Figures and data in Dopamine promotes instrumental motivation, but reduces reward-related vigour

Version of Record: November 30, 2020
Version of Record: October 30, 2020
Accepted Manuscript: October 1, 2020

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John P Grogan

Timothy R Sandhu

Michele T Hu

Sanjay G Manohar

(2020)
Dopamine promotes instrumental motivation, but reduces reward-related vigour

eLife 9:e58321.

https://doi.org/10.7554/eLife.58321
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Figures
Tables
Additional files

8 figures, 4 tables and 5 additional files

Figures

Figure 1

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Saccade task design and example eye-tracking traces.

(a) Trial design: participants fixated on the centre, heard a cue for the condition (Performance/Random/10 p/0 p), waited a delay (1400/1500/1600 ms) and then looked towards to the circle that lit …

Figure 2

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Differential effects of dopamine on two types of motivation.

The mean measures for the four conditions (Performance, Random, Guaranteed 10p, Guaranteed 0p) for each variable, with individual data points. The difference between Performance and Random shows the …

Figure 2—source data 1 Source individual data for all saccade measures for PD ON, OFF and HC. The figures can be constructed using the DrawSaccadeFigures.m Matlab file available from the ContingentAnalysis GitHub repo (see Data and Code Availability section of manuscript).: https://cdn.elifesciences.org/articles/58321/elife-58321-fig2-data1-v3.mat.zip
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Figure 3 with 1 supplement

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Motivational effects on instantaneous velocity and acceleration within a saccade.

The top row shows the effects of contingent rewards (i.e. measures in Performance conditions minus the Random condition), and the bottom row shows effects of guaranteed rewards (10 p condition minus …

Figure 3—source data 1 Source individual data for saccade velocity and acceleration for PD ON, OFF and HC. The figures can be constructed using the DrawVelFigures.m Matlab file available from the ContingentAnalysis GitHub repo (see Data and Code Availability section of manuscript).: https://cdn.elifesciences.org/articles/58321/elife-58321-fig3-data1-v3.mat.zip
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Figure 3—figure supplement 1

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Individual participants’ velocity and acceleration traces.

Individual data showing each participant’s mean effects of contingent (Performance – Random) and guaranteed (10 p – 0 p) rewards on velocity and acceleration during saccades.

Figure 4 with 1 supplement

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Motivational effects on eye-position autocorrelation within saccades.

Each image shows the effect of reward on mean correlation coefficient between the eye-position at one (interpolated) time-point within a saccade with all other time-points in that same saccade. As …

Figure 4—source data 1 Source individual data for autocorrelation coefficients for PD ON, OFF and HC. The figures can be constructed using the DrawAutocorrelFigures.m Matlab file available from the ContingentAnalysis GitHub repo (see Data and Code Availability section of manuscript).: https://cdn.elifesciences.org/articles/58321/elife-58321-fig4-data1-v3.mat.zip
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Figure 4—source data 2 Individual participants’ autocorrelation matrices. Individual data showing each participant’s mean effects of contingent (Performance – Random) and guaranteed (10 p – 0 p) rewards on (Fisher transformed) eye-position autocorrelation matrices. Blank matrices for PD patients reflect excluded participants.: https://cdn.elifesciences.org/articles/58321/elife-58321-fig4-data2-v3.pdf
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Figure 4—figure supplement 1

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Motivational effects on time-time covariance within saccades.

Each plot shows the effect of motivation (top row = contingent, bottom row = guaranteed) on the signed log covariance matrix, for PD ON, OFF, HC, and the difference between PD ON and OFF. Green …

Figure 5

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No correlations between contingent and guaranteed rewards.

Scatter plots of the effect of contingent and guaranteed rewards (i.e. contingent effect = Performance minus Random trials, guaranteed effect = guaranteed 10 p minus guaranteed 0 p trials) on peak …

Figure 5—source data 1 Source individual data for velocity residual correlations for PD ON, OFF and HC. The figures can be constructed using the DrawCorrelFigures.m Matlab file available from the ContingentAnalysis GitHub repo (see Data and Code Availability section of manuscript).: https://cdn.elifesciences.org/articles/58321/elife-58321-fig5-data1-v3.mat.zip
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Figure 6 with 2 supplements

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No effects of motivation on pupil dilatation.

The effects of contingent (top) and guaranteed rewards (bottom) on pupil dilatation in the different conditions up to 1400 ms after the reward cue. Pupil dilatation is baselined to the time of cue …

Figure 6—source data 1 Source individual data for pupil dilatation for PD ON, OFF and HC. The figures can be constructed using the DrawPupilFigures.m Matlab file available from the ContingentAnalysis GitHub repo (see Data and Code Availability section of manuscript).: https://cdn.elifesciences.org/articles/58321/elife-58321-fig6-data1-v3.mat.zip
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Figure 6—figure supplement 1

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No correlation of pupil dilatation and motivational effects on velocity.

Scatter plots of the effect of contingent and guaranteed rewards (i.e. contingent effect = Performance minus Random trials, guaranteed effect = guaranteed 10 p minus guaranteed 0 p trials) on pupil …

Figure 6—figure supplement 2

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Individual data for pupil dilatation.

Individual participants’ mean pupil dilatation traces for each condition, showing the effects of contingent (Performance – Random) and guaranteed (10 p – 0 p) rewards.

Figure 7

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Proposed model for dopaminergic dissociation of reward expectation and contingent motivation.

We propose that dopamine (in PD patients) increases contingent motivation by acting on the caudate nucleus, which disinhibits the superior colliculus (via the basal ganglia output nuclei) and …

Author response image 1

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Tables

Table 1

Participant demographics for PD patients and Healthy Controls (HC) included in the analysis.

Standard deviations are given in parentheses. **=p < 0.01 (independent samples t-test). ACE = Addenbrooke’s Cognitive Exam, AMI = Apathy and Motivation Index, HADS = Hospital Anxiety and Depression …

	PD	HC
Number	26	29
Age	67.69 (1.48)	67.41 (6.83)
Gender (M:F)	19:7	15:14
ACE	93.04 (6.47)	97.10 (2.11)**
AMI	1.48 (0.56)	1.28 (0.47)
HADS-A	2.92 (2.92)	4.29 (2.79)
HADS-D	2.50 (1.84)	2.17 (1.83)
BDI-II	4.90 (3.60)	5.84 (3.78)
FSS	3.19 (1.21)	3.02 (1.03)
UPDRS-III ON	26.69 (9.20)	N/A
UPDRS-III OFF	35.04 (11.17)	N/A
LED	490.23 (324.28)	N/A
# on agonists	6	N/A

Table 2

Statistics for main behavioural analyses.

Three-way (motivation*contingency*drug) repeated-measures ANOVA on each behavioural measure, for the PD patients ON and OFF medication. An effect of contingency means the guaranteed conditions (10 …

Measure	Effect	F (1, 200)	p	$η_{p}^{2}$
Peak Velocity Residuals	Motivation	9.7704	*.0020	.0466
	Contingency	0.0194	. 8895	. 0001
	Drug	0.0004	. 9850	. 0000
	Motivation * Contingency	0.0051	. 9429	. 0000
	Motivation * Drug	0.2626	. 6089	. 0013
	Contingency * Drug	11.1072	**.0010	. 0526
	Contingency * Motivation * Drug	9.5190	**.0023	. 0454
Amplitude	Motivation	3.5577	. 0607	. 0175
	Contingency	1.2284	. 2690	. 0061
	Drug	0.0000	. 9984	. 0000
	Motivation * Contingency	0.5545	. 4573	. 0028
	Motivation * Drug	0.2278	. 6337	. 0011
	Contingency * Drug	1.7763	. 1841	. 0088
	Contingency * Motivation * Drug	0.0287	. 8655	. 0001
Saccadic RT	Motivation	3.4333	. 0654	. 0169
	Contingency	4.2922	*.0396	. 0210
	Drug	0.3560	. 5514	. 0018
	Motivation * Contingency	0.3663	. 5457	. 0018
	Motivation * Drug	0.0694	. 7925	. 0003
	Contingency * Drug	0.6246	. 4303	. 0031
	Contingency * Motivation * Drug	0.0185	. 8920	. 0001
Endpoint Variability	Motivation	2.6780	. 1033	. 0132
	Contingency	3.6181	. 0586	. 0178
	Drug	1.0095	. 3162	. 0050
	Motivation * Contingency	3.9524	*.0482	. 0194
	Motivation * Drug	1.2787	. 2595	. 0064
	Contingency * Drug	1.3819	. 2412	. 0069
	Contingency * Motivation * Drug	0.1626	. 6872	. 0008
Raw Peak Velocity	Motivation	6.5921	*.0110	.0319
	Contingency	0.3831	.5366	.0019
	Drug	1.8937	.1703	.0094
	Motivation * Contingency	0.1179	.7316	.0006
	Motivation * Drug	0.0563	.8126	.0003
	Contingency * Drug	0.5462	.4608	.0027
	Contingency * Motivation * Drug	2.4061	.1224	.0119

Table 3

Statistics for behavioural analysis on HC saccade data.

HC had a motivation*contingency interaction for endpoint variability, as only expected rewards decreased variability. **=p < 0.01.

Group	Effect	F (df = 1, 112)	p	$η_{p}^{2}$
Peak Velocity Residuals	Motivation	0.9019	. 3443	. 0080
	Contingency	0.3463	. 5574	. 0031
	Motivation * Contingency	0.6995	. 4047	. 0062
Amplitude	Motivation	2.3510	. 1280	. 0206
	Contingency	0.0255	. 8734	. 0002
	Motivation * Contingency	1.2551	. 2650	. 0111
Saccade RT	Motivation	3.2227	. 0753	. 0280
	Contingency	2.5743	. 1114	. 0225
	Motivation * Contingency	2.7992	. 0971	. 0244
Endpoint Variability	Motivation	0.9304	. 3368	. 0082
	Contingency	0.6651	. 4165	. 0059
	Motivation * Contingency	8.2781	**.0048	. 0688
Raw Peak Velocity	Motivation	1.1321	.2896	.0100
	Contingency	0.1615	.6885	.0014
	Motivation * Contingency	0.2538	.6154	.0023

Author response table 1

	Effect	Estimate	t	p
Peak Velocity Residuals	Motivation	3.0488	1.922	0.0546
	Contingency	0.1392	0.0878	0.9301
	Drug	-0.0539	-0.0339	0.9729
	Motivation * Contingency	0.2380	0.1500	0.8808
	Motivation * Drug	0.5420	0.3417	0.7326
	Contingency * Drug	2.6239	1.6542	0.0981
	Contingency * Motivation * Drug	3.5318	2.2266	*0.0260