Dopamine neurons encode performance error in singing birds

Abstract

Many behaviors are learned through trial and error by matching performance to internal goals. Yet neural mechanisms of performance evaluation remain poorly understood. We recorded basal ganglia-projecting dopamine neurons in singing zebra finches as we controlled perceived song quality with distorted auditory feedback. Dopamine activity was phasically suppressed after distorted syllables, consistent with a worse-than-predicted outcome, and was phasically activated at the precise moment of the song when a predicted distortion did not occur, consistent with a better-than-predicted outcome. Error response magnitude depended on distortion probability. Thus, dopaminergic error signals can evaluate behaviors that are not learned for reward and are instead learned by matching performance outcomes to internal goals.

Fig. 1. Experimental test of performance error signals in birdsong

(A) Evaluation of auditory feedback during singing is hypothesized to result in ‘error’ signals that reach the song system. (B) Strategy for antidromic identification of VTAx dopamine neurons. (C) Antidromic spikes (black) and spike collisions (red) of a VTAx neuron. (D) VTAx neurons labeled by injection of retrograde tracer into Area X (green, top) and co-labeled dopamine neurons stained with anti-tyrosine hydroxylase (TH) antibody (purple, bottom). White arrows point to the visible path of the electrode that recorded the VTAx unit shown in Fig. 2A (Scale, 100 μm; anterior-right, dorsal-top). (E) Example of displaced-syllable DAF. A snippet of syllable ‘c’ was played back during production of the target syllable ‘b’ (Target time, black triangles and white dashed lines). Randomly interleaved target renditions were left undistorted (undistorted trials, blue dashed line). (F) Expanded view of the target syllable. (G) Pitch-contingent displaced-syllable DAF drives learning. Grey dots denote mean pitch of 49716 target syllable renditions sung over 23 days for one bird. Shading demarcates distorted renditions; green, low pitch variants distorted (up days); blue, high pitch variants distorted (down days). (H) Histogram of pitch changes learned during each day (n=4 birds).

Fig. 2. VTA neurons encode performance error during singing

(A) Spectrogram, voltage trace and the instantaneous firing rate of a VTAx neuron (DAF, red shading; undistorted targets, blue lines). (B) Top to bottom: spectrograms, spiking activity during undistorted and distorted trials, corresponding spike raster plots and rate histograms, and z-scored difference between undistorted and distorted rate histograms (plots aligned to target onset). Horizontal bars in histograms indicate significant deviations from baseline (P < 0.05, z-test) (24). (C) and (D) Two additional VTAerror neurons as in (B). (E) Each row plots the z-scored difference between undistorted and distorted target-aligned rate histograms. VTAx neurons (top, n=14) and non-antidromic neurons (bottom, n=111) are independently sorted by maximal z-score. (F) Top, distribution of error responses(24). Bottom, spikewidth versus error response (triangles: antidromic, circles: non-antidromic neurons). (G) Normalized response to distorted and undistorted targets (mean ± SEM) for VTAother (top) and VTAerror neurons (middle). Bottom, scatterplot of normalized rate in the 50–125 milliseconds following distorted and undistorted trials (solid fills indicate P < 0.05, bootstrap). (H) Distributions of phasic response durations (top) and latencies (bottom). (I) For each VTAerror neuron, the time of maximal firing rate relative to motif onset is plotted against target time.

Fig. 3. VTAerror responses depend on error probability

(A) Displaced-syllable DAF scheme with 2 targets per motif (syllable b: target-1, distortion rate: 50%; syllable d, target-2, distortion rate: 20%, target times marked with dashed white line and black triangle). The distorted versions of the two target syllables are shown at right (color scheme as in Fig. 1E). (B) Target-1 and (C) target-2 error responses for the same neuron. Top to bottom: spectrograms, spiking activity during undistorted and distorted trials, corresponding spike raster plots and rate histograms, and z-scored difference between undistorted and distorted rate histograms (all plots aligned to target onset). Horizontal bars in histograms indicate significant deviations from baseline (P < 0.05, z-test) (24). (D) Top, normalized responses to distorted targets (mean ± SEM) for VTAerror neurons. Bottom, scatterplot of normalized rate in the 50–125 milliseconds following target time (solid fills indicate P < 0.05, bootstrap). (E) Same as (D) but for undistorted targets.

Fig. 4. Response of VTAerror neurons to birdsong during non-singing

(A) Distorted and undistorted renditions of the bird’s own song was played back during non-singing periods. (B) Top to bottom: spectrograms, spiking activity of the VTAx neuron shown in Fig. 3 during playback of undistorted and distorted songs, corresponding spike raster plots and rate histograms, and z-scored difference between undistorted and distorted rate histograms (all plots aligned to target onset). (C) Normalized responses to distorted and undistorted targets (mean ± SEM) for VTAerror neurons during passive playback (top). Bottom, scatterplot of normalized rate in the 50–125 milliseconds following target time (empty fills indicate no significant response, P > 0.05, bootstrap) (24)).