Short Photoperiods Impair Spatial Learning and Alter Hippocampal Dendritic Morphology in Adult Male White-Footed Mice (Peromyscus leucopus)
Open accessAbstract
Although seasonal changes in brain morphology and function are well established in songbirds, seasonal plasticity of brain structure and function remain less well documented in mammals. Nontropical animals display many adaptations to reduce energy use to survive winter, including cessation of reproductive activities. Because of the high energetic costs of brain tissue, we hypothesized that male white-footed mice (Peromyscus leucopus) would reduce brain size in response to short days as well as regress their reproductive systems. Because short days may decrease hippocampal volume and impair spatial learning and memory in rodents and because of the potential for seasonal plasticity in the hippocampus, we hypothesized that photoperiod alters hippocampal morphology to affect spatial learning and memory. Mice housed in either long or short days for 10 weeks were examined for performance in a water maze; brains were then removed and weighed, and hippocampal volumes were determined. We also measured dendritic morphology and spine density in the CA1, CA3, and dentate gyrus. Short days decreased brain mass and hippocampal volume compared with long days. Short days also impaired long-term spatial learning and memory relative to long days but did not affect sensory discrimination or other types of memory. Short days decreased apical (stratum lacunosum-moleculare) CA1 spine density, as well as increased basilar (stratum oriens) CA3 spine density. Results from this study suggest that photoperiod alters brain size and morphology, as well as cognitive function. Understanding the mechanisms mediating these photoperiod-induced alterations may provide insight for treatment of seasonal cognitive and affective disorders.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In rodents such as white-footed mice, exposure to a short-day, winter-like photoperiod impairs spatial learning and alters hippocampal plasticity, such as dendritic spine density and decreased long-term potentiation in the CA1.
“In rodents, such as white-footed mice, exposure to a short-day, winter-like, photoperiod impairs spatial learning and alters hippocampal plasticity, such as dendritic spine density and decreased LTP in the CA1 (Pyter et al., 2005; Pyter et al., 2008) .”
From Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges (2009) · cites this paper as Pyter et al., 2008
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180 · see citing works
Place navigation impaired in rats with hippocampal lesions
Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982) · Nature · doi:10.1038/297681a0 · Cited by 6,340 · see citing works
Beaton, A. E., & Keppel, G. (1975) · American Educational Research Journal · doi:10.2307/1162588 · Cited by 5,857 · see citing works
The efficiency of systematic sampling in stereology and its prediction *
Gundersen, H., & Jensen, E. B. V. (1987) · Journal of Microscopy · doi:10.1111/j.1365-2818.1987.tb02837.x · Cited by 3,586 · see citing works
STRESS AND HIPPOCAMPAL PLASTICITY
McEwen, B. S. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.105 · Cited by 2,087 · see citing works
(2000) · Cited by 919 · see citing works
Goldman, B. D. (2001) · Journal of Biological Rhythms · doi:10.1177/074873001129001980 · Cited by 771 · see citing works
The Organization of the Cerebral Cortex
Sholl, D. A. (1957) · The American Journal of the Medical Sciences · doi:10.1097/00000441-195711000-00015 · Cited by 762 · see citing works
Rampon, C., Tang, Y.-P., Goodhouse, J., Shimizu, E., Kyin, M., & Tsien, J. Z. (2000) · Nature Neuroscience · doi:10.1038/72945 · Cited by 737 · cited 1× · see citing works
“For example, environmental enrichment (Diamond et al., 1976; Rampon et al., 2000) and awakening after hibernation (Popov et al.”
BackgroundGlucocorticoids and the regulation of memory consolidation
Roozendaal, B. (2000) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(99)00058-x · Cited by 665 · see citing works
Moser, M., Trommald, M., & Andersen, P. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.26.12673 · Cited by 615 · see citing works
Mammalian Reproduction: An Ecological Perspective 1
Bronson, F. H. (1985) · Biology of Reproduction · doi:10.1095/biolreprod32.1.1 · Cited by 601 · see citing works
Spatial memory and adaptive specialization of the hippocampus
Sherry, D. F., Jacobs, L. F., & Gaulin, S. J. C. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90080-r · Cited by 393 · see citing works
Stress Effects on Morphology and Function of the Hippocampusa
McEwen, B. S., & Magariños, A. M. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb48286.x · Cited by 393 · see citing works
Estrogen-Mediated Structural and Functional Synaptic Plasticity in the Female Rat Hippocampus
Woolley, C. S. (1998) · Hormones and Behavior · doi:10.1006/hbeh.1998.1466 · Cited by 387 · see citing works
Seasonal plasticity in the adult brain
Tramontin, A. D., & Brenowitz, E. A. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01558-7 · Cited by 376 · see citing works
Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size.
Jacobs, L. F., Gaulin, S. J. C., Sherry, D. F., & Hoffman, G. E. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.16.6349 · Cited by 366 · see citing works
Sex Differences in Spatial Ability: An Evolutionary Hypothesis and Test
FitzGerald, R. W. (1986) · The American Naturalist · doi:10.1086/284468 · Cited by 355 · see citing works
Biology of Peromyscus (Rodentia)
King, J. A. (1968) · Biodiversity Heritage Library (Smithsonian Institution) · doi:10.5962/bhl.title.39510 · Cited by 341 · see citing works
Magariños, A. M., Deslandes, A., & McEwen, B. S. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00163-6 · Cited by 330 · see citing works
Galea, L. A. M., & McEwen, B. S. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00345-5 · Cited by 276 · see citing works
Sexual selection for spatial-learning ability
Gaulin, S. J. C., & FitzGerald, R. W. (1989) · Animal Behaviour · doi:10.1016/0003-3472(89)90121-8 · Cited by 246 · see citing works
Popov, V. I., Bocharova, L. S., & Bragin, A. G. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90336-z · Cited by 241 · see citing works
Galea, L. A. M., Kavaliers, M., Ossenkopp, K., & Hampson, E. (1995) · Hormones and Behavior · doi:10.1006/hbeh.1995.1008 · Cited by 225 · see citing works
Birth, migration, incorporation, and death of vocal control neurons in adult songbirds
Álvarez-Buylla, A., & Kirn, J. R. (1997) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(19971105)33:5 · Cited by 208 · see citing works
Effects of environment on morphology of rat cerebral cortex and hippocampus
Diamond, M. C., Ingham, C. A., Johnson, R. E., Bennett, E. L., & Rosenzweig, M. R. (1976) · Journal of Neurobiology · doi:10.1002/neu.480070108 · Cited by 192 · see citing works
Melatonin receptors in rat hippocampus: molecular and functional investigations
Mußhoff, U., Riewenherm, D., Berger, E., Fauteck, J., & Speckmann, E. (2002) · Hippocampus · doi:10.1002/hipo.1105 · Cited by 169 · see citing works
Sexually dimorphic spatial learning varies seasonally in two populations of deer mice
Galea, L. A. M., Kavaliers, M., Ossenkopp, K., Innes, D., & Hargreaves, E. L. (1994) · Brain Research · doi:10.1016/0006-8993(94)91419-2 · Cited by 167 · see citing works
O’Malley, A., O’Connell, C., Murphy, K. J., & Regan, C. M. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00182-2 · Cited by 152 · see citing works
Aste, N., Balthazart, J., Absil, P., Grossmann, R., M�lhbauer, E., Viglietti‐Panzica, C., & Panzica, G. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980629)396:2 · Cited by 147 · see citing works
Seasonal neuroplasticity in the songbird telencephalon: A role for melatonin
Bentley, G. E., Hof, T. J. V., & Ball, G. F. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.8.4674 · Cited by 139 · see citing works
Sexual selection and the brain
Jacobs, L. F. (1996) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(96)81048-2 · Cited by 119 · see citing works
Melatonin regulates neuronal plasticity in the hippocampus
El‐Sherif, Y., Tesoriero, J., Hogan, M. V., & Wieraszko, A. (2003) · Journal of Neuroscience Research · doi:10.1002/jnr.10605 · Cited by 114 · see citing works
Lavenex, P., Steele, M. A., & Jacobs, L. F. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00949.x · Cited by 108 · see citing works
The hippocampus, spatial memory and food hoarding: a puzzle revisited
Healy, S. D., de Kort, S. R., & Clayton, N. S. (2004) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2004.10.006 · Cited by 106 · see citing works
Development of SHIRPA to characterise the phenotype of gene-targeted mice
Hatcher, J. P., Jones, D. N. C., Rogers, D. C., Hatcher, P. D., Reavill, C., Hagan, J. J., & Hunter, A. J. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00275-3 · Cited by 100 · see citing works
Behavioral Phenotyping of Transgenic and Knockout Mice
Crawley, J. N. (1999) · CRC Press eBooks · doi:10.1201/9780849333644.pt3 · Cited by 100 · see citing works
Galea, L. A. M., Perrot-Sinal, T. S., Kavaliers, M., & Ossenkopp, K. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01100-2 · Cited by 90 · see citing works
Tramontin, A. D., Perfito, N., Wingfield, J. C., & Brenowitz, E. A. (2001) · General and Comparative Endocrinology · doi:10.1006/gcen.2000.7597 · Cited by 71 · see citing works
Weaver, D. R., Carlson, L. L., & Reppert, S. M. (1990) · Brain Research · doi:10.1016/0006-8993(90)91280-t · Cited by 69 · see citing works
Whitaker, W. L. (1940) · Journal of Experimental Zoology · doi:10.1002/jez.1400830103 · Cited by 69 · see citing works
The Economy of Winter: Phenotypic Plasticity in Behavior and Brain Structure
Jacobs, L. F. (1996) · Biological Bulletin · doi:10.2307/1543068 · Cited by 63 · see citing works
Potential role of synaptopodin in spine motility by coupling actin to the spine apparatus
Deller, T., Mundel, P. H., & Frotscher, M. (2000) · Hippocampus · doi:10.1002/1098-1063(2000)10:5 · Cited by 61 · see citing works
Commons, K. G., & Milner, T. A. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970512)381:3 · Cited by 58 · see citing works
Perrot-Sinal, T. S., Kavaliers, M., & Ossenkopp, K. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00131-6 · Cited by 57 · see citing works
D'Costa, A. P., Prevette, D. M., Houenou, L. J., Wang, S., Zackenfels, K., Rohrer, H., Zapf, J., Caroni, P., & Oppenheim, R. W. (1998) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(19980905)36:3 · Cited by 49 · see citing works
Dispersion Patterns in a Peromyscus Population
Metzgar, L. H. (1979) · Journal of Mammalogy · doi:10.2307/1379764 · Cited by 37 · see citing works
Ruf, T., Korytko, Z., Stieglitz, A., et al. (1997) · Journal of Comparative Physiology B · doi:10.1007/s003600050063 · Cited by 35 · see citing works
Long day lengths increase brain weight and DNA content in the meadow vole, Microtus pennsylvanicus
Dark, J. G., Dark, K. A., & Zucker, I. (1987) · Brain Research · doi:10.1016/0006-8993(87)90715-3 · Cited by 29 · see citing works
A brain for all seasons: cellular and molecular mechanisms of photoperiodic plasticity
Hofman, M. A., & Swaab, D. F. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)38082-8 · Cited by 25 · see citing works
The increasingly plastic, hormone-responsive adult brain
Breedlove, S. M., & Jordan, C. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.071054098 · Cited by 24 · see citing works
Feist, C. F., Feist, D. D., & Lynch, G. R. (1988) · Physiological Zoology · doi:10.1086/physzool.61.1.30163733 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges
Benca, R., Duncan, M. J., Frank, E., McClung, C., Nelson, R. J., & Vicentic, A. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.09.005 · Cited by 125 · see citing works
Self-citation
- Authors
- Pyter, L. M., Reader, B. F., & Nelson, R. J.
- Affiliations
- The Ohio State University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2005-05-04
- Volume
- 25
- Issue
- 18
- Pages
- 4521-4526
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6725029
- OpenAlex
- W2008176966
- Cited by
- 113
- References
- 53
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 2 · 2023: 6 · 2022: 4 · 2021: 7 · 2020: 4 · 2019: 2 · 2018: 5 · 2017: 5 · 2016: 10 · 2015: 6 · 2014: 10 · 2013: 8 · 2012: 6
- FWCI
- 1.98
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (P30NS045758, 0416897)
- National Institutes of Health
- National Institute of Mental Health (MH-57535, R01MH057535, R01MH066144, MH-66144)
- National Institute of Neurological Disorders and Stroke (P30NS045758)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- photoperiod, seasonal plasticity, hippocampus, dendritic morphology, dendritic spines, spatial learning and memory, hippocampal volume, brain size, white-footed mouse, CA1, CA3, dentate gyrus, winter adaptation
- MeSH terms
- Analysis of Variance, Animals, Avoidance Learning, Dendrites, Discrimination, Psychological, Hippocampus, Learning Disabilities, Male, Neurons, Reaction Time, Spatial Behavior, Time Factors, Photoperiod, Maze Learning, Cell Size, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
