Dopamine Neurons Encoding Long-Term Memory of Object Value for Habitual Behavior

• Published in: Cell Vol. 163; no. 5; pp. 1165 - 1175
• Main Authors: Kim, Hyoung F., Ghazizadeh, Ali, Hikosaka, Okihide
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 19.11.2015
• Subjects: Animals; Basal Ganglia - physiology; Behavior, Animal; Dopamine - metabolism; Habits; Macaca mulatta - physiology; Male; Memory, Long-Term; Neurons - cytology; Neurons - physiology; Ocular Physiological Phenomena
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2015.10.063

Dopamine neurons promote learning by processing recent changes in reward values, such that reward may be maximized. However, such a flexible signal is not suitable for habitual behaviors that are sustained regardless of recent changes in reward outcome. We discovered a type of dopamine neuron in the monkey substantia nigra pars compacta (SNc) that retains past learned reward values stably. After reward values of visual objects are learned, these neurons continue to respond differentially to the objects, even when reward is not expected. Responses are strengthened by repeated learning and are evoked upon presentation of the objects long after learning is completed. These “sustain-type” dopamine neurons are confined to the caudal-lateral SNc and project to the caudate tail, which encodes long-term value memories of visual objects and guides gaze automatically to stably valued objects. This population of dopamine neurons thus selectively promotes learning and retention of habitual behavior. [Display omitted] •Dopamine neurons with a unique function were found in monkey substantia nigra•They retain past-learned reward values stably and promote habitual behavior•This mechanism guides gaze and attention automatically to valuable objects•The behavior is achieved by a local circuit between substantia nigra and caudate tail A population of dopamine neurons in the basal ganglia is involved in learning and sustaining habitual behavior in monkeys, providing a possible neural framework for the dysfunction in performing daily routines in Parkinson’s disease.