Tonically active neurons in the primate caudate nucleus and putamen differentially encode instructed motivational outcomes of action.
To achieve a goal, animals procure immediately available rewards, escape from aversive events, or endure the absence of rewards. The neuronal substrates for these goal-directed actions include the limbic system and the basal ganglia. In the striatum, tonically active neurons (TANs), presumed cholinergic interneurons, were originally shown to respond to reward-associated stimuli and to evolve their activity through learning. Subsequent studies revealed that they also respond to aversive event-associated stimuli such as an airpuff on the face and that they are less selective to whether the stimuli instruct reward or no reward. To address this paradox, we designed a set of experiments in which macaque monkeys performed a set of visual reaction time tasks while expecting a reward, during escape from an aversive event, and in the absence of a reward. We found that TANs respond to instruction stimuli associated with motivational outcomes (312 of 390; 80%) but not to unassociated ones (51 of 390; 13%), and that they mostly differentiate associated instructions (217 of 312; 70%). We also found that a higher percentage of TANs in the caudate nucleus respond to stimuli associated with motivational outcomes (118 of 128; 92%) than in the putamen (194 of 262; 74%), whereas a higher percentage of TANs in the putamen respond to go signals for the lever release (112 of 262; 43%) than in the caudate nucleus (27 of 128; 21%), especially for an action expecting a reward. These findings suggest a distinct, pivotal role of TANs in the caudate nucleus and putamen in encoding instructed motivational contexts for goal-directed action planning and learning.
Yamada
Hiroshi
H
Department of Physiology, Kyoto Prefectural University of Medicine, Kawaramachi-Hirokoji, Kamigyo-ku, Kyoto 602-8566, Japan.
Matsumoto
Naoyuki
N
Kimura
Minoru
M
D000161:Acoustic Stimulation; D000200:Action Potentials / Q000502:physiology; D000818:Animals; D002421:Caudate Nucleus / Q000166:cytology / Q000502:physiology*; D004576:Electromyography; D005260:Female; D006040:Goals; D008251:Macaca / Q000502:physiology*; D008297:Male; D009042:Motivation; D009043:Motor Activity / Q000502:physiology; D017072:Neostriatum / Q000166:cytology / Q000502:physiology; D009474:Neurons / Q000502:physiology*; D010812:Physical Stimulation; D011699:Putamen / Q000166:cytology / Q000502:physiology*; D011930:Reaction Time / Q000502:physiology; D012201:Reward; D013647:Task Performance and Analysis