Opponent and bidirectional control of movement velocity in the basal ganglia

Abstract

For goal-directed behavior it is critical that we can both select the appropriate action and learn to modify the underlying movements (e.g. the pitch of a note or velocity of a reach) to improve outcomes. The basal ganglia are a critical nexus where circuits necessary for the production of behavior, such as neocortex and thalamus, are integrated with reward signaling 1 to reinforce successful, purposive actions 2. Dorsal striatum, a major input structure of basal ganglia is composed of two opponent pathways, direct and indirect, thought to select actions that elicit positive outcomes or suppress actions that do not, respectively 3,4. Activity-dependent plasticity modulated by reward is thought to be sufficient for selecting actions in striatum 5,6. Although perturbations of basal ganglia function produce profound changes in movement 7, it remains unknown whether activity-dependent plasticity is sufficient to produce learned changes in movement kinematics, such as velocity. Here we used cell-type specific stimulation delivered in closed-loop during movement to demonstrate that activity in either the direct or indirect pathway is sufficient to produce specific and sustained increases or decreases in velocity without affecting action selection or motivation. These behavioral changes were a form of learning that accumulated over trials, persisted after the cessation of stimulation, and were abolished in the presence of dopamine antagonists. Our results reveal that the direct and indirect pathways can each bidirectionally control movement velocity, demonstrating unprecedented specificity and flexibility in the control of volition by the basal ganglia.

Parvalbumin Interneurons Modulate Striatal Output and Enhance Performance during Associative Learning

“…The striatum is a major information processing hub and site of plasticity for a variety of reward-conditioned behaviors (Balleine et al, 2007; Gerfen and Surmeier, 2011; Kreitzer and Malenka, 2008; Liljeholm and O’Doherty, 2012; Silberberg and Bolam, 2015; Yin and Knowlton, 2006). In recent years much attention has been drawn toward unveiling the function of direct and indirect pathway projection neurons in movement (Barbera et al, 2016; Cui et al, 2013; Kravitz et al, 2010; Oldenburg and Sabatini, 2015; Rothwell et al, 2015; Tecuapetla et al, 2016; Yttri and Dudman, 2016), reinforcement (Kravitz et al, 2012; Vicente et al, 2016), and sensory processing (Reig and Silberberg, 2014; Sippy et al, 2015). In comparison, the role of inhibitory striatal interneurons in these behavioral functions is less well understood (Fino and Venance, 2011; Kreitzer and Malenka, 2008; Tepper et al, 2010).…”

Physiological Markers of Motor Inhibition during Human Behavior

“…Converging lines of evidence implicate the STN in a threshold setting process [11, 12, 101]. In a manner similar to how this structure can shut down the motor system to abort a planned movement, it could also modulate the threshold required to select and initiate a movement (e.g., low threshold to favor speed over accuracy) [102–104]. While these predictions have not been tested with TMS probes of corticospinal excitability, there is evidence that low-frequency oscillatory activity associated with the STN is modulated as a function of whether task instructions emphasize speed or accuracy [105].…”

Baseline Motor Cortex Activity Contains an Internal Model Representation

“…Interestingly, population encoding of a forward model of movement velocity was recently demonstrated in the cerebellum (Herzfeld et al, 2015). An alternative to parameter control is presented by the authors in the present study, who argue for a dynamical systems perspective of motor cortex activity, in which encoding of movement parameters is deemphasized for analysis of how neural activity patterns produce temporal sequences required for movement (Shenoy et al, 2013). Finally, as the current study was limited to examining the effects of motor adaptation, it remains unknown what other aspects of the internal model may be encoded by baseline motor cortex activity.…”

“…This process is termed adaptation. While brain structures, such as the cerebellum, have been implicated in the learning and storage of adapted motor responses (Wolpert and Miall, 1996), motor command structures, such as motor cortex, are thought to be responsible for implementation of the updated motor plan (Guo et al, 2015). Thus, conventional wisdom suggests that internal model information should be present in motor cortex during movement preparation and execution (MandelblatCerf et al, 2011).…”

“…In response, our nervous system must adapt to its new physical relationship with the world. One way to handle the everchanging interaction between our bodies and our environment is to create and update internal models that relate neural activity to movement (Shadmehr et al, 2010). In other words, these models represent how the body is expected to respond when a specific motor command is issued.…”