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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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“Spontaneous alternation was tested in a Y-shaped maze with three white, opaque plastic arms (each with 15 cm × 5 cm × 12 cm) at a 120° angle from each other, as previously described (Hughes, 2004).”
BackgroundMethod
Sitagliptin Attenuates the Cognitive Deficits in L‐Methionine‐Induced Vascular Dementia in Rats
Khodir, S. A., Faried, M. A., Abd-Elhafiz, H. I., & Sweed, E. M. (2022) · BioMed Research International · doi:10.1155/2022/7222590 · Cited by 25
“The altered behavior of rodents in the Y-maze suggested that spatial working or short-term memory was active [36].”
Spontaneously hypertensive rats vs. Wistar Kyoto and Wistar rats: An assessment of anxiety, motor activity, memory performance, and seizure susceptibility
Tchekalarova, J. D., Krushovlieva, D., Ivanova, P., & Kortenska, L. (2023) · Physiology & Behavior · doi:10.1016/j.physbeh.2023.114268 · Cited by 22
“Although the SAB is accepted as a test for assessing spatial working memory, Hughes [31] raised the question of whether this test should be considered a reliable method for retention rather than a mere index of reaction to a novel environment.”
Complete or partial reduction of the Met receptor tyrosine kinase in distinct circuits differentially impacts mouse behavior
Thompson, B. L., & Levitt, P. (2015) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-015-9131-8 · Cited by 23
“Spontaneous alternation in the T-maze was used to assess working memory and attention, although performance is known to be influenced by states of anxiety, arousal, and altered novelty preference [37, 38].”
Method
Decreased Anxiety-Related Behaviour but Apparently Unperturbed NUMB Function in Ligand of NUMB Protein-X (LNX) 1/2 Double Knockout Mice
Lenihan, J. A., Saha, O., Heimer‐McGinn, V., Cryan, J. F., Feng, G., & Young, P. W. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0261-0 · Cited by 21
“If working memory is impaired, mice will fail to remember the positions of the arms just visited and the number of alternations will be reduced [25].”
BackgroundMethod
Individual and sex differences in high and low responder phenotypes
Carreira, M. B., Cossio, R., & Britton, G. B. (2017) · Behavioural Processes · doi:10.1016/j.beproc.2017.01.006 · Cited by 22
“Animals were placed at the center and allowed to freely explore the three arms for five min during which the sequence of entries into the arms was recorded (Hughes, 2004).”
BackgroundMethod
Spontaneous alternation: A potential gateway to spatial working memory in Drosophila
Lewis, S. A., Negelspach, D., Kaladchibachi, S., Cowen, S. L., & Fernandez, F. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.05.013 · Cited by 22
“The connection between spontaneous alternation behavior and spatial working memory has been validated by several decades of work in rodents and primates (Douglas, 1989; Hughes, 2004; Schultz, 1964).”
Background
Elaeagnus glabra f. oxyphylla Attenuates Scopolamine-Induced Learning and Memory Impairments in Mice by Improving Cholinergic Transmission via Activation of CREB/NGF Signaling
Sohn, E., Lim, H.-S., Kim, Y. J., Kim, B., Kim, J., & Jeong, S. (2019) · Nutrients · doi:10.3390/nu11061205 · Cited by 23
Kynurenine pathway is altered in BDNF Val66Met knock-in mice: Effect of physical exercise
Ieraci, A., Beggiato, S., Ferraro, L., Barbieri, S. S., & Popoli, M. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.07.031 · Cited by 22
Calcium Dobesilate Reverses Cognitive Deficits and Anxiety-Like Behaviors in the D-Galactose-Induced Aging Mouse Model through Modulation of Oxidative Stress
Hakimizadeh, E., Zamanian, M. Y., Giménez‐Llort, L., Sciorati, C., Nikbakhtzadeh, M., Kujawska, M., Kaeidi, A., Hassanshahi, J., & Fatemi, I. (2021) · Antioxidants · doi:10.3390/antiox10050649 · Cited by 22
“The percentage of correct alternations was calculated as the index: the number of alternations/total arm visits (minus 2) × 100 [19].”
Method
Delayed alternation performance following subchronic phencyclidine administration in rats depends on task parameters
Marquis, J., Audet, M., Doré, F. Y., & Goulet, S. (2007) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2007.03.017 · Cited by 22
Acetylcholine efflux from retrosplenial areas and hippocampal sectors during maze exploration
Anzalone, S., Roland, J. J., Vogt, B. A., & Savage, L. M. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.02.023 · Cited by 22
“Performance on the spontaneous alternation is not a direct measure of spatial memory per se; however, spontaneous alternation performance is related to spatial memory ability [34, 35].”
Background
An automated Y-maze based on a reduced instruction set computer (RISC) microcontroller for the assessment of continuous spontaneous alternation in rats
Heredia-López, F. J., Álvarez-Cervera, F. J., Alfaro, J. G. C., Bata-García, J. L., Arankowsky‐Sandoval, G., & Góngora-Alfaro, J. L. (2015) · Behavior Research Methods · doi:10.3758/s13428-015-0674-0 · Cited by 24
“This has led to the design of another paradigm known as continuous SAB in which animals freely explore the arms of a Y-maze for several minutes, without repeated manipulation by the experimenter (Hughes, 2004; Morellini, 2013).”
BackgroundMethodInfluential
Lack of placental neurosteroid alters cortical development and female somatosensory function
Bakalar, D., O’Reilly, J. J., Lacaille, H., Salzbank, J., Ellegood, J., Lerch, J. P., Sasaki, T., Kawasawa, Y. I., Hashimoto‐Torii, K., Vacher, C., et al. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.972033 · Cited by 25
“Spontaneous alternation behavior was scored by determining the number of three unique arm entries (alternation) divided by the total number of arm entries minus 1 (59).”
Method
Effect of pioglitazone and simvastatin in lipopolysaccharide-induced amyloidogenesis and cognitive impairment in mice: possible role of glutamatergic pathway and oxidative stress
Ekladious, S. T., & Sayed, N. S. E. (2018) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000407 · Cited by 21
Network-guided analysis of hippocampal proteome identifies novel proteins that colocalize with Aβ in a mice model of early-stage Alzheimer’s disease
Aladeokin, A. C., Akiyama, T. H., Kimura, A., Kimura, Y., Jitsuki‐Takahashi, A., Nakamura, H., Makihara, H., Masukawa, D., Nakabayashi, J., Hirano, H., et al. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104603 · Cited by 23
Evaluation of cognitive function in weanling rats: A review of methods suitable for chemical screening
Ehman, K. D., & MOSER, V. C. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2005.12.002 · Cited by 21
S-SCAM, A Rare Copy Number Variation Gene, Induces Schizophrenia-Related Endophenotypes in Transgenic Mouse Model
Zhang, N., Zhong, P., Shin, S. M., Metallo, J., Danielson, E., Olsen, C. M., Liu, Q.-S., & Lee, S. H. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3658-14.2015 · Cited by 23
“To study the cognitive function of Tg mice, we assessed spatial working memory using spontaneous alternation behavior in the Y-maze (Hughes, 2004).”
MethodInfluential
Cognitive impairments following cranial irradiation can be mitigated by treatment with a tropomyosin receptor kinase B agonist
Yang, P., Leu, D., Ye, K., Srinivasan, C., Fike, J. R., & Huang, T. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.02.021 · Cited by 21
“Defects in SAB in Veh/Irr mice increased with time, and the mice performed significantly worse than DHF/Irr mice when re-examined 5 weeks later (Fig.”
MethodInfluential
First Behavioural Characterisation of a Knockout Mouse Model for the Transforming Growth Factor (TGF)-β Superfamily Cytokine, MIC-1/GDF15
Low, J. K., Ambikairajah, A., Shang, K., Brown, D. A., Tsai, V. W.-W., Breit, S. N., & Karl, T. (2017) · PLoS ONE · doi:10.1371/journal.pone.0168416 · Cited by 20
Cordycepin improves behavioral‐LTP and dendritic structure in hippocampal CA1 area of rats
Han, Y., Chen, Z., Shang, Y., Yan, W., Wu, B., & Li, C. (2019) · Journal of Neurochemistry · doi:10.1111/jnc.14826 · Cited by 20
IGF1 Gene Therapy Reversed Cognitive Deficits and Restored Hippocampal Alterations After Chronic Spinal Cord Injury
Jure, I., Lockhart, E. F., Nicola, A. F. D., Bellini, M. J., & Labombarda, F. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02545-0 · Cited by 20
Silver Nanoparticles Conjugate Attenuates Highly Active Antiretroviral Therapy-Induced Hippocampal Nissl Substance and Cognitive Deficits in Diabetic Rats
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Trace amine-associated receptor 1 modulates motor hyperactivity, cognition, and anxiety-like behavior in an animal model of ADHD
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Shisa7 phosphorylation regulates GABAergic transmission and neurodevelopmental behaviors
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“Mice were allowed to freely explore for 5Lmin and spontaneous alternation behavior was defined as consecutive entry into all three arms without repetition (Hughes, 2004).”
Method
Effects of beta-amyloid on behavioral and amino acids spectrum in rats’ brain and their modulation by embryonic proteins
Yenkoyan, K. B., Safaryan, K., Navasardian, G. A., Mkrtchyan, L. N., & Aghajanov, M. I. (2008) · Neurochemistry International · doi:10.1016/j.neuint.2008.12.010 · Cited by 20
“…ensure normal associative functioning of brain structures (cerebral cortex, hippocampus, striatum), which are involved in learning and short-term memory formation, as well as normal locomotor activity and sensory/attentional factors (Hughes, 2004), that can be damaged in AD (Lalonde et al., 2003).”
Background
Morphological characterization of optimized risperidone-loaded in-situ gel forming implants with pharmacokinetic and behavioral assessments in rats
Ibrahim, T. M., Eissa, R. G., El-Megrab, N. A., & El-Nahas, H. M. (2020) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2020.102195 · Cited by 19
Exploring Refinement Strategies for Single Housing of Male C57BL/6JRj Mice: Effect of Cage Divider on Stress-Related Behavior and Hypothalamic-Pituitary-Adrenal-Axis Activity
Buckinx, A., Schuerbeek, A. V., Bossuyt, J., Allaoui, W., Herrewegen, Y. V. D., Smolders, I. J., & Bundel, D. D. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.743959 · Cited by 19
Cognitive Aging and Early Diagnosis Challenges in Alzheimer's Disease
Britton, G. B., & Rao, K. S. J. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-110239 · Cited by 21
“manipulations to genes associated with AD [40].”
Differential cortical neurotrophin and cytogenetic adaptation after voluntary exercise in normal and amnestic rats
Hall, J. M., Vetreno, R. P., & Savage, L. M. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.10.075 · Cited by 20
“Spontaneous alternation was chosen as it is a reliable measure of spatial working memory that does not require extensive training or reinforcement (Lalonde, 2002; Hughes, 2004).”
Method
Quinolinic acid lesions of the pedunculopontine nucleus impair sleep architecture, but not locomotion, exploration, emotionality or working memory in the rat
Hernández‐Chan, N. G., Góngora-Alfaro, J. L., Álvarez-Cervera, F. J., Solı́s-Rodrı́guez, F., Heredia-López, F. J., & Arankowsky‐Sandoval, G. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.08.007 · Cited by 19
Prenatal Cocaine Disrupts Serotonin Signaling-Dependent Behaviors:Implications for Sex Differences, Early Stress and Prenatal SSRI Exposure
Williams, S. K., Lauder, J. M., & Johns, J. M. (2011) · Current Neuropharmacology · doi:10.2174/157015911796557957 · Cited by 18
“Preclinical models investigating the impact of PC and prenatal SSRI exposure on attention have primarily used the spontaneous alteration test as a measure of working memory and attention; although, the testing protocol, age of the test subject, and motivational factors can play important roles in the interpretation of…”
Method
Wip1 phosphatase positively modulates dendritic spine morphology and memory processes through the p38MAPK signaling pathway
Fernandez, F., Soon, I., Li, Z., Kuan, T. C., Min, D. H., Wong, E. S. M., Demidov, O. N., Paterson, M. C., Dawe, G. S., Bulavin, D. V., et al. (2012) · Cell Adhesion & Migration · doi:10.4161/cam.20892 · Cited by 19
“Performance in the spontaneous alternation task was assessed using a T-maze as previously described.(61,62) This procedure was performed in an enclosed “T”shaped maze in which the long arm of the T (40 cm 10 cm) served as a start arm and the short arms of the T (29 cm 10 cm) served as the goal arms.”
Method
Effect of Fluvoxamine on Amyloid-β Peptide Generation and Memory
Kim, W., Fu, Y.-H., Dobson-Stone, C., Hsiao, J.-H. T., Shang, K.-N., Hallupp, M., Schofield, P., Garner, B., Karl, T., & Kwok, J. B. J. (2018) · Journal of Alzheimer's Disease · doi:10.3233/jad-171001 · Cited by 15
“The version of Y-maze used for this study assesses short-term memory of the familiarity to a spe-ciﬁc context [17].”
Zika Virus Infection Leads to Variable Defects in Multiple Neurological Functions and Behaviors in Mice and Children
Zhao, Z., Shang, Z., de Vasconcelos, Z. F. M., Li, C., Jiang, Y., Zu, S., Zhang, J., Wang, F., Yao, L., Jung, J. U., et al. (2020) · Advanced Science · doi:10.1002/advs.201901996 · Cited by 18
Electroconvulsive stimulation reverses anhedonia and cognitive impairments in rats exposed to chronic mild stress
Henningsen, K., Woldbye, D. P. D., & Wiborg, O. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.03.011 · Cited by 21
“The results of the present study showed a marked effect of ECS on the performance in a working memory dependent task (Hughes, 2004).”
Result
Antiamnesic Effects of a Hydroethanolic Extract of Crinum macowanii on Scopolamine-Induced Memory Impairment in Mice
Mugwagwa, A. T., Gadaga, L. L., Pote, W., & Tagwireyi, D. (2015) · Journal of Neurodegenerative Diseases · doi:10.1155/2015/242505 · Cited by 20
“The SAP and object recognition tasks used in this study have effects on the hippocampus region of the brain which is also associated with neurological damage [12, 13].”
Method
Preclinical development of an EP2 antagonist for post-seizure cognitive deficits
Varvel, N. H., Amaradhi, R., Espinosa‐García, C., Duddy, S. K., Franklin, R. B., Banik, A., Alemán-Ruiz, C., Blackmer‐Raynolds, L., Wang, W., Honoré, T., et al. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109356 · Cited by 18
nNOS in Erbb4-positive neurons regulates GABAergic transmission in mouse hippocampus
Wan, C., Xia, Y., Yan, J., Lin, W.-P., Yao, L., Zhang, M., Gaisler‐Salomon, I., Mei, L., Yin, D., & Chen, Y. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06557-1 · Cited by 18
“Y maze was performed as previously described [72].”
Method
Analysis of sensory, motor and cognitive functions of the coloboma (C3Sn.Cg-Cm/J) mutant mouse
Gunn, R. K., Keenan, M.-E., & Brown, R. E. (2011) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2011.00697.x · Cited by 20
“Each arm entry was recorded, and the total number of arm entries, total number of alternations (number of successive entries in each of the three arms using overlapping triplet sets, in which the three difference arms were entered) and percent spontaneous alternation [(number of alternations/total number of arm entrie…”
Method
Adult-onset focal expression of mutated human tau in the hippocampus impairs spatial working memory of rats
Mustroph, M. L., King, M. A., Klein, R. L., & Ramirez, J. J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.034 · Cited by 23
“Among the advantages of this apparatus over other behavioral tasks are its high sensitivity at detecting memory impairments [50], its ability to tap into spatial working hippocampal memory, and its utility over other methods (such as spontaneous alternation) as a measure of retention [51].”
Background
Effect of three different regimens of repeated methamphetamine on rats’ cognitive performance
Tamijani, S. M. S., Beirami, E., Ahmadiani, A., & Dargahi, L. (2017) · Cognitive Processing · doi:10.1007/s10339-017-0839-0 · Cited by 18
“Spontaneous alternation behavior (SAB) test One week after last MA injections, rats were subjected to the test of Y-maze spontaneous alternation behavior (SAB) as a measure of the spatial working memory (Hughes 2004).”
BackgroundMethodInfluential

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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