Abstract
Neuronal firing in the substantia nigra (SN) immediately following reward is thought to play a crucial role in human reinforcement learning. As in Ramayya et al. (2014a) we applied microstimulation in the SN of patients undergoing deep brain stimulation (DBS) for the treatment of Parkinson's disease as they engaged in a two-alternative reinforcement learning task. We obtained microelectrode recordings to assess the proximity of the electrode tip to putative dopaminergic and GABAergic SN neurons and applied stimulation to assess the functional importance of these neuronal populations for learning. We found that the proximity of SN microstimulation to putative GABAergic neurons predicted the degree of stimulation-related changes in learning. These results extend previous work by supporting a specific role for SN GABA firing in reinforcement learning. Stimulation near these neurons appears to dampen the reinforcing effect of rewarding stimuli.
Highlights
Thorndike’s “Law of Effect” states that rewards strengthen associations between preceding stimuli and actions, resulting in reinforcement learning (Thorndike, 1932)
In the only prior study relating microstimulation to human learning (Ramayya et al, 2014a), we showed that substantia nigra (SN) microstimulation near putative DA neurons impaired performance on a reinforcement learning task where rewards were contingent on stimuli, but unrelated to actions
We hypothesized that the effect of SN microstimulation on learning would vary based on their relative proximity to dopaminergic (DA) neurons that guide reinforcement learning (Glimcher, 2011) or GABAergic neurons that exert inhibitory control on DA neurons (Damier et al, 1999a; Lobb et al, 2011; Ramayya et al, 2014b)
Summary
Thorndike’s “Law of Effect” states that rewards strengthen associations between preceding stimuli and actions, resulting in reinforcement learning (Thorndike, 1932). SN dopamine (DA) neurons display phasic bursts that encode reward prediction error (RPE), a latent variable that tracks subsequent changes in associative strength (Sutton and Barto, 1990; Montague et al, 1996; Schultz et al, 1997; Bayer and Glimcher, 2005). They send prominent projections to dorsal striatal regions (Montague et al, 1996; Haber et al, 2000) that mediate action selection (Williams et al, 2006; Lau and Glimcher, 2008). Patients undergoing deep brain stimulation (DBS) surgery for the treatment of Parkinson’s Disease (PD) offers a rare opportunity to directly study the functional role of phasic SN activity during reinforcement learning
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