Specific excitatory connectivity for feature integration in mouse primary visual cortex

PLoS Comput Biol. 2017 Dec 14;13(12):e1005888. doi: 10.1371/journal.pcbi.1005888. eCollection 2017 Dec.

Abstract

Local excitatory connections in mouse primary visual cortex (V1) are stronger and more prevalent between neurons that share similar functional response features. However, the details of how functional rules for local connectivity shape neuronal responses in V1 remain unknown. We hypothesised that complex responses to visual stimuli may arise as a consequence of rules for selective excitatory connectivity within the local network in the superficial layers of mouse V1. In mouse V1 many neurons respond to overlapping grating stimuli (plaid stimuli) with highly selective and facilitatory responses, which are not simply predicted by responses to single gratings presented alone. This complexity is surprising, since excitatory neurons in V1 are considered to be mainly tuned to single preferred orientations. Here we examined the consequences for visual processing of two alternative connectivity schemes: in the first case, local connections are aligned with visual properties inherited from feedforward input (a 'like-to-like' scheme specifically connecting neurons that share similar preferred orientations); in the second case, local connections group neurons into excitatory subnetworks that combine and amplify multiple feedforward visual properties (a 'feature binding' scheme). By comparing predictions from large scale computational models with in vivo recordings of visual representations in mouse V1, we found that responses to plaid stimuli were best explained by assuming feature binding connectivity. Unlike under the like-to-like scheme, selective amplification within feature-binding excitatory subnetworks replicated experimentally observed facilitatory responses to plaid stimuli; explained selective plaid responses not predicted by grating selectivity; and was consistent with broad anatomical selectivity observed in mouse V1. Our results show that visual feature binding can occur through local recurrent mechanisms without requiring feedforward convergence, and that such a mechanism is consistent with visual responses and cortical anatomy in mouse V1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium Signaling / physiology
  • Computational Biology
  • Female
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Models, Neurological*
  • Nerve Net / physiology
  • Neurons / physiology
  • Orientation / physiology
  • Photic Stimulation
  • Synapses / physiology
  • Visual Cortex / cytology
  • Visual Cortex / physiology*
  • Visual Pathways / cytology
  • Visual Pathways / physiology
  • Visual Perception / physiology

Grants and funding

This work was supported by the Velux Stiftung (grant number 787 to DRM); the Novartis Foundation (grants to DRM and BMK); the Swiss National Science Foundation (grant number 31–120480 to BMK); the European Commission FP7 program (grant BrainScales 269921 to FH and BMK); and by the Convergent Science Network (fellowships to DRM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.