Striatal Local Circuitry: A New Framework for Lateral Inhibition

Abstract

This Perspective will examine the organization of intrastriatal circuitry, review recent findings in this area, and discuss how the pattern of connectivity between striatal neurons might give rise to the behaviorally observed synergism between the direct/indirect pathway neurons. The emphasis of this Perspective is on the underappreciated role of lateral inhibition between striatal projection cells in controlling neuronal firing and shaping the output of this circuit. We review some classic studies in combination with more recent anatomical and functional findings to lay out a framework for an updated model of the local intra-striatal circuitry and its contribution to the formation of functional units of processing with the striatum and the integration and filtering of inputs to generate motor patterns and learned behaviors.

Synchronized activation of striatal direct and indirect pathways underlies the behavior in unilateral dopamine‐depleted mice

“…The proposed involvement of DA in the generation of striatal neuronal assemblies (Burke, Rotstein, & Alvarez, ; Nicola, Surmeier, & Malenka, ; O'Donnell, ) became testable through calcium imaging that allows simultaneous measurement of many individual neurons (Carrillo‐Reid et al., ; Jaidar et al., ). With the use of population calcium imaging that allows the indirect measurement of neuronal spiking in striatal networks in vitro (Carrillo‐Reid et al., ; Jaidar et al., ; Lopez‐Huerta et al., ) we characterized the population activity of SPNs in slices obtained from naïve controls and mice depleted of DA for at least 9 days.…”

“…The reasons for the differences in neuronal recruitment between patterned and continuous stimulation, although interesting, are not the focus of this paper; methodological aspects perhaps involving a ChR2‐activated calcium conductance; reciprocal multisynaptic influences between direct and indirect SPNs and motor cortex (Burke et al., ; Freeze, Kravitz, Hammack, Berke, & Kreitzer, ; O'Hare et al., ; Oldenburg & Sabatini, ; Shipp, ), intrastriatal influences on SPNs (Planert, Szydlowski, Hjorth, Grillner, & Silberberg, ; Taverna, Ilijic, & Surmeier, ) and or the participation of interneurons (Damodaran, Evans, & Blackwell, ; Dehorter et al., ) should be considered in further analyses. Modulation of neuronal assemblies by specific patterns of neuronal stimulation may represent a modified animal model to study the pathogenesis in basal ganglia.…”

“…The reasons for the differences in neuronal recruitment between patterned and continuous stimulation, although interesting, are not the focus of this paper; methodological aspects perhaps involving a ChR2-activated calcium conductance; reciprocal multisynaptic influences between direct and indirect SPNs and motor cortex (Burke et al, 2017;Freeze, Kravitz, Hammack, Berke, & Kreitzer, 2013;O'Hare et al, 2016;Oldenburg & Sabatini, 2015;Shipp, 2017), intrastriatal F I G U R E 7 Analysis of network dynamics of D1 and D2 SPNs. The similarity index matrices of the stimulation induced by continuous (a) and stimulation in patterned pulses (b) show that continuous delivery of light activated sets of neurons with higher similarity index across stimulations, than stimulation delivered in patterned pulses.…”

Loss of striatal tyrosine‐hydroxylase interneurons impairs instrumental goal‐directed behavior

“…Dopamine increases the excitability of striatal THINs, which themselves act to inhibit striatal SPN's (Ibanez‐Sandoval et al., , ). This feedforward inhibition may have an important function in selecting striatal cell ensembles representing appropriate actions and inhibiting inappropriate actions (Burke, Rotstein, & Alvarez, ; Markowitz et al., ; Roux & Buzsaki, ). Alternatively, THINs may provide a similar action selection function based on their interactions with other striatal interneurons, including striatal cholinergic interneurons (English et al., ; Lee et al., ; Yamanaka et al., ).…”

Cell-type Specific Learning of Attentional Gating in Primate Striatum

“…Fast learning in the anterior striatum might involve dopaminergic modulation of synaptic weights among neurons receiving updates about the value of visual objects during learning [7,14]. In the striatum these neurons are spiny projection neurons (SPNs) and recent in-vivo evidence in rodent striatum supports the view that synaptic connections among SPN's are trained by inhibition from fast spiking interneurons (FSI's) [15][16][17]. According to this model cognitive flexibility is achieved through selective FSI-mediated inhibition of SPN neurons processing cortical inputs about distractors and disinhibition of SPNs processing reward predictive, relevant information [18].…”