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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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Background
Protective effects of isofraxidin against scopolamine-induced cognitive and memory impairments in mice involve modulation of the BDNF-CREB-ERK signaling pathway
Lian, B., Gu, J., Zhang, C., Zou, Z., Yu, M., Li, F., Wu, X., & Zhao, A. Z. (2022) · Metabolic Brain Disease · doi:10.1007/s11011-022-00980-z · Cited by 13
“During the training trial, one arm (C) was closed, and the animals were positioned in one of the open arms (A) and allowed 15 min to explore the open arms (A and B) of the Y-maze(Ennaceur and Delacour 1988; Hughes 2004).”
BackgroundMethod
Longitudinal assessment of infarct progression, brain metabolism and behavior following anterior cerebral artery occlusion in rats
Endepols, H., Mertgens, H., Backes, H., Himmelreich, U., Neumaier, B., Graf, R., & Mies, G. (2014) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2014.11.003 · Cited by 13
Muscle Injury Induces Postoperative Cognitive Dysfunction
Guéniot, L., Lepère, V., de Medeiros, G. F., Danckaert, A., Flamant, P., Dudal, M. L., Langeron, O., Goossens, P. L., Chrétien, F., & Jouvion, G. (2020) · Scientific Reports · doi:10.1038/s41598-020-59639-3 · Cited by 13
Cognitive and Affective Dysregulation in Neuropathic Pain: Associated Hippocampal Remodeling and Microglial Activation
Tyrtyshnaia, A. A., Manzhulo, I., Egoraeva, A. A., & Ivashkevich, D. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26136460 · Cited by 12
“…previous studies have demonstrated that the spared nerve injury (SNI) model does not substantially impair gross locomotor abilities, and that spontaneous alternation performance is a reliable measure of hippocampal-dependent cognition, relatively unaffected by minor variations in movement [15–18].”
The electro-responsive nanoliposome as an on-demand drug delivery platform for epilepsy treatment
Sabet, F. S., Dabirmanesh, B., Sabet, H. S., Zarei, P., Hosseini, M., Fathollahi, Y., & Khajeh, K. (2024) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2024.124610 · Cited by 13
Age-related behavioural phenotype and cellular characterisation of mice with progressive ablation of D1 dopamine receptor-expressing cells
Babovic, D., Jiang, L., Gantois, I., Lawrence, A. J., Ferreri, V., Schütz, G., Waddington, J. L., & Drago, J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.08.036 · Cited by 12
Gastrin-releasing peptide regulates fear learning under stressed conditions via activation of the amygdalostriatal transition area
Goto, F., Kiyama, Y., Ogawa, I., Okuno, H., Ichise, T., Ichise, H., Anai, M., Kodama, T., Yoshida, N., Bito, H., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-021-01408-3 · Cited by 12
Toxicity effects evaluation of green synthesized silver nanoparticles on intraperitoneally exposed male Wistar rats
Tarbali, S., Mehrian, S. K., & Khezri, S. (2022) · Toxicology Mechanisms and Methods · doi:10.1080/15376516.2022.2049412 · Cited by 12
“Therefore, the Y-maze was selected to assess the working memory (Hughes 2004).”
Method
The neuroendocrine stress response impairs hippocampal vascular function and memory in male and female rats
Johnson, A. C., Uhlig, F., Einwag, Z., Cataldo, N., & Erdös, B. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105717 · Cited by 12
“3B) (Hughes, 2004; Lalonde, 2002).”
Dexpramipexole ameliorates cognitive deficits in sepsis-associated encephalopathy through suppressing mitochondria-mediated pyroptosis and apoptosis
Zhang, Y., Fu, Q., Ruan, J., Shi, C.-X., Lu, W., Wu, J., & Zhou, Z. (2023) · Neuroreport · doi:10.1097/wnr.0000000000001882 · Cited by 12
Nicotine exposure during adolescence: cognitive performance and brain gene expression in adult heterozygous reeler mice
Romano, E., Angelis, F. D., Ulbrich, L., Jaco, A. D., Fuso, A., & Laviola, G. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3388-y · Cited by 14
Erythropoietin protects polychlorinated biphenyl (Aroclor 1254) induced neurotoxicity in mice
Chellammal, H. S. J., Syeda, T., Kakalij, R. M., Prasad, V. V. L. N., & Diwan, P. V. (2013) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2013.03.009 · Cited by 12
“The alterated behaviour of rodents in Y-maze indicates operation of spatial working or short-term memory (Hughes, 2004).”
Background
Rice Research: Open Access
(2019) · Rice Research Open Access · doi:10.4172/2375-4338 · Cited by 12
The primary cilia are associated with the axon initial segment in neurons
Wang, H., Li, Y., Li, X., Sun, Z., Yu, F., Pashang, A., Kulasiri, D., Li, H. W., Chen, H., Hou, H., et al. (2025) · Advanced Science · doi:10.1002/advs.202407405 · Cited by 13
Mining the brain metabolome to understand behavioural disruptions induced in mouse fed Hypochoeris radicata (L.), a neurotoxic plant for horse
Domange, C., Schroeder, H., Violle, N., Peiffer, J., Canlet, C., Paris, A., & Priymenko, N. (2013) · NeuroToxicology · doi:10.1016/j.neuro.2013.06.005 · Cited by 11
“…of spontaneous alternation was calculated as the ratio of actual successful overlapping alternations by the total possible triplets (defined as the total number of arm entries minus two) multiplied by 100, and was considered as representative of the immediate learning performance (Hughes, 2004).”
Method
GLP-2 restores impairments in spatial working memory and hippocampal LTD via the MEK/ERK pathway in juvenile-onset diabetes rats
Sasaki‐Hamada, S., Fujiwara, A., Satoh, S., Iwai, T., & Oka, J. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113235 · Cited by 11
Spatial working memory is disparately interrelated with social status through different developmental stages in rats
suha, A. J., Hosseinmardi, N., & Janahmadi, M. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113547 · Cited by 11
Ca V 3.1 T-type calcium channels regulate spatial memory processing in the dorsal subiculum
Joksimovic, S. M., Ghodsi, S. M., Heinsbroek, J. A., Orfila, J. E., Busquet, N., Tešić, V., Valdez, R., Fine-Raquet, B., Jevtović‐Todorović, V., Raol, Y. H., et al. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109400 · Cited by 10
Evaluating the Protective Effects of Melatonin Against Chronic Iron Administration in Male Wistar Rats: a Comparative Analysis of Affective, Cognitive, and Oxidative Stress with EDTA Chelator
Rezqaoui, A., Boumlah, S., Hessni, A. E., Brouzi, M. Y. E., Hamzaoui, A. E., Ibouzine‐Dine, L., Benkirane, S., Adnani, M., & Mesfioui, A. (2023) · Biological Trace Element Research · doi:10.1007/s12011-023-04006-2 · Cited by 11
“It is still called the spontaneous alternation test because of the absence of a reinforcer, such as food [36].”
Thiamine deficiency degrades the link between spatial behavior and hippocampal synapsin I and phosphorylated synapsin I protein levels
Resende, L. D. S., Ribeiro, Â. M., Werner, D. F., Hall, J. M., & Savage, L. M. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.004 · Cited by 11
Loss of Lypd6 leads to reduced anxiety-like behaviour and enhanced responses to nicotine
Arvaniti, M., Polli, F. S., Kohlmeier, K. A., Thomsen, M. S., & Andreasen, J. T. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.11.025 · Cited by 11
“Furthermore, we use the SAB task (Hughes, 2004) to assess possible alterations in cognitive performance.”
Influential
Translation-Focused Approaches to GPCR Drug Discovery for Cognitive Impairments Associated with Schizophrenia
Hatzipantelis, C. J., Langiu, M., Vandekolk, T. H., Pierce, T. L., Nithianantharajah, J., Stewart, G. D., & Langmead, C. J. (2020) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.0c00117 · Cited by 13
Assessment of 9-OH- and 7,8-diol-benzo[a]pyrene in Blood as Potent Markers of Cognitive Impairment Related to benzo[a]pyrene Exposure: An Animal Model Study
Cherif, L. S., Cao-Lei, L., Farinelle, S., Muller, C. P., Turner, J. D., Schroeder, H., & Grova, N. (2021) · Toxics · doi:10.3390/toxics9030050 · Cited by 12
“Observers counted spontaneous alternation between arms using the four-paw criteria for “successive entries into the three arms on overlapping triplet sets”[40].”
Method
Quercetin mitigates scopolamine-induced memory dysfunction: impact on oxidative stress and cholinergic mechanisms
Olayinka, J. N., Eduviere, A. T., Adeoluwa, O. A., Akinluyi, E. T., Obisesan, A. O., Akawa, O. B., & Adebanjo, A. (2021) · Metabolic Brain Disease · doi:10.1007/s11011-021-00861-x · Cited by 12
Association between Novel Object Recognition/Spontaneous Alternation Behavior and Emission of Ultrasonic Vocalizations in Rats: Possible Relevance to the Study of Memory
Costa, G., Serra, M., & Simola, N. (2021) · Brain Sciences · doi:10.3390/brainsci11081053 · Cited by 11
“Indeed, curiosity may be associated with increased arousal [41], and curiosity is thought to be a factor that drives the exploratory behavior of rats exposed to a Y maze [22].”
BackgroundMethodInfluential
Comparison of intranasal and intraperitoneal administration of Eugenia caryophyllata (clove) essential oil on spatial memory, anxiety-like behavior and locomotor activity in a pilocarpine-induced status epilepticus rat model
Parvizi, F., Mehrabi, S., Naghizadeh, A., Kamalinejad, M., Goudarzi, S., & Farahmandfar, M. (2022) · BMC Complementary Medicine and Therapies · doi:10.1186/s12906-022-03711-0 · Cited by 11
“In a recent study exploring these effects, a descrease in spontaneous alteration behavior was seen in Y-maze test [78].”
MethodInfluential
Vitamin D 3 exerts immunomodulatory and memory improving properties in rats with lipopolysaccharide-induced inflammation
Doncheva, N., Mihaylova, A., Zlatanova, H., Ivanovska, M., Delev, D. P., Murdjeva, M., & Kostadinov, I. (2022) · Folia Medica · doi:10.3897/folmed.64.e67739 · Cited by 12
“An alternation represents consecutive entries into three different arms of the Y-maze.[46] In this task the memory improving effect of cholecalciferol was evaluated by calculating the % SA.”
Method
Antiamnesic Effects of Novel Phthalimide Derivatives in Scopolamine-Induced Memory Impairment in Mice: A Useful Therapy for Alzheimer’s Disease
Karim, N., Khan, I., Khan, I., Halim, S. A., Khalid, A., Abdalla, A. N., Rehman, N. U., Khan, A., & Al‐Harrasi, A. (2023) · ACS Omega · doi:10.1021/acsomega.2c07951 · Cited by 10
Neuroprotective effect of dexmedetomidine on autophagy in mice administered intracerebroventricular injections of Aβ25–35
Lee, Y. Y., Han, J. I., Cho, S., Suh, E. C., & Lee, K. E. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1184776 · Cited by 10
Treadmill Running Regulates Adult Neurogenesis, Spatial and Non-spatial Learning, Parvalbumin Neuron Activity by ErbB4 Signaling
Yi, Y., Zhang, Y., Song, Y., & Lu, Y. (2024) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-023-01439-0 · Cited by 10
“A forced-choice paradigm was employed to encourage a higher level of alternation (Hughes 2004).”
Age-related changes in species-typical behaviours in the 5xFAD mouse model of Alzheimer’s disease from 4 to 16 months of age
O’Leary, T. P., & Brown, R. E. (2024) · Behavioural Brain Research · doi:10.1016/j.bbr.2024.114970 · Cited by 11
Reciprocating Motion of a Self-Propelled Rotor Induced by Forced Halt and Release Operations
Nakata, S., Kayahara, K., Yamamoto, H., Skrobanska, P., Górecki, J., Awazu, A., Nishimori, H., & Kitahata, H. (2018) · The Journal of Physical Chemistry C · doi:10.1021/acs.jpcc.7b12089 · Cited by 10
Automation of Continuous Spontaneous Alternation to Increase the Throughput for In Vivo Screening of Cognitive Enhancers. Optimization of the Ethovision System for the Y-maze Test in Mice
Detrait, E., Brohez, C., Hanon, É., & Ryck, M. D. (2010) · Cited by 10
A Sphingosine-1-Phosphate Receptor Modulator Attenuated Secondary Brain Injury and Improved Neurological Functions of Mice after ICH
Bobinger, T., Bäuerle, T., Seyler, L., von Hörsten, S., Schwab, S., Huttner, H. B., & Manaenko, A. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/3214350 · Cited by 10
“We investigated effects of ICH and Siponimod treatment on short-term, working memory by using a short-term (working) memory test, the T-Maze test [17].”
Method
Vaccinium bracteatum Improves Spatial Learning and Memory by Regulating N-methyl-D-aspartate Receptors and Tau Phosphorylation in Chronic Restraint Stress-Induced Memory Impaired Mice
Oh, D.-R., Kim, Y., Im, S., Oh, K.-N., Shin, J., Jeong, C., Kim, Y., Choi, E. J., & Choi, C. (2020) · The American Journal of Chinese Medicine · doi:10.1142/s0192415x2150004x · Cited by 10
S327 phosphorylation of the presynaptic protein SEPTIN5 increases in the early stages of neurofibrillary pathology and alters the functionality of SEPTIN5
Ferreira, C. B., Marttinen, M., Coelho, J. E., Paldanius, K. M. A., Takalo, M., Mäkinen, P. M., Leppänen, L., Miranda‐Lourenço, C., Fonseca‐Gomes, J., Tanqueiro, S. R., et al. (2021) · Neurobiology of Disease · doi:10.1016/j.nbd.2021.105603 · Cited by 10
“Spatial working memory was assessed using the spontaneous alternation version of the Y-maze test (Hughes, 2004; Spellman et al., 2015).”
Method
Neuroprotective evaluation of diospyrin against drug-induced Alzheimer’s disease
Alam, A., Ali, G., Nawaz, A., AlOmar, T. S., Rauf, A., Ayaz, M., Ahmad, S., Almasoud, N., AlOmar, A. S., Khalil, A. A., et al. (2023) · Fitoterapia · doi:10.1016/j.fitote.2023.105703 · Cited by 9
Amelioration of Scopolamine-Induced Cognitive Dysfunction in Experimental Mice Using the Medicinal Plant Salvia moorcroftiana
Wahid, F., Jan, T., Al-Joufi, F. A., Ali Shah, S. W., Nisar, M., & Zahoor, M. (2022) · Brain Sciences · doi:10.3390/brainsci12070894 · Cited by 10
“The results obtained in this study are in accordance with previously reported studies [34,35].”
Result
Influence of chrysin on D‐galactose induced‐aging in mice: Up regulation of AMP kinase/liver kinase B1/peroxisome proliferator‐activated receptor‐γ coactivator 1‐α signaling pathway
Salama, A., & Elgohary, R. (2023) · Fundamental and Clinical Pharmacology · doi:10.1111/fcp.12895 · Cited by 9
“In recent years, spontaneous alternation behavior has been enthusiastically embraced by behavioral pharmacologists and others as a quick and relatively simple test of memory [32].”
Background
Dose-Dependent Cognitive Decline, Anxiety, and Locomotor Impairments Induced by Doxorubicin: Evidence from an Animal Model
Amaro-Leal, Â., Afonso, A., Machado, F. S., Shvachiy, L., Rocha, I., Outeiro, T. F., & Geraldes, V. (2024) · Biology · doi:10.3390/biology13110939 · Cited by 9
Dexmedetomidine Attenuated Neuron Death, Cognitive Decline, and Anxiety-Like Behavior by Inhibiting CXCL2 in CA1 Region of AD Mice
Ma, K., An, C., Li, M., Zhang, Y., Ren, M., Wei, Y., Xu, W., Wang, R., Bai, Y., Zhang, H., et al. (2024) · Drug Design Development and Therapy · doi:10.2147/dddt.s489860 · Cited by 9
Comorbidities in the mouse model of temporal lobe epilepsy induced by intrahippocampal kainate
Samalens, L., Beets, C., Courivaud, C., Kahane, P., & Depaulis, A. (2025) · Epilepsia · doi:10.1111/epi.18553 · Cited by 9
Distinct signatures on d ‐galactose‐induced aging and preventive/protective potency of two low‐dose vitamin D supplementation regimens on working memory, muscular damage, cardiac and cerebral oxidative stress, and SIRT1 and calstabin2 downregulation
Salemi, S., Zamanian, M. Y., Giménez‐Llort, L., Jalali, Z., Mahmoodi, M., Golmohammadi, M., Kaeidi, A., Taghipour, Z., Khademalhosseini, M., Modanloo, M., et al. (2023) · Food Science & Nutrition · doi:10.1002/fsn3.3422 · Cited by 10
Simple shelter-style environmental enrichment alters behavior in mice
Coke-Murphy, C., Buendia, M. A., Saborido, T. P., & Stanwood, G. D. (2014) · Translational Neuroscience · doi:10.2478/s13380-014-0228-4 · Cited by 9
The puzzle of spontaneous alternation and inhibition of return: How they might fit together
Phillmore, L. S., & Klein, R. M. (2019) · Hippocampus · doi:10.1002/hipo.23102 · Cited by 9
“Consequently, measurement of spontaneous alternation has become a common component of test batteries used to assess this type of memory in the face of various manipulations, such as lesions, developmental adversity, or pharmacological administration (Hughes, 2004).”
BackgroundInfluential
Characterization of aged male BALB/ccenp mice as a model of dementia
Esquivel, N., García, Y., Lores, B., Gutiérrez, M., & Martínez, C. R. (2020) · Laboratory Animal Research · doi:10.1186/s42826-020-00038-0 · Cited by 9
Differential Effects of Human P301L Tau Expression in Young versus Aged Mice
Hunsberger, H. C., Setti, S. E., Rudy, C. C., Weitzner, D. S., Pfitzer, J. C., McDonald, K. L., Hong, H., Bhattacharya, S., Suppiramaniam, V. D., & Reed, M. N. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111637 · Cited by 10
“We next examined spatial working memory by measuring the number of alterations made during the 8 min trial, where alternation is defined as the successive entries of the three arms on overlapping triplet sets, in which three different arms are entered [58].”
Method
Tenofovir-silver nanoparticles conjugate ameliorates neurocognitive disorders and protects ultrastructural and cytoarchitectonic properties of the prefrontal cortex in diabetic rats
Lawal, S. K., Olojede, S. O., Sulaiman, S. O., Aladeyelu, O. S., Moodley, R., Naidu, E. C., Rennie, C. O., & Azu, O. O. (2022) · Biomolecules and Biomedicine · doi:10.17305/bjbms.2021.6699 · Cited by 9
“The “spontaneous alternation performance” and “same arm return (SAR)” was done following previously used methods [38,39].”
Method

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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