title: Reward-modulated motor information in identified striatum neurons.
abstract: It is widely accepted that dorsal striatum neurons participate in either the direct pathway (expressing dopamine D1 receptors) or the indirect pathway (expressing D2 receptors), controlling voluntary movements in an antagonistically balancing manner. The D1- and D2-expressing neurons are activated and inactivated, respectively, by dopamine released from substantia nigra neurons encoding reward expectation. However, little is known about the functional representation of motor information and its reward modulation in individual striatal neurons constituting the two pathways. In this study, we juxtacellularly recorded the spike activity of single neurons in the dorsolateral striatum of rats performing voluntary forelimb movement in a reward-predictable condition. Some of these neurons were identified morphologically by a combination of juxtacellular visualization and in situ hybridization for D1 mRNA. We found that the striatal neurons exhibited distinct functional activations before and during the forelimb movement, regardless of the expression of D1 mRNA. They were often positively, but rarely negatively, modulated by expecting a reward for the correct motor response. The positive reward modulation was independent of behavioral differences in motor performance. In contrast, regular-spiking and fast-spiking neurons in any layers of the motor cortex displayed only minor and unbiased reward modulation of their functional activation in relation to the execution of forelimb movement. Our results suggest that the direct and indirect pathway neurons cooperatively rather than antagonistically contribute to spatiotemporal control of voluntary movements, and that motor information is subcortically integrated with reward information through dopaminergic and other signals in the skeletomotor loop of the basal ganglia.
authors.affiliation: Neural Circuit Theory, RIKEN Brain Science Institute, Saitama 351-0198, Japan. isomura@lab.tamagawa.ac.jp
authors.forename: Yoshikazu
authors.initials: Y
authors.lastname: Isomura
authors.forename: Takashi
authors.initials: T
authors.lastname: Takekawa
authors.forename: Rie
authors.initials: R
authors.lastname: Harukuni
authors.forename: Takashi
authors.initials: T
authors.lastname: Handa
authors.forename: Hidenori
authors.initials: H
authors.lastname: Aizawa
authors.forename: Masahiko
authors.initials: M
authors.lastname: Takada
authors.forename: Tomoki
authors.initials: T
authors.lastname: Fukai
mesh_terms: D000818:Animals; D001479:Basal Ganglia / Q000502:physiology; D001710:Biotin / Q000031:analogs & derivatives; D003216:Conditioning, Operant / Q000502:physiology; D003911:Dextrans; D055724:Electrophysiological Phenomena; D005456:Fluorescent Dyes; D005552:Forelimb / Q000502:physiology; D017403:In Situ Hybridization; D008297:Male; D009044:Motor Cortex / Q000166:cytology / Q000502:physiology; D009068:Movement / Q000502:physiology*; D017072:Neostriatum / Q000166:cytology / Q000502:physiology*; D009415:Nerve Net / Q000502:physiology; D009474:Neurons / Q000502:physiology*; D051381:Rats; D020318:Rats, Long-Evans; D017447:Receptors, Dopamine D1 / Q000235:genetics / Q000502:physiology; D017448:Receptors, Dopamine D2 / Q000235:genetics / Q000502:physiology; D012201:Reward
chemical_list: D003911:Dextrans; D005456:Fluorescent Dyes; D017447:Receptors, Dopamine D1; D017448:Receptors, Dopamine D2; C076397:biotinylated dextran amine; D001710:Biotin