Motivational systems in adolescence: Possible implications for age differences in substance abuse and other risk-taking behaviors

Doremus-Fitzwater, Tamara L.; Varlinskaya, Elena I.; Spear, Linda P.

doi:10.1016/j.bandc.2009.08.008

Cited by 397Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesSubstance Abuse Treatment and Outcomes

Motivational systems in adolescence: Possible implications for age differences in substance abuse and other risk-taking behaviors

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Doremus-Fitzwater, Tamara L., Varlinskaya, Elena I., Spear, Linda P.·2010·Brain and Cognition

DOI 10.1016/j.bandc.2009.08.008PMC PMC2814912

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Abstract

Adolescence is an evolutionarily conserved developmental phase characterized by hormonal, physiological, neural and behavioral alterations evident widely across mammalian species. For instance, adolescent rats, like their human counterparts, exhibit elevations in peer-directed social interactions, risk-taking/novelty seeking and drug and alcohol use relative to adults, along with notable changes in motivational and reward-related brain regions. After reviewing these topics, the present paper discusses conditioned preference and aversion data showing adolescents to be more sensitive than adults to positive rewarding properties of various drugs and natural stimuli, while less sensitive to the aversive properties of these stimuli. Additional experiments designed to parse specific components of reward-related processing using natural rewards have yielded more mixed findings, with reports of accentuated positive hedonic sensitivity during adolescence contrasting with studies showing less positive hedonic affect and reduced incentive salience at this age. Implications of these findings for adolescent substance abuse will be discussed.

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Reward circuitry includes the dopamine neurotransmitter system and its projections to reward-relevant subcortical regions such as the ventral striatum.
“This reward circuitry includes the DA neurotransmitter system and its projections to reward-relevant subcortical regions such as the ventral striatum (38).”
From Adolescent Neurodevelopment (2013) · cites this paper as [38]
Adolescent rats are often more sensitive than adults to the rewarding properties of stimuli ranging from desirable tastes, social peers, and novelty to drugs of abuse including cocaine, amphetamine, nicotine, and alcohol.
“Data supporting a strong biological component to this enhanced reward responsivity have been obtained using simple animal models, with adolescent rats likewise often more sensitive than adults to the rewarding properties of stimuli that range from desirable tastes, social peers, and novelty, to drugs of abuse including cocaine, amphetamine, nicotine, and alcohol (for review, see 38).”
From Adolescent Neurodevelopment (2013) · cites this paper as [38]
Adolescent rats are often less sensitive than adults to aversive properties of both non-drug and drug stimuli, with drug effects emerging at higher doses of the same drugs that at lower doses they find more reinforcing than adults.
“For instance, adolescent rats are often less sensitive than adults to aversive properties of both non-drug and drug stimuli, with the latter emerging at higher doses of the same drugs that, at lower doses, they conversely find more reinforcing than adults (cocaine, amphetamine, nicotine and alcohol)(38; 60; 61).”
From Adolescent Neurodevelopment (2013) · cites this paper as [38]
Non-deprived adolescent rats consistently show notably less sign-tracking than adults.
“We have found non-deprived adolescents to consistently exhibit notably less sign-tracking than adults (Doremus-Fitzwater et al, 2010; Anderson & Spear, 2011; Ung et al, 2010).”
From Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data (2011) · cites this paper as Doremus-Fitzwater et al, 2010
The exact nature of changes in affective processing, the relation with gonadal hormones, and how they affect motivational behavior in adolescents is not yet well understood.
“However, the exact nature of these changes, the relation with gonadal hormones, and how they affect motivational behavior in adolescents is not yet well understood (Doremus-Fitzwater et al., 2010).”
From Testosterone levels correspond with increased ventral striatum activation in response to monetary rewards in adolescents (2011) · cites this paper as Doremus-Fitzwater et al., 2010

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Brenhouse, H. C., & Andersen, S. L. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.2.460 · Cited by 155 · see citing works
Chronic nicotine differentially alters cocaine-induced locomotor activity in adolescent vs. adult male and female rats
Collins, S. L., & Izenwasser, S. (2003) · Neuropharmacology · doi:10.1016/j.neuropharm.2003.09.024 · Cited by 154 · see citing works
Differential Sensitivity to Alcohol Reinforcement in Groups of Men at Risk for Distinct Alcoholism Subtypes
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Sensitivity to cocaine conditioned reward depends on sex and age
Захарова, Е., Wade, D., & Izenwasser, S. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.11.002 · Cited by 142 · see citing works
Differential effects of methamphetamine and cocaine on conditioned place preference and locomotor activity in adult and adolescent male rats
Захарова, Е., Leoni, G., Kichko, I., & Izenwasser, S. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.10.019 · Cited by 140 · see citing works
A unique hormonal and behavioral hyporesponsivity to both forced novelty and d-amphetamine in periadolescent mice
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Behavioral and Neurochemical Responses to Cocaine in Periadolescent and Adult Rats
Frantz, K. J., O’Dell, L. E., & Parsons, L. H. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301130 · Cited by 136 · see citing works
Individual differences in drug abuse vulnerability: d-Amphetamine and sensation-seeking status
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Inhibition of shock-elicited ultrasonic vocalization by opioid peptides in the rat: A psychotropic effect
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Synergistic interaction between nicotine and social rewards in adolescent male rats
Thiel, K. J., Sanabria, F., & Neisewander, J. L. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1470-2 · Cited by 131 · see citing works
Effect of stress on the voluntary intake of a sweetened ethanol solution in pair-housed adolescent and adult rats
Brunell, S. C., & Spear, L. P. (2005) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000179382.64752.13 · Cited by 128 · see citing works
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Pharmacological and behavioral characteristics of 22 kHz alarm calls in rats
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Expectancy for social facilitation from drinking: The divergent paths of high-expectancy and low-expectancy adolescents.
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Comparing personality constructs of risk-taking behavior
Trimpop, R. M., Kerr, J., & Kirkcaldy, B. D. (1998) · Personality and Individual Differences · doi:10.1016/s0191-8869(98)00048-8 · Cited by 114 · see citing works
Cocaine and morphine-induced place conditioning in adolescent and adult rats
CAMPBELL, J., WOOD, R., & SPEAR, L. P. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00225-5 · Cited by 114 · see citing works
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Chlordiazepoxide directly enhances positive ingestive reactions in rats
Berridge, K. C., & Treit, D. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90341-2 · Cited by 111 · see citing works
Neural mechanisms of resistance to peer influence in early adolescence
Grosbras, M.-H., Jansen, M., Leonard, G., McIntosh, A., Osswald, K., Poulsen, C., Steinberg, L., Toro, R., & Paus, T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1360-07.2007 · Cited by 103 · see citing works
Differences in the social consequences of ethanol emerge during the course of adolescence in rats: Social facilitation, social inhibition, and anxiolysis
Varlinskaya, E. I., & SPEAR, L. P. (2006) · Developmental Psychobiology · doi:10.1002/dev.20124 · Cited by 100 · see citing works
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Adolescent but Not Adult Rats Exhibit Ethanol‐Mediated Appetitive Second‐Order Conditioning
Pautassi, R. M., Myers, M. L., SPEAR, L. P., Molina, J. C., & Spear, N. E. (2008) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2008.00789.x · Cited by 99 · see citing works
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Neural mechanisms supporting flexible performance adjustment during development
Crone, E. A., Zanolie, K., Van Leijenhorst, L., Westenberg, P. M., & Rombouts, S. A. R. B. (2008) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.8.2.165 · Cited by 98 · see citing works
A prospective investigation of relations between social influences and alcohol involvement during the transition into college.
Read, J. P., Wood, M. D., & Capone, C. (2005) · Journal of Studies on Alcohol · doi:10.15288/jsa.2005.66.23 · Cited by 97 · see citing works
Hedonic sensitivity in adolescent and adult rats: Taste reactivity and voluntary sucrose consumption
Wilmouth, C. E., & Spear, L. P. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.02.009 · Cited by 96 · see citing works
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Cocaine differentially alters behavior and neurochemistry in periadolescent versus adult rats
Collins, S. L., & Izenwasser, S. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00471-6 · Cited by 94 · see citing works
Increasing Interaction of amygdalar afferents with GABAergic interneurons between birth and adulthood
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Cannabis, Cannabinoids and Schizophrenia: Integration of the Evidence
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The Developing Brain and Adolescent-Typical Behavior Patterns
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Adolescent psychopathology and the developing brain : integrating brain and prevention science
Römer, D., & Walker, E. F. (2007) · Cited by 87 · see citing works
Developmental changes in amphetamine-induced taste aversions
Infurna, R. N., & SPEAR, L. P. (1979) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(79)90293-4 · Cited by 82 · see citing works
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Changes in the second messenger cyclic AMP during development may underlie motoric symptoms in attention deficit/hyperactivity disorder (ADHD)
Andersen, S. L. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00417-x · Cited by 80 · see citing works
Antidepressant-like effects of 1-aminocyclopropanecarboxylic acid and d-cycloserine in an animal model of depression
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Enhanced behavioral response to repeated-dose cocaine in adolescent rats
Caster, J. M., Walker, Q. D., & Kuhn, C. M. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0159-4 · Cited by 79 · see citing works
Which psychosocial factors moderate or directly affect substance use among inner-city adolescents?
Epstein, J. A., Bang, H., & Botvin, G. J. (2006) · Addictive Behaviors · doi:10.1016/j.addbeh.2006.06.011 · Cited by 79 · see citing works
High-frequency ultrasonic vocalization induced by intracerebral glutamate in rats
Fu, X.-W., & Brudzyński, S. M. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90231-3 · Cited by 74 · see citing works
Biochemistry and Behavior
Goldstein, A. C., Eiduson, S., Geller, E., Yuwiler, A., & Eiduson, B. T. (1965) · The American Journal of Psychology · doi:10.2307/1420526 · Cited by 66 · see citing works
High-frequency (35–70 kHz) ultrasonic vocalizations in rats confronted with anesthetized conspecifics: Effects of gepirone, ethanol, and diazepam
Blanchard, R. J., Yudko, E. B., Blanchard, D. C., & Taukulis, H. K. (1993) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(93)90467-8 · Cited by 65 · see citing works
Conditioned place aversion induced by intragastric administration of ethanol in rats
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Effect of MDMA (ecstasy) on activity and cocaine conditioned place preference in adult and adolescent rats
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Age-specific behavioral responses to psychostimulants in mice
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Attenuated incubation of cocaine seeking in male rats trained to self-administer cocaine during periadolescence
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Chronic tolerance to the social consequences of ethanol in adolescent and adult Sprague-Dawley rats
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Evaluation of a pharmacokinetic hypothesis for reduced locomotor stimulation from methamphetamine and cocaine in adolescent versus adult male C57BL/6J mice
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Adolescent Maturation of Cocaine-Sensitive Neural Mechanisms
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Individual Differences in Responses to Ethanol and d-Amphetamine: A Within-Subject Study
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Social interactions and 50kHz ultrasonic vocalizations in adolescent and adult rats
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Play deprivation without social isolation: Housing controls
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A single high dose of cocaine induces differential sensitization to specific behaviors across adolescence
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Substance use and abuse in adolescence: An overview
Segal, B. M., & Stewart, J. C. (1996) · Child Psychiatry & Human Development · doi:10.1007/bf02353237 · Cited by 48 · see citing works
Dependence of adolescent novelty-seeking behavior on response phenotype and effects of apparatus scaling.
Philpot, R. M., & Wecker, L. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.4.861 · Cited by 47 · see citing works
Age-dependent morphine intake and cue-induced reinstatement, but not escalation in intake, by adolescent and adult male rats
Doherty, J. M., Ogbomnwan, Y., Williams, B., & Frantz, K. J. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.11.009 · Cited by 47 · see citing works
Adolescent Psychopathology and Developing Brain/ Integrating Brain and Prevention Science
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EndogenousκOpioid Receptor Systems Modulate the Responsiveness of Mesoaccumbal Dopamine Neurons to Ethanol
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Changes in hyporesponsiveness to acute amphetamine and age differences in tyrosine hydroxylase immunoreactivity in the brain over adolescence in male and female rats
Zovkic, I. B., Waters, P., & McCormick, C. M. (2009) · Developmental Psychobiology · doi:10.1002/dev.20381 · Cited by 40 · see citing works
Cam: An animal learning model of excessive and compulsive implementassisted drug-taking in humans
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Adolescent and adult heart rate responses to self-administered ethanol
Ristuccia, R. C., & Spear, L. P. (2008) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2008.00752.x · Cited by 35 · see citing works
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Dopamine receptor pruning during the peripubertal period is not attenuated by NMDA receptor antagonism in rat
Teicher, M. H., Krenzel, E., Thompson, A. P., & Andersen, S. L. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(02)01475-1 · Cited by 34 · see citing works
Handling alters cocaine-induced activity in adolescent but not adult male rats
Maldonado‐Devincci, A. M., & Kirstein, C. L. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.12.007 · Cited by 33 · see citing works
Cocaine-induced locomotor activity is increased by prior handling in adolescent but not adult female rats
Maldonado‐Devincci, A. M., & Kirstein, C. L. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.08.026 · Cited by 32 · see citing works
Drugs, Crime, and other Deviant Adaptations: Longitudinal Studies
White, H. R. (1996) · Journal of Studies on Alcohol · doi:10.15288/jsa.1996.57.677 · Cited by 24 · see citing works
The Psychobiology of Adolescence
SPEAR, L. P. (2007) · Springer eBooks · doi:10.1007/978-0-387-72721-9_12 · Cited by 18 · see citing works
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Behavioral responses during the initial exposures to a low dose of cocaine in late preweanling and adult rats
Smith, K. S., & Morrell, J. I. (2008) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2008.01.003 · Cited by 15 · see citing works
Stimulus selection in passive avoidance learning and retention: weanling, periadolescent, and young adult rats
Barrett, B. A., Rizzo, T., Spear, N. E., & SPEAR, L. P. (1984) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(84)90388-1 · Cited by 5 · see citing works
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SPECIAL ISSUE: GENDER & ALCOHOL Sex Differences in Ethanol Intake and Sensitivity to Aversive Effects during Adolescence and Adulthood
Vetter-O’Hagen, C. S., Varlinskaya, E. I., & SPEAR, L. P. (2009) · Cited by 1 · see citing works
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“Adolescence is a transitional period between childhood and adulthood characterized by behavioral, hormonal, and neurochemical changes designed to prepare organisms for independent survival (Casey et al., 2008; Doremus-Fitzwater et al., 2010; Spear, 2003).”
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Authors: Doremus-Fitzwater, T. L., Varlinskaya, E. I., & Spear, L. P.
Affiliations: Binghamton University (US)
Corresponding author: Spear, Linda P.
ORCID: Varlinskaya, Elena I.
Spear, Linda P.
Venue: Brain and Cognition
Publisher: Elsevier BV
Published: 2010-02
Volume: 72
Issue: 1
Pages: 114-123
ISSN: 0278-2626 (ISSN-L)
DOI: 10.1016/j.bandc.2009.08.008
PMC: PMC2814912
OpenAlex: W2041697442
Cited by: 397
References: 152
Citations by year: 2026: 5 · 2025: 11 · 2024: 9 · 2023: 12 · 2022: 20 · 2021: 13 · 2020: 25 · 2019: 22 · 2018: 34 · 2017: 25 · 2016: 28 · 2015: 33 · 2014: 30 · 2013: 42 · 2012: 28
FWCI: 2.53
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain and Cognition (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute on Alcohol Abuse and Alcoholism (R01AA016887, R01AA012453)
National Institute on Drug Abuse (R01DA019071)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
Keywords: adolescence, motivation system, substance abuse, risk-taking, novelty seeking, reward processing, conditioned aversion, natural reward, incentive salience, adolescent rats, age differences
MeSH terms: Adolescent, Animals, Brain, Humans, Motivation, Neural Pathways, Reward, Risk-Taking, Substance-Related Disorders

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Motivational systems in adolescence: Possible implications for age differences in substance abuse and other risk-taking behaviors

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