Locomotion induces stimulus-specific response enhancement in adult visual cortex

Abstract

SUMMARYThe responses of neurons in the visual cortex (V1) of adult mammals have long been thought to be stable over long periods. Here, we investigated whether repeated exposure to specific stimuli would enhance V1 visual responses in mice using intrinsic signal imaging through the intact skull and two-photon imaging of calcium signals in single neurons. Mice ran on Styrofoam balls floating on air while viewing one of three different, high-contrast visual stimuli. V1 responses to the stimuli that were viewed by the animal were specifically enhanced, while responses to other stimuli were unaffected. Similar exposure in stationary mice, or in mice in which NMDA receptors were partially blocked, did not significantly enhance responses. These findings indicate that stimulus-specific plasticity in the adult visual cortex depends on concurrent locomotion, presumably as a result of the high-gain state of visual cortex induced by locomotion.Significance StatementWe report a rapid and persistent increase in visual cortical responses to visual stimuli presented during locomotion in intact mice. We first used a method that is completely non-invasive, intrinsic signal imaging through the intact skull. We then measured the same effects on single neurons using 2-photon calcium imaging and found that the increase in response to a particular stimulus produced by locomotion depends on how well the neuron is initially driven by the stimulus. To our knowledge, this is the first time such enhancement has been described in single neurons or using non-invasive measurements.

Experience-dependent structural plasticity at pre- and postsynaptic sites of layer 2/3 cells in developing visual cortex

“…Headplate and Cranial Window Implantation. For long-term visualization of neuronal morphology under a 2-photon microscope, animals at P22-25 (4 to 5 d before imaging) were implanted with a stainless headplate and a cranial window was made as previously described (54)(55)(56). Briefly, animals were anesthetized with isoflurane (3% induction; 1.5% surgery), and injected s.c. with atropine (0.15 mg/kg), dexamethasone (1.5 mg/kg), and carprofen (15 mg/kg).…”

Gamma rhythms and visual information in mouse V1 specifically modulated by somatostatin+ neurons in reticular thalamus

“…Locomotion increases both gamma power and visual responses in mouse V1, and gates a form of adult plasticity (Niell and Stryker, 2010;Kaneko and Stryker, 2014;Kaneko et al, 2017;Hoseini et al, 2019).…”

Three brain states in the hippocampus and cortex

“…Enhanced signal‐to‐noise ratios and other integrated measures of stimulus encoding have also been reported (Bennett et al, ; Dadarlat & Stryker, ; Erisken et al, ; McGinley, David, & McCormick, ; Polack et al, ; Poulet & Petersen, ; Reimer et al, ; Vinck et al, ; Zagha et al, ; Zhou et al, ). Importantly, the motor state and associated circuit mechanisms (e.g., Fu et al, ) have begun to be linked to functional consequences: for example, enhancement of performance on psychophysical tasks (Bennett et al, ) and enhancement of experience‐dependent plasticity (Fu, Kaneko, Tang, Alvarez‐Buylla, & Stryker, ; Kaneko, Fu, & Stryker, ; Kaneko & Stryker, ).…”