The striatum multiplexes contextual and kinematic information to constrain motor habits execution

Abstract

The striatum is required for the acquisition of procedural memories but its contribution to motor control once learning has occurred is unclear. Here we created a task in which rats learned a difficult motor sequence characterized by fine-tuned changes in running speed adjusted to spatial and temporal constraints. After training and extensive practice, we found that the behavior was habitual yet tetrode recordings in the dorsolateral striatum (DLS) revealed continuous integrative representations of running speed, position and time. These representations were weak in naive rats hand-guided to perform the same sequence and developed slowly after learning. Finally, DLS inactivation in well-trained animals preserved the structure of the sequence while increasing its trial-by-trial variability. We conclude that after learning the DLS continuously integrates task-relevant information to constrain the execution of motor habits. Our work provides a straightforward mechanism by which the basal ganglia may contribute to habit formation and motor control.

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

“…These observations show that discriminating MSNs were more selective for licking and were equally selective for running speed relative to nondiscriminating MSNs. Thus it appears that some discriminating MSNs are modulated by both licking and running, which is consistent with a study showing that MSNs can multiplex multiple aspects of behavior (Rueda-Orozco and Robbe 2015). Furthermore, our definition of discriminating cells does not preclude that these neurons encode other behaviors, including nonmotor aspects of the task.…”

“…However, running speed was equally correlated to both discriminating and nondiscriminating neuron firing. This may also be evidence that some discriminatory neurons are modulated by both types of behaviors, supporting a report on the multiplexed coding properties of striatal neurons (Rueda-Orozco and Robbe 2015). These results do not rule out that other aspects of the task also contribute to discriminating MSN coding.…”

Discrete Circuits Support Generalized versus Context-Specific Vocal Learning in the Songbird

“…Indeed, neural signals indicating sequential context are present in mammalian cortical-basal ganglia circuitry (Dudman and Krakauer, 2016; Mello et al, 2015; Mushiake and Strick, 1995; Tanji and Shima, 1994; Turner and Desmurget, 2010), and the contributions of basal ganglia circuitry to motor production may include a role in flexible fine time-scale modulation of movement kinematics (Dudman and Krakauer, 2016; Rueda-Orozco and Robbe, 2015; Turner and Desmurget, 2010). Hence, the critical contributions of frontal cortical-basal ganglia circuits to sequence-dependent vocal learning in the songbird may reflect a general role of these circuits in integrating contextual cues to enable adaptive, context-dependent learning and execution of motor skills.…”

Pathway-Specific Striatal Substrates for Habitual Behavior

“…As demonstrated by behavioral assays designed to assess the mode of behavioral control, the transition from goal-directed to habitual behavior, as well as the maintenance of habit, requires DLS (Furlong et al, 2014; Yin et al, 2006; Yin and Balleine, 2004). Habit formation is also accompanied by altered in vivo activity (Desrochers et al, 2015; Rueda-Orozco and Robbe, 2015; Tang et al, 2007) in this region.…”