Boyer Winters
https://twitter.com/Winters_Lab
My group investigates the neurobiology of cognition, with an emphasis on learning and memory. Topics of interest include memory acquisition, consolidation, and reconsolidation in rats and mice, as well as cognitive testing in rodent models of human disorders such as Alzheimer's disease and schizophrenia.
Education
Undergraduate (1994-1998): Experimental Psychology (with Dr. Richard Brown), Dalhousie University, Halifax, NS, Canada
Graduate (1998-2001): PhD in Experimental Psychology (with Dr. Barry Everitt and Dr. Trevor Robbins), University of Cambridge, Cambridge, UK
Post-doctoral (2001-2007): With Dr. Timothy Bussey and Dr. Lisa Saksida, University of Cambridge, Cambridge, UK
Research
Mammalian memory is a complex cognitive process involving the integration of disparate types of information. Our research emphasizes the hierarchical and distributed nature of declarative memory (memory for facts and events) in the brain.
A primary interest of the lab is the neural basis of object recognition memory. We use the spontaneous object recognition paradigm to study the anatomical, pharmacological, and molecular bases of memory acquisition, consolidation, and reconsolidation in rats and mice. Furthermore, we have developed various simple modifications to the basic object recognition task to enable the study of information integration and other cognitive functions in the service of higher-order memories. We use these tasks, in combination with numerous touchscreen-based operant tests, to study the neural bases of cognitive processes in animal models of the normal and diseased brain.
This approach has the potential to provide insight into not only the ‘building blocks' of declarative memory, but also the progressive decline of cognitive function in neurodegenerative diseases such as Alzheimer's disease, in which rather specific memory deficits (e.g., failing to recognise objects such as faces) expand into a marked global amnesia affecting all aspects of autobiographical and factual memory.
Please visit our lab website at https://winterslab.uoguelph.ca/
Selected Publications
(* co-first authors)
Jardine, K.H., Minard, E., Wideman, C.E., Edwards, H., Abouelnaga, K., Messer, W.S., & Winters, B.D. (2024). M1 muscarinic receptor activation reverses age-related memory updating impairment in mice. Neurobiology of Aging, in press.
O’Neill, O.S., Huff, A.E., Jardine, K.H., & Winters, B.D. (2024). Dopamine D1 receptor activation is involved in overcoming boundary conditions for destabilizing and updating object memories. Behavioral Neuroscience, in press.
Abouelnaga, K., Huff, A.E., Jardine, K.H., O’Neill, O. S., & Winters, B.D. (2024). Reactivation-dependent transfer of fear memory between contexts requires M1 muscarinic receptor stimulation in dorsal hippocampus. Learning & Memory, in press.
Mitchnick, K.A., Nicholson, K., Wideman, C.E., Jardine, K.H., Jamieson-Williams, R., Creighton, S.D., Lacoursiere, A., Milite, C., Castellano, S., Sbardella, G., MacLusky, N.J., Choleris, E., & Winters, B.D. (2024). The lysine acetyltransferase PCAF functionally interacts with estrogen receptor alpha in the hippocampus of gonadally intact male - but not female - rats to enhance short-term memory. Journal of Neuroscience, 44 (36), e1574232024.
Huff, E.A., O’Neill, O.S., Messer, W.S., & Winters, B.D. (2024). Muscarinic receptor activation promotes destabilization and updating of object location memories in mice. Behavioural Brain Research, 461, 114847.
Abouelnaga, K., Huff, A.E., O’Neill, O.S., Messer, W.S., & Winters, B.D. (2023). Activating M1 muscarinic cholinergic receptors induces destabilization of resistant contextual fear memories in rats. Neurobiology of Learning and Memory, 205, 107821.
Sanchez-Roige, S., Jennings, M.V., Thorpe, H.H.A., Mallari, J.E., van der Werf. L., Bianchi, S.B., Lee, C., Mallard, T.T., Barnes, S.A., Wu, J.Y., Barkley-Levenson, A.M., Boussaty, E.C., Schafer, D., Snethlage, C., Babic, Z., Winters, B.D., Watters, K.E., Biederer, T., 23andMe Research Team, Mackillop, J., Stephens, D.N., Elson, S.L., Fontanillas, P., Khokhar, J.Y., Young, J.W., Palmer, A.A. (2023). CADM2 is implicated in impulsive personality and numerous other traits by genome- and phenome-wide association studies in humans and mice. Translational Psychiatry, 13, 167.
Wideman, C.E., Huff, A.E., Messer, W.S., & Winters, B.D. (2023). Muscarinic receptor activation overrides boundary conditions on memory updating in a calcium/calmodulin-dependent manner. Neuropsychopharmacology, 48, 1358-1366.
Wolter, M., Lapointe, T., Baidoo, N., Mitchnick, K.A., Wideman, C.A., Winters, B.D., & Leri, F. (2023). Double dissociation of perirhinal nicotinic acetylcholine receptors and dopamine D2 receptors in modulation of object memory consolidation by nicotine, cocaine and their conditioned stimuli. European Neuropsychopharmacology, 72, 50-59.
Wideman, C.E., Minard, E.P., Zacharia, J.M., Capistrano, J.D.R., Scott, G.A., & Winters, B.D. (2022). Dissociating the involvement of muscarinic and nicotinic cholinergic receptors in object memory destabilization and reconsolidation. Neurobiology of Learning and Memory, 195, 107686.
Gattas, S., Collett, H. A., Huff, A.E., Creighton, S.D., Weber, S.E., Buckhalter, S., Manning, S.A., Ryait, H.S., McNaughton, B.L., & Winters, B.D. (2022). A rodent obstacle course for controlled environmental enrichment enhances complex cognitive functions. npj Science of Learning, 7, 21. https://doi.org/10.1038/s41539-022-00134-x.
Narkaj, K., Singh, G., Brimble, M.A., Stefanelli, G., Hall, M., Mitchnick, K.A., Creighton, S.D., Ianov, L., Winters, B.D., Walters, B., Davidoff, A.M., Mitchell, J., Zovkic, I.B. (2022). The histone variant macroH2A1 is a stronger regulator of learning-induced gene expression and memory formation compared to macroH2A2 in mice. Communications Biology, 5, 482. https://doi.org/10.1038/s42003-022-03435-4
Jardine, K.H.*, Wideman, C.E.*, Huff, A.E.*, McGraw, S., & Winters, B.D. (2022). The evidence for and against reactivation-induced memory updating in humans and nonhuman animals. Neuroscience and Biobehavioral Reviews, 136, 104598.
Creighton S.D., Jardine, K.H., Desimone, A., Zmetana, M., Castellano, S., Milite, C., Sbardella, G. & Winters, B.D. (2022). Age-dependent attenuation of spatial memory deficits by the histone acetyltransferase p300/CBP Associated Factor (PCAF) in 3xTG Alzheimer’s disease mice. Learning & Memory, 29, 71-76.
Huff, A.E., McGraw, S., & Winters, B.D. (2022). Muscarinic (M1) cholinergic receptor activation within the dorsal hippocampus promotes destabilization of strongly encoded object location memories. Hippocampus, 32, 55-66.
Wolter, M., Lapointe, T., Melanson, B., Baidoo, N., Winters, B.D., & Leri, F. (2021). Memory enhancing effects of nicotine, cocaine, and their conditioned stimuli; effects of beta-adrenergic and dopamine D2 receptor antagonists. Psychopharmacology, 238(9), 2617-2628.
Wideman, C.E., Nguyen, J., Jeffries, S., & Winters, B.D. (2021). Fluctuating levels of NMDA receptor subunit proteins in perirhinal cortex relate to their dynamic roles in object memory destabilization and reconsolidation. International Journal of Molecular Sciences, 22, 67.
Hamidullah, S., Lutelmowski, C.D., Creighton, S.D., Luciani, K.R., Frie, J.A., Winters, B.D., & Khokhar, J. (2021). Effects of Vapourized THC and Voluntary Alcohol Drinking During Adolescence on Cognition, Reward, and Anxiety-like Behaviours in Rats. Progress in Neuropsychopharmacology & Biological Psychiatry, 106, 110141. doi: 10.1016/j.pnpbp.2020.110141.
Baidoo, N., Wolter, M., Holohan, M., Winters, B.D., & Leri, F. (2021). The effects of morphine withdrawal and conditioned withdrawal on object memory and c-fos expression in the central nucleus of the amygdala. Addiction Biology, 26(2), 1-11.
Jardine, K.H.*, Wideman, C.E.*, MacGregor, C.C., Sgarbossa, C., Orr, D., Mitchnick, K.A., & Winters. B.D. (2020). Activation of cortical M1 muscarinic receptors and related intracellular signaling is necessary for reactivation-induced object memory updating. Scientific Reports, 10: 9209; https://doi.org/10.1038/s41598-020-65836-x.
Mendell, A.L., Creighton, S., Wilson, H., Isaacs, L., Jardine, K., Winters, B.D., & MacLusky, N.J. (2020). Inhibition of 5a reductase impairs cognitive performance, alters dendritic morphology and increases tau phosphorylation in the hippocampus of male 3xTg-AD mice. Neuroscience, 429, 185-202.
Wolter, M., Huff, E., Baidoo, N., Jardine, K., Pulles, Z., Winters, B.D., & Leri, F. (2020). Modulation of object memory consolidation by heroin and heroin-conditioned stimuli: role of opioid and noradrenergic systems. European Neuropsychopharmacology, 33, 146-157.
Beraldo, F.H.*, Palmer, D.*, Wasserman, D.I., Lee, W.V., Liang, S., Kouchehbagh, S.M., Creighton, S.C., Kolisnyk, B., Cowan, M.F., Mels, J., Masood, T.S., Fodor,C., Al-Onaizi, M.A., Bartha, R., Gee, T., Saksida, L.M., Bussey, T.J., Strother, S.S., Prado, V. F., Winters, B.D. & Prado, M.A.M. (2019). MouseBytes, an open-access high throughput pipeline and database for rodent touchscreen-based cognitive assessment. eLife; 8: e49630; DOI: https://doi.org/10.7554/eLife.49630.
Creighton, S.D.*, Collett, H.A.*, Zonneveld, P.M., Pandit, R.A., Huff, A.E., Jardine, K.H., McNaughton, B.L., and Winters, B.D. (2019). Development of an “object category recognition task” for mice: involvement of muscarinic acetylcholine receptors. Behavioral Neuroscience, 133, 527-536.
Mitchnick, K.A., Mendell, A.L., Wideman, C.E., Jardine, K.H., Creighton, S.D., Mueller, A., Choleris, E., MacLusky, N.J., & Winters, B.D. (2019). Dissociable involvement of estrogen receptors in perirhinal cortex-mediated object-place memory in male rats. Psychoneuroendocrinology, 107, 98-108.
Duong, A.T.H., Reitz, C.J., Louth, E.L., Creighton, S.D., Rasouli, M., Zwaiman, A., Kroetsch, J.T., Bolz, S., Winters, B.D., Bailey, C.D.C., & Martino, T.A. (2019). The clock mechanism influences neurobiology and adaptations to heart failure in clock∆19/∆19 mice with implications for circadian medicine. Scientific Reports, 9: 4994; DOI:10.1038/s41598-019-41469-7.
Creighton, S.D., Mendell, A.L., Palmer, D., Kalisch, B.E., MacLusky, N.J., Prado, V. F., Prado, M. A. M., & Winters, B.D. (2019). Dissociable cognitive impairments in two strains of transgenic Alzheimer’s disease mice revealed by a battery of object-based tests. Scientific Reports, 9: 57; DOI:10.1038/s41598-018-37312-0.
Wolter, M., Huff, E., Speigel, T., Winters, B.D., & Leri. F. (2019). Cocaine, nicotine, and their conditioned contexts enhance consolidation of object memory in rats. Learning & Memory, 26, 46-55.
Wideman, C.E., Jardine, K.H., & Winters, B.D. (2018). Involvement of classical neurotransmitter systems in memory reconsolidation: focus on destabilization. Neurobiology of Learning and Memory, 156, 68-79.
Creighton, S.D., Palmer, D., Mitchnick, K.A., & Winters, B.D. (2018). Exploiting novelty and oddity exploratory preferences in rodents to study multisensory object memory and perception. In A. Ennaceur & M. de Souza Silva (Eds), Handbook of Research on Object Novelty Recognition (pp. 103-123). London: Elsevier.
Mitchnick, K.A., Wideman, C., Huff, A.E., Palmer, D., McNaughton, B., & Winters, B.D. (2018). Development of novel tasks for studying view-invariant object recognition in rodents: sensitivity to scopolamine. Behavioral Brain Research, 344, 48-56.
Stiver, M.L., Cloke, J.M., Nightingale, N., Rizos, J., & Winters, B.D. (2017). Linking muscarinic receptor activation to UPS-mediated object memory destabilization: implications for long-term memory modification and storage. Neurobiology of Learning and Memory, 145, 151-164.
Lymer, J., Robinson, A., Winters, B.D., Choleris, E. (2017). Rapid effects of dorsal hippocampal G-protein coupled estrogen receptor on learning in female mice. Psychoneuroendocrinology, 77, 131-140.
Cloke, J.M., Nguyen, R., Chung, B. Y. T., Wasserman, D.I., De Lisio, S., Kim, J.C., Bailey, C.D.C., & Winters, B.D. (2016). A novel multisensory integration task reveals robust deficits in rodent models of schizophrenia: converging evidence for remediation via nicotinic receptor stimulation of inhibitory transmission in the prefrontal cortex. Journal of Neuroscience, 36, 12570-12585. Featured Article.
Chung, B.Y.T., Bignell, W., Jacklin, D.L., Winters, B.D., & Bailey, C.D.C. (2016). Postsynaptic nicotinic acetylcholine receptors facilitate excitation of developing CA1 pyramidal neurons. Journal of Neurophysiology, 116, 2043-2055.
Mitchnick, K.A., Creighton, S.D., van Tiggelen, M., Zaika, O., O’Hara, M., Christen, B., Cloke, J.M., Kalisch, B.E., & Winters, B.D. (2016). Dissociable roles for histone acetyltransferases p300 and PCAF in hippocampus- and perirhinal cortex-mediated object memory. Genes, Brain, and Behavior, 15, 542-557.
Palmer, D., Creighton, S.D., Prado, V.F., Prado, M.A.M., Choleris, E., & Winters, B.D. (2016). Mice deficient for striatal Vesicular Acetylcholine Transporter (VAChT) display impaired short-term but normal long-term object recognition memory. Behavioural Brain Research, 311, 267-278.
Jacklin, D.L., Cloke, J.M., Potvin, A., Garrett, I., & Winters, B.D. (2016). The dynamic multisensory engram: neural circuitry underlying crossmodal object recognition in rats changes with the nature of object experience. Journal of Neuroscience, 36, 1273-1289.
Mitchnick, K.A., Creighton, S.D., O’Hara, M., Kalisch, B.E., & Winters, B.D. (2015). Dissociable contributions of de novo and maintenance DNA methyltransferases to object memory processing in the rat hippocampus and perirhinal cortex. European Journal of Neuroscience, 41, 773-786.
Stiver, M.L., Jacklin, D.L., Mitchnick, K.A, Vicic, N., Carlin, J., O’Hara, M., & Winters, B.D. (2015). Cholinergic manipulations bidirectionally regulate object memory destabilization. Learning & Memory, 22, 203-214.
Jacklin, D.L., Kelly, P., Bianchi, C., MacDonald, T., Traquair, H., & Winters, B.D. (2015). Evidence for a specific role for muscarinic receptors in crossmodal object recognition in rats. Neurobiology of Learning and Memory, 118, 125-132.
Cloke, J.M. & Winters, B.D. (2015). α4β2 nicotinic receptor stimulation of the GABAergic system within the orbitofrontal cortex ameliorates the severe crossmodal object recognition impairment in ketamine-treated rats: implications for cognitive dysfunction in schizophrenia. Neuropharmacology, 90, 42-52.
Sticht, M.A., Jacklin, D.L., Parker, L.A., & Winters, B.D. (2015). Intra-perirhinal cortex administration of the synthetic cannabinoid, HU210, disrupts object recognition memory in rats. NeuroReport, 26, 258-262.
Cloke, J.M., Jacklin, D.L., & Winters, B.D. (2014). The neural bases of crossmodal object recognition in non-human primates and rodents: a review. Behavioural Brain Research, 285, 118-130.
O’Brien, L., Limebeer, C.L., Parker, L.A., & Winters, B.D. (2014). CB1 receptor antagonism in the granular insular cortex or somatosensory area facilitates consolidation of object recognition memory. Neuroscience Letters, 578, 192-196.
Bartko, S.J., Winters, B.D., Saksida, L.M. & Bussey, T.J. (2014). Different roles for M1 and M2 receptors within perirhinal cortex in object recognition and discrimination. Neurobiology of Learning and Memory, 110, 16-26.
Reid, J.M., Jacklin, D.L., & Winters, B.D. (2014). Delineating prefrontal cortex region contributions to crossmodal object recognition in rats. Cerebral Cortex, 24, 2108-2119.
Rkieh, N., Cloke, J.M., Gallagher, N., Winters, B.D., & Leri, F. (2014). Drugs of abuse as memory modulators: a study of cocaine in rats. Psychopharmacology, 231, 2339-2348.
Flavell, C.R., Lambert, E., Winters, B.D., & Bredy, T.W. (2013). Mechanisms governing the reactivation-dependent destabilization of memories and their role in extinction. Frontiers in Behavioral Neuroscience, 7:214. doi: 10.3389/fnbeh.2013.00214
Reid, J.M., Jacklin, D.L., & Winters, B.D. (2012). Crossmodal object recognition in rats with and without multimodal object pre-exposure: no effect of hippocampal lesions. Neurobiology of Learning and Memory, 98, 311-319.
Jacklin, D.L., Goel, A., Clementino, K., Hall, A., Talpos, J.C., & Winters, B.D. (2012). Severe crossmodal object recognition deficits in rats treated sub-chronically with NMDA receptor antagonists are reversed by systemic nicotine: implications for abnormal multisensory integration in schizophrenia. Neuropsychopharmacology, 37, 2322-2331.
Melichercik, A., Elliott, K.S., Bianchi, C., Ernst, S.M., & Winters, B.D. (2012). Nicotinic receptor activation in perirhinal cortex and hippocampus enhances object memory in rats. Neuropharmacology, 62, 2096-2105
Tuerke, K.J., Winters, B.D., & Parker, L.A. (2012). Ondansetron interferes with unconditioned lying-on-belly and acquisition of conditioned gaping induced by LiCl as models of nausea-induced behaviors in rats. Physiology & Behavior, 105, 856-860.
Winters, B.D., Tucci, M.C., Jacklin, D.L., Reid, J.M., & Newsome, J. (2011). On the dynamic nature of the engram: evidence for circuit-level reorganization of object memory traces following reactivation. Journal of Neuroscience, 31, 17719-17728.
McTighe S.M., Cowell, R.A., Winters, B.D., Bussey, T.J., & Saksida, L.M. (2010). Paradoxical false memory for objects after brain damage. Science, 330, 1408-1410.
Bartko, S.J., Cowell, R.A., Winters, B.D., Saksida, L.M. & Bussey, T.J. (2010). Heightened susceptibility to interference in an animal model of amnesia: impairment in encoding, storage, retrieval - or all three? Neuropsychologia, 48, 2987-2997.
Winters, B.D., Bussey, T.J., & Saksida, L.M. (2010). Implications of animal object memory research for human amnesia. Neuropsychologia, 48, 2251-2261.
Winters, B.D. & Reid, J.M. (2010). A distributed cortical representation underlies crossmodal object recognition in rats. Journal of Neuroscience, 30, 6253-6261.
Winters, B.D., Bartko, S.J., Saksida, L.M., & Bussey, T.J. (2010). Muscimol, AP5, or scopolamine infused into perirhinal cortex impairs two-choice visual discrimination learning in rats. Neurobiology of Learning and Memory, 93, 221-228.
Winters, B.D., Tucci, M.C, & DaCosta-Furtado, M. (2009). Older and stronger object memories are selectively destabilized by reactivation in the presence of new information. Learning and Memory, 16, 545-553.
I regularly teach the following courses:
PSYC*2410 - Behavioural Neuroscience I
PSYC*3030 - Neurochemical Basis of Behaviour
PSYC*4470 - Advanced Topics in Behavioural and Cognitive Neuroscience
PSYC*6800 - Neurobiology of Learning (Graduate Seminar)