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

Abstract

Filtering out familiar, irrelevant stimuli eases the computational burden on the cerebral cortex. Inhibition is a candidate mechanism in this filtration process. Oscillations in the cortical local field potential (LFP) serve as markers of the engagement of different inhibitory neurons. In awake mice, we find pronounced changes in LFP oscillatory activity present in layer 4 of primary visual cortex (V1) with progressive stimulus familiarity. Over days of repeated stimulus presentation, low frequency (alpha/beta ∼15 Hz peak) power increases while high frequency (gamma ∼65 Hz peak) power decreases. This high frequency activity re-emerges when a novel stimulus is shown. Thus, high frequency power is a marker of novelty while low frequency power signifies familiarity. Two-photon imaging of neuronal activity reveals that parvalbumin-expressing inhibitory neurons disengage with familiar stimuli and reactivate to novelty, consistent with their known role in gamma oscillations, whereas somatostatin-expressing inhibitory neurons show opposing activity patterns, indicating a contribution to the emergence of lower frequency oscillations. We also reveal that stimulus familiarity and novelty have differential effects on oscillations and cell activity over a shorter timescale of seconds. Taken together with previous findings, we propose a model in which two interneuron circuits compete to drive familiarity or novelty encoding.

Layer-specific stimulations of parvalbumin-positive cortical interneurons in mice entrain brain rhythms to different frequencies

“…EEG and cortical LFP oscillatory activities are good readouts of cognitive processes (Ding et al, 2016; Bastos et al, 2020; Hayden et al, 2021) and vigilance states (Vyazovskiy et al, 2011). Therefore, we investigated how these signals were affected by our layer-specific optogenetic stimulation of PV neurons.…”

“…EEG and cortical LFP oscillatory activities are good readouts of cognitive processes (Ding et al, 2016;Bastos et al, 2020;Hayden et al, 2021) and vigilance states (Vyazovskiy et al, 2011).…”

Electrophysiological signatures of visual recognition memory across all layers of mouse V1

“…Indeed, recent findings indicate that SRP expressed as VEP potentiation in L4 is most parsimoniously explained by an experience-dependent reduction in inhibition mediated by PV+ interneurons in this layer (Kaplan et al, 2016;Hayden et al, 2021). Our aims in the current study were therefore to reexamine participation of excitatory neurons in the mechanisms of SRP, with a particular focus on L6 cells known to be a direct target of thalamocortical input, and to perform a laminar analysis of how SRP is expressed across all layers of V1.…”

“…First, pharmacological elimination of intracortical activity that spares TC synaptic transmission in L4 abolishes SRP expression (Cooke and Bear, 2014; Kaplan et al, 2016). Second, the activity of specific populations of GABAergic inhibitory neurons in V1 is modified with visual experience and significantly diverges for familiar and novel stimuli (Hayden et al, 2021). Third, SRP expression in L4 VEPs is disrupted by selective perturbations of activity in cortical parvalbumin-expressing (PV+) interneurons (Kaplan et al, 2016).…”

Functional and pharmacological analyses of visual habituation learning in larval zebrafish

“…Physiological and genetic work in Aplysia , and C. elegans were consistent with a model in which homosynaptic depression of excitatory synapses drives habituation ( Bailey and Chen, 1983 ; Rose et al, 2003 ) ( although see ( Glanzman, 2009 )). In contrast, work in the Drosophila olfactory and gustatory systems indicate that the potentiation of inhibitory neurons drives habituation rather than depression of excitatory connections ( Das et al, 2011 ; Paranjpe et al, 2012 ; Trisal et al, 2022 ), and habituation to specific orientations of visual cues in mice is associated with the potentiation of neuronal activity and synapses in the visual cortex ( Cooke et al, 2015 ), which requires GABAergic interneurons ( Kaplan et al, 2016 ; Hayden et al, 2021 ). These studies are more consistent with a model in which the potentiation of inhibition, rather than depression of excitation, drives habituation ( Cooke and Ramaswami, 2020 ).…”