Brain reward region responsivity of adolescents with and without parental substance use disorders

Abstract

The present study tested the competing hypotheses that adolescents at risk for future substance abuse and dependence by virtue of parental substance use disorders show either weaker or stronger responsivity of brain regions implicated in reward relative to youth without parental history of substance use disorders. Adolescents (n = 52) matched on demographics with and without parental substance use disorders, as determined by diagnostic interviews, who denied substance use in the past year were compared on functional MRI (fMRI) paradigms assessing neural response to receipt and anticipated receipt of monetary and food reward. Parental-history-positive versus -negative adolescents showed greater activation in the left dorsolateral prefrontal cortex and bilateral putamen, and less activation in the fusiform gyrus and inferior temporal gyrus in response to anticipating winning money, as well as greater activation in the left midbrain and right paracentral lobule, and less activation in the right middle frontal gyrus in response to milkshake receipt. Results indicate that adolescents at risk for future onset of substance use disorders show elevated responsivity of brain regions implicated in reward, extending results from 2 smaller prior studies that found that individuals with versus without parental alcohol use disorders showed greater reward region response to anticipated monetary reward and pictures of alcohol. Collectively, results provide support for the reward surfeit model of substance use disorders, rather than the reward deficit model.

Figures

Figure 1

Example of timing and ordering of presentation of A) images and notification of monetary reward during the monetary reward paradigm and of B) pictures and beverages during the food reward paradigm.

Figure 2

The gustatory manifold was anchored to the table. New tubing and syringes were used for each subject and the mouthpiece was cleaned and sterilized between uses.

Figure 3

Activation in the parental-history-positive group in A) bilateral putamen (square MNI: −27, −16, 1, Z = 4.94, k = 34, circle MNI: 30, −16, 1, Z = 4.11, k = 77) in response to monetary receipt, B) bilateral putamen (square MNI: −27, −16, 1, Z = 6.43, k = 337, circle MNI: 30, −7, −2, Z = 5.58, k = 293) in response to anticipated monetary receipt, C) bilateral striatum (square MNI peak activation: 27, −10, −2, Z = 5.28, k = 124, circle MNI peak activation: −27, −19, 4, Z = 5.05, k = 62) in response to milkshake receipt. Activation in the parental-history-negative group in D) right medial orbitofrontal cortex (MNI: 0, 38, −11, Z = 3.88, k = 70) in response to monetary receipt, E) left amygdala (MNI: −21, −7, −20, Z = 3.87, k = 12) in response to anticipated monetary receipt, and F) bilateral putamen (square MNI: −24, −4, 4, Z = 4.56, k = 97, circle MNI: 27, −1, 4, Z = 4.58, k = 80) in response to milkshake receipt.

Figure 4

Parental-history-positive versus –negative adolescents exhibited greater activation in A) the left putamen (MNI: −27, −16, 4, Z = 4.12, k = 59) and B) the right putamen (MNI: 30, −4, −11, Z = 3.83, k = 20) in response to anticipated monetary receipt.

Figure 5

Parental-history-positive versus –negative adolescents exhibited greater activation in the left midbrain (MNI: −15, −22, −14, Z = 3.97, k = 14) in response to milkshake receipt.