Journal Article

Synaptic organization of visual space in primary visual cortex

Iacaruso, M. Florencia, Gasler, Ioana T., Hofer, Sonja B.

2017

Overview

Mapping the organization of excitatory inputs onto the dendritic spines of individual mouse visual cortex neurons reveals how inputs representing features from the extended visual scene are organized and establishes a computational unit suited to amplify contours and elongated edges. Synapses set the scene Processing a visual stimulus requires various connections between neurons, with each encoding for particular features that integrate and generate the overall representation of a scene. The precise logic of this connectivity and what information an individual neuron receives regarding various parts of the visual field are unknown. Here, Sonja Hofer and colleagues mapped the organization of excitatory inputs onto the dendritic spines of individual mouse visual cortex neurons. Inputs representing similar visual features in similar visual field positions were more likely to cluster on neighbouring spines and inputs beyond the receptive field of the observed neuron were located on higher-order dendritic branches. Connections between neurons with dissimilar receptive fields were more likely when these fields were spatially displaced. These arrangements establish a computational unit suited to amplify contours and elongated edges, features that are common elements of our visual space. How a sensory stimulus is processed and perceived depends on the surrounding sensory scene. In the visual cortex, contextual signals can be conveyed by an extensive network of intra- and inter-areal excitatory connections that link neurons representing stimulus features separated in visual space 1 , 2 , 3 , 4 . However, the connectional logic of visual contextual inputs remains unknown; it is not clear what information individual neurons receive from different parts of the visual field, nor how this input relates to the visual features that a neuron encodes, defined by its spatial receptive field. Here we determine the organization of excitatory synaptic inputs responding to different locations in the visual scene by mapping spatial receptive fields in dendritic spines of mouse visual cortex neurons using two-photon calcium imaging. We find that neurons receive functionally diverse inputs from extended regions of visual space. Inputs representing similar visual features from the same location in visual space are more likely to cluster on neighbouring spines. Inputs from visual field regions beyond the receptive field of the postsynaptic neuron often synapse on higher-order dendritic branches. These putative long-range inputs are more frequent and more likely to share the preference for oriented edges with the postsynaptic neuron when the receptive field of the input is spatially displaced along the axis of the receptive field orientation of the postsynaptic neuron. Therefore, the connectivity between neurons with displaced receptive fields obeys a specific rule, whereby they connect preferentially when their receptive fields are co-oriented and co-axially aligned. This organization of synaptic connectivity is ideally suited for the amplification of elongated edges, which are enriched in the visual environment, and thus provides a potential substrate for contour integration and object grouping.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 14/35 / 631/378/2613/1875 / 631/378/3917 / 64/60 / Amplification / Analysis / Animals / Calcium imaging / Cell Shape / Dendritic spines / Dendritic Spines - physiology / Elongation / Female / Humanities and Social Sciences / letter / Male / Mice / Mice, Inbred C57BL / multidisciplinary / Neural networks / Neurobiology / Neuroimaging / Neurons / Orientation behavior / Physiological aspects / Receptive field / Science / Somatosensory cortex / Synapses / Synapses - physiology / Synaptic transmission / Visual cortex / Visual Cortex - cytology / Visual Cortex - physiology / Visual field / Visual fields / Visual Fields - physiology / Visual perception / Visual signals / Visual stimuli / Visual task performance