title: A basal ganglia circuit for evaluating action outcomes.
abstract: The basal ganglia, a group of subcortical nuclei, play a crucial role in decision-making by selecting actions and evaluating their outcomes. While much is known about the function of the basal ganglia circuitry in selection, how these nuclei contribute to outcome evaluation is less clear. Here we show that neurons in the habenula-projecting globus pallidus (GPh) in mice are essential for evaluating action outcomes and are regulated by a specific set of inputs from the basal ganglia. We find in a classical conditioning task that individual mouse GPh neurons bidirectionally encode whether an outcome is better or worse than expected. Mimicking these evaluation signals with optogenetic inhibition or excitation is sufficient to reinforce or discourage actions in a decision-making task. Moreover, cell-type-specific synaptic manipulations reveal that the inhibitory and excitatory inputs to the GPh are necessary for mice to appropriately evaluate positive and negative feedback, respectively. Finally, using rabies-virus-assisted monosynaptic tracing, we show that the GPh is embedded in a basal ganglia circuit wherein it receives inhibitory input from both striosomal and matrix compartments of the striatum, and excitatory input from the 'limbic' regions of the subthalamic nucleus. Our results provide evidence that information about the selection and evaluation of actions is channelled through distinct sets of basal ganglia circuits, with the GPh representing a key locus in which information of opposing valence is integrated to determine whether action outcomes are better or worse than expected.
authors.affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA.
authors.forename: Marcus
authors.initials: M
authors.lastname: Stephenson-Jones
authors.affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA.
authors.forename: Kai
authors.initials: K
authors.lastname: Yu
authors.affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA.
authors.forename: Sandra
authors.initials: S
authors.lastname: Ahrens
authors.affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA.|Medical Scientist Training Program &Program in Neuroscience, Stony Brook University, Stony Brook, New York 11790, USA.
authors.forename: Jason M
authors.initials: JM
authors.lastname: Tucciarone
authors.affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA.
authors.forename: Aile N
authors.initials: AN
authors.lastname: van Huijstee
authors.affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA.
authors.forename: Luis A
authors.initials: LA
authors.lastname: Mejia
authors.affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA.
authors.forename: Mario A
authors.initials: MA
authors.lastname: Penzo
authors.affiliation: Department of Psychology, University of California Berkeley, Berkeley, California 94720, USA.
authors.forename: Lung-Hao
authors.initials: LH
authors.lastname: Tai
authors.affiliation: Department of Psychology, University of California Berkeley, Berkeley, California 94720, USA.|Helen Wills Neuroscience Institute, University of California Berkeley, Berkeley, California 94720, USA.
authors.forename: Linda
authors.initials: L
authors.lastname: Wilbrecht
authors.affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA.
authors.forename: Bo
authors.initials: B
authors.lastname: Li
mesh_terms: D000818:Animals; D001479:Basal Ganglia / Q000166:cytology* / Q000502:physiology*; D003214:Conditioning, Classical; D003657:Decision Making; D025461:Feedback, Physiological; D005260:Female; D005917:Globus Pallidus / Q000166:cytology / Q000502:physiology; D018698:Glutamic Acid / Q000378:metabolism; D019262:Habenula / Q000166:cytology / Q000502:physiology; D008297:Male; D051379:Mice; D009434:Neural Pathways / Q000502:physiology*; D009474:Neurons / Q000378:metabolism; D062308:Optogenetics; D011678:Punishment; D011820:Rabies virus / Q000502:physiology; D012201:Reward; D013569:Synapses / Q000378:metabolism; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
chemical_list: D018698:Glutamic Acid; D005680:gamma-Aminobutyric Acid