Biology subjects

Leonard, E. S. P.

Publications and source records attributed to Leonard, E. S. P..

3 recordsLinked to original sources

bioRxiv2022

A dynamic sequence of visual processing initiated by gaze shifts

Animals move their head and eyes as they explore and sample the visual scene. Previous studies have demonstrated neural correlates of head and eye movements in rodent primary visual cortex (V1), but the sources and computational roles of these signals are unclear. We addressed this by combining measurement of head and eye movements with high density neural recordings in freely moving mice. V1 neurons responded primarily to gaze shifts, where head movements are accompanied by saccadic eye movements, but not to head movements where compensatory eye movements stabilize gaze. A variety of activity patterns immediately followed gaze shifts, including units with positive, biphasic, or negative responses, and together these responses formed a temporal sequence following the gaze shift. These responses were greatly diminished in the dark for the vast majority of units, replaced by a uniform suppression of activity, and were similar to those evoked by sequentially flashed stimuli in head-fixed conditions, suggesting that gaze shift transients represent the temporal response to the rapid onset of new visual input. Notably, neurons responded in a sequence that matches their spatial frequency preference, from low to high spatial frequency tuning, consistent with coarse-to-fine processing of the visual scene following each gaze shift. Recordings in foveal V1 of freely gazing head-fixed marmosets revealed a similar sequence of temporal response following a saccade, as well as the progression of spatial frequency tuning. Together, our results demonstrate that active vision in both mice and marmosets consists of a dynamic temporal sequence of neural activity associated with visual sampling. HighlightsO_LIDuring free movement, neurons in mouse V1 respond to head movements that are accompanied by a gaze-shifting saccadic eye movement, but not a compensatory eye movement. C_LIO_LINeurons respond to gaze shifts with diverse temporal dynamics that form a sequence across the population, from early positive responses to biphasic and negative responses. C_LIO_LIIn darkness, most neurons show a uniform suppression following a gaze shift. C_LIO_LITemporal dynamics of responses correspond to a neurons temporal and spatial frequency preferences, consistent with a coarse-to-fine processing sequence. C_LIO_LIA similar temporal sequence following saccades is observed in foveal V1 of freely gazing head-fixed marmosets, demonstrating shared aspects of active visual processing across species. C_LI

neuroscience↗

bioRxiv2022

Joint coding of visual input and eye/head position in V1 of freely moving mice

SUMMARYVisual input to the brain during natural behavior is highly dependent on movements of the eyes, head, and body. Neurons in mouse primary visual cortex (V1) respond to eye and head movements, but how information about eye and head position is integrated with visual processing during free movement is unknown, since visual physiology is generally performed under head-fixation. To address this, we performed single-unit electrophysiology in V1 of freely moving mice while simultaneously measuring the mouses eye position, head orientation, and the visual scene from the mouses perspective. Based on these measures we were able to map spatiotemporal receptive fields during free movement, using a generalized linear model (GLM) that predicted the activity of V1 neurons based on gaze-corrected visual input. Furthermore, we found that a significant fraction of visually-responsive neurons showed tuning for eye position and head orientation. Incorporating these variables into the GLM revealed that visual and positional signals are integrated through a multiplicative mechanism in the majority of modulated neurons, consistent with computation via gain fields and nonlinear mixed selectivity. These results provide new insight into coding in mouse V1, and more generally provide a paradigm for performing visual physiology under natural conditions, including active sensing and ethological behavior. HIGHLIGHTSO_LINeurons in mouse V1 respond to both vision and self-motion, but it is unclear how these are combined. C_LIO_LIWe record neural activity in V1 concurrent with measurement of the visual input from the mouses perspective during free movement. C_LIO_LIThese data provide the first measurement of visual receptive fields in freely moving animals. C_LIO_LIWe show that many V1 neurons are tuned to eye position and head orientation, and these contribute a multiplicative gain on visual responses in the majority of modulated neurons. C_LI

neuroscience↗

bioRxiv2021

Distance estimation from monocular cues in an ethological visuomotor task

In natural contexts, sensory processing and motor output are closely coupled, which is reflected in the fact that many brain areas contain both sensory and movement signals. However, standard reductionist paradigms decouple sensory decisions from their natural motor consequences, and head-fixation prevents the natural sensory consequences of self-motion. In particular, movement through the environment provides a number of depth cues beyond stereo vision that are poorly understood. To study the integration of visual processing and motor output in a naturalistic task, we investigated distance estimation in freely moving mice. We found that mice use vision to accurately jump across a variable gap, thus directly coupling a visual computation to its corresponding ethological motor output. Monocular eyelid suture did not affect gap jumping success, thus mice can use cues that do not depend on binocular disparity and stereo vision. Under monocular conditions, mice altered their head positioning and performed more vertical head movements, consistent with a shift from using stereopsis to other monocular cues, such as motion or position parallax. Finally, optogenetic suppression of primary visual cortex impaired task performance under both binocular and monocular conditions when optical fiber placement was localized to binocular or monocular zone V1, respectively. Together, these results show that mice can use monocular cues, relying on visual cortex, to accurately judge distance. Furthermore, this behavioral paradigm provides a foundation for studying how neural circuits convert sensory information into ethological motor output.

neuroscience↗