Locomotion Induces Stimulus-Specific Response Enhancement in Adult Visual Cortex

Abstract

The 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 the visual cortex induced by locomotion. We 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 noninvasive to image intrinsic signals through the intact skull. We then measured the same effects on single neurons using two-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 noninvasive measurements.

Action and learning shape the activity of neuronal circuits in the visual cortex

“…Initially the mice would respond to novel gratings with fidget-like movements of the forepaws, but these movements habituated in a stimulus-specific manner and over the same time course as the potentiation of V1 responses [ 30 ]. Another study using intrinsic signal imaging and chronic two-photon calcium imaging in anaesthetised animals also showed a stimulus-specific increase in the responses of layer 2/3 neurons to a daily presented stimulus [ 31 ]. However, this effect was only observed in mice that had been running for a cumulative time of at least one hour during the stimulus presentations across days [ 31 ].…”

Regulation of expression site and generalizability of experience-dependent plasticity in visual cortex

“…The loss of SRP in layer 4 is interesting, but not unexpected, as LRx induces an increase in the activity of the extracellular protease MMP9 at thalamo-cortical synapses and is proposed to decrease feedforward excitation to cortical layer 4 (Murase et al, 2017). SRP, although typically absent in superficial layers, is also observed in supragranular cortical layers following the enhancement of plasticity in primary visual cortex by locomotion (Kaneko et al, 2017). The locus of expression as well as the generalizability of response potentiation is regulated by the temporal frequency of repetitive visual stimulation, as HFVS induces a non-selective potentiation of VEP amplitudes in layers 4 and 5/6.…”

Pull-Push Neuromodulation of Cortical Plasticity Enables Rapid Bi-Directional Shifts in Ocular Dominance

“…Several other non-invasive manipulations have been reported to enhance adult cortical plasticity after the critical period, but through other mechanisms. For example, dark exposure (He et al, 2007), environmental enrichment (Sale et al, 2007), antidepressant treatments (Maya Vetencourt et al, 2008), locomotion (Kaneko et al, 2017), and retinal inactivation (Duffy et al, 2018), are thought to rejuvenate cortical plasticity by decreasing the intracortical inhibition, while cross-modal deprivation is thought to reactivate thalamocortical plasticity (Rodríguez et al, 2018;Teichert et al, 2019). It would be of therapeutical interest to explore complementary synergies between these manipulations and the neuromodulatory pairings in the recovery from long-term monocular deprivation.…”