Distinct behavioural and network correlates of two interneuron types in prefrontal cortex

Abstract

Neurons in prefrontal cortex exhibit diverse behavioural correlates1–4, an observation that has been attributed to cell-type diversity. To link identified neuron types with network and behavioural functions, we recorded from the two largest genetically-defined inhibitory interneuron classes, the perisomatically-targeting parvalbumin (Pv) and the dendritically-targeting somatostatin (Som) neurons5–8 in anterior cingulate cortex (ACC) of mice performing a reward foraging task. Here we show that Pv and a subtype of Som neurons form functionally homogeneous populations showing a double dissociation between both their inhibitory impact and behavioural correlates. Out of a number of events pertaining to behaviour, a subtype of Som neurons selectively responded at reward approach, while Pv neurons responded at reward leaving encoding preceding stay duration. These behavioural correlates of Pv and Som neurons defined a behavioural epoch and a decision variable important for foraging (whether to stay or to leave), a crucial function attributed to ACC9–11. Furthermore, Pv neurons could fire in millisecond synchrony exerting fast and powerful inhibition on principal cell firing, while the inhibitory impact of Som neurons on firing output was weak and more variable, consistent with the idea that they respectively control the outputs of and inputs to principal neurons12–16. These results suggest a connection between the circuit-level function of different interneuron-types in regulating the flow of information, and the behavioural functions served by the cortical circuits. Moreover these observations bolster the hope that functional response diversity during behaviour can in part be explained by cell-type diversity.

Matching Cell Type to Function in Cortical Circuits

“…In the final phase of the trial, Pinto and Dan (2015) discovered that dmPFC GABA-ergic interneurons exhibited distinct responses depending on whether the outcome was a reward or a punishment, consistent with previous studies (Courtin et al, 2014;Kvitsiani et al, 2013). Once again, PYR neurons behaved heterogeneously while PV neurons nonselectively responded to both reward and punishment.…”

“…A recent study in dmPFC using extracellular electrophysiological recordings showed that PV and SST neurons displayed distinct firing patterns during a reward behavior at relatively slow timescale . Interestingly, Kvitsiani et al (2013) found that at a faster timescale (< 5 ms) significant correlations were present in PV but not in SST neurons. Thus, although Pinto and Dan (2015) observed consistent intra-type tuning curves in GABA-ergic interneurons on long timescales, distinct processing strategies may exist between groups at timescales as yet undetectable by calcium imaging.…”

“…Previous work in PFC has shown the importance of local inhibition in regulating PFC processing and behavioral output (Constantinidis et al, 2002;Courtin et al, 2014;Kvitsiani et al, 2013). The study by Pinto and Dan (2015), to our knowledge, represents the first time that the functional calcium responses of three major subclasses of interneurons have been directly compared in dmPFC to cover sensory, motor, and motivational aspects of behavior through a single trained behavioral task.…”

Oxytocin Modulates Female Sociosexual Behavior through a Specific Class of Prefrontal Cortical Interneurons

“…While it is clear that they can be broadly categorized based on expression of calcium binding proteins and neuropeptides (Kubota et al, 1994; Markram et al, 2004), abundant evidence that these “cardinal” interneuron types can be further subdivided into functionally relevant subtypes has been obtained (Kvitsiani et al, 2013; Xu et al, 2013). However, molecular definition of these classes of cortical interneurons and determination of their contributions to cortical function and behavior has been difficult.…”

Pain in the ACC?

“…Electrophysiological and optogenetic studies have identified neuronal populations activated during foraging behavior, attention, emotion, reward expectancy, skeletomotor and visceromotor activity, and other functions (e.g., refs. [2][3][4][5]. Only a small minority of dACC neurons are pain-related.…”