Research ArticleNEUROSCIENCE

Dopamine and beta-band oscillations differentially link to striatal value and motor control

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Science Advances  25 Sep 2020:
Vol. 6, no. 39, eabb9226
DOI: 10.1126/sciadv.abb9226
  • Fig. 1 Systems for multimodal recording of physiological activity in behaving primates.

    (A) Setup for recording electrical activity (left) and dopamine activity (right) from an implanted moveable silica probe (inset photo left) or fixed microinvasive probe (photo right) in the striatum. (B) Example of synchronous recording of dopamine (Δ[DA]), LFP, filtered beta-band (β) LFP power, pupil diameter, lick activity, and pulse during task performance recorded from M1. C, central cue onset; T, peripheral target onset; RW, reward onset. (C) Visually guided reward-biased task. In the block shown, the contralateral (Contra) target was associated with a big RW. Contralateral and ipsilateral (Ipsi) target trials were introduced randomly in sequence within a block, and the target side associated with a big RW switched between blocks (15 to 45 trials). (D) Physiological responses and reaction time from M1, aggregated over groups of big and small RW trials, demonstrating discrimination of RW size in a single session. Trace thickness is equal to ±SE.

  • Fig. 2 Correlations between dopamine and beta-band signals as defined over short time scales.

    (A) T-aligned Δ[DA] (left) and β LFP (center) measured in the putamen across trials (rows) sorted for increasing peak Δ[DA] for an individual session with corresponding average early (0.2 to 0.8 s) β LFP (right, vertical line represents median value). (B) Covariance between dopamine and beta as a function of time relative to T for each of the two measurements, averaged across all sessions (left). Trial averaged time course of Δ[DA] (top) and β LFP (bottom) for big RW trials in a single session (right). Trace thickness is equal to ±SE. (C) Peak changes in dopamine (Δ[DA]) plotted versus early β LFP for the same site pair shown in (A), displaying significant anticorrelation (r and P values indicated in plot). (D) Matrices of the fraction of sites in the CN (left two plots) or putamen (right two plots), displaying significant positive (r > 0) or negative (r < 0) correlations between dopamine peaks and β LFP as computed by averaging over windows with different start (x axis) and end (y axis) times relative to T. Color indicates the ratio of sites displaying significant correlations, and a uniform scale is applied to all plots. All measurements are from M1.

  • Fig. 3 Dopamine and beta selectivity to reward size inversely modulated in the CN but not putamen.

    (A) Illustration of trial procedure. The monkey holds its gaze on a contralateral target for 4 s to receive a big or small RW depending on the target side–RW size contingency for the given block of trials. (B) Δ[DA] (top left) and its paired β LFP (bottom left; early beta time window shaded) concurrently recorded from a single session in the CN, aligned to T (at 0 s). Line thickness is equal to ±SE. Scatter plots show normalized Δ[DA] peaks (top right) and paired early beta signals (bottom right) recorded concurrently for all sites in CN as averaged for each session (each circle) for contralateral movement conditions from M1. Δ[DA] and beta were normalized to the median or the minimum and maximum values, respectively (details in Materials and Methods). Lines are drawn between conditions for each site that showed a significant difference (P < 0.05, t test, colored circles), and the ratio of these sites is shown above the plot. Error bars indicate 95% confidence intervals. (C) Same as (B) but for putamen. (D) Sagittal views of dopamine-recorded sites in M1 (circles) and M2 (squares). Symbols denoted by color indicating specific RW condition and outline/fill pattern indicating specific movement condition, where Δ[DA] was significantly greater. AC, anterior commissure.

  • Fig. 4 Dopamine and beta signaling to reward and performance history.

    (A) (Left) Representative Δ[DA] and concurrently recorded β LFP from a paired site in the CN during a series of big and small RW trials. Δ[DA] increases immediately after T (26 to 30 s) when a small RW had been obtained on the previous trial, and decreases (42 to 46 s) when a big RW had been delivered on the previous trial. (Right) Same as left for measured Δ[DA] and β LFP over a sequence of failed and rewarded trials to demonstrate influence of performance history on recorded signals. Δ[DA] increases after T (26 to 30 s) when the animal failed to fixate on the target for a full 4 s on the preceding trial (failure) and increases to a smaller degree on the next trial (42 to 46 s) when it successfully completed the sequence of eye movements and received an RW on the previous trial. (B) (Left) Concurrently recorded Δ[DA] (top) and paired β LFP (bottom) on large reward trials, as shown in Fig. 3B, averaged for different outcomes on previous trial: failure (fixation break, brown), small RW (blue), and big RW (red) in CN. (Right) Scatter plot, as shown in Fig. 3B, for different outcome histories, for big RW trials. (C) Same as (B) but for putamen. All measurements are from M1.

  • Fig. 5 Dopamine and beta signals associated with movement control.

    (A) Trial procedure in which the monkey fixated either a contralateral or ipsilateral target for 4 s to receive a small RW. (B) (Left) Representative measurements of Δ[DA] (top) and β LFP (bottom) in CN. (Right) Scatter plots of all measured sites in the CN from M1, comparing signals evoked by contralateral and ipsilateral targets for small RW as shown in Fig. 3B. (C) Same as (B) but for putamen. β LFP in the putamen best discriminated target positions when averaged over the entire target window (0.2 to 3.8 s, shaded). β LFP norm averaged over target window (right) for putamen sites only. (D) Spatial map of recorded responses as shown in Fig. 3D.

  • Fig. 6 Online measures of arousal, motivation, and motor performance related to dopamine and beta as well as past experiences (a task defined proxy of ongoing motivational drive).

    (A) Trial-by-trial measures of dopamine as shown in Fig. 2A but for a different session, sorted by max Δ[DA] (left) with the corresponding z score of the licking activity (right). (B) Max Δ[DA] (left) and early beta (right) versus licking. Only dopamine shows a significant correlation to licking in this session. (C to E) Same as (B) for HRV (C), reaction time (D), and pupil diameter (E). (F) Scatter plot, as shown in Fig. 4B, of licking activity, HRV, pupil diameter, and reaction time for different outcome histories, measured for fixed big RW trial conditions. All measurements are from M1.

Supplementary Materials

  • Supplementary Materials

    Dopamine and beta-band oscillations differentially link to striatal value and motor control

    H. N. Schwerdt, K. Amemori, D. J. Gibson, L. L. Stanwicks, T. Yoshida, N. P. Bichot, S. Amemori, R. Desimone, R. Langer, M. J. Cima, A. M. Graybiel

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