Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Synaptic Organization of Visual Space in Primary Visual Cortex

 

Nature† 547, 449Ė452 (27 July 2017)

Synaptic organization of visual space in primary visual cortex

M. Florencia Iacaruso, et.al.

Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.

Biozentrum, University of Basel, Klingelbergstrasse 50/70, CH-4056 Basel, Switzerland

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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. 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.

Understanding the mechanisms of sensory processing requires uncovering the precise relationship between synaptic connectivity and function of neurons in cortical circuits. Local connectivity between neurons follows certain rules. For example, neighbouring layer (L)2/3 pyramidal neurons in rodent visual cortex preferentially connect if they receive common synaptic input or if they respond to similar stimulus features within their receptive fields (RFs). However, the rules of long-range synaptic connectivity remain poorly understood. A substantial fraction of the synaptic inputs a cortical neuron receives originate outside its local network and, in sensory cortices, many inputs stem from neurons representing distant topographic positions. Long-range lateral projections in cat and primate primary visual cortex (V1) preferentially (but not exclusively) link orientation columns with similar preferences, and in some species these extend along the axis of the retinotopic map that corresponds to their preferred stimulus orientation. While these studies reveal a degree of functional specificity of long-range projections, at least in animals with cortical columns, it is still unclear what repertoire of visual information a single neuron receives from the extended visual scene, and how this visual input relates to a neuronís preference for particular visual features. This knowledge is important for uncovering the circuit mechanisms of contextual processing and related perceptual Gestalt phenomena, such as integration of contours and object grouping in the visual environment.

To determine the visual response properties of synaptic inputs onto neurons in mouse primary visual cortex (V1) we used two-photon imaging of calcium signals in dendritic spines on L2/3 pyramidal cells sparsely expressing the genetically encoded calcium indicator GCaMP6s. Using sparse noise stimuli, we mapped the structure of spatial RFs on the basis of calcium signals observed in individual dendritic spines and nearby dendritic stretches.

In this study we show that individual L2/3 pyramidal cells in mouse visual cortex receive diverse excitatory inputs encoding distinct visual features from an expansive area of the visual field. Inputs representing similar visual features from overlapping locations in visual space were more likely to terminate on nearby spines, consistent with the idea that co-active inputs cluster on dendritic branches. Neighbouring inputs might cooperate to generate nonlinear dendritic events that contribute to a neuronís output. On average, synaptic input was functionally biased for the stimulus orientation preferred by the postsynaptic neuron, consistent with previous work. However, retinotopically displaced inputs provided specific contextual information, whereby neurons representing the same orientations preferentially connected if their RFs were separated along the axis of their preferred orientation. Our results are in keeping with predictions of studies in visual cortex of higher mammals, which revealed an anisotropic spread of axonal projections and correlated firing of L5 and L6 neurons with overlapping RFs and matched orientation preference, but which could not determine the functional identity of inputs received by individual neurons.

Potential sources of input from regions of visual space outside a neuronís RF include lateral axonal connections within V1, as well as projections from the thalamus or feedback from higher visual areas. Irrespective of the sources of retinotopically displaced inputs, the preferential connectivity between neurons with co-linearly aligned RFs may arise via activity-dependent mechanisms of synaptic plasticity driven by the exposure to extended contours in the visual environment. Indeed, the composition of retinotopically displaced inputs reflects the long-range image statistics of natural scenes, in which co-linearly aligned edges are enriched. Thus the patterns of synaptic connectivity may store the history of correlated firing of feature detectors in primary visual cortex.

Neurons with co-axially aligned and orientation-matched RFs would be co-activated by contours or edges extending in visual space, and may thus contribute to the facilitation of V1 responses by collinearly arranged line segments. This specific organization of long-range connectivity, in combination with feedback from other cortical areas, provides a plausible circuit substrate for perceptual phenomena such as edge detection, visual contour integration and object grouping.

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