Abstract

Neurons in the primary visual cortex receive subliminal information originating from the periphery of their receptive fields (RF) through a variety of cortical connections. In the cat primary visual cortex, long-range horizontal axons have been reported to preferentially bind to distant columns of similar orientation preferences, whereas feedback connections from higher visual areas provide a more diverse functional input. To understand the role of these lateral interactions, it is crucial to characterize their effective functional connectivity and tuning properties. However, the overall functional impact of cortical lateral connections, whatever their anatomical origin, is unknown since it has never been directly characterized. Using direct measurements of postsynaptic integration in cat areas 17 and 18, we performed multi-scale assessments of the functional impact of visually driven lateral networks. Voltage-sensitive dye imaging showed that local oriented stimuli evoke an orientation-selective activity that remains confined to the cortical feedforward imprint of the stimulus. Beyond a distance of one hypercolumn, the lateral spread of cortical activity gradually lost its orientation preference approximated as an exponential with a space constant of about 1 mm. Intracellular recordings showed that this loss of orientation selectivity arises from the diversity of converging synaptic input patterns originating from outside the classical RF. In contrast, when the stimulus size was increased, we observed orientation-selective spread of activation beyond the feedforward imprint. We conclude that stimulus-induced cooperativity enhances the long-range orientation-selective spread.

Highlights

  • Glutamate and dopamine (DA) receptor interactions are vital to numerous functions including learning and memory, motor coordination, and reward mechanisms (Calabresi et al, 2000; Surmeier et al, 2007; Schultz, 2010)

  • Using D1 and D2 receptor EGFP-expressing mice, we demonstrate that NR2A subunits contribute more to NMDA responses in D1-medium-sized spiny neurons (MSSNs), whereas NR2B subunits contribute more to NMDA responses in D2 cells

  • Because synaptic inputs are mostly eliminated in dissociated MSSNs, these results suggest that either the NR2A subunit does not contribute significantly to mostly extrasynaptic NMDA receptors, or that compensatory effects result from genetic ablation of this subunit

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Summary

Introduction

Glutamate and dopamine (DA) receptor interactions are vital to numerous functions including learning and memory, motor coordination, and reward mechanisms (Calabresi et al, 2000; Surmeier et al, 2007; Schultz, 2010) When dysfunctional, these receptor interactions contribute to the manifestation of psychiatric and neurodegenerative disorders (Andre et al, 2010b). Modulation can occur through a variety of mechanisms including multiple transduction pathways, voltage-gated Ca2+ channels, receptor subunit phosphorylation and mobilization, changes in receptor surface expression, and direct protein–protein coupling (Cepeda et al, 1998; Snyder et al, 1998; Lee et al, 2002; Surmeier et al, 2007; Pascoli et al, 2011)

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