Journal Article

Activation of specific interneurons improves V1 feature selectivity and visual perception

Masmanidis, Sotiris C., Phoumthipphavong, Victoria, Lee, Seung-Hee, Deisseroth, Karl, Boyden, Edward S., Huang, Z. Josh, Taniguchi, Hiroki, Dan, Yang, Kwan, Alex C., Flannery, John G., Zhang, Siyu, Zhang, Feng

2012

Overview

Optogenetic activation of parvalbumin-expressing versus other classes of interneurons is found to have distinct effects on the response properties of individual and populations of excitatory cells, as well as on visual behaviour in awake mice, providing evidence that this specific interneuron subtype has a unique role in visual coding and perception. Class distinction in cortical interneurons Cortical networks consist of a range of neuronal cells, including multiple classes of inhibitory interneurons. Intracortical inhibition is essential for normal brain function, but little is known about the specific roles of the neuronal subtypes. Two independent papers from the groups of Mriganka Sur and Yang Dan explore the functional consequences of activating different classes of interneurons in the mouse visual cortex. Using a variety of techniques, both papers demonstrate that activating parvalbumin-expressing versus other classes of interneurons has distinct effects on the response properties of individual excitatory cells, as well as on populations of these cells. The paper from Dan's group also finds effects on visual behaviour in awake mice. 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 1 , 2 , 3 . 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 4 , 5 and channelrhodopsin-2 (ChR2)-mediated optical activation 6 , 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 7 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.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/378/1697 / 631/378/2649/1723 / 631/378/87 / Animals / Biological and medical sciences / Calcium-Calmodulin-Dependent Protein Kinase Type 2 - deficiency / Calcium-Calmodulin-Dependent Protein Kinase Type 2 - genetics / Calcium-Calmodulin-Dependent Protein Kinase Type 2 - metabolism / Channelrhodopsins / Discrimination Learning / Eye and associated structures. Visual pathways and centers. Vision / Fundamental and applied biological sciences. Psychology / gamma-Aminobutyric Acid - metabolism / Humanities and Social Sciences / Interneurons - physiology / Kinases / Lasers / letter / Methods / Mice / Models, Neurological / multidisciplinary / Neural Inhibition - physiology / Neurons / Parvalbumins - metabolism / Physiological aspects / Rhodopsins, Microbial - metabolism / Science / Science (multidisciplinary) / Vertebrates: nervous system and sense organs / Visual cortex / Visual Cortex - cytology / Visual Cortex - physiology / Visual perception / Visual Perception - physiology / Wakefulness - physiology