Temporal correlations among functionally specialized striatal neural ensembles in reward-conditioned mice

Abstract

Bakhurin KI, Mac V, Golshani P, Masmanidis SC. Temporal correlations among functionally specialized striatal neural ensembles in reward-conditioned mice. J Neurophysiol 115: 1521-1532, 2016. First published January 13, 2016; doi:10.1152/jn.01037.2015.-As the major input to the basal ganglia, the striatum is innervated by a wide range of other areas. Overlapping input from these regions is speculated to influence temporal correlations among striatal ensembles. However, the network dynamics among behaviorally related neural populations in the striatum has not been extensively studied. We used large-scale neural recordings to monitor activity from striatal ensembles in mice undergoing Pavlovian reward conditioning. A subpopulation of putative medium spiny projection neurons (MSNs) was found to discriminate between cues that predicted the delivery of a reward and cues that predicted no specific outcome. These cells were preferentially located in lateral subregions of the striatum. Discriminating MSNs were more spontaneously active and more correlated than their nondiscriminating counterparts. Furthermore, discriminating fast spiking interneurons (FSIs) represented a highly prevalent group in the recordings, which formed a strongly correlated network with discriminating MSNs. Spike time cross-correlation analysis showed the existence of synchronized activity among FSIs and feedforward inhibitory modulation of MSN spiking by FSIs. These findings suggest that populations of functionally specialized (cue-discriminating) striatal neurons have distinct network dynamics that sets them apart from nondiscriminating cells, potentially to facilitate accurate behavioral responding during associative reward learning.

Spatially Compact Neural Clusters in the Dorsal Striatum Encode Locomotion Relevant Information

“…The neural clusters identified in this manuscript may contribute to the formation of the cell assemblies identified in previous studies (Adler et al, 2012; Bakhurin et al, 2016; Carrillo-Reid et al, 2008; Jaidar et al, 2010; Ponzi and Wickens, 2012). Computation modeling of striatal networks (Ponzi and Wickens, 2012) has predicted that a real striatal network at its characteristic sparse connectivity level should display a connectivity distribution following the power-law distribution that were scale-free and capable of self-organizing (Barabasi and Albert, 1999).…”

“…Previous studies employing neural clustering approach identified cell assemblies that represented functional states of the striatal network (Adler et al, 2012; Bakhurin et al, 2016; Carrillo-Reid et al, 2008; Jaidar et al, 2010; Ponzi and Wickens, 2012). We therefore applied similar neural clustering approach (Humphries, 2011; Ozden et al, 2008) to our data and identified neural clusters of D1- or D2- MSN based solely on their calcium activity correlation (Figure S4).…”

“…In this network, cell assemblies would form spontaneously and fire sequentially in a behavior relevant time scale (Ponzi and Wickens, 2012). Experimentally, dynamic striatal cell assemblies have recently been identified to display sequential activity in a behavior relevant manner (Adler et al, 2012; Bakhurin et al, 2016), suggesting that these cell assemblies likely carry behavior relevant information. Here we speculate that spatial and temporal coordination of neural cluster activities leads to the formation of different cell assemblies that encode distinct striatal network states.…”

“…These results suggest that glutamatergic transmissions likely drive cell assembly formation. Recent in vivo experiments demonstrated that at rest, striatal neurons displayed resting state correlations that were spatially clustered, and the resting state network dynamics resembled behavior-modulated network dynamics (Bakhurin et al, 2016). Correlated activities of both spontaneous and behavior relevant network dynamics suggest a common structural basis to support the network dynamics, which could be attributed to common glutamatergic inputs (Cohen and Kohn, 2011).…”

Principles of Synaptic Organization of GABAergic Interneurons in the Striatum

“…Thus, with the exception of the separation into patch and matrix compartments, there is no anatomical evidence for spatial organization in the striatum. Nevertheless, SPNs are active in dynamically-organized, competing functional assemblies (Bakhurin et al, 2016; Redgrave et al, 2011), suggesting the existence of microcircuits that underlie such spatial ensembles.…”