Stable representation of sounds in the posterior striatum during flexible auditory decisions

Abstract

The neuronal pathways that link sounds to rewarded actions remain elusive. For instance, it is unclear whether neurons in the posterior tail of the dorsal striatum (which receive direct input from the auditory system) mediate action selection, as other striatal circuits do. Here, we examine the role of posterior striatal neurons in auditory decisions in mice. We find that, in contrast to the anterior dorsal striatum, activation of the posterior striatum does not elicit systematic movement. However, activation of posterior striatal neurons during sound presentation in an auditory discrimination task biases the animals' choices, and transient inactivation of these neurons largely impairs sound discrimination. Moreover, the activity of these neurons during sound presentation reliably encodes stimulus features, but is only minimally influenced by the animals' choices. Our results suggest that posterior striatal neurons play an essential role in auditory decisions, and provides a stable representation of sounds during auditory tasks.

Contrasting patterns of ERK activation in the tail of the striatum in response to aversive and rewarding signals

“…Indeed, lesion of TS-projecting DA did not affect the time spent moving and the velocity (Menegas et al 2018). Moreover, while direct activation of D1R-SPN in the dorsal striatum (rostral part) using optogenetics promotes motor activity (Kravitz et al 2010), activation of TS D1R-SPNs failed to elicit movement (Guo et al 2018). Instead, D1R-SPNs of the TS appear to play an important role in auditory decisions (Guo et al 2018;Xiong et al 2015) and contribute to reinforcement learning that promotes avoidance of threatening stimuli (Menegas et al 2018).…”

“…Moreover, while direct activation of D1R-SPN in the dorsal striatum (rostral part) using optogenetics promotes motor activity (Kravitz et al 2010), activation of TS D1R-SPNs failed to elicit movement (Guo et al 2018). Instead, D1R-SPNs of the TS appear to play an important role in auditory decisions (Guo et al 2018;Xiong et al 2015) and contribute to reinforcement learning that promotes avoidance of threatening stimuli (Menegas et al 2018). Future studies are warranted to establish whether a causal relationship may exist between the aforementioned functions and the activation of D1R-SPNs within specific TS territories.…”

Opposing Influence of Sensory and Motor Cortical Input on Striatal Circuitry and Choice Behavior

“…The roles of sensory and motor cortical areas in the control of movement is a fundamental unresolved issue [15][16][17] . Primary sensory areas could play important roles through their corticostriatal projections, but this possibility has only recently begun to be explored [18][19][20][21][22] . Notably, the anterior dorsal striatum, which has been shown to be important for sensory-guided learning and behavior, receives overlapping projections from both sensory and motor cortical areas [3,4,8,9,23,24] Excitatory afferents to the striatum innervate both classes of projection neurons known as D1-and D2-receptor expressing spiny projection neurons (SPNs), as well as an increasingly appreciated diversity of interneurons, including parvalbumin (PV)-expressing, GABAergic fast spiking interneurons [25][26][27][28][29][30][31][32] .…”

Cognitive capacity limits are remediated by practice-induced plasticity between the Putamen and Pre-Supplementary Motor Area

“…allowing each combination of connections to be modulated by the multitasking factor) and then grouped the model space into 3 families: those that allowed any combination of corticocortical modulations, but not striatal-cortical ( corticocortical family, with 3 models in total M 1-3 = 3), those that allowed the reverse pattern ( striatal-cortical family, with 15 models in total, M 4-18 , and those that allowed modulations to both types of connections ( both family , with 45 models in total, M 19-63 ). As both the IPS and the putamen receive sensory inputs (Vossel, Geng, and Fink 2014;Anderson et al 2010;Grefkes and Fink 2005;Alloway et al 2017;Saint-Cyr, Ungerleider, and Desimone 1990;Guo et al 2018;Reig and Silberberg 2014) , we implemented the full set of models [M 1-63 ] with inputs to either the IPS, or to the putamen. Thus we fit a total of 126 (2x63) models to the pre-practice data.…”

“…First we asked which region in the network received driving inputs that are modulated by multitasking demands. As the IPS shows sensitivity to sensory inputs across modalities (Vossel, Geng, and Fink 2014;Anderson et al 2010;Grefkes and Fink 2005) , and as the striatum receives sensory-inputs from both the thalamus (Alloway et al 2017) and from sensory cortices (Saint-Cyr, Ungerleider, and Desimone 1990; Guo et al 2018;Reig and Silberberg 2014) , both IPS and putamen were considered as possible candidates. We therefore fit each of the 63 modulatory models twice, once allowing driving inputs to occur via the IPS, and once allowing input via the putamen (therefore, total models [ M i ] = 126 ).…”