Adult age differences in frontostriatal representation of prediction error but not reward outcome

Samanez-Larkin, Gregory R.; Worthy, Darrell A.; Mata, Rui; McClure, Samuel M.; Knutson, Brian

doi:10.3758/s13415-014-0297-4

Cited by 96 publications

(144 citation statements)

References 51 publications

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“…For example, a recent study showed that ventral striatal activity was increased in older adults when receiving reward but not during anticipation (Vink et al 2015). This is also consistent with findings indicating that representation of reward outcome is stable in aging, compared with representation of prediction error (Samanez-Larkin et al 2014). Thus, despite the well-documented decline in dopaminergic activity in older adults (for review, see Li and Rieckmann 2014), it is possible that at least a subset of older adults exhibit enhanced processing of rewarding information, however, this account remains speculative.…”

supporting

confidence: 76%

Positivity effect specific to older adults with subclinical memory impairment

et al. 2016

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Numerous studies have suggested that older adults preferentially remember positive information ("positivity effect"), however others have reported mixed results. One potential source of conflict is that aging is not a unitary phenomenon and individual differences exist. We modified a standard neuropsychological test to vary emotional content and tested memory at three time points (immediate/20 min/1 wk). Cognitively normal older adults were stratified into those with and without subclinical memory impairment. We found that the positivity effect was limited to those with subclinical memory impairment, suggesting that consideration of subclinical memory impairment is necessary for understanding age-related emotional memory alterations.[Supplemental material is available for this article.]Increasing age is the greatest risk factor for developing mild cognitive impairment (MCI) and Alzheimer's disease (AD) (Thies and Bleiler 2011). Thus, it is vital to understand neurocognitive changes that occur during the aging process to identify early phenotypes that may be associated with later cognitive decline. Memory impairment is one of the hallmark cognitive dysfunctions in healthy aging and is a major symptom of MCI and AD. There is extensive evidence that episodic memory, or memory for events, generally declines with age (Craik and Simon 1980;Glisky 2007). However, some studies suggest that there is a "positivity effect," where older adults may be more likely to attend to and remember positive information (Mather and Carstensen 2005;Wong et al. 2012). On the other hand, some studies have suggested that older adults are biased toward remembering negative details (Kensinger et al. 2007) or show no evidence of such an age-related positivity bias (Grühn et al. 2005;Fernandes et al. 2008). One potential source of conflict is that aging is not a uniform phenomenon and individual differences are frequently observed in older adults.There are numerous approaches to examining individual differences with age. One such approach dichotomizes older rats into two groups (Gallagher et al. 1993). One group of older rats performs on par with young rats on the Morris Water Maze (i.e., "aged-unimpaired"-AU), while another group performs outside of the range of young rat performance (i.e., "aged-impaired"-AI). This approach has been used to examine the aged brain in which this dichotomy maps onto neurobiological alterations associated with medial temporal lobe dysfunction, including synaptic loss in the perforant path (Smith et al. 2000), loss of inhibitory tone (Spiegel et al. 2013), hyperexcitability in the CA3 subregion of the hippocampus (Wilson et al. 2004(Wilson et al. , 2005, as well as loss of reelin and increased phosphorylated tau expression in the lateral entorhinal cortex (Stranahan et al. 2011). In humans, we have used a similar approach and have found that individual differences in age-related memory impairment (as defined by performance on the Rey Auditory Verbal Learning Test-RAVLT, a word-list learning task) was associated w...

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confidence: 76%

Positivity effect specific to older adults with subclinical memory impairment

et al. 2016

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“…Task-related activity in the fronto-striatal circuit was also affected by age, where older adults generally showed stronger responses to factual and counterfactual consequences in the striatum, but a non-significant correlation with reward predictions in the vmPFC. Our findings are in general agreement with previous literature showing that relatively poor decision making in multialternative choice tasks in older adults is related to aberrant reward prediction and prediction error processing in this fronto-striatal circuit (Chowdhury et al, 2013;Eppinger, Walter et al, 2013;Eppinger, Nystrom, et al, 2012;Eppinger, Schuck, et al, 2013;Grady, 2012;Hedden & Gabrieli, 2004;Rademacher, Saalma, Grunder, & Sprecklemeyer, 2014;SamanezLarkin et al, 2007;Samanez-Larkin et al, 2011;Samanez-Larkin et al, 2014;Samanez-Larkin & Knutson, 2015;Vink et al, 2015;), and extends these findings to include altered processing of counterfactual consequences. Finally, this study advocates the modelbased fMRI experimental design to study both behavioral and neural systems for decision making between age groups but cautions that model fits be carefully taken into account when drawing conclusions about group differences.…”

Section: Discussionsupporting

confidence: 82%

Altered behavioral and neural responsiveness to counterfactual gains in the elderly

Tobia

Guo

Gläscher

et al. 2016

Cogn Affect Behav Neurosci

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Counterfactual information processing refers to the consideration of events that did not occur in comparison to those actually experienced, in order to determine optimal actions, and can be formulated as computational learning signals, referred to as fictive prediction errors. Decision making and the neural circuitry for counterfactual processing are altered in healthy elderly adults. This experiment investigated age differences in neural systems for decision making with knowledge of counterfactual outcomes. Two groups of healthy adult participants, young (N = 30; ages 19-30 years) and elderly (N = 19; ages 65-80 years), were scanned with fMRI during 240 trials of a strategic sequential investment task in which a particular strategy of differentially weighting counterfactual gains and losses during valuation is associated with more optimal performance. Elderly participants earned significantly less than young adults, differently weighted counterfactual consequences and exploited task knowledge, and exhibited altered activity in a fronto-striatal circuit while making choices, compared to young adults. The degree to which task knowledge was exploited was positively correlated with modulation of neural activity by expected value in the vmPFC for young adults, but not in the elderly. These findings demonstrate that elderly participants' poor task performance may be related to different counterfactual processing.

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Section: Introductionmentioning

confidence: 99%

“…This reward prediction error (RPE) signal is thought to have an interplay with prefrontal cortical areas such as the prefrontal cortex (PFC) and the anterior cingulate cortex (ACC) [14,17,18]. This frontostriatal circuit with dopaminergic activation plays an essential role in reward seeking behavior and decision making [19,20], and the ERPs related to feedback evaluation, like the FRN and the reward positivity, are assumed to be the correlates of the activity of this dopaminergic circuit [17,21,22].The FRN occurring at approximately 250 ms after feedback onset corresponds mainly to the erroneous nature of the outcome [22,23]. Contrary to this, the reward positivity (occurring in a similar time window as the FRN) is elicited by positive feedback informing about reward [24][25][26].…”

mentioning

confidence: 99%

“…Accordingly, imaging approaches suggest that the elderly have difficulties in representing outcome values during predictive processing due to decreased frontostriatal connectivity with age [5,20]. Furthermore, the activity of the dopaminergic system also declines during aging, which results in higher signal-to-noise ratio in the frontostriatal communication pathway [37][38][39].…”

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confidence: 99%

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Age-related characteristics of risky decision-making and progressive expectation formation

Kardos

Kóbor

Takács

et al. 2016

Behavioural Brain Research

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During daily encounters, it is inevitable that people take risks. Investigating the sequential processing of risk hazards involve expectation formation about outcome contingencies. The present study aimed to explore risk behavior and its neural correlates in sequences of decision making, particularly in old age, which represents a critical period regarding risk-taking propensity. The Balloon Analogue Risk Task was used in an electrophysiological setting with young and elderly age groups. During the task each additional pump on a virtual balloon increased the likelihood of a balloon burst but also increased the chance to collect more reward. Event-related potentials associated with rewarding feedback were analyzed based on the forthcoming decisions (whether to continue or to stop) in order to differentiate between states of expectation towards gain or loss. In the young, the reward positivity ERP component increased as a function of reward contingencies with the largest amplitude for rewarding feedback followed by the decision to stop. In the elderly, however, reward positivity did not reflect the effect of reward structure. Behavioral indices of risk-taking propensity suggest that the performance of the young and the elderly were dissociable only with respect to response times: The elderly was characterized by hesitation and more deliberative decision making throughout the experiment. These findings signify that sequential tracking of outcome contingencies has a key role in cost-efficient action planning and progressive expectation formation.Keywords: Aging; Decision making; Feedback-related ERPs; Reward positivity; Risk-taking behavior Whether we are aware of the fact or not, risk-taking behavior occurs more frequently during our everyday actions than generally thought. Besides those simple and common examples like taking only one more drink before driving, a temporary excursion from one's self-regulatory goals, i.e., risking the long-term goals for short-term advantages such as making a cheat in a diet, can be considered as a more complex form of 'gambling' [1]. Risk-taking behavior can be defined as a decision making propensity motivated by gain reward beside the possible opportunity to lose [2][3][4]. Since natural circumstances usually include continuous fluctuations in risk, the ability of making decisions based on the acquisition of action-outcome contingencies is an essential part of adaptive risk behavior [5]. In particular, old age represents a critical period due to substantial neurocognitive changes having an effect on both frontal cortical and subcortical brain areas known to be involved in decision making [6,7]. The question remains, however, whether there is a specific inability of the acquisition of relevant information behind the possibly reduced decision quality of the elderly.From the perspective of self-report questionnaires, elderly are characterized by higher risk-avoidance tendency [8]. However, regarding risk behavior, results show evidence for both normal and altered patterns of ...

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Adult age differences in frontostriatal representation of prediction error but not reward outcome

Cited by 96 publications

References 51 publications

Positivity effect specific to older adults with subclinical memory impairment

Positivity effect specific to older adults with subclinical memory impairment

Altered behavioral and neural responsiveness to counterfactual gains in the elderly

Age-related characteristics of risky decision-making and progressive expectation formation

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