Task-dependent encoding of space and events by striatal neurons is dependent on neural subtype

Abstract

The dorsal striatum plays a critical role in procedural learning and memory. Current models of basal ganglia assume that striatal neurons and circuitry are critical for the execution of overlearned, habitual sequences of action. However, less is known about how the striatum encodes task information that guides the performance of actions in procedural tasks. To explore the striatal encoding of task information, we compared the behavioral correlates of striatal neurons tested in two tasks: a Multiple-T-maze task in which reward delivery was entirely predictable based on spatial cues (the Multiple-T task), and a task in which rats ran on a rectangular track, but food delivery depended on the distance traveled on the track and was not dependent solely on spatial location (the Take-5 task). Striatal cells recorded on these tasks were divisible into three cell types: phasic-firing neurons (PFNs), tonically firing neurons (TFNs), and high-firing neurons (HFNs) and similar proportions of each cell type were found in each task. However, the behavioral correlates of each cell type were differentially sensitive to the type of task rats were performing. PFNs were responsive to specific task-parameters on each task. TFNs showed reliable burst-andpause responses following food delivery and other events that were consistent with tonically active-neurons (TANs) on the Take-5 (non-spatial) task but not on the Multiple-T (spatial) task. HFNs showed spatial oscillations on the Multiple-T (spatial) task but not the Take-5 (non-spatial) task. Reconstruction of the rats' position on the maze was highly accurate when using striatal ensembles recorded on the Multiple-T (spatial) task, but not when using ensembles recorded on the Take-5 (non-spatial) task. In contrast, reconstruction of time following food delivery was successful in both tasks. The results indicated a strong task dependency of the quality of the spatial, but not the reward-related, striatal representations on these tasks. These results suggest that striatal spatial representations depend on the degree to which spatial task-parameters can be unambiguously associated with goals.

Hippocampus and subregions of the dorsal striatum respond differently to a behavioral strategy change on a spatial navigation task

“…Previous work has reported that both HC (O'Keefe and Nadel 1978; Redish 1999) and aDLS Schmitzer-Torbert 2004;Yeshenko et al 2004) neurons were spatially tuned on a task in which spatial cues provided information about how to obtain rewards; however, on a spatial task in which spatial cues did not provide information about how to obtain rewards, only HC neurons were spatially tuned (Berke et al 2009;Wikenheiser and Redish 2011) while aDLS neurons were not (Berke et al 2009;Schmitzer-Torbert and Redish 2008). We found that HC and aDLS neurons responded in a similar fashion to spatial context in the present study, such that many neurons in both structures were spatially tuned to one side of the maze or the other.…”

“…HC neurons that are spatially tuned form a cognitive map, allowing for integration of past and potential future experiences in order to plan behavior (O'Keefe and Nadel 1978;McNaughton et al 2006;Redish 1999;Wikenheiser and Redish 2015a). Neurons in the dorsolateral striatum also respond to spatial cues Redish 2004, 2008;Yeshenko et al 2004), but only when spatial cues contain information about obtaining rewards (Berke et al 2009;Schmitzer-Torbert and Redish 2008). Neural activity in the dorsolateral striatal neurons is related to specific motor movements and actions DeLong 1985a, 1985b;Carelli and West 1991;Cho and West 1997;Jog et al 1999;Schmitzer-Torbert and Redish 2008), likely ones that have consistently led to reinforcement.…”

Theta Phase Precession in Rat Ventral Striatum Links Place and Reward Information

“…Cell type categorization. As described previously, ventral striatal units were assigned to one of three cell type categories: phasically firing neuron (putative medium spiny neuron), high-firing neuron (putative fast-spiking interneuron), or tonically firing neuron, based on spiking statistics (Schmitzer-Torbert and Redish, 2008;van der Meer et al, 2010a). Hippocampal units were separated into putative pyramidal neurons and interneurons based on average firing rate (interneurons, Ͼ2 Hz) (Ranck 1973;Csicsvari et al, 1999).…”

Corticostriatal Interactions during Learning, Memory Processing, and Decision Making

“…However, these cells have been argued to have a critical role filtering out unwanted actions, and postmortem studies have found a deficit in striatal FSIs in Tourette syndrome (Kalanithi et al, 2005). Several groups studied putative FSIs in awake, behaving animals, identifying them on the basis of characteristic brief waveforms, tonic activity, and high-frequency discharges (Berke et al, 2004;Berke, 2008;Gage et al, 2008;Schmitzer-Torbert and Redish, 2008). In rats, FSIs show complex temporal sequences of activity during choice tasks, and do not normally act as a coordinated cell population with closely linked firing rates, even within striatal microregions (Berke, 2008).…”