Parvalbumin-Positive Interneurons Regulate Cortical Sensory Plasticity in Adulthood and Development Through Shared Mechanisms

Abstract

Parvalbumin-positive neurons are the largest class of GABAergic, inhibitory neurons in the central nervous system. In the cortex, these fast-spiking cells provide feedforward and feedback synaptic inhibition onto a diverse set of cell types, including pyramidal cells, other inhibitory interneurons, and themselves. Cortical inhibitory networks broadly, and cortical parvalbumin-expressing interneurons (cPVins) specifically, are crucial for regulating sensory plasticity during both development and adulthood. Here we review the functional properties of cPVins that enable plasticity in the cortex of adult mammals and the influence of cPVins on sensory activity at four spatiotemporal scales. First, cPVins regulate developmental critical periods and adult plasticity through molecular and structural interactions with the extracellular matrix. Second, they activate in precise sequence following feedforward excitation to enforce strict temporal limits in response to the presentation of sensory stimuli. Third, they implement gain control to normalize sensory inputs and compress the dynamic range of output. Fourth, they synchronize broad network activity patterns in response to behavioral events and state changes. Much of the evidence for the contribution of cPVins to plasticity comes from classic models that rely on sensory deprivation methods to probe experience-dependent changes in the brain. We support investigating naturally occurring, adaptive cortical plasticity to study cPVin circuits in an ethologically relevant framework, and discuss recent insights from our work on maternal experience-induced auditory cortical plasticity.

Experience-dependent plasticity of gustatory insular cortex circuits and taste preferences

“…3, D and E ) ( 29 ). We focused on PV + γ-aminobutyric acid (GABA)–releasing (GABAergic) neurons because they are highly sensitive to changes in postnatal sensory experience in other cortices ( 30 , 31 ) and influence taste-based memory formation in GC ( 32 ). We recorded 5224 neurons over 12 sessions from five mice for the naïve group (4994 PV − putative PYR; 230 PV + neurons) and 4795 neurons in 15 sessions from five mice for the EE group (4573 PYR; 222 PV + neurons).…”

Experience-dependent plasticity of gustatory insular cortex circuits and taste preferences

“…3d-e) (Pnevmatikakis and Giovannucci, 2017). We focused on PV + GABAergic neurons because they are highly sensitive to changes in postnatal sensory experience in other cortices (Fagiolini et al, 2004; Hensch, 2005; Di Cristo et al, 2007; Rupert and Shea, 2022) and influence taste-based memory formation in GC (Yiannakas et al, 2021). We recorded 5224 neurons over 12 sessions from 5 mice for the naïve group (4994 non-PV neurons, putative pyramidal, PYR; 230 PV + neurons), and 4795 neurons in 15 sessions from 5 mice for the EE group (4573 PYR; 222 PV + neurons).…”

The role of parvalbumin neurons in the evolution of skilled behaviours

“…Because the pattern of PV expression in woodpeckers resembles the convergent evolution of PV neurons in areas for vocal learning in birds [ 4 , 5 ] and because PV neurons regulate many forms of neural and behavioural plasticity [ 9 , 10 ], one of the primary questions raised by these findings is the role of learning in woodpecker drumming. Little is known about the degree to which rhythmic drumming is learned but, like learned vocalisations in vocal-learning species [ 3 ], the rhythmic drumming of woodpeckers involves a protracted period of development and is acutely modulated by social interactions.…”

“…Little is known about the degree to which rhythmic drumming is learned but, like learned vocalisations in vocal-learning species [ 3 ], the rhythmic drumming of woodpeckers involves a protracted period of development and is acutely modulated by social interactions. If drumming is indeed learned, it will be important to discern how PV neurons shape neural dynamics to allow for learning; for example, PV neurons in mammals are hypothesised to influence learning by modulating oscillatory patterns (e.g., gamma oscillations) and the balance of excitation and inhibition in focal circuits [ 9 , 10 ].…”

“…to discern how PV neurons shape neural dynamics to allow for learning; for example, PV neurons in mammals are hypothesised to influence learning by modulating oscillatory patterns (e.g., gamma oscillations) and the balance of excitation and inhibition in focal circuits [9,10].…”