Distributional coding of associative learning in discrete populations of midbrain dopamine neurons
Riccardo Avvisati,
Anna-Kristin Kaufmann,
Callum J. Young,
Gabriella E. Portlock,
Sophie Cancemi,
Rui Ponte Costa,
Peter J. Magill,
Paul D. Dodson
Affiliations
Riccardo Avvisati
School of Physiology, Pharmacology, and Neuroscience, University of Bristol, Bristol BS8 1TD, UK; Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX1 3TH, UK
Anna-Kristin Kaufmann
Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX1 3TH, UK
Callum J. Young
School of Physiology, Pharmacology, and Neuroscience, University of Bristol, Bristol BS8 1TD, UK; Computational Neuroscience Unit, Department of Computer Science, SCEEM, Faculty of Engineering, University of Bristol, Bristol BS8 1UB, UK
Gabriella E. Portlock
School of Physiology, Pharmacology, and Neuroscience, University of Bristol, Bristol BS8 1TD, UK
Sophie Cancemi
School of Physiology, Pharmacology, and Neuroscience, University of Bristol, Bristol BS8 1TD, UK
Rui Ponte Costa
Computational Neuroscience Unit, Department of Computer Science, SCEEM, Faculty of Engineering, University of Bristol, Bristol BS8 1UB, UK
Peter J. Magill
Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX1 3TH, UK
Paul D. Dodson
School of Physiology, Pharmacology, and Neuroscience, University of Bristol, Bristol BS8 1TD, UK; Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX1 3TH, UK; Corresponding author
Summary: Midbrain dopamine neurons are thought to play key roles in learning by conveying the difference between expected and actual outcomes. Recent evidence suggests diversity in dopamine signaling, yet it remains poorly understood how heterogeneous signals might be organized to facilitate the role of downstream circuits mediating distinct aspects of behavior. Here, we investigated the organizational logic of dopaminergic signaling by recording and labeling individual midbrain dopamine neurons during associative behavior. Our findings show that reward information and behavioral parameters are not only heterogeneously encoded but also differentially distributed across populations of dopamine neurons. Retrograde tracing and fiber photometry suggest that populations of dopamine neurons projecting to different striatal regions convey distinct signals. These data, supported by computational modeling, indicate that such distributional coding can maximize dynamic range and tailor dopamine signals to facilitate specialized roles of different striatal regions.
