Single caudate neurons encode temporally discounted value for formulating motivation for action

  1. Yukiko Hori
  2. Koki Mimura
  3. Yuji Nagai
  4. Atsushi Fujimoto
  5. Kei Oyama
  6. Erika Kikuchi
  7. Ken-ichi Inoue
  8. Masahiko Takada
  9. Tetsuya Suhara
  10. Barry J Richmond
  11. Takafumi Minamimoto  Is a corresponding author
  1. Department of Functional Brain Imaging, National Institutes for Quantum and Radiological Science and Technology, Japan
  2. Systems Neuroscience Section, Primate Research Institute, Kyoto University, Japan
  3. Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, United States
8 figures and 1 additional file

Figures

Figure 1 with 2 supplements
Task, behavioral performance, and recording sites.

(A) Sequence of events of behavioral tasks. (B) Example of relationship between cue and outcome in delayed reward task. (C) Ratio of error trials (mean ± sem) as a function of delay duration in …

Figure 1—source data 1

Souce data of error rates as a function of delay duration and reward size.

https://cdn.elifesciences.org/articles/61248/elife-61248-fig1-data1-v2.xls
Figure 1—figure supplement 1
Error type and timing, and reaction time and eye position.

(A) Proportion of early error for each monkey. Thick and thin dots indicate mean and data of each session, respectively. (B) Distribution of timing for early and late bar release for each monkey. …

Figure 1—figure supplement 2
Eye position during cue period.

(A) Density plots of eye position during cue period of delayed reward task obtained from monkey RI. Colors indicate normalized looking-time. White squares indicate the frame of cue stimulus. (B) …

Task-related responses of dCDh neurons.

(A) Example of a neuron that responded exclusively to cue. Rasters and spike density histograms for all trials are aligned at the cue signal (left), bar release (middle), and reward delivery …

Figure 3 with 2 supplements
Cue responses of temporally discounted value coding.

(A, B) Activity of example neurons during cue period. Rasters and spike density histograms are aligned at cue onset. The color corresponds to each reward condition. Rasters are shown in order of …

Figure 3—figure supplement 1
Error trial analysis.

Table shows that the number of neurons whose activity is explained best by models 1–4. Note that linear mixed model (LMM) analysis was applied to 22 of 27 DV-coding neurons recorded in a session in …

Figure 3—figure supplement 2
Error trial analysis.

Example of differential activity between error and correct trials of a DV-coding neuron. Thin and thick dots indicate relationship between firing rate and temporally discounted value (Equation 1) in …

Figure 4 with 1 supplement
Impact of DV and comparison with delay and size on cue response.

(A, B) Scatterplots of standardized partial regression coefficients (SPRC) of DV (ordinate) against those for reward size or delay (abscissa) for discharge rates during cue period, respectively. …

Figure 4—figure supplement 1
Impact of DV and comparison with delay and size on release and reward response.

(A) Scatterplot of standardized partial regression coefficients (SPRC) of DV (ordinate) against those of size and delay on release response, respectively (abscissa). (B) Same as (A), but for reward …

Time course of DV coding.

(A, B) Time-dependent change of DV coding. Each row represents color-coded effect size (R2) of DV for a single DV-coding neuron. Responses were aligned by cue onset and bar release, respectively. (C,…

Figure 5—source data 1

Source data of time-dependent change of DV coding in individual neurons.

https://cdn.elifesciences.org/articles/61248/elife-61248-fig5-data1-v2.xls
Figure 6 with 1 supplement
Negligible effect of satiation on DV-coding.

(A) Ratio of error trials (mean ± sem) as a function of normalized cumulative reward (Rcum) on average across nine monkeys. Dotted curves are the best fit of Equation 4 to the data. (B) Error rates …

Figure 6—figure supplement 1
Impact of discounted value and satiation on cue response.

(A) Scatterplot of standardized regression coefficients (SRC) of discharge rates during cue period for DV (ordinate) against those for cumulative reward (abscissa). Red dots indicate DV-coding …

Figure 7 with 4 supplements
Bilateral inactivation of dCDh disrupted normal motivational performance based on size and delay.

(A) CT-based localization of muscimol injection sites. CT image visualizing injection cannulae targeting CD bilaterally (hot color) overlaid on MR image (gray scale) in monkey BI. Scale bar, 5 mm. (B

Figure 7—source data 1

Source data of error rates in control and inactivation sessions.

https://cdn.elifesciences.org/articles/61248/elife-61248-fig7-data1-v2.xls
Figure 7—figure supplement 1
No significant effects of dCDh inactivation on reaction time in delayed reward task.

Comparison of reaction time (mean ± SD) between baseline, control, and inactivation session in monkeys BI, RI, and ST.

Figure 7—figure supplement 2
No effect of dCDh inactivation on eye position.

Density plots of eye position during cue period of delayed reward task obtained from monkey RI. Colors indicate normalized looking-time. Left and right panels for control and inactivation sessions, …

Figure 7—figure supplement 3
Normalized error rates in baseline, control, and inactivation session of delayed reward task.

Symbols represent normalized error rates for each reward condition by maximum error rates in each session. Thick lines connect average error rates for three delay conditions in each reward size. …

Figure 7—figure supplement 4
Effect of dCDh inactivation on satiation.

Error rates (mean ± sem) as a function of normalized cumulative reward (Rcum) in baseline, control, and inactivation session of delayed reward task. Dotted curves are the best fit of Equation 4 to …

Figure 8 with 1 supplement
Reward-size task and behavioral performance.

(A) Cue stimuli used in reward-size task uniquely associated with forthcoming reward size (one, two, four, or eight drops). (B) Top: Error rates (mean ± sem) as function of reward size in muscimol …

Figure 8—source data 1

Source data of error rates in reward size task.

https://cdn.elifesciences.org/articles/61248/elife-61248-fig8-data1-v2.xls
Figure 8—figure supplement 1
Comparison of learning in reward size and delayed reward task.

(A) Monkey RI was trained with reward-size task followed by delayed reward task. (Top) Error rates as a function of session were plotted for both tasks. (Bottom) Error rates as a function of reward …

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