround suppression is only partially known. In mouse, local horizontal integration by somatostatin-expressing inhibitory neurons contributes to surround suppression [4]. In primates, however, surround suppression in V1 arises too quickly to come from local horizontal integration alone, and myelinated axons from higher visual areas, where cells have larger receptive fields, are thought to provide additional surround suppression [5, 6]. Silencing higher visual areas indeed decreased surround suppression in the awake primate by increasing responses to large stimuli [7, 8], although results in anesthetized studies differ [9, 10]. In smaller mammals, like mice, fast surround suppression could be possible without involvement of feedback. Recent studies revealed a small reduction in V1 responses when higher visual areas were silenced [11, 12], but have Manuscript 2 not investigated surround suppression. To determine whether higher visual areas contribute to V1 surround suppression, even when this contribution is not necessary for fast visual processing, we inhibited the higher visual areas directly lateral to V1, in particular LM, a possible mouse homologue of primate V2 [13], while measuring neuronal activity in V1 of awake and anesthetized mice. We found that part of the surround suppression depends on activity from lateral visual areas in the awake, but not anesthetized, mouse. Inhibiting the lateral visual areas specifically increased responses in V1 to large stimuli. We present a model that explains how excitatory feedback to V1 can have these suppressive effects to large stimuli.
The representation of space in mouse visual cortex was thought to be relatively uniform. Here we reveal, using population receptive-field (pRF) mapping techniques, that mouse visual cortex contains a region in which pRFs are considerably smaller. This region, the “focea,” represents a location in space in front of, and slightly above, the mouse. Using two-photon imaging we show that the smaller pRFs are due to lower scatter of receptive-fields at the focea and an over-representation of binocular regions of space. We show that receptive-fields of single-neurons in areas LM and AL are smaller at the focea and that mice have improved visual resolution in this region of space. Furthermore, freely moving mice make compensatory eye-movements to hold this region in front of them. Our results indicate that mice have spatial biases in their visual processing, a finding that has important implications for the use of the mouse model of vision.
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