Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model

Adriani, W.; Laviola, G.

doi:10.1097/00008877-200409000-00005

Cited by 267Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchNeural and Behavioral Psychology Studies

Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model

Adriani, W., Laviola, G.·2004·Behavioural Pharmacology

DOI 10.1097/00008877-200409000-00005

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Abstract

Adolescence comes in association with puberty, when maturation and rearrangement of major neurotransmitter pathways and functions are still taking place. The neurobiological processes occurring in the brain during this developmental period have been so far poorly investigated. Yet, it is during adolescence that some major neuropsychiatric disorders may become evident, including ADHD, schizophrenia, and drug abuse. Moreover, the age-related neurobehavioural plasticity renders adolescents particularly vulnerable to the consequences of psychoactive drug exposure. In this view, there is an increased likelihood that addiction will develop when psychoactive drug use starts early during adolescence. From all these observations adolescence emerges as a critical phase in development. In the present review, we focus on recent neurobiological characterization of adolescent rats and mice. As for vulnerability to addictive behaviour, nicotine exposure during adolescence dose-dependently down-regulated levels of AMPA GluR2/3 subunits in the striatum, suggesting a reduced neurobehavioural plasticity in adult subjects. Comparable exposure during adulthood had opposite effects. It was found consistently that exposure to nicotine during adolescence, but not similar exposure in the post-adolescent period, increased the expression of specific subunits of the acetylcholine receptor in adult rats, thus enhancing the reinforcing efficacy of nicotine in a self-administration paradigm. The present data identified a specific age-window, characterized by long-term effects on behavioural and neurochemical indexes, of vulnerability. With respect to potential therapeutic approaches in ADHD, we studied the adolescent spontaneously-hypertensive-rat (SHR) in an intolerance-to-delay operant-behaviour paradigm. The model was further validated by the finding that impulsivity was reduced by chronic methylphenidate administration. Impulsive SHR animals were characterized by reduced cannabinoid CB1 receptor density in the prefrontal cortex. Interestingly, an acute cannabinoid agonist increased levels of self-control behaviour in these animals. The present data suggest that pharmacological modulation of the cannabinoid system might improve some behavioural anomalies seen in ADHD. In conclusion, modelling the adolescent phase in rats and mice appears to be useful for the investigation of determinants of vulnerability to addiction and to other early-onset neuropsychiatric disorders.

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In Adriani et al. (2004), time spent in the open arms of the elevated plus maze was increased in pre-adolescents versus age-matched controls.
“Time spent in the open arms: Pre- adolescents ↑ vs age-matched controls”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani et al. (2004)
In Adriani et al. (2004), post-adolescents showed no differences in time spent in the open arms versus age-matched controls.
“Post-adolescents no differences vs age-matched controls.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani et al. (2004)
In Adriani et al. (2004), time spent in the open arms was decreased in mid-adolescents versus age-matched controls.
“mid-adolescents ↓ vs age- matched controls.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani et al. (2004)
Exposure to nicotine during adolescence increased the vulnerability of developing nicotine addiction compared to similar exposure in adulthood.
“Evidence for this claim has been found in a study by Adriani and colleagues (2003) who found exposure to nicotine during adoles cence increased the vulnerability of developing nicotine addiction compared to when a similar exposure took place in adulthood (Adriani and Laviola, 2004).”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani and Laviola, 2004
Across the two studies using the OFT and three studies using the EPM, increased anxiety-related behaviour was displayed in adolescent-exposed rodents compared to adult-exposed and their relative age-matched controls.
“Across the two studies using the OFT and three studies using the EPM, increased anxiety-related behaviour was displayed in adolescent-exposed rodents compared to adult-exposed and their rela tive age-matched controls”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani et al., 2004

Five of the six anxiety studies showed an interaction effect between age and sensitivity to nicotine-induced anxiety.
“Five of the six studies showed an interaction effect between age and sensi tivity to nicotine-induced anxiety”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani et al., 2004
Reduced levels of GluR2/3 subunits were found in the striatum and hippocampus of adolescent mice compared to all other groups 60 days post nicotine dosing.
“Another study reported reduced levels of GluR2/3 subunits in the striatum and hippocampus of adolescent mice compared to all other groups 60 days post nicotine dosing (Adriani et al., 2004).”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani et al., 2004
In the striatum, nicotine increased levels of GluR2/3 subunits in adults relative to age-matched controls, but there was no effect of nicotine on GluR2/3 levels in the hippocampus.
“In the stria tum, nicotine increased levels of GluR2/3 subunits in adults relative to age-matched controls, but there was no effect of nicotine on GluR2/3 levels in the hippocampus.”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani et al., 2004
The findings suggest there are differing adaptations of neural mechanisms depending on whether exposure takes place during adolescence or adulthood, which may result in opposing effects on the risk of the development of nicotine addiction.
“Nevertheless, the findings suggest there are differing adaptations of neural mechanisms depending on whether exposure takes place during adolescence or adulthood, which may result in opposing effects on the risk of the development of nicotine addiction (Adriani et al., 2004).”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani et al., 2004
No nicotine-induced age-related differences in levels of nitric oxide metabolites were found, but adolescent nicotine exposure selectively reduced levels of GluR2/3 subunits in the hippocampus.
“Similar to the amygdala, no nicotine-induced age-related differences in levels of nitric oxide metabolites were found (Keser et al., 2013), but adolescent nicotine exposure selectively reduced levels of GluR2/3 subunits in the hippocampus (Adriani et al., 2004).”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani et al., 2004
Nicotine exposure appears to consistently increase anxiety-related behaviour in adolescents, particularly when exposure takes place during mid-adolescence, although there were sex differences in this effect in one study.
“Regarding anxiety, nicotine exposure appears to consistently increase anxietyrelated behaviour in adolescents, particularly when exposure takes place during mid-adolescence (Adriani et al., 2004; Elliott et al., 2004; Jobson et al., 2019; Smith et al., 2006; Holliday et al., 2016), although there were sex differences in this effect in one study (Elliott et al., 2004).”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani et al., 2004
Age-related differences in several studies were found during specific stages of adolescence (Pre- PND23-35, Mid- PND36-48, Post- PND49-61), with mid-adolescents displaying heightened vulnerability to the effects of nicotine on anxiety-related behaviour compared to both adult-exposed and pre- and post-adolescent exposed rats.
“That is, age-related differences in several studies were found during a specific stage of adolescence i.e., Pre- (PND23 -35), Mid(PND36 -48) and Post-(PND49 -61), with mid-adolescents displaying heightened vulnerability to the effects of nicotine on anxiety-related behaviour compared to both adult-exposed and preand postadolescent exposed rats (Adriani et al., 2004).”
From Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults. (2023) · cites this paper as Adriani et al., 2004
Across many species, many effects of infant abuse remain latent until peri-adolescence.
“Across many species, many of the effects of infant abuse remain latent until peri-adolescence (Adriani and Laviola, 2004, Amaral, 2003, Andersen and Teicher, 2008, Bauman et al., 2006, Costello et al., 2003).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Adriani and Laviola, 2004

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“Evidence for this claim has been found in a study by Adriani and colleagues (2003) who found exposure to nicotine during adolescence increased the vulnerability of developing nicotine addiction compared to when a similar exposure took place in adulthood (Adriani and Laviola, 2004).”
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Authors: Adriani, W., & Laviola, G.
Affiliations: Istituto Superiore di Sanità (IT)
ORCID: Adriani, W.
Venue: Behavioural Pharmacology
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2004-09
Volume: 15
Issue: 5
Pages: 341-352
ISSN: 0955-8810 (ISSN-L)
DOI: 10.1097/00008877-200409000-00005
OpenAlex: W2082376482
Cited by: 267
References: 124
Citations by year: 2026: 5 · 2025: 4 · 2024: 11 · 2023: 4 · 2022: 4 · 2021: 9 · 2020: 7 · 2019: 1 · 2018: 5 · 2017: 14 · 2016: 14 · 2015: 9 · 2014: 15 · 2013: 19 · 2012: 22
FWCI: 1.11
Type: journal article
Language: en
Open access: closed
Locations: Behavioural Pharmacology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: adolescence, vulnerability to psychopathology, nicotine exposure, AMPA receptor subunits, acetylcholine receptor, nicotine self-administration, impulsivity, spontaneously hypertensive rats, attention deficit hyperactivity disorder, methylphenidate, CB1 receptor, self-control, addiction, neuropsychiatric disorders
MeSH terms: Adolescent, Adolescent Behavior, Animals, Attention Deficit Disorder with Hyperactivity, Cannabinoids, Disease Models, Animal, Ganglionic Stimulants, Humans, Nicotine, Rats, Inbred SHR, Risk-Taking, Substance-Related Disorders, Rats

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Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model

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