Dissociation of response and feedback negativity in schizophrenia: electrophysiological and computational evidence for a deficit in the representation of value (original) (raw)
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Neuropsychology, 2011
Objective: Patients with schizophrenia (SZ) show reinforcement learning impairments related to both the gradual/procedural acquisition of reward contingencies, and the ability to use trial-to-trial feedback to make rapid behavioral adjustments. Method: We used neurocomputational modeling to develop plausible mechanistic hypotheses explaining reinforcement learning impairments in individuals with SZ. We tested the model with a novel Go/NoGo learning task in which subjects had to learn to respond or withhold responses when presented with different stimuli associated with different probabilities of gains or losses in points. We analyzed data from 34 patients and 23 matched controls, characterizing positive-and negative-feedback-driven learning in both a training phase and a test phase. Results: Consistent with simulations from a computational model of aberrant dopamine input to the basal ganglia patients, patients with SZ showed an overall increased rate of responding in the training phase, together with reduced response-time acceleration to frequently rewarded stimuli across training blocks, and a reduced relative preference for frequently rewarded training stimuli in the test phase. Patients did not differ from controls on measures of procedural negative-feedback-driven learning, although patients with SZ exhibited deficits in trial-to-trial adjustments to negative feedback, with these measures correlating with negative symptom severity. Conclusions: These findings support the hypothesis that patients with SZ have a deficit in procedural "Go" learning, linked to abnormalities in DA transmission at D1-type receptors, despite a "Go bias" (increased response rate), potentially related to excessive tonic dopamine. Deficits in trial-to-trial reinforcement learning were limited to a subset of patients with SZ with severe negative symptoms, putatively stemming from prefrontal cortical dysfunction.
PLOS ONE
Several studies of self-monitoring dysfunction in schizophrenia have focused on the sense of agency to motor action using behavioral and psychophysiological techniques. So far, no study has ever tried to investigate whether the sense of agency or causal attribution for external events produced by self-generated decision-making is abnormal in schizophrenia. The purpose of this study was to investigate neural responses to feedback information produced by self-generated or other-generated decision-making in a multiplayer gambling task using even-related potentials and electroencephalogram synchronization. We found that the late positive component and theta/alpha synchronization were increased in response to feedback information in the self-decision condition in normal controls, but that these responses were significantly decreased in patients with schizophrenia. These neural activities thus reflect the self-reference effect that affects the cognitive appraisal of external events following decision-making and their impairment in schizophrenia.
NeuroImage, 2010
In patients with schizophrenia, the ability to learn from reinforcement is known to be impaired. The present fMRI study aimed at investigating the neural correlates of reinforcement-related trial-and-error learning in 19 schizophrenia patients and 20 healthy volunteers. A modified gambling paradigm was applied where each cue indicated a subsequent number which had to be guessed. In order to vary predictability, the cuenumber associations were based on different probabilities (50%, 81%, 100%) which the participants were not informed about. Patients' ability to learn contingencies on the basis of feedback and reward was significantly impaired. While in healthy volunteers increasing predictability was associated with decreasing activation in a fronto-parietal network, this decrease was not detectable in patients. Analysis of expectancy-related reinforcement processing yielded a hypoactivation in putamen, dorsal cingulate and superior frontal cortex in patients relative to controls. Present results indicate that both reinforcement-associated processing and reinforcement learning might be impaired in the context of the disorder. They moreover suggest that the activation deficits which patients exhibit in association with the processing of reinforcement might constitute the basis for the learning deficits and their accompanying activation alterations.
Biological psychiatry. Cognitive neuroscience and neuroimaging, 2018
While many have emphasized impaired reward prediction error signaling in schizophrenia, multiple studies suggest that some decision-making deficits may arise from overreliance on stimulus-response systems together with a compromised ability to represent expected value. Guided by computational frameworks, we formulated and tested two scenarios in which maladaptive representations of expected value should be most evident, thereby delineating conditions that may evoke decision-making impairments in schizophrenia. In a modified reinforcement learning paradigm, 42 medicated people with schizophrenia and 36 healthy volunteers learned to select the most frequently rewarded option in a 75-25 pair: once when presented with a more deterministic (90-10) pair and once when presented with a more probabilistic (60-40) pair. Novel and old combinations of choice options were presented in a subsequent transfer phase. Computational modeling was employed to elucidate contributions from stimulus-respon...
Decision-Making Impairments in the Context of Intact Reward Sensitivity in Schizophrenia
Biological Psychiatry, 2008
BACKGROUND: Deficits in motivated behavior and decision-making figure prominently in the behavioral syndrome that characterizes schizophrenia and are difficult both to treat and to understand. One explanation for these deficits is that schizophrenia decreases sensitivity to rewards in the environment. An alternate explanation is that sensitivity to rewards is intact but that poor integration of affective with cognitive information impairs the ability to use this information to guide behavior.
Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 2019
BACKGROUND: Motivational deficits in people with schizophrenia (PSZ) are associated with an inability to integrate the magnitude and probability of previous outcomes. The mechanisms that underlie probability-magnitude integration deficits, however, are poorly understood. We hypothesized that increased reliance on "valueless" stimulus-response associations, in lieu of expected value (EV)-based learning, could drive probability-magnitude integration deficits in PSZ with motivational deficits. METHODS: Healthy volunteers (n = 38) and PSZ (n = 49) completed a learning paradigm consisting of four stimulus pairs. Reward magnitude (3, 2, 1, 0 points) and probability (90%, 80%, 20%, 10%) determined each stimulus's EV. Following a learning phase, new and familiar stimulus pairings were presented. Participants were asked to select stimuli with the highest reward value. RESULTS: PSZ with high motivational deficits made increasingly less optimal choices as the difference in reward value (probability 3 magnitude) between two competing stimuli increased. Using a previously validated computational hybrid model, PSZ relied less on EV ("Q-learning") and more on stimulus-response learning ("actor-critic"), which correlated with Scale for the Assessment of Negative Symptoms motivational deficit severity. PSZ specifically failed to represent reward magnitude, consistent with model demonstrations showing that response tendencies in the actor-critic were preferentially driven by reward probability. CONCLUSIONS: Probability-magnitude deficits in PSZ with motivational deficits arise from underutilization of EV in favor of reliance on valueless stimulus-response associations. Confirmed by our computational hybrid framework, probability-magnitude integration deficits were driven specifically by a failure to represent reward magnitude. This work provides a first mechanistic explanation of complex EV-based learning deficits in PSZ with motivational deficits that arise from an inability to combine information from different reward modalities. Many people with schizophrenia (PSZ) suffer from a reduced tendency to engage in goal-directed behavior (1,2), termed amotivation or avolition. These deficits in motivation can contribute substantially to poor functional capacity and quality of life (3-5). One explanation suggests that motivational deficits result from a specific impairment in the ability to precisely represent the value of an action or choice (expected value [EV]) coupled with overreliance on "valueless" stimulus-response associations (6-8). Support for this computational account, however, comes from studies using reinforcement learning (RL) paradigms in which reward probability (the chance of obtaining a reward) solely determines EV. Importantly, other evidence indicates that EV estimation deficits in PSZ (with motivational deficits) are most prominent when EV depends on the successful integration of reward magnitude (size) and probability. One important line of evidence suggesting prominent deficits in EV representation comes from the Iowa Gambling Task (9), in which participants select from four card decks with varying reward magnitude and probability. Performance deficits on this task, in PSZ, are driven by a reduced ability to integrate long-term outcome magnitude and probability (10-12). These deficits extend to contexts in which participants choose between earning a small certain reward or gamble for a larger reward (a "framing" task) (13). When reward magnitude and probability vary continuously, impaired EV computations in PSZ with motivational deficits are primarily driven by decreased sensitivity to reward magnitude (14). In contrast, 280
Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 2018
BACKGROUND: The current study was designed to test the hypothesis that motivational deficits in schizophrenia (SZ) are tied to a reduced ability to differentially signal gains and instances of loss-avoidance in the brain, leading to reduced ability to form adaptive representations of expected value. METHODS: We administered a reinforcement learning paradigm to 27 medicated SZ patients and 27 control subjects in which participants learned three probabilistic discriminations. In regions of interest in reward networks identified a priori, we examined contrasts between trial types with different expected values (e.g., expected gain–nonmonetary) and between outcomes with the same prediction error valence but different experienced values (e.g., gain–loss- avoidance outcome, miss–loss outcome). RESULTS: Both whole-brain and region of interest analyses revealed that SZ patients showed reduced differentiation between gain and loss-avoidance outcomes in the dorsal anterior cingulate cortex and bilateral anterior insula. That is, SZ patients showed reduced contrasts between positive prediction errors of different objective values in these areas. In addition, we observed significant correlations between gain–loss-avoidance outcome contrasts in the ventral striatum and ratings for avolition/anhedonia and between expected gain–nonmonetary contrasts in the ventral striatum and ventromedial prefrontal cortex. CONCLUSIONS: These results provide further evidence for intact prediction error signaling in medicated SZ patients, especially with regard to loss-avoidance. By contrast, components of frontostriatal circuits appear to show reduced sensitivity to the absolute valence of expected and experienced outcomes, suggesting a mechanism by which motivational deficits may emerge.
Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 2017
BACKGROUND: The current study was designed to test the hypothesis that motivational deficits in schizophrenia (SZ) are tied to a reduced ability to differentially signal gains and instances of loss-avoidance in the brain, leading to reduced ability to form adaptive representations of expected value. METHODS: We administered a reinforcement learning paradigm to 27 medicated SZ patients and 27 control subjects in which participants learned three probabilistic discriminations. In regions of interest in reward networks identified a priori, we examined contrasts between trial types with different expected values (e.g., expected gain-nonmonetary) and between outcomes with the same prediction error valence but different experienced values (e.g., gain-lossavoidance outcome, miss-loss outcome). RESULTS: Both whole-brain and region of interest analyses revealed that SZ patients showed reduced differentiation between gain and loss-avoidance outcomes in the dorsal anterior cingulate cortex and bilateral anterior insula. That is, SZ patients showed reduced contrasts between positive prediction errors of different objective values in these areas. In addition, we observed significant correlations between gain-loss-avoidance outcome contrasts in the ventral striatum and ratings for avolition/anhedonia and between expected gain-nonmonetary contrasts in the ventral striatum and ventromedial prefrontal cortex. CONCLUSIONS: These results provide further evidence for intact prediction error signaling in medicated SZ patients, especially with regard to loss-avoidance. By contrast, components of frontostriatal circuits appear to show reduced sensitivity to the absolute valence of expected and experienced outcomes, suggesting a mechanism by which motivational deficits may emerge.
Abnormal Responses to Monetary Outcomes in Cortex, but not in the Basal Ganglia, in Schizophrenia
Neuropsychopharmacology, 2010
Psychosis has been associated with aberrant brain activity concurrent with both the anticipation and integration of monetary outcomes. The extent to which abnormal reward-related neural signals can be observed in chronic, medicated patients with schizophrenia (SZ), however, is not clear. In an fMRI study involving 17 chronic outpatients with SZ and 17 matched controls, we used a monetary incentive delay (MID) task, in which different-colored shapes predicted gains, losses, or neutral outcomes. Subjects needed to respond to a target within a time window in order to receive the indicated gain or avoid the indicated loss. Group differences in blood-oxygen-leveldependent responses to cues and outcomes were assessed through voxel-wise whole-brain analyses and regions-of-interest analyses in the neostriatum and prefrontal cortex (PFC). Significant group by outcome valence interactions were observed in the medial and lateral PFC, lateral temporal cortex, and amygdalae, such that controls, but not patients, showed greater activation for gains, relative to losses. In the striatum, neural activity was modulated by outcome magnitude in both groups. Additionally, we found that ratings of negative symptoms in patients correlated with sensitivity to obtained losses in medial PFC, obtained gains in lateral PFC, and anticipated gains in left ventral striatum. Sensitivity to obtained gains in lateral PFC also correlated with positive symptom scores in patients. Our findings of systematic relationships between clinical symptoms and neural responses to stimuli associated with rewards and punishments offer promise that reward-related neural responses may provide sensitive probes of the effectiveness of treatments for negative symptoms.