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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

ROI analyses during immediate reward anticipation: correlations with trait hedonic pleasure. HC = black circles, red correlation values; SZ = white circles, blue correlation values.
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f0020: ROI analyses during immediate reward anticipation: correlations with trait hedonic pleasure. HC = black circles, red correlation values; SZ = white circles, blue correlation values.

Mentions: SZ patients exhibited marginally reduced levels of future representations of anticipatory pleasure (i.e., TEPS anticipatory pleasure) compared to healthy participants (p = .08), although they exhibited similar arousal levels when viewing the Win cue, as well as similar levels of consummatory pleasure (i.e., TEPS consummatory pleasure) as HC participants (all p values > .20). However, interestingly, we found distinct differences between the HC and SZ groups in terms of their neural signal association with the TEPS consummatory pleasure scale. Specifically, the HC group revealed neural activity in four regions during reward anticipation that predicted higher self-ratings of TEPS consummatory pleasure; this association was found in: left putamen (r = .53, df = 18, p = .02), VS (r = .48, df = 18, p = .03), mPFC (r = .45, df = 18, p = .04), and right putamen (r = .44, df = 18, p = .05). In contrast, the SZ group revealed signal increase in only one region, the right IPL, that predicted higher self-ratings in TEPS consummatory pleasure (r = .35, df = 33, p = .04) (Fig. 4). Signal in right IPL was also associated with higher self-ratings on BAS-Drive (r = .39, df = 33, p = .02) while signal in the left IPL predicted better real-world functional capacity, as measured by the UPSA (r = .34, df = 33, p = .05). Finally, whole-brain regression analyses provide additional confirmatory evidence that TEPS anticipatory pleasure, TEPS consummatory pleasure and BAS-Drive predicted R. IPL signal during immediate reward anticipation in schizophrenia patients (see Supplementary Fig. 1). Although, Fisher r-to-z transformations did not reveal any significant between-group difference in the strength of the association between R. IPL and TEPS consummatory pleasure (z = .58, p = .28), we did find a significant between-group difference in the relation between TEPS consummatory pleasure and ventral striatum (z = 1.91, p = .03), left putamen (z = 2.57, p = .005), as well as mPFC (z = 2.57, p = .005). Together, these findings suggest that SZ and HC participants show significantly different associations between frontal–striatal activation during anticipation of immediate rewards, and self-ratings of real-world reward responsivity.


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)

ROI analyses during immediate reward anticipation: correlations with trait hedonic pleasure. HC = black circles, red correlation values; SZ = white circles, blue correlation values.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

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

f0020: ROI analyses during immediate reward anticipation: correlations with trait hedonic pleasure. HC = black circles, red correlation values; SZ = white circles, blue correlation values.
Mentions: SZ patients exhibited marginally reduced levels of future representations of anticipatory pleasure (i.e., TEPS anticipatory pleasure) compared to healthy participants (p = .08), although they exhibited similar arousal levels when viewing the Win cue, as well as similar levels of consummatory pleasure (i.e., TEPS consummatory pleasure) as HC participants (all p values > .20). However, interestingly, we found distinct differences between the HC and SZ groups in terms of their neural signal association with the TEPS consummatory pleasure scale. Specifically, the HC group revealed neural activity in four regions during reward anticipation that predicted higher self-ratings of TEPS consummatory pleasure; this association was found in: left putamen (r = .53, df = 18, p = .02), VS (r = .48, df = 18, p = .03), mPFC (r = .45, df = 18, p = .04), and right putamen (r = .44, df = 18, p = .05). In contrast, the SZ group revealed signal increase in only one region, the right IPL, that predicted higher self-ratings in TEPS consummatory pleasure (r = .35, df = 33, p = .04) (Fig. 4). Signal in right IPL was also associated with higher self-ratings on BAS-Drive (r = .39, df = 33, p = .02) while signal in the left IPL predicted better real-world functional capacity, as measured by the UPSA (r = .34, df = 33, p = .05). Finally, whole-brain regression analyses provide additional confirmatory evidence that TEPS anticipatory pleasure, TEPS consummatory pleasure and BAS-Drive predicted R. IPL signal during immediate reward anticipation in schizophrenia patients (see Supplementary Fig. 1). Although, Fisher r-to-z transformations did not reveal any significant between-group difference in the strength of the association between R. IPL and TEPS consummatory pleasure (z = .58, p = .28), we did find a significant between-group difference in the relation between TEPS consummatory pleasure and ventral striatum (z = 1.91, p = .03), left putamen (z = 2.57, p = .005), as well as mPFC (z = 2.57, p = .005). Together, these findings suggest that SZ and HC participants show significantly different associations between frontal–striatal activation during anticipation of immediate rewards, and self-ratings of real-world reward responsivity.

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