Activation of Specific Interneurons Improves V1 Feature Selectivity and Visual Perception

By Seung-Hee Lee, A. Kwan, Siyu Zhang, Victoria Phoumthipphavong, J. Flannery, S. Masmanidis, H. Taniguchi, Z. J. Huang, Ed Boyden, Karl Deisseroth and 1 more. Nature, 2012

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Inhibitory interneurons are essential components of the neural circuits underlying various brain functions. In the neocortex, a large diversity of GABA (γ-aminobutyric acid) interneurons has been identified on the basis of their morphology, molecular markers, biophysical properties and innervation pattern. However, how the activity of each subtype of interneurons contributes to sensory processing remains unclear. Here we show that optogenetic activation of parvalbumin-positive (PV+) interneurons in the mouse primary visual cortex (V1) sharpens neuronal feature selectivity and improves perceptual discrimination. Using multichannel recording with silicon probes and channelrhodopsin-2 (ChR2)-mediated optical activation, we found that increased spiking of PV+ interneurons markedly sharpened orientation tuning and enhanced direction selectivity of nearby neurons. These effects were caused by the activation of inhibitory neurons rather than a decreased spiking of excitatory neurons, as archaerhodopsin-3 (Arch)-mediated optical silencing of calcium/calmodulin-dependent protein kinase IIα (CAMKIIα)-positive excitatory neurons caused no significant change in V1 stimulus selectivity. Moreover, the improved selectivity specifically required PV+ neuron activation, as activating somatostatin or vasointestinal peptide interneurons had no significant effect. Notably, PV+ neuron activation in awake mice caused a significant improvement in their orientation discrimination, mirroring the sharpened V1 orientation tuning. Together, these results provide the first demonstration that visual coding and perception can be improved by increased spiking of a specific subtype of cortical inhibitory interneurons.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/74154b1d36ab5b9bad627f490be2a064f7a1e095

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Citations in the corpus

A cortical circuit for gain control by behavioral state (2014, background): “Furthermore, activating SST neurons also suppresses the visual response without changing OSI (Lee et al., 2012).”
Parvalbumin-expressing interneurons linearly control olfactory bulb output (2013, neutral): “…December 4, 2013 ª2013 Elsevier Inc. classes of inhibitory neurons have begun to shed light on how inhibitory neurons regulate cortical processing of sensory information (Adesnik et al., 2012; Atallah et al., 2012; Gentet et al., 2012; Lee et al., 2012; Sohal et al., 2009; Wilson et al., 2012).”
Fast-spiking, parvalbumin+ GABAergic interneurons: From cellular design to microcircuit function (2014, background): “In the primary visual cortex, activation or inactivation of PV interneurons changes the gain of orientation tuning curves in pyramidal neurons, whereas the width of these curves remains largely unchanged [(94, 95), but see (102)].”
Neural Elements for Predictive Coding (2016, background): “…of perception, Bayesian formulations of probabilistic representation and constructs borrowed from information theory and statistical physics (Helmholtz, 1860/1962; Gregory, 1980; Mumford, 1992; Dayan et al., 1995; Rao and Ballard, 1999; Lee and Mumford, 2003; Knill and Pouget, 2004; Friston, 2010).”
Neuromodulation of brain states. (2012, neutral): “, 2008; Fishell and Rudy, 2011), and they play different roles in sensory processing (Lee et al., 2012; Wilson et al., 2012).”