Stimulus-Selective Response Plasticity in Primary Visual Cortex: Progress and Puzzles

Abstract

Stimulus-selective response plasticity (SRP) is a robust and lasting modification of primary visual cortex (V1) that occurs in response to exposure to novel visual stimuli. It is readily observed as a pronounced increase in the magnitude of visual evoked potentials (VEPs) recorded in response to phase-reversing grating stimuli in neocortical layer 4. The expression of SRP at the individual neuron level is equally robust, but the qualities vary depending on the neuronal type and how activity is measured. This form of plasticity is highly selective for stimulus features such as stimulus orientation, spatial frequency, and contrast. Several key insights into the significance and underlying mechanisms of SRP have recently been made. First, it occurs concomitantly and shares core mechanisms with behavioral habituation, indicating that SRP reflects the formation of long-term familiarity that can support recognition of innocuous stimuli. Second, SRP does not manifest within a recording session but only emerges after an off-line period of several hours that includes sleep. Third, SRP requires not only canonical molecular mechanisms of Hebbian synaptic plasticity within V1, but also the opposing engagement of two key subclasses of cortical inhibitory neuron: the parvalbumin- and somatostatin-expressing GABAergic interneurons. Fourth, pronounced shifts in the power of cortical oscillations from high frequency (gamma) to low frequency (alpha/beta) oscillations provide respective readouts of the engagement of these inhibitory neuronal subtypes following familiarization. In this article we will discuss the implications of these findings and the outstanding questions that remain to gain a deeper understanding of this striking form of experience-dependent plasticity.

Efficient Temporal Coding in the Early Visual System: Existing Evidence and Future Directions

“…Many related studies have shown evidence for cortical novelty responses across brain regions, with wide variation in the effort to control for adaptation ( Kato et al, 2015 ; Makino and Komiyama, 2015 ; Garrett et al, 2020 ; Poort et al, 2021 ; Schulz et al, 2021 ; Homann et al, 2022 ; Montgomery et al, 2022 ). In most cases, consistent with efficient coding, novel stimuli evoke more spiking activity than familiar.…”

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

“…Despite abundant evidence supporting the hypothesis that potentiation of thalamocortical synapses is the molecular basis for SRP (Frenkel et al, 2006;Cooke and Bear, 2010), it is now very clear that this does not occur on excitatory neurons in L4 (Montgomery et al, 2021).…”

“…Despite abundant evidence supporting the hypothesis that potentiation of thalamocortical synapses is the molecular basis for SRP (Frenkel et al, 2006; Cooke and Bear, 2010), it is now very clear that this does not occur on excitatory neurons in L4 (Montgomery et al, 2021). 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).…”

“…Third, SRP is eye-specific, indicating that modifications likely occur at TC synapses conveying information exclusively from one eye, prior to binocular integration by V1 neurons (Frenkel et al, 2006; Cooke et al, 2015). Hence, an early model proposed that long-term visual recognition memory is stored as NMDAR-dependent potentiation of TC synapses within V1 (Montgomery et al, 2021). Subsequent observations challenged this simple view, however.…”

Molecular Mechanisms of Neural Plasticity: From Basic Research to Implications for Visual Functional Rescue

“…While, in wild-type mice, chronic deprivation initiated at eye opening significantly decreased the strength of deprived-eye visual responses and affected orientation and direction selectivity, these changes did not occur in MMP9 −/− mice raised with conventional binocular vision. However, MMP9 −/− mice turned out to be insensitive to visual cortex plasticity in response to chronic deprivation, while they appeared totally normal when considering other forms of experience-dependent plasticity, such as the well-established mechanism of stimulus-selective response potentiation [ 12 ]. These results will help to expand the knowledge concerning the molecular specificity of distinct forms of activity-dependent plasticity in the mouse visual system.…”