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Abnormal striatal BOLD responses to reward anticipation and reward delivery in ADHD.

Furukawa E, Bado P, Tripp G, Mattos P, Wickens JR, Bramati IE, Alsop B, Ferreira FM, Lima D, Tovar-Moll F, Sergeant JA, Moll J - PLoS ONE (2014)

Bottom Line: The neurobiological mechanism underlying this alteration remains unclear.Data from 14 high-functioning and stimulant-naïve young adults with elevated lifetime symptoms of ADHD (8 males, 6 females) and 15 well-matched controls (8 males, 7 females) were included in the analyses.The opposite pattern was observed in response to reward delivery; the ADHD group demonstrated significantly greater BOLD responses in the ventral striatum bilaterally and the left dorsal striatum relative to controls.

View Article: PubMed Central - PubMed

Affiliation: Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan.

ABSTRACT
Altered reward processing has been proposed to contribute to the symptoms of attention deficit hyperactivity disorder (ADHD). The neurobiological mechanism underlying this alteration remains unclear. We hypothesize that the transfer of dopamine release from reward to reward-predicting cues, as normally observed in animal studies, may be deficient in ADHD. Functional magnetic resonance imaging (fMRI) was used to investigate striatal responses to reward-predicting cues and reward delivery in a classical conditioning paradigm. Data from 14 high-functioning and stimulant-naïve young adults with elevated lifetime symptoms of ADHD (8 males, 6 females) and 15 well-matched controls (8 males, 7 females) were included in the analyses. During reward anticipation, increased blood-oxygen-level-dependent (BOLD) responses in the right ventral and left dorsal striatum were observed in controls, but not in the ADHD group. The opposite pattern was observed in response to reward delivery; the ADHD group demonstrated significantly greater BOLD responses in the ventral striatum bilaterally and the left dorsal striatum relative to controls. In the ADHD group, the number of current hyperactivity/impulsivity symptoms was inversely related to ventral striatal responses during reward anticipation and positively associated with responses to reward. The BOLD response patterns observed in the striatum are consistent with impaired predictive dopamine signaling in ADHD, which may explain altered reward-contingent behaviors and symptoms of ADHD.

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Related in: MedlinePlus

Classical conditioning fMRI paradigm.One of two neutral stimuli (Cue A or Cue B) was followed by an outcome stimulus (reward or non-reward) after a 6-second delay. Cue A was followed by the delivery of the reward 66% of the time and non-reward 33% of the time. Cue B was always followed by non-reward. Participants were told they would receive the equivalent of R$3 for each reward outcome. The length of the inter-trial delay was varied.
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pone-0089129-g001: Classical conditioning fMRI paradigm.One of two neutral stimuli (Cue A or Cue B) was followed by an outcome stimulus (reward or non-reward) after a 6-second delay. Cue A was followed by the delivery of the reward 66% of the time and non-reward 33% of the time. Cue B was always followed by non-reward. Participants were told they would receive the equivalent of R$3 for each reward outcome. The length of the inter-trial delay was varied.

Mentions: A classical conditioning paradigm was developed to examine BOLD responses to reward anticipation and delivery, unconfounded by operant behavioral responses, decision-making or complex reward probability and magnitude estimation (Figure 1). One of two initially neutral stimuli (Cue A or Cue B) was followed by a 6 second delay (anticipation period) after which an outcome stimulus (reward or non-reward) was presented. The delay was kept constant to maintain the temporal predictability of the outcome delivery. A picture of coins was presented as a reward outcome and the participants were told they would receive the equivalent of R$3 for each reward outcome and nothing for the non-reward outcomes. Cue A was followed by reward 66% of the time (44 trials) and non-reward 33% of the time (22 trials) to allow a level of uncertainty. Cue B was always followed by non-reward (22 trials). Participants were asked to press a button when a target appeared after the outcome (Lumina, Cedrus Corporation, CA). The length of the inter-trial delay was varied to reduce the temporal predictability of the next trial (Poisson distribution: min = 4.5 s, max = 14.5 s, average = 6.5 s, sd = 2.05 s).


Abnormal striatal BOLD responses to reward anticipation and reward delivery in ADHD.

Furukawa E, Bado P, Tripp G, Mattos P, Wickens JR, Bramati IE, Alsop B, Ferreira FM, Lima D, Tovar-Moll F, Sergeant JA, Moll J - PLoS ONE (2014)

Classical conditioning fMRI paradigm.One of two neutral stimuli (Cue A or Cue B) was followed by an outcome stimulus (reward or non-reward) after a 6-second delay. Cue A was followed by the delivery of the reward 66% of the time and non-reward 33% of the time. Cue B was always followed by non-reward. Participants were told they would receive the equivalent of R$3 for each reward outcome. The length of the inter-trial delay was varied.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3935853&req=5

pone-0089129-g001: Classical conditioning fMRI paradigm.One of two neutral stimuli (Cue A or Cue B) was followed by an outcome stimulus (reward or non-reward) after a 6-second delay. Cue A was followed by the delivery of the reward 66% of the time and non-reward 33% of the time. Cue B was always followed by non-reward. Participants were told they would receive the equivalent of R$3 for each reward outcome. The length of the inter-trial delay was varied.
Mentions: A classical conditioning paradigm was developed to examine BOLD responses to reward anticipation and delivery, unconfounded by operant behavioral responses, decision-making or complex reward probability and magnitude estimation (Figure 1). One of two initially neutral stimuli (Cue A or Cue B) was followed by a 6 second delay (anticipation period) after which an outcome stimulus (reward or non-reward) was presented. The delay was kept constant to maintain the temporal predictability of the outcome delivery. A picture of coins was presented as a reward outcome and the participants were told they would receive the equivalent of R$3 for each reward outcome and nothing for the non-reward outcomes. Cue A was followed by reward 66% of the time (44 trials) and non-reward 33% of the time (22 trials) to allow a level of uncertainty. Cue B was always followed by non-reward (22 trials). Participants were asked to press a button when a target appeared after the outcome (Lumina, Cedrus Corporation, CA). The length of the inter-trial delay was varied to reduce the temporal predictability of the next trial (Poisson distribution: min = 4.5 s, max = 14.5 s, average = 6.5 s, sd = 2.05 s).

Bottom Line: The neurobiological mechanism underlying this alteration remains unclear.Data from 14 high-functioning and stimulant-naïve young adults with elevated lifetime symptoms of ADHD (8 males, 6 females) and 15 well-matched controls (8 males, 7 females) were included in the analyses.The opposite pattern was observed in response to reward delivery; the ADHD group demonstrated significantly greater BOLD responses in the ventral striatum bilaterally and the left dorsal striatum relative to controls.

View Article: PubMed Central - PubMed

Affiliation: Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan.

ABSTRACT
Altered reward processing has been proposed to contribute to the symptoms of attention deficit hyperactivity disorder (ADHD). The neurobiological mechanism underlying this alteration remains unclear. We hypothesize that the transfer of dopamine release from reward to reward-predicting cues, as normally observed in animal studies, may be deficient in ADHD. Functional magnetic resonance imaging (fMRI) was used to investigate striatal responses to reward-predicting cues and reward delivery in a classical conditioning paradigm. Data from 14 high-functioning and stimulant-naïve young adults with elevated lifetime symptoms of ADHD (8 males, 6 females) and 15 well-matched controls (8 males, 7 females) were included in the analyses. During reward anticipation, increased blood-oxygen-level-dependent (BOLD) responses in the right ventral and left dorsal striatum were observed in controls, but not in the ADHD group. The opposite pattern was observed in response to reward delivery; the ADHD group demonstrated significantly greater BOLD responses in the ventral striatum bilaterally and the left dorsal striatum relative to controls. In the ADHD group, the number of current hyperactivity/impulsivity symptoms was inversely related to ventral striatal responses during reward anticipation and positively associated with responses to reward. The BOLD response patterns observed in the striatum are consistent with impaired predictive dopamine signaling in ADHD, which may explain altered reward-contingent behaviors and symptoms of ADHD.

Show MeSH
Related in: MedlinePlus