Research ArticleCOGNITIVE NEUROSCIENCE

Signal dynamics of midbrain dopamine neurons during economic decision-making in monkeys

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Science Advances  01 Jul 2020:
Vol. 6, no. 27, eaba4962
DOI: 10.1126/sciadv.aba4962
  • Fig. 1 Economic decision-making task, monkeys’ behavior, and recording sites.

    (A) Economic decision-making task. ITI, intertrial interval. (B) Choice rate of the first object in monkey A (n = 216 sessions) (left) and monkey E (n = 165 sessions) (right). (C) Rate of trials in which the monkey did not release the button within the second object presentation among trials in which the animal did not choose the first object. (D) Latency of the button release to choose the first object (circles) and to respond to the appearance of the second object (squares). Double asterisks indicate a significant difference between the latencies for the first and second objects (P < 0.01, two-tailed Wilcoxon signed-rank test). (E) Effects of the first (green) and second (orange) object values in the previous trial (t−1) and the first object value in the current trial (t) (purple) on the monkey’s choice. Double asterisks indicate a significant logistic regression coefficient (P < 0.01). Error bars in (B) to (E) indicate SEM, which are very small and hidden in most cases. (F and G) Recording sites shown on the images obtained by an MRI scan, in which the position of electrodes targeting the left SNc/VTA (red) (F) and the right OFC (yellow) (G) in monkey E is displayed.

  • Fig. 2 Dopamine and OFC neurons representing value and/or choice during economic decision-making.

    (A to F) Activity of six example neurons [(A to C) dopamine neurons; (D to F) OFC neurons]. Top: Spike density functions (SDFs) aligned at the onset of the first object. The SDFs are shown for each object value (red, value 6; pink, value 5; yellow, value 4; light blue, value 3; blue, value 2; dark blue, value 1) and for chosen (solid curves) and unchosen trials (dotted curves). Gray horizontal bars indicate the time window to calculate the magnitude of neuronal activity. Bottom: Magnitude of neuronal activity plotted against the object value shown for chosen (filled circles) and unchosen trials (open circles). Gray plots showed the baseline activity (−500 to 0 ms) for each value condition. Error bars indicate SEM.

  • Fig. 3 Model comparison analysis.

    (A) Value (left) and choice (right) models. (B) Schematic diagram illustrating the procedure to identify value-modulated (red), intermediate (white), and choice-modulated neurons (blue). R2 is compared between the value (y axis) and the choice models (x axis). Horizontal and vertical dotted lines indicate the significance level (P < 0.05, two-tailed F test) of the value- and choice-model fits, respectively. Diagonal dotted lines indicate the significance level (P < 0.05, two-tailed bootstrap test) of the R2 difference between the models. Gray area indicates neurons that exhibited neither a significant R2 difference between the models (P > 0.05, two-tailed bootstrap test) nor a significant fit to either model (P > 0.05, two-tailed F test). (C and D) Temporal profile of the R2 difference between the models for each dopamine (n = 96) (C) and OFC neuron (n = 263) (D). The color of pixels represents the normalized magnitude of the R2 difference (red, better fit by the value model; white, intermediate fit between the value and the choice models; blue, better fit by the choice model). Open yellow rectangles show choice-modulated neurons. Red, gray, and blue triangles indicate the example neurons shown in Fig. 2, A and D, Fig. 2, B and E, and Fig. 2, C and F, respectively.

  • Fig. 4 Proportions and averaged activities of value-modulated, intermediate, and choice-modulated neurons.

    (A and B) Left: Proportions of identified neurons (i.e., value-modulated, intermediate, and choice-modulated neurons) and non-identified neurons. Right: Proportions of value-modulated, intermediate, and choice-modulated neurons among all the identified neurons. These proportions are shown for dopamine neurons (n = 96) (A) and OFC neurons (n = 263) (B). (C) Comparison of the proportions of value-modulated, intermediate, and choice-modulated neurons between dopamine (open bars) and OFC neurons (filled bars). n.s. indicates no significant difference (P > 0.05, two-tailed Fisher’s exact test). (D and E) Averaged magnitudes of value-modulated (left), intermediate (middle), and choice-modulated neuron activities (right) shown for dopamine neurons (n = 38, 52, and 32, respectively) (D) and OFC neurons (n = 54, 54, and 34, respectively) (E). Note that the OFC neurons that positively represented the option’s value and/or monkey’s choice were used in this analysis (see fig. S2 for OFC neurons that negatively represented the value and/or choice). Conventions are as the bottom panels in Fig. 2 (A to F).

  • Fig. 5 Temporal dynamics of the dopamine and OFC signals corresponding to the time course of the decision-making process.

    (A and B) Time-varying proportions of value-modulated (red), intermediate (gray), and choice-modulated neurons (blue) shown for dopamine neurons (n = 96) (A) and OFC neurons (n = 263) (B). Arrowheads represent the onsets of the value-modulated (red), intermediate (gray), and choice-modulated signals (blue). (C and D) Cumulative histograms of the latencies of the value-modulated (red), intermediate (gray), and choice-modulated signals (blue) shown for dopamine neurons (n = 96) (C) and OFC neurons (n = 263) (D). Vertical dotted lines indicate mean latencies, and numbers are means ± SD. Single and double asterisks indicate a significant difference between the latencies (P < 0.05 and 0.01, respectively, two-tailed Wilcoxon signed-rank test). (E and F) Comparison of the R2 between the value model (y axis) and the choice model (x axis) in dopamine neurons (n = 96) (E) and OFC neurons (n = 263) (F). Each panel indicates the R2 for each 100-ms time bin. Pink lines indicate linear regression lines. Red, gray, and blue circles indicate the example neurons shown in Fig. 2 (A and D, B and E, and C and F, respectively). (G and H) Regression slopes calculated for each time bin in dopamine (G) and OFC neurons (H).

  • Fig. 6 Onsets of the choice-modulated signal and monkey’s choice behavior.

    (A and C) Averaged SDFs of choice-modulated dopamine neurons (n = 31) (A) and OFC neurons (n = 34) (C) aligned at the onset of the first object shown for chosen trials (blue) and unchosen trials (gray) under the condition in which “object value = 4”. One choice-modulated dopamine neuron was excluded from this analysis because the monkey chose the first object associated with the value 4 in all trials during the recording session, and, consequently, we were unable to collect data in unchosen trials. (B and D) Averaged SDFs of the same choice-modulated dopamine neurons (n = 31) (B) and OFC neurons (n = 34) (D) aligned at the onset of the button release. Shaded areas around the curves indicate SEM. Vertical dotted lines and numbers indicate the time when the difference in the averaged firing rate between chosen and unchosen trials became significant (P < 0.05, one-tailed Wilcoxon signed-rank test).

  • Fig. 7 Neuronal modulation evoked by the button release in the control task.

    (A) Control task. (B) Latency of the button release in monkey A (n = 182 sessions) and monkey E (n = 165 sessions) in the control task. (C and E) Averaged SDFs of the choice-modulated dopamine neurons (n = 20) (C) and OFC neurons (n = 34) (E) aligned at the onset of the button release in the control task. Shaded areas around the curves indicate SEM. Horizontal white and blue bars indicate the time windows used to calculate the baseline firing rate (−400 to −200 ms) and the firing rate around the onset of the button release (−200 to 200 ms) of each neuron, respectively. (D and F) Comparison between the baseline firing rate and the firing rate around the onset of the button release in the control task for the 20 choice-modulated dopamine neurons (D) and the 34 choice-modulated OFC neurons (F). Each gray line indicates the data obtained from each neuron. Double asterisk indicates a significant difference between the firing rates (P < 0.01, two-tailed Wilcoxon signed-rank test). n.s. indicates no significant difference (P > 0.05, two-tailed Wilcoxon signed-rank test). Error bars indicate SEM.

Supplementary Materials

  • Supplementary Materials

    Signal dynamics of midbrain dopamine neurons during economic decision-making in monkeys

    Mengxi Yun, Takashi Kawai, Masafumi Nejime, Hiroshi Yamada, Masayuki Matsumoto

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