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The value of spontaneous alternation behavior (SAB) as a test of retention in pharmacological investigations of memory

Hughes, Robert N.·2004·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2004.06.006

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Abstract

Because of its reliance on memory, the tendency for rats, mice and other animals to alternate successive choices of T- or Y-maze arms has assumed considerable popularity in pharmacological studies of spatial memory as a quick and simple measure of retention that avoids the need for extensive training and the use of conventional reinforcers. Two forms of this tendency have been utilized, namely two-trial and continuous spontaneous alternation behavior (SAB). However, as the behavior can also reflect drug-related changes in sensory/attentional, motivational and performance processes, SAB should not be unquestionably accepted as a measure of memory alone. While assessments of post-acquisition drug effects on longer term memory may be possible through the appropriate timing of drug administration, this is more problematic if SAB is used as a measure of shorter term memory. Even though SAB can be a useful index of responsiveness to novelty, its value as a measure of retention is less certain. In this latter respect, a possible alternative to SAB testing might be the recently developed form of the related procedure, responsiveness to change.

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“Forced alternation tests [29] were conducted using a symmetrical Y-maze (BIOCEN, Havana, Cuba).”
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“Hughes, 2004 STOP null mice exhibited deficits in learning Another major aspect of cognitive impairments in schizophrenia is impaired long-term explicit or declarative memory.”
Late effects of a perinatal exposure to a 16 PAH mixture: Increase of anxiety-related behaviours and decrease of regional brain metabolism in adult male rats
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HDAC2-dependent Antipsychotic-like Effects of Chronic Treatment with the HDAC Inhibitor SAHA in Mice
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“Spontaneous alternation (%), defined as successive entries into the three arms on overlapping triplet sets, is associated with spatial short-term memory (Hughes 2004).”
Background
Hippocampal Interneuronal α7 nAChRs Modulate Theta Oscillations in Freely Moving Mice
Gu, Z., Smith, K. G., Alexander, G. M., Guerreiro, I. C., Dudek, S. M., Gutkin, B. S., Jensen, P., & Yakel, J. L. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107740 · Cited by 44
“…the theta oscillations are closely related to Y-maze spontaneous alternation performance (Gu et al., 2017), which depends on spatial working memory (Hughes, 2004) and involves multiple brain regions including the hippocampus (Blampied and Wilby, 1975; Dillon et al., 2008; Lalonde, 2002; Means et…”
BackgroundInfluential
High sucrose consumption during pregnancy induced ADHD-like behavioral phenotypes in mice offspring
Choi, C. S., Kim, P., Park, J. H., Gonzales, E. L., Kim, K. C., Cho, K. S., Ko, M. J., Yang, S. M., Seung, H., Han, S., et al. (2015) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2015.07.018 · Cited by 42
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Background
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“Spontaneous alternation is the tendency of an individual to visit a location not previously visited or which has not been recently visited (Hughes, 2004) and can facilitate the discovery of new habitats, resources, or mates (Ramey et al., 2009).”
Background
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“Alternation in a T-maze provides a test of spatial working memory for rodents that has been used in numerous neuroscientific investigations (Hughes, 2004).”
Effects of fisetin on hyperhomocysteinemia-induced experimental endothelial dysfunction and vascular dementia
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“The alternated behavior of rodents in y-maze indicates operation of spatial working or short-term memory (Hughes 2004).”
Background
Enhancing Executive Functions Through Social Interactions: Causal Evidence Using a Cross-Species Model
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“…a widely used spontaneous alternation task, which is based on the tendency of rodents to explore a prior unexplored arm of a maze, and thus requires that the rodent remember which maze arms were most frequently visited (e.g., Lalonde, 2002; Hughes, 2004; Liet et al., 2015; Kraeuter et al., 2019).”
Background
Modeling Down syndrome in animals from the early stage to the 4.0 models and next
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“Those cognitive phenotypes have been assessed in trisomic mouse models using different tests such as the Y-maze or T-maze for working memory (Hughes, 2004), the long-term novel object recognition (NOR) task for explicit long-term memory (Cohen and Stackman, 2015) or the Morris water maze (MWM) task for spatial learnin…”
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“…over the course of multiple arm entries, animals have a natural tendency to enter the recently visited arm less frequently, thus increasing the number of alternations in turn-direction across the test (Drew, Miller, & Baugh, 1973; Hughes, 2004; Kokkinidis & Anisman, 1976; Swonger & Rech, 1972).”
Background
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“However, to some extent, any memory basis for continuous SAB could be supported by the inclusion of other tests within a given study for which drug-induced changes might be more confidently ascribed to modified retention, such as the radial-arm maze or the Morris water maze (Hughes, 2004).”
BackgroundMethod
Variants in SNCA Gene Are Associated with Parkinson’s Disease Risk and Cognitive Symptoms in a Brazilian Sample
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“PD was diagnosed by a neurologist according to UK Parkinson’s Disease Society Brain Bank Clinical Criteria (Hughes, 2004).”
Method
Lingonberries and their two separated fractions differently alter the gut microbiota, improve metabolic functions, reduce gut inflammatory properties, and improve brain function in ApoE−/− mice fed high-fat diet
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The procognitive effects of 5-HT6 receptor ligands in animal models of schizophrenia
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“Tasks that utilize the natural tendency of rodents to alternate successive choices in T- or Y-maze arms have gained considerable popularity in recent years (Hughes, 2004).”
Background
Neuroprotective effect of chronic administration of cannabidiol during the abstinence period on methamphetamine-induced impairment of recognition memory in the rats
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“Moreover, the animals, which performed less than eight arm entries in 8 min were eliminated from the experiment (Hughes, 2004).”
A Novel Selective PKR Inhibitor Restores Cognitive Deficits and Neurodegeneration in Alzheimer Disease Experimental Models
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“Its rating, in a Y maze, allows the evaluation of spatial orientation capabilities (Hughes, 2004).”
Background
The role of cholinergic and GABAergic medial septal/diagonal band cell populations in the emergence of diencephalic amnesia
Roland, J. J., & Savage, L. M. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.02.044 · Cited by 37
“Such alternation behavior has been described to be memory-dependent action to the environment driven by a natural response to novelty (Hughes, 2004).”
Background
Caffeic acid protects against atherosclerotic lesions and cognitive decline in ApoE−/− mice
Sun, R., Wu, T., Xing, S., Wei, S., Bielicki, J. K., Pan, X., Zhou, M., & Chen, J. (2022) · Journal of Pharmacological Sciences · doi:10.1016/j.jphs.2022.12.006 · Cited by 34
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“A Y-maze spontaneous alternation test was performed in order to evaluate recognition memory, as described previously (24).”
Molecular docking and antiamnesic effects of nepitrin isolated from Rosmarinus officinalis on scopolamine-induced memory impairment in mice
Karim, N., Khan, I., Abdelhalim, A., Abdel‐Halim, H., & Hanrahan, J. R. (2017) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2017.09.121 · Cited by 34
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Neuroprotection by Melatonin after Germinal Matrix Hemorrhage in Neonatal Rats
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“The T-Maze assessed short-term (working) memory [29].”
Silencing of murine transthyretin and retinol binding protein genes has distinct and shared behavioral and neuropathologic effects
Buxbaum, J. N., Roberts, A. J., Adame, A., & Masliah, E. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.019 · Cited by 34
Glucocorticoid-glucocorticoid receptor-HCN1 channels reduce neuronal excitability in dorsal hippocampal CA1 neurons
Kim, J., Lei, Y., Lu, X.-Y., & Kim, C. S. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01682-9 · Cited by 33
“The Y maze test is a frequently used method for assessing spatial learning and memory in mice by monitoring their propensity to explore novel surroundings [53].”
Method
Modulation of benzo[a]pyrene induced neurotoxicity in female mice actively immunized with a B[a]P–diphtheria toxoid conjugate
Schellenberger, M. T., Grova, N., Farinelle, S., Willième, S., Schroeder, H., & Muller, C. P. (2013) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2013.05.007 · Cited by 33
“Immediate working memory performance was assessed by recording spontaneous alternation behavior in a Y maze (Hughes, 2004).”
Method
Peganum harmala enhanced GLP-1 and restored insulin signaling to alleviate AlCl3-induced Alzheimer-like pathology model
Saleh, R. A., Eissa, T. F., Abdallah, D. M., Saad, M. A., & El-Abhar, H. S. (2021) · Scientific Reports · doi:10.1038/s41598-021-90545-4 · Cited by 36
MPTP-Treated Zebrafish Recapitulate ‘Late-Stage’ Parkinson’s-like Cognitive Decline
Bashirzade, A. A., Cheresiz, S. V., Belova, A. S., Drobkov, A. V., Korotaeva, A. D., Azizi‐Arani, S., Azimirad, A., Odle, E., Gild, E.-Y. V., Ardashov, O. V., et al. (2022) · Toxics · doi:10.3390/toxics10020069 · Cited by 33
“To address this knowledge gap, here we applied an MPTP model to characterize PD-like cognitive deficits in adult zebrafish by assessing their spatial working memory and spontaneous alternation behavior (SAB) [24,25].”
Method
MMP-9 inhibition alleviates postoperative cognitive dysfunction by improving glymphatic function via regulating AQP4 polarity
Zhu, B., Cao, A., Chen, C., Zhou, W., Luo, W., Gui, Y., Wang, Q., Xu, Z., & Wang, J. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.111215 · Cited by 32
Delayed Remote Ischemic Postconditioning Improves Long Term Sensory Motor Deficits in a Neonatal Hypoxic Ischemic Rat Model
Perera, P. N. D., Hu, Q., Tang, J., Li, L., Barnhart, M., Doycheva, D. M., Zhang, J. H., & Tang, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090258 · Cited by 32
“A test to ascertain short-term or working memory, as well as complex cortical function [11].”

Authors: Hughes, R. N.
Affiliations: University of Canterbury (NZ)
Corresponding author: Hughes, Robert N.
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2004-09
Volume: 28
Issue: 5
Pages: 497-505
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2004.06.006
OpenAlex: W2143302321
Cited by: 641
References: 116
Citations by year: 2026: 37 · 2025: 47 · 2024: 38 · 2023: 39 · 2022: 54 · 2021: 45 · 2020: 55 · 2019: 41 · 2018: 35 · 2017: 38 · 2016: 28 · 2015: 18 · 2014: 26 · 2013: 24 · 2012: 24
FWCI: 0.65
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Social Sciences › Psychology › Experimental and Cognitive Psychology › Spatial Cognition and Navigation
Keywords: spatial memory, memory retention, T-maze, Y-maze, responsiveness to change, drug effects on memory, attentional processes, motivation
MeSH terms: Acetylcholine, Animals, Attention, Behavior, Animal, Brain Chemistry, Humans, Light, Memory, Reinforcement, Psychology, Smell, Space Perception

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The value of spontaneous alternation behavior (SAB) as a test of retention in pharmacological investigations of memory

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