Dopamine neurons evaluate natural fluctuations in performance quality

• Published in: Cell reports (Cambridge) 2022-03, Vol.38 (13), p.110574-110574, Article 110574
• Main Authors: Duffy, Alison, Latimer, Kenneth W., Goldberg, Jesse H., Fairhall, Adrienne L., Gadagkar, Vikram
• Format: Article
• Language: English
• Subjects: Animals; basal ganglia; Basal Ganglia - physiology; birdsong; dopamine; Dopamine - physiology; Dopaminergic Neurons; Gaussian process model; generalized linear model; Learning - physiology; motor skill learning; natural behavior; performance prediction error; skill maintenance; ventral tegmental area; Vocalization, Animal - physiology
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2022.110574

Many motor skills are learned by comparing ongoing behavior to internal performance benchmarks. Dopamine neurons encode performance error in behavioral paradigms where error is externally induced, but it remains unknown whether dopamine also signals the quality of natural performance fluctuations. Here, we record dopamine neurons in singing birds and examine how spontaneous dopamine spiking activity correlates with natural fluctuations in ongoing song. Antidromically identified basal ganglia-projecting dopamine neurons correlate with recent, and not future, song variations, consistent with a role in evaluation, not production. Furthermore, maximal dopamine spiking occurs at a single vocal target, consistent with either actively maintaining the existing song or shifting the song to a nearby form. These data show that spontaneous dopamine spiking can evaluate natural behavioral fluctuations unperturbed by experimental events such as cues or rewards. [Display omitted] •Songbird dopamine activity correlates with natural song fluctuations•The form and timing of the dopamine activity is consistent with song evaluation Learning and producing skilled behavior requires an internal measure of performance. Duffy et al. examine dopamine neurons’ relationship to natural song in singing birds. Spontaneous dopamine activity correlates with song fluctuations in a manner consistent with evaluation of natural behavioral variations, independent of external perturbations, cues, or rewards.