Abstract
SummaryTo interpret visual-motion events, the underlying computation must involve internal reference to the motion status of the observer’s head. We show here that layer 6 (L6) principal neurons in mouse primary visual cortex (V1) receive a diffuse, vestibular-mediated synaptic input that signals the angular velocity of horizontal rotation. Behavioral and theoretical experiments indicate that these inputs, distributed over a network of 100 L6 neurons, provide both a reliable estimate and, therefore, physiological separation of head-velocity signals. During head rotation in the presence of visual stimuli, L6 neurons exhibit postsynaptic responses that approximate the arithmetic sum of the vestibular and visual-motion response. Functional input mapping reveals that these internal motion signals arrive into L6 via a direct projection from the retrosplenial cortex. We therefore propose that visual-motion processing in V1 L6 is multisensory and contextually dependent on the motion status of the animal’s head.
Highlights
Throughout the visual system, the activity of individual neurons signals specific features of object motion (Barlow and Levick, 1965; Dra€ger, 1975; Hubel, 1960; Hubel and Wiesel, 1959, 1968; Niell, 2015; Van Essen and Gallant, 1994)
Using a dense silicon probe that enables us to record simultaneously across all cortical layers (Jun et al, 2017), we found that well-isolated units (n = 28 units, n = 3 mice) located in layers 5 (L5) and 6 were most likely to show rotation-evoked activity (L5, 2/7; layer 6 (L6), 9/14; compared to L4, n = 1/7, significance threshold p = 0.05, Wilcoxon signed-rank test; Figure 1A)
In line with the extracellular data, while rotation-evoked action potential activity was not observed in L2/3 regular spiking neurons (L2/3, 0/8, significance threshold p = 0.05, Wilcoxon signed-rank test), responses were observed in deep-layer principal cells (L5, 2/5 cells; L6, 9/16 cells; significance threshold p = 0.05, Wilcoxon signed-rank test)
Summary
Throughout the visual system, the activity of individual neurons signals specific features of object motion (Barlow and Levick, 1965; Dra€ger, 1975; Hubel, 1960; Hubel and Wiesel, 1959, 1968; Niell, 2015; Van Essen and Gallant, 1994). To detect the motion trajectory and speed of an object in the external world, visual stimuli must be placed within a context that includes information regarding the motion status of the observer This integrative process is fundamental, since it underlies judgments of spatiotemporal coincidence (Hoy et al, 2016), including the distance (Barlow et al, 1967), direction (Hubel and Wiesel, 1959, 1968), and speed (Roth et al, 2012; Van Essen and Gallant, 1994) of potential animate activity (Grossman and Blake, 2002) that may indicate the presence of a threat, food source, or conspecific. While the involvement of vestibular signaling in limbic regions known to contribute to spatial processing is well described, the extent to which this internal signal is involved in primary sensory cortical representation is not known
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