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Neural signal during immediate reward anticipation in schizophrenia: Relationship to real-world motivation and function.

Subramaniam K, Hooker CI, Biagianti B, Fisher M, Nagarajan S, Vinogradov S - Neuroimage Clin (2015)

Bottom Line: In healthy comparison (HC) participants, reward anticipation is associated with activity in frontal-striatal networks.SZ patients showed hypoactivation in ventral striatum during reward anticipation.Additionally, we found distinct differences between HC and SZ groups in their association between reward-related immediate anticipatory neural activity and their reported experience of pleasure.

View Article: PubMed Central - PubMed

Affiliation: San Francisco Department of Veterans Affairs Medical Center, Department of Psychiatry, University of California, San Francisco, CA 94121, USA.

ABSTRACT
Amotivation in schizophrenia is a central predictor of poor functioning, and is thought to occur due to deficits in anticipating future rewards, suggesting that impairments in anticipating pleasure can contribute to functional disability in schizophrenia. In healthy comparison (HC) participants, reward anticipation is associated with activity in frontal-striatal networks. By contrast, schizophrenia (SZ) participants show hypoactivation within these frontal-striatal networks during this motivated anticipatory brain state. Here, we examined neural activation in SZ and HC participants during the anticipatory phase of stimuli that predicted immediate upcoming reward and punishment, and during the feedback/outcome phase, in relation to trait measures of hedonic pleasure and real-world functional capacity. SZ patients showed hypoactivation in ventral striatum during reward anticipation. Additionally, we found distinct differences between HC and SZ groups in their association between reward-related immediate anticipatory neural activity and their reported experience of pleasure. HC participants recruited reward-related regions in striatum that significantly correlated with subjective consummatory pleasure, while SZ patients revealed activation in attention-related regions, such as the IPL, which correlated with consummatory pleasure and functional capacity. These findings may suggest that SZ patients activate compensatory attention processes during anticipation of immediate upcoming rewards, which likely contribute to their functional capacity in daily life.

No MeSH data available.


Related in: MedlinePlus

Illustration of one MID trial.
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f0005: Illustration of one MID trial.

Mentions: We used a standard Monetary Incentive Delay (MID) task, as described by Knutson et al. (2001), to assay the neural patterns associated with immediate anticipation and outcome of monetary reward (gain) and punishment (loss) in SZ and HC participants (Knutson et al., 2001). The MID paradigm is a Reaction Time (RT) task in which each trial has a pre-established monetary value. At the beginning of each trial, a cue (i.e., marking the onset of an anticipatory period) indicates the amount of money at stake on that trial: Win cues indicate potential monetary gain, Null cues indicate no monetary gain/no outcome, and Lose cues indicate potential monetary loss (Fig. 1). When the cue is presented, participants anticipate making a speeded response to the target (a white square), which is presented on the screen after a variable fixation interval (i.e., the anticipation period, duration from 2, 4, 6 or 8 s, randomized across all trials). Such variable delays were used to jitter the events and optimize deconvolution of the fMRI signal from successive events. After participants respond to the target, they receive feedback on how they performed on that trial in terms of receiving rewarding, punishing or neutral feedback. Specifically, on Win trials, participants are informed as to whether or not they won money; on Null trials, participants receive neutral feedback that they did not win/lose money; and on Lose trials, participants are informed as to whether or not they lost money on that trial. After the feedback prompt, there is a variable inter-trial-interval (ITI), jittered between 2, 4, 6, or 8 s randomized across all trials, after which the next cue is presented (marking the onset of the next anticipatory period). Participants succeed on the trial if the response happens within a fixed time window. For example, for each participant, performance level was titrated at 68% accuracy, such that the response window determining success was based on the participant's mean RT within one standard deviation of the mean averaged across performance based on the previous run. Responses to the first run were roughly titrated at 68% accuracy based on a previous practice run. Responses to the white square were captured for the total target presentation duration (i.e., 0.5 s); however, participants were specifically instructed to respond as fast as possible as soon as the target appeared. Early responses prior to target onset were not considered and participants were instructed not to make multiple responses. Each run consisted of 60 trials: 20 Win trials, 20 Null trials and 20 Loss trials, pseudorandomized. Participants completed 3 runs altogether, with each run lasting for a total time of 12 min and 24 s. Participants were provided with money based on their maximum earnings on their best performance run. Overall accuracy for each participant was calculated by computing the total number of Win trials and No-Loss trials, averaged across the three runs.


Neural signal during immediate reward anticipation in schizophrenia: Relationship to real-world motivation and function.

Subramaniam K, Hooker CI, Biagianti B, Fisher M, Nagarajan S, Vinogradov S - Neuroimage Clin (2015)

Illustration of one MID trial.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4556736&req=5

f0005: Illustration of one MID trial.
Mentions: We used a standard Monetary Incentive Delay (MID) task, as described by Knutson et al. (2001), to assay the neural patterns associated with immediate anticipation and outcome of monetary reward (gain) and punishment (loss) in SZ and HC participants (Knutson et al., 2001). The MID paradigm is a Reaction Time (RT) task in which each trial has a pre-established monetary value. At the beginning of each trial, a cue (i.e., marking the onset of an anticipatory period) indicates the amount of money at stake on that trial: Win cues indicate potential monetary gain, Null cues indicate no monetary gain/no outcome, and Lose cues indicate potential monetary loss (Fig. 1). When the cue is presented, participants anticipate making a speeded response to the target (a white square), which is presented on the screen after a variable fixation interval (i.e., the anticipation period, duration from 2, 4, 6 or 8 s, randomized across all trials). Such variable delays were used to jitter the events and optimize deconvolution of the fMRI signal from successive events. After participants respond to the target, they receive feedback on how they performed on that trial in terms of receiving rewarding, punishing or neutral feedback. Specifically, on Win trials, participants are informed as to whether or not they won money; on Null trials, participants receive neutral feedback that they did not win/lose money; and on Lose trials, participants are informed as to whether or not they lost money on that trial. After the feedback prompt, there is a variable inter-trial-interval (ITI), jittered between 2, 4, 6, or 8 s randomized across all trials, after which the next cue is presented (marking the onset of the next anticipatory period). Participants succeed on the trial if the response happens within a fixed time window. For example, for each participant, performance level was titrated at 68% accuracy, such that the response window determining success was based on the participant's mean RT within one standard deviation of the mean averaged across performance based on the previous run. Responses to the first run were roughly titrated at 68% accuracy based on a previous practice run. Responses to the white square were captured for the total target presentation duration (i.e., 0.5 s); however, participants were specifically instructed to respond as fast as possible as soon as the target appeared. Early responses prior to target onset were not considered and participants were instructed not to make multiple responses. Each run consisted of 60 trials: 20 Win trials, 20 Null trials and 20 Loss trials, pseudorandomized. Participants completed 3 runs altogether, with each run lasting for a total time of 12 min and 24 s. Participants were provided with money based on their maximum earnings on their best performance run. Overall accuracy for each participant was calculated by computing the total number of Win trials and No-Loss trials, averaged across the three runs.

Bottom Line: In healthy comparison (HC) participants, reward anticipation is associated with activity in frontal-striatal networks.SZ patients showed hypoactivation in ventral striatum during reward anticipation.Additionally, we found distinct differences between HC and SZ groups in their association between reward-related immediate anticipatory neural activity and their reported experience of pleasure.

View Article: PubMed Central - PubMed

Affiliation: San Francisco Department of Veterans Affairs Medical Center, Department of Psychiatry, University of California, San Francisco, CA 94121, USA.

ABSTRACT
Amotivation in schizophrenia is a central predictor of poor functioning, and is thought to occur due to deficits in anticipating future rewards, suggesting that impairments in anticipating pleasure can contribute to functional disability in schizophrenia. In healthy comparison (HC) participants, reward anticipation is associated with activity in frontal-striatal networks. By contrast, schizophrenia (SZ) participants show hypoactivation within these frontal-striatal networks during this motivated anticipatory brain state. Here, we examined neural activation in SZ and HC participants during the anticipatory phase of stimuli that predicted immediate upcoming reward and punishment, and during the feedback/outcome phase, in relation to trait measures of hedonic pleasure and real-world functional capacity. SZ patients showed hypoactivation in ventral striatum during reward anticipation. Additionally, we found distinct differences between HC and SZ groups in their association between reward-related immediate anticipatory neural activity and their reported experience of pleasure. HC participants recruited reward-related regions in striatum that significantly correlated with subjective consummatory pleasure, while SZ patients revealed activation in attention-related regions, such as the IPL, which correlated with consummatory pleasure and functional capacity. These findings may suggest that SZ patients activate compensatory attention processes during anticipation of immediate upcoming rewards, which likely contribute to their functional capacity in daily life.

No MeSH data available.


Related in: MedlinePlus