Effects of adolescent alcohol consumption on the brain and behaviour

An Author Correction to this article was published on 15 May 2018

This article has been updated

Key Points

  • Per occasion, alcohol use is higher among adolescents than adults in both humans and laboratory animals, suggesting that maturational changes in the adolescent brain contribute to the elevation in alcohol consumption seen at this time.

  • Human prospective studies have revealed evidence that certain neural and cognitive or personality associates of heavy adolescent alcohol use may predate and serve as risk factors for such use.

  • There is substantial evidence for notable neural and cognitive consequences of repeated exposure to alcohol during adolescence emerging from both human prospective studies and studies using rodent models. Although dependent measures often differ considerably across species, where comparable measures have been used, evidence for concordance in neural alterations has emerged across species, including disrupted myelination, poorer white matter integrity, alterations in connectivity between frontal and limbic regions and electroencephalographic changes.

  • Studies have revealed that adolescent alcohol exposure is associated with various cognitive and other functional deficits. The consequences that have emerged in human longitudinal work include deficits in verbal learning, attention, and visuospatial and memory tasks, whereas studies using animal models of adolescent alcohol exposure have revealed that such exposure is linked to decreases in cognitive flexibility, behavioural inefficiencies, increases in anxiety-like behaviour, disinhibition, elevated risk-taking, augmented later voluntary consumption and motivation for alcohol, and the persistence of adolescent-like phenotypes into adulthood.

  • In rodent studies, repeated exposure to alcohol during adolescence induces reliable and specific neural alterations that include decreases in cholinergic tone in the basal forebrain, neuroinflammation, disruptions in neurogenesis, epigenetic alterations and the persistence of certain adolescent-like neural characteristics into adulthood.

  • There are numerous critical areas for future work in this area using human longitudinal designs as well as studies in laboratory animals — work that could benefit from an increasing focus on assessment of comparable measures across species. Studies examining functional consequences of adolescent alcohol exposure have largely used different measures to date, with a focus on neuropsychological or cognitive tests in humans contrasting with an emphasis on alterations in risk-taking, anxiety, and later motivation for and sensitivity to alcohol in rodent studies.

Abstract

Per occasion, alcohol consumption is higher in adolescents than in adults in both humans and laboratory animals, with changes in the adolescent brain probably contributing to this elevated drinking. This Review examines the contributors to and consequences of the use of alcohol in adolescents. Human adolescents with a history of alcohol use differ neurally and cognitively from other adolescents; some of these differences predate the commencement of alcohol consumption and serve as potential risk factors for later alcohol use, whereas others emerge from its use. The consequences of alcohol use in human adolescents include alterations in attention, verbal learning, visuospatial processing and memory, along with altered development of grey and white matter volumes and disrupted white matter integrity. The functional consequences of adolescent alcohol use emerging from studies of rodent models of adolescence include decreased cognitive flexibility, behavioural inefficiencies and elevations in anxiety, disinhibition, impulsivity and risk-taking. Rodent studies have also showed that adolescent alcohol use can impair neurogenesis, induce neuroinflammation and epigenetic alterations, and lead to the persistence of adolescent-like neurobehavioural phenotypes into adulthood. Although only a limited number of studies have examined comparable measures in humans and laboratory animals, the available data provide evidence for notable across-species similarities in the neural consequences of adolescent alcohol exposure, providing support for further translational efforts in this context.

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Figure 1: Binge drinking in individuals aged 15–16 years from various European countries and the United States.
Figure 2: Alterations in cortical grey matter volume and task-related brain activation that predate adolescent alcohol use or emerge as a consequence of that use.
Figure 3: Predictors and consequences of alcohol exposure in adolescent humans and rodents.

Change history

  • 15 May 2018

    In the initially published version of this article, the following sentence was incorrect: "Studies that have compared equivalent exposures to alcohol in adolescent and adult animals have found that the effects of alcohol exposure during adolescence are generally not evident or are less pronounced than after comparable alcohol exposure in adulthood". The sentence should have read: "Studies that have compared equivalent exposures to alcohol in adolescent and adult animals have found that the effects of alcohol exposure during adulthood are generally not evident or are less pronounced than after comparable alcohol exposure in adolescence". The sentence has been corrected in the HTML and PDF versions of the article.

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Acknowledgements

Preparation of this review was supported by the National Institute on Alcohol Abuse and Alcoholism of the US National Institutes of Health (NIH) under award numbers U01 AA019972 and P50 AA017823. The author thanks A. MacDonald for aiding in the preparation of the reference section, including the reference numbering. The content is solely the responsibility of the author and does not necessarily represent the official views of the NIH.

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Correspondence to Linda P. Spear.

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PowerPoint slides

Glossary

Binge drinking

As defined by the National Institute on Alcohol Abuse and Alcoholism (NIAAA), a pattern of alcohol use that results in blood alcohol concentrations in the range of 0.08 g/dl or greater; typically, alcohol concentrations in this range are achieved by consumption of five or more or four or more drinks within a 2 hour period in males and females, respectively.

Prospective longitudinal studies

Studies that track individuals over time, ideally starting before the emergence of the target measure (for example, in this context, before the initiation of alcohol use or problematic alcohol use).

Set-shifting task

A task in which animals are first taught one rule about the stimulus that predicts a rewarded operant response. There is then a rule shift, and the animals must learn to ignore the initial rule and instead use another stimulus to determine which response will be rewarded.

Extinction

Learning not to respond when a reinforcer is no longer received.

Elevated plus maze

A test of anxiety that uses a four-armed, cross-shaped apparatus that is well elevated from the floor. Two of the arms are surrounded by high walls (the 'closed arms') whereas the other two arms do not contain walls (the 'open arms'). Anxiety-like behaviour in this test is indexed by animals spending less time and exhibiting fewer entries into the open arms than typically seen in control animals.

Disinhibition

A lack of restraint, often associated with increases in impulsivity or risk-taking.

Probability discounting

In an operant probability discounting task, animals are given a choice between a 'safe' lever associated with a small but consistent reward versus a 'risky' lever associated with a reward that is greater but less probable. In such tasks, increased risk-taking is indexed by animals persisting in choosing the risky lever even when the probability of receiving the higher reward is low.

Diffusion tensor imaging

Type of MRI that examines the diffusion of water molecules (which move more rapidly along, rather than across, myelinated axon pathways) to assess the functional integrity of white matter fibre bundles and to index their neuropathology.

Pons

A sensory relay area in the brainstem that helps regulate arousal, sleep and autonomic processes.

Dendritic spines

Protuberances on neuronal dendrites that are specialized for receiving synaptic inputs.

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Spear, L. Effects of adolescent alcohol consumption on the brain and behaviour. Nat Rev Neurosci 19, 197–214 (2018). https://doi.org/10.1038/nrn.2018.10

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