Dissociation of response and feedback negativity in schizophrenia: electrophysiological and computational evidence for a deficit in the representation of value

Sarah E Morris, Clay B Holroyd, Monica C Mann-Wrobel, James M Gold, Sarah E Morris, Clay B Holroyd, Monica C Mann-Wrobel, James M Gold

Abstract

Contrasting theories of schizophrenia propose that the disorder is characterized by a deficit in phasic changes in dopamine activity in response to ongoing events or, alternatively, by a weakness in the representation of the value of responses. Schizophrenia patients have reliably reduced brain activity following incorrect responses but other research suggests that they may have intact feedback-related potentials, indicating that the impairment may be specifically response-related. We used event-related brain potentials and computational modeling to examine this issue by comparing the neural response to outcomes with the neural response to behaviors that predict outcomes in patients with schizophrenia and psychiatrically healthy comparison subjects. We recorded feedback-related activity in a passive gambling task and a time estimation task and error-related activity in a flanker task. Patients' brain activity following an erroneous response was reduced compared to comparison subjects but feedback-related activity did not differ between groups. To test hypotheses about the possible causes of this pattern of results, we used computational modeling of the electrophysiological data to simulate the effects of an overall reduction in patients' sensitivity to feedback, selective insensitivity to positive or negative feedback, reduced learning rate, and a decreased representation of the value of the response given the stimulus on each trial. The results of the computational modeling suggest that schizophrenia patients exhibit weakened representation of response values, possibly due to failure of the basal ganglia to strongly associate stimuli with appropriate response alternatives.

Keywords: dopamine; error-related negativity; feedback; reward; schizophrenia.

Figures

Figure 1
Figure 1
Group averages for feedback ERN elicited by second stimulus in the passive gambling task. Data shown in waveforms are from Cz. The scoring window for the difference waves is indicated by the rectangle.
Figure 2
Figure 2
Five-trial running average of absolute RT deviation from target RT for the time estimation task. Bar graph shows mean of absolute RT deviation. Error bars indicate SE.
Figure 3
Figure 3
Feedback-locked ERN group averages for the time estimation task. Data shown in waveforms are from FCz. Data in maps are shown at latency of maximal difference wave amplitude. The scoring window for the difference waves is indicated by the rectangle.
Figure 4
Figure 4
Mean accuracy (top) and RT (bottom) for the flanker task. Error bars indicate SE.
Figure 5
Figure 5
Response-locked ERN group averages for the flanker task. Data shown in waveforms are from FCz. Topographical maps depict distribution of difference wave at latency of peak negativity. The scoring window for the difference waves is indicated by the rectangle.
Figure 6
Figure 6
Empirical control and schizophrenia ERN difference wave data (mean amplitude and SE) for the probabilistic learning task, for the response ERN (top) and feedback ERN (bottom). Note that “80%v” and “80%i” correspond to trials in the 80% condition with either valid or invalid feedback, respectively. Data recorded at FCz and re-analyzed from Morris et al. (2008).
Figure 7
Figure 7
Simulated control (default model) and schizophrenia (maximum value model) ERN difference wave data for the probabilistic learning task, for the response ERN (top) and feedback ERN (bottom). Note that “80%v” and “80%i” correspond to 80% condition trials with either valid or invalid feedback, respectively.
Figure 8
Figure 8
Sum of squared errors (SSE) for each of the probabilistic learning task simulations. Note that the horizontal dashed line at SSE = 0.14 indicates the error value associated with the control simulation compared to the empirical control data and the horizontal gray dotted line at SSE = 0.36 indicates the SSE of the control simulation data compared to the empirical schizophrenia data; values below this line indicate better fits.
Figure 9
Figure 9
Error-related negativity difference wave data for the probabilistic learning task, for the response ERN (top) and feedback ERN (bottom), for the simulated and empirical schizophrenia data. Note that “80%v” and “80%i” correspond to 80% condition trials with either valid or invalid feedback, respectively. Empirical data are from FCz.
Figure 10
Figure 10
Simulated response ERNs for the Eriksen flanker task.

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