The Cognition-Enhancing Effects of Psychostimulants Involve Direct Action in the Prefrontal Cortex

Spencer, Robert C.; Devilbiss, David M.; Berridge, Craig W.

doi:10.1016/j.biopsych.2014.09.013

Cited by 164Attention Deficit Hyperactivity DisorderNeurotransmitter Receptor Influence on BehaviorNeuroethics, Human Enhancement, Biomedical Innovations

The Cognition-Enhancing Effects of Psychostimulants Involve Direct Action in the Prefrontal Cortex

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Spencer, Robert C., Devilbiss, David M., Berridge, Craig W.·2015·Biological Psychiatry

DOI 10.1016/j.biopsych.2014.09.013PMC PMC4377121

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Abstract

Psychostimulants are highly effective in the treatment of attention-deficit/hyperactivity disorder. The clinical efficacy of these drugs is strongly linked to their ability to improve cognition dependent on the prefrontal cortex (PFC) and extended frontostriatal circuit. The procognitive actions of psychostimulants are only associated with low doses. Surprisingly, despite nearly 80 years of clinical use, the neurobiology of the procognitive actions of psychostimulants has only recently been systematically investigated. Findings from this research unambiguously demonstrate that the cognition-enhancing effects of psychostimulants involve the preferential elevation of catecholamines in the PFC and the subsequent activation of norepinephrine α2 and dopamine D1 receptors. In contrast, while the striatum is a critical participant in PFC-dependent cognition, where examined, psychostimulant action within the striatum is not sufficient to enhance cognition. At doses that moderately exceed the clinical range, psychostimulants appear to improve PFC-dependent attentional processes at the expense of other PFC-dependent processes (e.g., working memory, response inhibition). This differential modulation of PFC-dependent processes across dose appears to be associated with the differential involvement of noradrenergic α2 versus α1 receptors. Collectively, this evidence indicates that at low, clinically relevant doses, psychostimulants are devoid of the behavioral and neurochemical actions that define this class of drugs and instead act largely as cognitive enhancers (improving PFC-dependent function). This information has potentially important clinical implications as well as relevance for public health policy regarding the widespread clinical use of psychostimulants and for the development of novel pharmacologic treatments for attention-deficit/hyperactivity disorder and other conditions associated with PFC dysregulation.

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DA acts as an inverted U-shaped pattern on cognitive performance; too low or too high DA levels elicited by clinically inappropriate doses of d-amphetamine impair cognition.
“DA acts as an inverted U-shaped pattern to cognitive performance. As is reported, too lower or higher DA level elicited by clinically-inappropriate doses of d-amphetamine impairs cognition (12).”
From Effects of Lisdexamfetamine, a Prodrug of D-Amphetamine, on Locomotion, Spatial Cognitive Processing and Neurochemical Profiles in Rats: A Comparison With Immediate-Release Amphetamine (2022) · cites this paper as [12]
The ‘Receptor Mechanisms in the PFC’ section states that dopamine has an inverted-U-shaped effect on prefrontal-cortex-dependent working memory. ‘Summary and Implications’ contrasts cognitive improvement at clinically relevant psychostimulant doses with impairment at higher doses. The copy does not establish that clinically inappropriate doses of d-amphetamine produce both the low and high dopamine levels described in the claim, and it does not extend the inverted-U relationship to all cognitive performance. (LLM, conf=0.86)
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The cognitive-enhancing effects of amphetamine occur through the dopaminergic transmission activation which, in turn, is mediated by both D1 dopamine receptors and α2-adrenoceptors in postsynaptic neurons in PFC.
“The cognitive-enhancing effects of amphetamine occur through the dopaminergic transmission activation which, in turn, is mediated by both D1 dopamine receptors and α2-adrenoceptors in postsynaptic neurons in PFC [188].”
From Molecular Characterisation of the Mechanism of Action of Stimulant Drugs Lisdexamfetamine and Methylphenidate on ADHD Neurobiology: A Review (2022) · cites this paper as [188]
The “Receptor Mechanisms in the PFC: NE α2 and DA D1 receptors” section (page unavailable) links the cognitive benefits of low-dose psychostimulants to PFC α2 and/or D1 receptor activation. It does not establish the claimed mechanism specifically for amphetamine, and it distinguishes noradrenergic α2 signaling from dopaminergic D1 signaling rather than describing both receptors as mediators of dopamine transmission. (LLM, conf=0.88)
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“However, the MPH effects on these signalling pathways were totally inhibited using ADRD1B blockers, showing that ADRD1B mediates the phosphorylation of PKA signalling through MPH in the PFC [143].”
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“As is reported, too lower or higher DA level elicited by clinicallyinappropriate doses of d-amphetamine impairs cognition (12).”
Background
A Dopamine D1 Agonist Versus Methylphenidate in Modulating Prefrontal Cortical Working Memory
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Psychostimulants as cognitive enhancers: The prefrontal cortex, catecholamines, and attention-deficit/hyperactivity disorder
Berridge, C. W., & Devilbiss, D. M. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.06.023 · Cited by 160 · see citing works
Self-citation
Differential Sensitivity to Psychostimulants Across Prefrontal Cognitive Tasks: Differential Involvement of Noradrenergic α1- and α2-Receptors
Berridge, C. W., Shumsky, J. S., Andrzejewski, M. E., McGaughy, J. A., Spencer, R. C., Devilbiss, D. M., & Waterhouse, B. D. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.07.022 · Cited by 94 · see citing works
Self-citation
Neurocircuitry Underlying the Preferential Sensitivity of Prefrontal Catecholamines to Low-Dose Psychostimulants
Schmeichel, B. E., & Berridge, C. W. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.6 · Cited by 45 · see citing works
Self-citation
Methylphenidate Preferentially Increases Catecholamine Neurotransmission within the Prefrontal Cortex at Low Doses that Enhance Cognitive Function
Berridge, C. W., Devilbiss, D. M., Andrzejewski, M. E., Arnsten, A. F. T., Kelley, A. E., Schmeichel, B., Hamilton, C., & Spencer, R. C. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.04.022 · Cited by 617 · see citing works
Self-citation
Cognition-Enhancing Doses of Methylphenidate Preferentially Increase Prefrontal Cortex Neuronal Responsiveness
Devilbiss, D. M., & Berridge, C. W. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.04.037 · Cited by 117 · see citing works
Self-citation

Authors: Spencer, R. C., Devilbiss, D. M., & Berridge, C. W.
Affiliations: University of Wisconsin–Madison (US)
Corresponding author: Berridge, Craig W.
ORCID: Spencer, Robert C.
Devilbiss, David M.
Berridge, Craig W.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2015-06
Volume: 77
Issue: 11
Pages: 940-950
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2014.09.013
PMC: PMC4377121
OpenAlex: W2080244900
Cited by: 164
References: 108
Citations by year: 2026: 7 · 2025: 13 · 2024: 8 · 2023: 15 · 2022: 18 · 2021: 22 · 2020: 9 · 2019: 20 · 2018: 13 · 2017: 17 · 2016: 14 · 2015: 8
FWCI: 1.80
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Rowan Digitals Works (Rowan University) (submittedVersion, cc-by-nc-nd)
Funders: Public Health Service (MH098631, MH081843, DA000389)
National Science Foundation (NSF 0918555)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Attention Deficit Hyperactivity Disorder
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroethics, Human Enhancement, Biomedical Innovations
Keywords: psychostimulants, cognitive enhancement, prefrontal cortex, attention deficit hyperactivity disorder, catecholamines, dopamine D1 receptor, striatum, frontostriatal circuits, dose-dependent effects, working memory, response inhibition, attention
MeSH terms: Central Nervous System Stimulants, Animals, Cognition, Humans, Prefrontal Cortex

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The Cognition-Enhancing Effects of Psychostimulants Involve Direct Action in the Prefrontal Cortex

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