TY - JOUR

T1 - Evaluating instrumental learning and striatal–cortical functional connectivity in adolescent alcohol and cannabis use

AU - Hubbard, Nicholas A.

AU - Miller, Kevin B.

AU - Aloi, Joseph

AU - Bajaj, Sahil

AU - Wakabayashi, Ken T.

AU - Blair, R. James R.

N1 - Funding Information: The authors wish to thank Jeffrey Stevens for helpful consultation on the manuscript. NAH was partially supported by the Brain and Behavior Research Foundation. NAH and KTW were partially supported by the Nebraska Biomedical Research Development Funds. NAH, KTW and RJRB were partially supported by the Rural Drug Addiction Research Center (P20GM130461). The content of this report is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or of any other sponsor. Publisher Copyright: © 2022 Society for the Study of Addiction.

PY - 2023/1

Y1 - 2023/1

N2 - Adolescence is a vulnerable time for the acquisition of substance use disorders, potentially relating to ongoing development of neural circuits supporting instrumental learning. Striatal–cortical circuits undergo dynamic changes during instrumental learning and are implicated in contemporary addiction theory. Human studies have not yet investigated these dynamic changes in relation to adolescent substance use. Here, functional magnetic resonance imaging was used while 135 adolescents without (AUD-CUDLow) and with significant alcohol (AUDHigh) or cannabis use disorder symptoms (CUDHigh) performed an instrumental learning task. We assessed how cumulative experience with instrumental cues altered cue selection preferences and functional connectivity strength between reward-sensitive striatal and cortical regions. Adolescents in AUDHigh and CUDHigh groups were slower in learning to select optimal instrumental cues relative to AUD-CUDLow adolescents. The relatively fast learning observed for AUD-CUDLow adolescents coincided with stronger functional connectivity between striatal and frontoparietal regions during early relative to later periods of task experience, whereas the slower learning for the CUDHigh group coincided with the opposite pattern. The AUDHigh group not only exhibited slower learning but also produced more instrumental choice errors relative to AUD-CUDLow adolescents. For the AUDHigh group, Bayesian analyses evidenced moderate support for no experience-related changes in striatal–frontoparietal connectivity strength during the task. Findings suggest that adolescent cannabis use is related to slowed instrumental learning and delays in peak functional connectivity strength between the striatal–frontoparietal regions that support this learning, whereas adolescent alcohol use may be more closely linked to broader impairments in instrumental learning and a general depression of the neural circuits supporting it.

AB - Adolescence is a vulnerable time for the acquisition of substance use disorders, potentially relating to ongoing development of neural circuits supporting instrumental learning. Striatal–cortical circuits undergo dynamic changes during instrumental learning and are implicated in contemporary addiction theory. Human studies have not yet investigated these dynamic changes in relation to adolescent substance use. Here, functional magnetic resonance imaging was used while 135 adolescents without (AUD-CUDLow) and with significant alcohol (AUDHigh) or cannabis use disorder symptoms (CUDHigh) performed an instrumental learning task. We assessed how cumulative experience with instrumental cues altered cue selection preferences and functional connectivity strength between reward-sensitive striatal and cortical regions. Adolescents in AUDHigh and CUDHigh groups were slower in learning to select optimal instrumental cues relative to AUD-CUDLow adolescents. The relatively fast learning observed for AUD-CUDLow adolescents coincided with stronger functional connectivity between striatal and frontoparietal regions during early relative to later periods of task experience, whereas the slower learning for the CUDHigh group coincided with the opposite pattern. The AUDHigh group not only exhibited slower learning but also produced more instrumental choice errors relative to AUD-CUDLow adolescents. For the AUDHigh group, Bayesian analyses evidenced moderate support for no experience-related changes in striatal–frontoparietal connectivity strength during the task. Findings suggest that adolescent cannabis use is related to slowed instrumental learning and delays in peak functional connectivity strength between the striatal–frontoparietal regions that support this learning, whereas adolescent alcohol use may be more closely linked to broader impairments in instrumental learning and a general depression of the neural circuits supporting it.

KW - adolescence

KW - alcohol

KW - cannabis

KW - functional magnetic resonance imaging

KW - instrumental learning

U2 - 10.1111/adb.13258

DO - 10.1111/adb.13258

M3 - Journal article

C2 - 36577718

AN - SCOPUS:85145070359

VL - 28

JO - Addiction Biology (Online)

JF - Addiction Biology (Online)

SN - 1369-1600

IS - 1

M1 - e13258

ER -