Adolescent Development of Forebrain Stimulant Responsiveness: Insights from Animal Studies
Abstract
Although initiation of drug abuse occurs primarily during adolescence, little is known about the central effects of nicotine and other abused drugs during this developmental period. Here evidence, derived from studies in rodents, is presented that suggests that tobacco use initiation during early adolescence results from a higher reward value of nicotine. The developmental profiles of the rewarding effects of other abused drugs, such as cocaine, differ from that of nicotine. Using in situ hybridization to quantify mRNA levels of the immediate early gene, cfos, the neuronal activating effects of nicotine in limbic and sensory cortices at different developmental stages are evaluated. Significant age changes in basal levels of cfos mRNA expression in cortical regions are observed, with a peak of responding of limbic cortices during early adolescence. A changing pattern of nicotine-induced neuronal activation is seen across the developmental spectrum, with unique differences in both limbic and sensory cortex responding during adolescence. An attentional set-shifting task was also used to evaluate whether the observed differences during adolescence reflect early functional immaturity of prefrontal cortices that regulate motivated behavior and psychostimulant responding. The finding of significantly better responding during adolescence suggests apparent functional maturity of prefrontal circuits and greater cognitive flexibility at younger ages. These findings in rodent models sugg…
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Activity of the early response genes arc and c-fos is elevated in adolescent PFC after nicotine exposure.
“The activity of specific early response genes (arc and c-fos) used as a marker for the functional activation of neurons was found to be elevated in adolescent PFC after nicotine exposure (Leslie et al. 2004; Schochet et al. 2005).”
From Short- and Long-Term Consequences of Nicotine Exposure during Adolescence for Prefrontal Cortex Neuronal Network Function (2012) · cites this paper as Leslie et al. 2004
Cites
Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making
Bechara, A., Damasio, H., Damasio, A. R., & Lee, G. P. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-13-05473.1999 · Cited by 2,001 · see citing works
Dissociation in prefrontal cortex of affective and attentional shifts
Dias, R., Robbins, T. W., & Roberts, A. C. (1996) · Nature · doi:10.1038/380069a0 · Cited by 1,527 · see citing works
Nucleus accumbens shell and core dopamine: differential role in behavior and addiction
Di Chiara, G. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00286-3 · Cited by 996 · see citing works
Lewis, D. (1997) · Neuropsychopharmacology · doi:10.1016/s0893-133x(96)00277-1 · Cited by 388 · see citing works
Tarazi, F. I., & Baldessarini, R. J. (2000) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(99)00108-2 · Cited by 327 · see citing works
Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats
Belluzzi, J., Lee, A., Oliff, H., & Leslie, F. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1758-6 · Cited by 280 · see citing works
Self-citationNicotine-induced conditioned place preference in adolescent and adult rats
Vastola, B. J., Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00818-1 · Cited by 251 · see citing works
Anatomical Markers of Activity in Neuroendocrine Systems: Are we all ‘Fos‐ed out’?
Hoffman, G. E., & Lyo, D. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2002.00775.x · Cited by 242 · see citing works
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Guidelines on nicotine dose selection for in vivo research
Matta, S. G., Balfour, D. J., Benowitz, N. L., Boyd, R. T., Buccafusco, J. J., Caggiula, A. R., Craig, C. R., Collins, A. C., Damaj, M. I., Donny, E. C., et al. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0441-0 · Cited by 824 · see citing works
<scp>N</scp> icotine and the adolescent brain
Yuan, M., Cross, S. J., Loughlin, S. E., & Leslie, F. M. (2015) · The Journal of Physiology · doi:10.1113/jp270492 · Cited by 582 · see citing works
Self-citationAndersen, S. L., & Teicher, M. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.09.009 · Cited by 326 · see citing works
Goriounova, N. A., & Mansvelder, H. D. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a012120 · Cited by 307 · see citing works
“The activity of specific early response genes (arc and c-fos) used as a marker for the functional activation of neurons was found to be elevated in adolescent PFC after nicotine exposure (Leslie et al. 2004; Schochet et al. 2005).”
Brenhouse, H. C., Sonntag, K. C., & Andersen, S. L. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5064-07.2008 · Cited by 287 · see citing works
Are adolescents more vulnerable to drug addiction than adults? Evidence from animal models
Schramm-Sapyta, N. L., Walker, Q. D., Caster, J. M., Levin, E. D., & Kuhn, C. M. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1585-5 · Cited by 215 · see citing works
Shram, M. J., Funk, D., Li, Z., & Lê, A. D. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0373-8 · Cited by 192 · see citing works
Lynch, W. J. (2008) · Psychopharmacology · doi:10.1007/s00213-007-1028-0 · Cited by 152 · see citing works
Mechanisms of Action and Persistent Neuroplasticity by Drugs of Abuse
Korpi, E. R., den Hollander, B., Farooq, U., Vashchinkina, E., Rajkumar, R., Nutt, D. J., Hyytiä, P., & Dawe, G. S. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.010967 · Cited by 148 · see citing works
Doremus-Fitzwater, T. L., & Spear, L. P. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.015 · Cited by 125 · see citing works
Low dose nicotine treatment during early adolescence increases subsequent cocaine reward
McQuown, S. C., Belluzzi, J. D., & Leslie, F. M. (2007) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.10.012 · Cited by 117 · see citing works
Self-citationNicotinic actions on neuronal networks for cognition: General principles and long-term consequences
Poorthuis, R. B., Goriounova, N. A., Couey, J. J., & Mansvelder, H. D. (2009) · Biochemical Pharmacology · doi:10.1016/j.bcp.2009.04.031 · Cited by 102 · see citing works
Schochet, T. L., Kelley, A. E., & Landry, C. F. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.057 · Cited by 93 · see citing works
Brielmaier, J. M., McDonald, C. G., & Smith, R. F. (2007) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.09.023 · Cited by 90 · see citing works
Peartree, N. A., Hood, L. E., Thiel, K. J., Sanabria, F., Pentkowski, N. S., Chandler, K. N., & Neisewander, J. L. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.10.001 · Cited by 90 · see citing works
Adolescents are more vulnerable to cocaine addiction: behavioral and electrophysiological evidence
Wong, W. C., Ford, K. A., Pagels, N. E., McCutcheon, J. E., & Marinelli, M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1371-12.2013 · Cited by 87 · see citing works
A psychobiological framework of the substrates that mediate nicotine use during adolescence
O'Dell, L. E. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.039 · Cited by 81 · see citing works
Cao, J., Belluzzi, J. D., Loughlin, S. E., Keyler, D. E., Pentel, P. R., & Leslie, F. M. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301327 · Cited by 67 · see citing works
Self-citationARNSTEN, A. F. T., & SHANSKY, R. M. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.017 · Cited by 66 · see citing works
Cass, D. K., Thomases, D. R., Caballero, A., & Tseng, K. Y. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.02.021 · Cited by 63 · see citing works
“Similar impairments in prefrontal-dependent executive functions have been observed after long-term exposure to psychostimulants during adolescence (2, 3, 45).”
Shram, M. J., Funk, D., Li, Z., & Lê, A. D. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.03.034 · Cited by 64 · see citing works
Shram, M. J., Siu, E. C. K., Li, Z., Tyndale, R. F., & Lê, A. D. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1115-x · Cited by 60 · see citing works
Locomotor and stress responses to nicotine differ in adolescent and adult rats
Cao, J., Belluzzi, J. D., Loughlin, S. E., Dao, J. M., Chen, Y., & Leslie, F. M. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2010.04.010 · Cited by 47 · see citing works
Self-citationMcQuown, S. C., Dao, J. M., Belluzzi, J. D., & Leslie, F. M. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1642-0 · Cited by 39 · see citing works
Self-citationHoegberg, B. G., Lomazzo, E., Lee, N. H., & Perry, D. C. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.08.015 · Cited by 17 · see citing works
Cardenas, A., Martinez, M., Saenz Mejia, A., & Lotfipour, S. (2021) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000593 · Cited by 21 · see citing works
Self-citationSchochet, T. L., Bremer, Q. Z., Brownfield, M. S., Kelley, A. E., & Landry, C. F. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06483.x · Cited by 14 · see citing works
- Authors
- LESLIE, F. M., LOUGHLIN, S. E., WANG, R., PEREZ, L., LOTFIPOUR, S., & BELLUZZIA, J. D.
- Affiliations
- University of California, Irvine (US)
- Corresponding author
- LESLIE, FRANCES M.
- Venue
- Annals of the New York Academy of Sciences
- Publisher
- Wiley
- Published
- 2004-06
- Volume
- 1021
- Issue
- 1
- Pages
- 148-159
- ISSN
- 0077-8923 (ISSN-L)
- 1749-6632
- OpenAlex
- W2057092764
- Cited by
- 81
- References
- 8
- Citations by year
- 2023: 1 · 2021: 1 · 2020: 4 · 2019: 2 · 2018: 1 · 2017: 3 · 2016: 4 · 2015: 7 · 2014: 4 · 2013: 4 · 2012: 4
- FWCI
- 0.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annals of the New York Academy of Sciences (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Drug Abuse (P50DA013332, DA 13332)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- adolescent development, nicotine reward, cocaine, neuronal activation, limbic cortex, sensory cortex, prefrontal cortex maturation, set-shifting, cognitive flexibility, psychostimulant sensitivity, forebrain
- MeSH terms
- Adolescent, Animals, Behavior, Animal, Conditioning, Operant, Discrimination Learning, Humans, Nicotine, Reward, Self Administration, Prosencephalon, Nicotinic Agonists, Models, Animal
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