The neural basis of reversal learning: An updated perspective

Izquierdo, A.; Brigman, J.L.; Radke, A.K.; Rudebeck, P.H.; Holmes, A.

doi:10.1016/j.neuroscience.2016.03.021

Cited by 670Neural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on BehaviorCognitive Functions and Memory

The neural basis of reversal learning: An updated perspective

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Izquierdo, A., Brigman, J.L., Radke, A.K., Rudebeck, P.H., Holmes, A.·2017·Neuroscience

DOI 10.1016/j.neuroscience.2016.03.021PMC PMC5018909

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Abstract

Reversal learning paradigms are among the most widely used tests of cognitive flexibility and have been used as assays, across species, for altered cognitive processes in a host of neuropsychiatric conditions. Based on recent studies in humans, non-human primates, and rodents, the notion that reversal learning tasks primarily measure response inhibition, has been revised. In this review, we describe how cognitive flexibility is measured by reversal learning and discuss new definitions of the construct validity of the task that are serving as a heuristic to guide future research in this field. We also provide an update on the available evidence implicating certain cortical and subcortical brain regions in the mediation of reversal learning, and an overview of the principal neurotransmitter systems involved.

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PRL performance depends on complex interactions between several component processes, including sensitivity to positive and negative feedback, response persistence, and exploration versus exploitation, each requiring functional activity in distinct PFC regions and brain regions outside the PFC.
“PRL performance depends on complex interactions between several component processes, including the sensitivity to positive and negative feedback, response persistence and exploration versus exploitation, each of which requires functional activity in distinct PFC regions (Verharen et al., 2018(Verharen et al., , 2020)), as well as brain regions outside the PFC (Izquierdo et al., 2017).”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Izquierdo et al., 2017
Extensive research in rodents and non-human primates emphasises major roles of fronto-striatal circuits in the ability to respond flexibly.
“Extensive research in rodents and non-human primates emphasises the major roles of fronto-striatal circuits in the ability to respond flexibly [34–42].”
From Linking haploinsufficiency of the autism- and schizophrenia-associated gene Cyfip1 with striatal-limbic-cortical network dysfunction and cognitive inflexibility (2024) · cites this paper as [40]
Reversal learning paradigms measure adaptive responding when stimulus-outcome or response-outcome contingencies change.
“These paradigms assess the ability to respond adaptively in the face of changing stimulus–outcome or response–outcome contingencies15.”
From Cognitive and behavioural flexibility: Neural mechanisms and clinical considerations (2021) · cites this paper as [15]
Inactivating the orbitofrontal cortex in rats impairs reversal learning because they perseverate on previously learned choices.
“OFC inactivation in rats impairs reversal learning owing to perseverance of previously learned choices15.”
From Cognitive and behavioural flexibility: Neural mechanisms and clinical considerations (2021) · cites this paper as [15]
Reversal learning paradigms are often used to study cognitive flexibility in both humans and animals.
“To study cognitive flexibility in both humans and animals, reversal learning paradigms are often used.19, 20”
From Behavioral flexibility in a mouse model for obsessive‐compulsive disorder: Impaired Pavlovian reversal learning in SAPAP3 mutants (2019) · cites this paper as [19]

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Selective lesions of the dorsomedial striatum impair serial spatial reversal learning in rats
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“Neuroimaging studies report increased activity in orbitofrontal cortex (OFC) and medial prefrontal cortex (mPFC) in human subjects performing reversals (Nagahama et al., 2001; Cools et al., 2002; Kringelbach and Rolls, 2003; Remijnse et al., 2005; Ghahremani et al., 2010), and patients with lesions of these regions ex…”
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Basolateral Amygdala Lesions Abolish Orbitofrontal-Dependent Reversal Impairments
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Paradoxical reversal learning enhancement by stress or prefrontal cortical damage: rescue with BDNF
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Assessment of Glutamate Transporter GLAST (EAAT1)-Deficient Mice for Phenotypes Relevant to the Negative and Executive/Cognitive Symptoms of Schizophrenia
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Chronic intermittent cold stress and serotonin depletion induce deficits of reversal learning in an attentional set-shifting test in rats
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Impaired discrimination learning in mice lacking the NMDA receptor NR2A subunitPreprint
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Enhancement of Spatial Reversal Learning by 5-HT<sub>2C</sub>Receptor Antagonism Is Neuroanatomically Specific
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“For instance, in rats antagonism of 5-HT2A (via MDL 100-907) impairs reversal performance, while 5-HT2C antagonism (with SB 242084) facilitates performance (Boulougouris et al., 2008; Boulougouris and Robbins, 2010; Nilsson et al., 2012; Furr et al., 2012b), though there is also a report of an overall impairment after…”
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Authors: Izquierdo, A., Brigman, J. L., Radke, A. K., Rudebeck, P. H., & Holmes, A.
Affiliations: University of California, Los Angeles (US)
University of New Mexico (US)
National Institutes of Health (US)
Icahn School of Medicine at Mount Sinai (US)
Corresponding author: Izquierdo, A.
ORCID: Izquierdo, A.
Brigman, J.L.
Radke, A.K.
Rudebeck, P.H.
Venue: Neuroscience
Publisher: Elsevier BV
Published: 2017-03
Volume: 345
Pages: 12-26
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/j.neuroscience.2016.03.021
PMC: PMC5018909
OpenAlex: W2294342312
Cited by: 670
References: 221
Citations by year: 2026: 66 · 2025: 93 · 2024: 89 · 2023: 69 · 2022: 77 · 2021: 79 · 2020: 68 · 2019: 47 · 2018: 36 · 2017: 31 · 2016: 14
FWCI: 4.47
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: UCLA Division of Life Sciences Recruitment and Retention
National Institute on Alcohol Abuse and Alcoholism (1P50AA022534-01)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
Keywords: reversal learning, cognitive flexibility, response inhibition, construct validity, neural basis, cortical regions, subcortical structures, neurotransmitter systems, neuropsychiatric disorders, non-human primates, rodents
MeSH terms: Animals, Brain, Humans, Neurons, Reversal Learning

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The neural basis of reversal learning: An updated perspective

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