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Chronic Δ9-tetrahydrocannabinol exposure in adolescent nonhuman primates: persistent abnormalities in economic demand and brain functional connectivity

Neuropsychopharmacology volume 50, pages 576–585 (2025)Cite this article

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Abstract

Although chronic cannabis use during adolescence can alter brain function and impair complex behavioral processes, it is unclear whether such deficits persist into adulthood. Using a coordinated awake neuroimaging and behavioral approach in nonhuman primates, we addressed this issue by examining the impact of chronic adolescent exposure to Δ9-tetrahydrocannabinol (THC) on brain functional connectivity and motivational processes during early adulthood. Female and male squirrel monkeys (n = 23) were treated daily for 6 months during adolescence with vehicle or either a low (0.32 mg/kg) or high dose (3.2 mg/kg) of THC. Regional homogeneity and seed-to-whole-brain functional connectivity were analyzed prior to, during, and following discontinuation of chronic treatment to examine changes in regions implicated in reward processing. Subsequently, motivation and reward sensitivity in these subjects, now young adults, were evaluated in economic demand studies by determining the relationship between escalating response requirements and consumption of differing magnitudes of a palatable food reinforcer. Results show that adolescent THC exposure led to persistent alterations in mOFC, caudate, and ventral striatum whole-brain connectivity. Moreover, subjects treated with vehicle during adolescence displayed an orderly and expected inverse relationship between reward magnitude and demand elasticity, whereas THC-treated subjects exhibited dosage-dependent disorder in reward sensitivity and motivational deficits. Changes in neural circuitry (local connectivity in ventral striatum and whole brain connectivity in mOFC) and economic demand were correlated with indices of reward sensitivity in vehicle- but not THC-treated subjects. Taken together, these data indicate that chronic adolescent THC exposure produced long-lasting neurocognitive abnormalities in reward processing.

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Fig. 1: Twelve-month timeline of experimental events.
Fig. 2: Economic demand functions that describe the exponential relationship between price (response requirement) and consumption (number of rewards earned) as a function of percent sweetened condensed milk (reward magnitude).
Fig. 3: Economic demand parameter analysis.
Fig. 4: Seed-to-whole brain FC in regions of interest for vehicle, low dose THC (0.32 mg/kg), and high dose THC (3.2 mg/kg) groups at the three timepoints (drug-naïve, chronic, discontinuation).
Fig. 5: Relationship between behavioral and neuroimaging endpoints. Data points represent relations for individual subjects.

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Funding

This project was supported by R01-DA047575 from the National Institute on Drug Abuse. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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  1. Harvard Medical School, McLean Hospital, Belmont, MA, 02478, USA

    Brian D. Kangas, Harshawardhan U. Deshpande, Sarah L. Withey, Roger D. Spealman, Jack Bergman & Stephen J. Kohut

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Contributions

BDK, SLW, RDS, JB, and SJK designed the research, BDK, SLW, and SJK performed the research, BDK, HUD, and SJK analyzed the data, and BDK, HUD, SLW, RDS, JB, SJK wrote the paper.

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Correspondence to Brian D. Kangas.

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Over the past 3 years, BDK has had sponsored research agreements with BlackThorn Therapeutics, Compass Pathways, Delix Therapeutics, Engrail Therapeutics, Neurocrine Biosciences, and Takeda Pharmaceuticals. No funding from these entities was used to support the current work. All other authors have no conflicts of interest or relevant disclosures.

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Kangas, B.D., Deshpande, H.U., Withey, S.L. et al. Chronic Δ9-tetrahydrocannabinol exposure in adolescent nonhuman primates: persistent abnormalities in economic demand and brain functional connectivity. Neuropsychopharmacol. 50, 576–585 (2025). https://doi.org/10.1038/s41386-024-02024-9

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