The Spatiotemporal Organization of the Striatum Encodes Action Space

Abstract

SummaryActivity in striatal direct- and indirect-pathway spiny projection neurons (SPNs) is critical for proper movement. However, little is known about the spatiotemporal organization of this activity. We investigated the spatiotemporal organization of SPN ensemble activity in mice during self-paced, natural movements using microendoscopic imaging. Activity in both pathways showed predominantly local but also some long-range correlations. Using a novel approach to cluster and quantify behaviors based on continuous accelerometer and video data, we found that SPN ensembles active during specific actions were spatially closer and more correlated overall. Furthermore, similarity between different actions corresponded to the similarity between SPN ensemble patterns, irrespective of movement speed. Consistently, the accuracy of decoding behavior from SPN ensemble patterns was directly related to the dissimilarity between behavioral clusters. These results identify a predominantly local, but not spatially compact, organization of direct- and indirect-pathway SPN activity that maps action space independently of movement speed.

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

“…Recently, in freely moving animals, it was reported that both SPN populations become active in localized compact groups of synchronized neurons, that alternate their activity over time (Barbera et al, 2016;Klaus et al, 2017;London et al, 2018), these results are similar to previous slice recordings treated with NMDA . In contrast, slices from DA-depleted animals report neuronal activity locked into a dominant network state with reduced alternations between the assemblies (Jaidar et al, 2010;Lopez-Huerta et al, 2013).…”

“…Consistent with the coordinated synchronous activation of indirect and direct SPNs necessary for the selection, initiation and performance of a particular movement, it has been reported that when the animal is not moving, SPNs remain inactive, but become coactive during movement initiation (Cui et al, 2013;Klaus et al, 2017). With the increase in the number of active cells and peaks of synchrony observed in DA-depleted tissue, we hypothesized that in the absence of DA, the observed increase in synchronous activation of large sets of striatal neurons could be responsible for the animal's motor impairments, such as deviated posture and persistent spontaneous turning (Costall, Marsden, Naylor, & Pycock, 1976;Dunnett & Iversen, 1982), Figure 1e.…”

“…A contour detection snapshot of a recorded mouse illustrates the deviated posture typical of an ipsilateral DA depletion, but in this case in an intact mouse during optogenetic stimulation | 1521 JÁIDAR et Al. Shen et al, 2008;Warre et al, 2011) but as the methodology became more sophisticated, the obvious interactions of both cell types with cortical activity and the beta power increase in the electrocorticogram, common in PD, has changed the emphasis from "faster or slower firing" to changes in the intrastriatal dynamics which result from the interactions of the many effects of DA removal on functional relationships within the striatal network (Cui et al, 2013;Klaus et al, 2017;Lindahl & Hellgren Kotaleski, 2016;Parker, Kim, Alberico, Emmons, & Narayanan, 2016;Parker et al, 2018;Perez-Ortega et al, 2016; da Silva, Tecuapetla, Paixao, & Costa, 2018).…”

Thalamic afferents to prefrontal cortices from ventral motor nuclei in decision‐making

“…The description of the innervation from the whole prefrontal cortex into segregated striatal areas, led to the exploration of basal ganglia functions associated with prefrontal cortical functions in monkeys (Graybiel, 1991;Romo et al, 1992;Joel & Weiner, 1994;Jaeger et al, 1995;Afifi, 2003). Some recently described striatal functions related to prefrontal cortical integration in rats that are of interest to this review, include motivational drive (Kreitzer & Berke, 2011), generation of self-paced movements (Klaus et al, 2017), and context-dependent facilitation of appropriate movements (Kreitzer & Berke, 2011), as well as learning involved in risk-based decisionmaking (Leblond et al, 2011), solution of cognitive conflicts between actions (Laurent et al, 2017), selection of action alternatives (Canales & Graybiel, 2000), decision-making particularly, in relation to the effort invested to obtain a reward (Carvalho Poyraz et al, 2016) and cost-benefit decision-making (Friedman et al, 2015).…”

MIN1PIPE: A Miniscope 1-Photon-Based Calcium Imaging Signal Extraction Pipeline

“…Recent advances in single-photon-based miniscope technology have further enabled imaging of neural ensemble activities in freely moving animals (Cai et al, 2016; Flusberg et al, 2008; Ghosh et al, 2011), thereby allowing circuits involved in a rich repertoire of animal behaviors to be examined. For example, this technology has been successfully used in probing dynamics of neural circuits involved in innate behaviors (Betley et al, 2015; Douglass et al, 2017; Jennings et al, 2015), decision making (Pinto and Dan, 2015; Carvalho Poyraz et al, 2016), motor control (Klaus et al, 2017), learning and memory (Grewe et al, 2017; Kamigaki and Dan, 2017; Kitamura et al, 2017; Roberts et al, 2017; Roy et al, 2017; Xu et al, 2016), social memory (Okuyama et al, 2016), hippocampal place coding (Ziv et al, 2013), sleep (Cox et al, 2016; Weber and Dan, 2016), bird song (Markowitz et al, 2015), and pathological processes (Berdyyeva et al, 2016). …”