Two spatiotemporally distinct value systems shape reward-based learning in the human brain.
Avoiding repeated mistakes and learning to reinforce rewarding decisions is critical for human survival and adaptive actions. Yet, the neural underpinnings of the value systems that encode different decision-outcomes remain elusive. Here coupling single-trial electroencephalography with simultaneously acquired functional magnetic resonance imaging, we uncover the spatiotemporal dynamics of two separate but interacting value systems encoding decision-outcomes. Consistent with a role in regulating alertness and switching behaviours, an early system is activated only by negative outcomes and engages arousal-related and motor-preparatory brain structures. Consistent with a role in reward-based learning, a later system differentially suppresses or activates regions of the human reward network in response to negative and positive outcomes, respectively. Following negative outcomes, the early system interacts and downregulates the late system, through a thalamic interaction with the ventral striatum. Critically, the strength of this coupling predicts participants' switching behaviour and avoidance learning, directly implicating the thalamostriatal pathway in reward-based learning.
Institute of Neuroscience &Psychology, University of Glasgow, 58 Hillhead Street, Glasgow G12 8QB, UK.
Elsa
E
Fouragnan
Institute of Neuroscience &Psychology, University of Glasgow, 58 Hillhead Street, Glasgow G12 8QB, UK.|Department of Behavioural &Social Sciences, University of Huddersfield, Huddersfield HD1 3DH, UK.
Chris
C
Retzler
Sir Peter Mansfield Magnetic Resonance Center, School of Physics and Astronomy, University of Nottingham, Nottingham NG7 2RD, UK.|Birmingham University Imaging Centre, School of Psychology, University of Birmingham, Birmingham B15 2TT, UK.
Karen
K
Mullinger
Institute of Neuroscience &Psychology, University of Glasgow, 58 Hillhead Street, Glasgow G12 8QB, UK.
Marios G
MG
Philiastides
D000293:Adolescent; D000328:Adult; D001362:Avoidance Learning / Q000502:physiology*; D001921:Brain / Q000502:physiology; D001931:Brain Mapping; D003657:Decision Making / Q000502:physiology*; D004569:Electroencephalography; D005260:Female; D059907:Functional Neuroimaging; D006801:Humans; D007091:Image Processing, Computer-Assisted; D007858:Learning / Q000502:physiology; D008279:Magnetic Resonance Imaging; D008297:Male; D009434:Neural Pathways; D009714:Nucleus Accumbens / Q000502:physiology*; D012201:Reward; D013788:Thalamus / Q000502:physiology*; D055815:Young Adult