Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex

Abstract

Daily exposure of awake mice to a phase-reversing visual grating stimulus leads to enhancement of the visual-evoked potential (VEP) in layer 4 of the primary visual cortex (V1). This stimulus-selective response potentiation (SRP) resembles and shares mechanistic requirements with canonical long-term synaptic potentiation (LTP). However, it remains to be determined how this augmentation of a population response translates into altered neuronal activity of individual V1 neurons. To address this question, we performed longitudinal calcium imaging of layer 4 excitatory neurons in V1 and tracked changes associated with the induction and expression of SRP. We found no evidence for a net change in the fraction of visually responsive neurons as the stimulus became familiar. However, endoscopic calcium imaging of layer 4 principal neurons revealed that somatic calcium transients in response to phase-reversals of the familiar visual stimulus are reduced and undergo strong within-session adaptation. Conversely, neuropil calcium responses and VEPs are enhanced during familiar stimulus viewing, and the VEPs show reduced within-session adaptation. Consistent with the exquisite selectivity of SRP, the plasticity of cellular responses to phase-reversing gratings did not translate into altered orientation selectivity to drifting gratings. Our findings suggest a model in which augmentation of fast, short-latency synaptic (dendritic) responses, manifested as enhanced layer 4 VEPs, recruits inhibition to suppress cellular activity. Reduced cellular activity to the familiar stimulus may account for the behavioral correlate of SRP, orientation-selective long-term habituation.

Visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex

“…There is no discernable familiar-novel difference between VEPs elicited by the transition from a gray screen to an oriented grating 36 . This finding and others 8,9 suggest that the memory of stimulus familiarity is not simply encoded by enhanced monosynaptic thalamocortical transmission in layer 4.…”

“…Like other manifestations of SRP, these changes in LFP oscillations and interneuron activity are not subtle-they reflect dramatic shifts in the mode of visual information processing as a visual stimulus becomes familiar over days. Although stimulus recognition is not expressed immediately on the transition from a gray screen to a familiar stimulus 36 , it does emerge quickly as evidenced by the rapid increase in low-frequency LFP power. Together, these observations constrain the potential mechanisms that give rise to SRP and visual recognition memory.…”

“…VEPs and principal cell calcium transients elicited in layer 4 by the transition from gray screen to an oriented grating stimulus are the same for both familiar and novel stimulil 36 . The robust familiar-novel differences observed in time-averaged VEPs and cellular responses emerge during the course of a block of stimulation.…”

“…Gamma oscillations additionally contribute to learning and memory processes in visual cortex 63,64 and maximize information acquisition 65 , consistent with our observations that these are at their peak during the initial exposure to a visual stimulus that will result in experience-dependent plasticity. It is noteworthy that although novel stimuli elicit smaller VEPs than familiar stimuli, calcium imaging of layer 4 principal neurons reveals much stronger responses to novel orientations than to familiar 36 . These calcium signals reflect changes in sustained activity of layer 4 neurons, as they do not report the augmentation in peak spiking rates that occur with each phase reversal of a familiar stimulus 3,7,66 .…”

Visual Sequences Drive Experience-Dependent Plasticity in Mouse Anterior Cingulate Cortex

“…These approaches will also enable future categorization of neurons by location, cell type, and firing properties. However, one of the advantages of VEPs and unit recordings, relative to calcium imaging, is that they have faster kinetics and are better suited to measure small changes in timing ( Chen et al, 2013 ; Kim et al, 2020 ).…”