Acute stress-induced impairment of spatial memory is associated with decreased expression of neural cell adhesion molecule in the hippocampus and prefrontal cortex

Sandi, Carmen; Woodson, James C.; Haynes, Vernon F.; Park, Collin R.; Touyarot, Katia; Lopez-Fernandez, Miguel A.; Venero, César; Diamond, David M.

doi:10.1016/j.biopsych.2004.12.034

Cited by 124Memory and Neural MechanismsStress Responses and CortisolNeuroscience and Neuropharmacology Research

Acute stress-induced impairment of spatial memory is associated with decreased expression of neural cell adhesion molecule in the hippocampus and prefrontal cortex

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Sandi, Carmen, Woodson, James C., Haynes, Vernon F., Park, Collin R., Touyarot, Katia, Lopez-Fernandez, Miguel A., Venero, César, Diamond, David M.·2005·Biological Psychiatry

DOI 10.1016/j.biopsych.2004.12.034

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Abstract

Background There is an extensive literature describing how stress disturbs cognitive processing and can exacerbate psychiatric disorders. There is, however, an insufficient understanding of the molecular mechanisms involved in stress effects on brain and behavior. Methods Rats were given spatial memory training in a hippocampus-dependent water maze task. We investigated how a fear-provoking experience (predator exposure) would affect their spatial memory and neural cell adhesion molecule (NCAM) levels in the hippocampus, prefrontal cortex (PFC), amygdala, and cerebellum. Results Whereas the control (nonstress) group exhibited excellent memory for the hidden platform location in the water maze, the cat-exposed (stress) group exhibited a profound impairment of memory and a marked suppression of levels of the NCAM-180 isoform in the hippocampus. Predator stress produced a more global reduction of NCAM levels in the PFC but had no effect on NCAM levels in the amygdala and cerebellum. Conclusions This work provides a novel perspective into dynamic and structure-specific changes in the molecular events involved in learning, memory, and stress. The selective suppression of NCAM-180 in the hippocampus and the more general suppression of NCAM in the PFC provide insight into the mechanisms underlying the great sensitivity of these two structures to be disturbed by stress.

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This observation of a predator stress-induced enhancement of memory is in complete contradistinction to our prior findings that exposing rats to a cat impaired their consolidation, as well as retrieval, of spatial memory.
“This observation of a predator stress-induced enhancement of memory is in complete contradistinction to our prior findings that exposing rats to a cat impaired their consolidation, as well as retrieval, of spatial memory (Diamond et al. [52]; Woodson et al. [135]; Sandi et al. [136]; Diamond et al. [137]; Park et al. [138]).”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Sandi et al. [136]
30 minutes of cat exposure suppressed molecular and structural measures of plasticity in the hippocampus.
“it also suppressed molecular (Sandi et al. [136]) and structural (Diamond et al. [137]) measures of plasticity in the hippocampus.”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Sandi et al. [136]
30 minutes of cat exposure dramatically reduced hippocampal levels of neural cell adhesion molecules (NCAMs).
“Specifically, 30 minutes of cat exposure impaired spatial memory and dramatically reduced hippocampal levels of neural cell adhesion molecules (NCAMs) (Sandi et al. [136])”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Sandi et al. [136]

A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
The role of prefrontal cortex in working-memory capacity, executive attention, and general fluid intelligence: An individual-differences perspective
Kane, M. J., & Engle, R. W. (2002) · Psychonomic Bulletin & Review · doi:10.3758/bf03196323 · Cited by 2,229 · 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
The stressed hippocampus, synaptic plasticity and lost memories
Kim, J. J., & Diamond, D. M. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn849 · Cited by 1,543 · see citing works
Self-citation
Stress and cognition: are corticosteroids good or bad guys?
de Kloet, E. R., Oitzl, M. S., & Joëls, M. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01438-1 · Cited by 1,258 · see citing works
Stress and glucocorticoids impair retrieval of long-term spatial memory
de Quervain, D. J.-F., Roozendaal, B., & McGaugh, J. L. (1998) · Nature · doi:10.1038/29542 · Cited by 1,182 · see citing works
The acute effects of corticosteroids on cognition: integration of animal and human model studies
LUPIEN, S., & MCEWEN, B. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00004-0 · Cited by 1,024 · see citing works
Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning
Cremer, H., Lange, R., Christoph, A., Plomann, M., Vopper, G., Roes, J., Brown, R. W., Baldwin, S. A., Kraemer, P. J., Scheff, S. W., et al. (1994) · Nature · doi:10.1038/367455a0 · Cited by 1,007 · see citing works
Course of illness, hippocampal function, and hippocampal volume in major depression
MacQueen, G. M., Campbell, S., McEwen, B. S., Macdonald, K., Amano, S., Joffe, R. T., Nahmias, C., & Young, L. T. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0337481100 · Cited by 980 · see citing works
Competition among multiple memory systems: converging evidence from animal and human brain studies
Poldrack, R. A., & Packard, M. G. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(02)00157-4 · Cited by 880 · see citing works
Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval
Roozendaal, B. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4080 · Cited by 838 · see citing works
Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults
Kirschbaum, C., Wolf, O. T., May, M., Wippich, W., & Hellhammer, D. H. (1996) · Life Sciences · doi:10.1016/0024-3205(96)00118-x · Cited by 815 · see citing works
Acute cortisone administration impairs retrieval of long-term declarative memory in humans
de Quervain, D. J.-F., Roozendaal, B., Nitsch, R. M., McGaugh, J. L., & Hock, C. (2000) · Nature Neuroscience · doi:10.1038/73873 · Cited by 745 · see citing works
MRI and PET Study of Deficits in Hippocampal Structure and Function in Women With Childhood Sexual Abuse and Posttraumatic Stress Disorder
Bremner, J. D., Vythilingam, M., Vermetten, E. H. G. J. M., Southwick, S. M., McGlashan, T. H., Nazeer, A., Khan, S., Vaccarino, V., Soufer, R., Garg, P. K., et al. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.5.924 · Cited by 721 · see citing works
Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation
Diamond, D. M., Bennett, M. C., Fleshner, M., & Rose, G. M. (1992) · Hippocampus · doi:10.1002/hipo.450020409 · Cited by 688 · see citing works
Self-citation
Catecholamine modulation of prefrontal cortical cognitive function
Arnsten, A. F. T. (1998) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(98)01240-6 · Cited by 608 · see citing works
Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM
Lüthi, A., Laurent, J., Figurovt, A., Mullert, D., & Schachnert, M. (1994) · Nature · doi:10.1038/372777a0 · Cited by 598 · see citing works
Schizophrenia: genes and environment
Tsuang, M. T. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00289-9 · Cited by 598 · see citing works
Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning
Kim, J. J., Lee, H. J., Han, J.-S., & Packard, M. G. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05222.2001 · Cited by 537 · see citing works
Glycans and neural cell interactions
KLEENE, R. B., & Schachner, M. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1349 · Cited by 518 · see citing works
Stress, memory, and the hippocampus: can't live with it, can't live without it
LUPIEN, S. J., & Lepage, M. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00361-8 · Cited by 515 · see citing works
Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective
Schafe, G. E., Nader, K., Blair, H. T., & LeDoux, J. E. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01969-x · Cited by 510 · see citing works
The impact of early adverse experiences on brain systems involved in the pathophysiology of anxiety and affective disorders
Heim, C., & Nemeroff, C. B. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00224-3 · Cited by 502 · see citing works
Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight
Paxinos, G., WATSON, C. R. R., Pennisi, M., & Topple, A. N. (1985) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(85)90026-3 · Cited by 483 · see citing works
Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory
Morris, R., Moser, E. I., Riedel, G., Martin, S. J., Sandin, J., Day, M., & O’Carroll, C. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1264 · Cited by 480 · see citing works
Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze
Sandi, C., Loscertales, M., & Guaza, C. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01412.x · Cited by 447 · see citing works
Self-citation
Behavioral stress impairs long-term potentiation in rodent hippocampus
Foy, M. R., Stanton, M. E., Levine, S., & Thompson, R. F. (1987) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(87)90664-9 · Cited by 436 · see citing works
Stress and development: Behavioral and biological consequences
Bremner, J., & Vermetten, E. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003042 · Cited by 405 · see citing works
Stress, cognitive impairment and cell adhesion molecules
Sandi, C. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1555 · Cited by 374 · see citing works
Self-citation
Modulation of an NCAM-Related Adhesion Molecule with Long-Term Synaptic Plasticity in Aplysia
Mayford, M. R., Barzilai, A., Keller, F., Schacher, S., & Kandel, E. R. (1992) · Science · doi:10.1126/science.1585176 · Cited by 371 · see citing works
Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders
McEwen, B. S., & Magarinos, A. M. (2001) · Human Psychopharmacology: Clinical and Experimental · doi:10.1002/hup.266 · Cited by 349 · see citing works
The biology of being frazzled
Arnsten, A. F. T. (1998) · Science · doi:10.1126/science.280.5370.1711 · Cited by 341 · see citing works
Psychological stress impairs spatial working memory: Relevance to electrophysiological studies of hippocampal function.
Diamond, D. M., Fleshner, M., Ingersoll, N., & Rose, G. M. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.4.661 · Cited by 340 · see citing works
Self-citation
Serotonin-Mediated Endocytosis of apCAM: an Early Step of Learning-Related Synaptic Growth in Aplysia
Bailey, C. H., Chen, M., Keller, F., & Kandel, E. R. (1992) · Science · doi:10.1126/science.1585177 · Cited by 314 · see citing works
Acute Stress-induced Changes in Hippocampal/Prefrontal Circuits in Rats: Effects of Antidepressants
Rocher, C. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhg122 · Cited by 307 · see citing works
The amygdala, fear, and memory
FANSELOW, M. S., & GALE, G. D. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07077.x · Cited by 299 · see citing works
Exposure to Acute Stress Blocks the Induction of Long-Term Potentiation of the Amygdala–Prefrontal Cortex Pathway<i>In Vivo</i>
Maroun, M., & Richter-Levin, G. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-11-04406.2003 · Cited by 293 · see citing works
Memory systems in the brain and localization of a memory
Thompson, R. F., & Kim, J. J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13438 · Cited by 291 · see citing works
Dissociable Roles of Mid-Dorsolateral Prefrontal and Anterior Inferotemporal Cortex in Visual Working Memory
Petrides, M. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-19-07496.2000 · Cited by 290 · see citing works
Time-Dependent Relationship between the Dorsal Hippocampus and the Prefrontal Cortex in Spatial Memory
Lee, I., & Kesner, R. P. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-04-01517.2003 · Cited by 287 · see citing works
Neural recognition molecules and synaptic plasticity
Schachner, M. (1997) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(97)80115-9 · Cited by 284 · see citing works
Neural cell adhesion molecules in activity-dependent development and synaptic plasticity
Fields, R. D., & Itoh, K. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)30013-1 · Cited by 281 · see citing works
Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: a microdialysis study in freely moving rats
Venero, C., & Borrell, J. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00668.x · Cited by 277 · see citing works
Self-citation
Exposing Rats to a Predator Blocks Primed Burst Potentiation in the Hippocampus<i>In Vitro</i>
Mesches, M. H., Fleshner, M., Heman, K. L., Rose, G. M., & Diamond, D. M. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-14-j0004.1999 · Cited by 276 · see citing works
Self-citation
Parallels between cerebellum- and amygdala-dependent conditioning
Medina, J. F., Repa, J. C., Mauk, M. D., & LeDoux, J. E. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn728 · Cited by 265 · see citing works
Stress Integration after Acute and Chronic Predator Stress: Differential Activation of Central Stress Circuitry and Sensitization of the Hypothalamo-Pituitary-Adrenocortical Axis
Figueiredo, H. F., Bodie, B., Tauchi, M., Dolgas, C. M., & Herman, J. P. (2003) · Endocrinology · doi:10.1210/en.2003-0713 · Cited by 245 · see citing works
Possible mechanisms for atrophy of the human hippocampus
McEwen, B. S. (1997) · Molecular Psychiatry · doi:10.1038/sj.mp.4000254 · Cited by 243 · see citing works
Cerebellar role in fear-conditioning consolidation
Sacchetti, B., Baldi, E., Lorenzini, C. A., & Bucherelli, C. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.112660399 · Cited by 233 · see citing works
Temporal dynamics of glutamate efflux in the prefrontal cortex and in the hippocampus following repeated stress: effects of pretreatment with saline or diazepam
Bagley, J., & Moghaddam, B. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00435-6 · Cited by 231 · see citing works
Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice
Cremer, H., Chazal, G., Carleton, A., Goridis, C., Vincent, J., & Lledo, P. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.22.13242 · Cited by 215 · see citing works
The neural cell adhesion molecule in synaptic plasticity and ageing
Rønn, L. C. B., Berezin, V., & Bock, E. (2000) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(99)00088-x · Cited by 213 · see citing works
Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning.
Cordero, M. I., Merino, J. J., & Sandi, C. (1998) · Behavioral Neuroscience · doi:10.1037//0735-7044.112.4.885 · Cited by 203 · see citing works
Self-citation
The effects of stress on memory and the hippocampus throughout the life cycle: Implications for childhood development and aging
BREMNER, J. D., & NARAYAN, M. (1998) · Development and Psychopathology · doi:10.1017/s0954579498001916 · Cited by 201 · see citing works
Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1
Sandi, C., Merino, J. J., Cordero, M. I., Touyarot, K., & Venero, C. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00484-x · Cited by 201 · see citing works
Self-citation
Stress impairs prefrontal cortical function in rats and monkeys: role of dopamine D1 and norepinephrine α-1 receptor mechanisms
Arnsten, A. F. T. (2000) · Progress in brain research · doi:10.1016/s0079-6123(00)26014-7 · Cited by 194 · see citing works
Immunoelectron‐microscopic localization of the 180 kD component of the neural cell adhesion molecule N‐CAM in postsynaptic membranes
Persohn, E., Pollerberg, G. E., & Schachner, M. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902880108 · Cited by 189 · see citing works
A role for the neural cell adhesion molecule in a late, consolidating phase of glycoprotein synthesis six hours following passive avoidance training of the young chick
Scholey, A. B., Rose, S. P. R., Zamani, R., Bock, E., & Schachner, M. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90519-l · Cited by 186 · see citing works
Intraventricular Infusions of Anti‐Neural Cell Adhesion Molecules in a Discrete Posttraining Period Impair Consolidation of a Passive Avoidance Response in the Rat
Doyle, E., Nolan, P. M., Bell, R., & Regan, C. M. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb08477.x · Cited by 180 · see citing works
Synaptic Strength as a Function of Post- versus Presynaptic Expression of the Neural Cell Adhesion Molecule NCAM
Dityatev, A. E., Dityatev, A. E., & Schachner, M. (2000) · Neuron · doi:10.1016/s0896-6273(00)81151-4 · Cited by 173 · see citing works
Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning.
Cordero, M. I., Merino, J. J., & Sandi, C. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.4.885 · Cited by 173 · see citing works
Self-citation
A Synthetic Neural Cell Adhesion Molecule Mimetic Peptide Promotes Synaptogenesis, Enhances Presynaptic Function, and Facilitates Memory Consolidation
Cambon, K., Hansen, S. M., Venero, C., Herrero, A. I., Skibo, G. G., Berezin, V., Bock, E., & Sandi, C. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0436-04.2004 · Cited by 169 · see citing works
Self-citation
Emotion-Induced Amnesia in Rats: Working Memory-Specific Impairment, Corticosterone-Memory Correlation, and Fear Versus Arousal Effects on Memory
Woodson, J. C., Macintosh, D., Fleshner, M., & Diamond, D. M. (2003) · Learning & Memory · doi:10.1101/lm.62903 · Cited by 169 · see citing works
Self-citation
Contribution of the Neural Cell Adhesion Molecule to Neuronal and Synaptic Plasticity
Kiss, J. Z., & Müller, D. (2001) · Reviews in the Neurosciences · doi:10.1515/revneuro.2001.12.4.297 · Cited by 167 · see citing works
Chronic psychosocial stress impairs learning and memory and increases sensitivity to yohimbine in adult rats
Park, C. R., Campbell, A. M., & Diamond, D. M. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01255-0 · Cited by 166 · see citing works
Self-citation
The effects of experimentally induced stress on false recognition
Payne, J. D., Nadel, L., Allen, J. J. B., Thomas, K. G. F., & Jacobs, W. J. (2002) · Memory · doi:10.1080/09658210143000119 · Cited by 161 · see citing works
NCAM-antibodies modulate induction of long-term potentiation in rat hippocampal CA1
Rønn, L. C. B., Bock, E., Linnemann, D., & Jahnsen, H. (1995) · Brain Research · doi:10.1016/0006-8993(95)00147-i · Cited by 156 · see citing works
Role of the Basolateral Amygdala in Memory Consolidation
McINTYRE, C. K., POWER, A. E., ROOZENDAAL, B., & McGAUGH, J. L. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07088.x · Cited by 147 · see citing works
Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation
Alfarez, D. N., Wiegert, O., Joëls, M., & Krugers, H. J. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00483-9 · Cited by 142 · see citing works
Long‐term behavioral and neurochemical effects of chronic stress exposure in rats
Mangiavacchi, S., Masi, F., Scheggi, S., Leggio, B., De Montis, M. G., & Gambarana, C. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00665.x · Cited by 137 · see citing works
The cerebellum in the spatial problem solving: a co-star or a guest star?
Petrosini, L. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00036-7 · Cited by 133 · see citing works
Effect of age on the radial arm water maze—a test of spatial learning and memory
Shukitt‐Hale, B., McEwen, J. J., Szprengiel, A., & Joseph, J. A. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(03)00041-1 · Cited by 128 · see citing works
Stress-induced alternative splicing of acetylcholinesterase results in enhanced fear memory and long-term potentiation
Nijholt, I., Farchi, N., Kye, M., Sklan, E. H., Shoham, S., Verbeure, B., Owen, D., Hochner, B., Spiess, J., Soreq, H., et al. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001446 · Cited by 126 · see citing works
Recovery of emotional behaviour in neural cell adhesion molecule (NCAM) null mutant mice through transgenic expression of NCAM180
Stork, O., Welzl, H., Wolfer, D. P., Schuster, T., Mantei, N., Stork, S., Hoyer, D., Lipp, H., Obata, K., & Schachner, M. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00197.x · Cited by 125 · see citing works
Increase in extracellular NCAM and amyloid precursor protein following induction of long-term potentiation in the dentate gyrus of anaesthetized rats
Fazeli, M. S., Breen, K. C., Errington, M. L., & Bliss, T. V. P. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90360-3 · Cited by 123 · see citing works
Progress in Psychiatry
Michels, R., & Marzuk, P. M. (1993) · New England Journal of Medicine · doi:10.1056/nejm199308193290808 · Cited by 121 · see citing works
Untitled work
(1995) · American Psychiatric Press eBooks · Cited by 118 · see citing works
The effect of continuous intraventricular infusion of L1 and NCAM antibodies on spatial learning in rats
Arami, S., Jucker, M., Schachner, M., & Welzl, H. (1996) · Behavioural Brain Research · doi:10.1016/s0166-4328(96)00046-0 · Cited by 116 · see citing works
Regulation of hippocampal cell adhesion molecules NCAM and L1 by contextual fear conditioning is dependent upon time and stressor intensity
Merino, J. J., Cordero, M. I., & Sandi, C. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00191.x · Cited by 109 · see citing works
Self-citation
The Amygdala Is Involved in the Modulation of Long-Term Memory, but Not in Working or Short-Term Memory
Bianchin, M. M., Souza, T. M. E., Medina, J. H., & Izquierdo, I. (1999) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3881 · Cited by 109 · see citing works
Chronic stress induces opposite changes in the mRNA expression of the cell adhesion molecules NCAM and L1
Venero, C., Tilling, T., Hermans‐Borgmeyer, I., Schmidt, R., Schachner, M., & Sandi, C. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00543-2 · Cited by 104 · see citing works
Self-citation
Serum corticosterone level predicts the magnitude of hippocampal primed burst potentiation and depression in urethane-anesthetized rats
Bennett, M. C., Diamond, D. M., Fleshner, M., & Rose, G. (1991) · Psychobiology · doi:10.3758/bf03332083 · Cited by 100 · see citing works
Self-citation
Spatial learning impairment induced by chronic stress is related to individual differences in novelty reactivity: search for neurobiological correlates
Touyarot, K., Venero, C., & Sandi, C. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00031-3 · Cited by 94 · see citing works
Self-citation
Immunohistological localization of the neural adhesion molecules L1 and N-CAM in the developing hippocampus of the mouse
Persohn, E., & Schachner, M. (1990) · Journal of Neurocytology · doi:10.1007/bf01186812 · Cited by 89 · see citing works
A Synthetic Peptide Ligand of Neural Cell Adhesion Molecule (NCAM) IgI Domain Prevents NCAM Internalization and Disrupts Passive Avoidance Learning
Foley, A., Hartz, B. P., Gallagher, H. C., Rønn, L. C. B., Berezin, V., Bock, E., & Regan, C. M. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0742607.x · Cited by 81 · see citing works
Modulation of hippocampal NCAM polysialylation and spatial memory consolidation by fear conditioning
Sandi, C., Merino, J. J., Cordero, M. I., Kruyt, N. D., Murphy, K. J., & Regan, C. M. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00182-3 · Cited by 81 · see citing works
Self-citation
Corticosterone accelerates hypoxia- and cyanide-induced ATP loss in cultured hippocampal astrocytes
Tombaugh, G. C., & Sapolsky, R. M. (1992) · Brain Research · doi:10.1016/0006-8993(92)91356-j · Cited by 72 · see citing works
Plasma catecholamines and pituitary adrenal hormones related to mental task demand under quiet and noise conditions
BRANDENBERGER, G., FOLLENIUS, M., Wittersheim, G., Salamé, P., Siméoni, M., & Reinhardt, B. (1980) · Biological Psychology · doi:10.1016/0301-0511(80)90037-x · Cited by 69 · see citing works
Opposite effects on NCAM expression in the rat frontal cortex induced by acute vs. chronic corticosterone treatments
Sandi, C., & Loscertales, M. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01346-3 · Cited by 62 · see citing works
Self-citation
Presynaptic Changes in Long‐Term Potentiation: Elevated Synaptosomal Calcium Concentration and Basal Phosphoinositide Turnover in Dentate Gyrus
Lynch, M. A., & Voss, K. L. (1991) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1991.tb02569.x · Cited by 62 · see citing works
Proteolysis of neuronal cell adhesion molecule by the tissue plasminogen activator–plasmin system after kainate injection in the mouse hippocampus
Endo, A., Nagai, N., Urano, T., Takada, Y., Hashimoto, K., & Takada, A. (1999) · Neuroscience Research · doi:10.1016/s0168-0102(98)00105-9 · Cited by 57 · see citing works
Post-training administration of a synthetic peptide ligand of the neural cell adhesion molecule, C3d, attenuates long-term expression of contextual fear conditioning
Cambon, K., Venero, C., Berezin, V., Bock, E., & Sandi, C. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00597-9 · Cited by 56 · see citing works
Self-citation
Corticosterone facilitates long-term memory formation via enhanced glycoprotein synthesis
Sandi, C., Rose, S. P. R., Mileusnić, R., & Lancashire, C. L. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00306-4 · Cited by 54 · see citing works
Self-citation
A novel family of ancient vertebrate odorant receptors
Berghard, A., & Dryer, L. (1998) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(19981115)37:3 · Cited by 50 · see citing works
Contributions of Cell Adhesion Molecules to Altered Synaptic Weightings during Memory Consolidation
Murphy, K. J., & Regan, C. M. (1998) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3839 · Cited by 48 · see citing works
Demonstration of an Extracellular ATP-Binding Site in NCAM: Functional Implications of Nucleotide Binding
Dzhandzhugazyan, K. N., & Bock, E. (1997) · Biochemistry · doi:10.1021/bi9709351 · Cited by 45 · see citing works
Activation of NMDA receptors stimulates extracellular proteolysis of cell adhesion molecules in hippocampus
Hoffman, K. B., Larson, J., Bahr, B. A., & LYNCH, G. S. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00907-x · Cited by 44 · see citing works
Water maze learning and forebrain mRNA expression of the neural cell adhesion molecule L1
Venero, C., Tilling, T., Hermans‐Borgmeyer, I., Herrero, A. I., Schachner, M., & Sandi, C. (2003) · Journal of Neuroscience Research · doi:10.1002/jnr.10857 · Cited by 43 · see citing works
Self-citation
Delayed and isoform-specific effect of NMDA exposure on neural cell adhesion molecules in hippocampus
Hoffman, K. B., Murray, B. A., LYNCH, G. S., Munirathinam, S., & Bahr, B. A. (2001) · Neuroscience Research · doi:10.1016/s0168-0102(00)00214-5 · Cited by 23 · see citing works
Stress alleviates reduced expression of cell adhesion molecules (NCAM, L1), and deficits in learning and corticosterone regulation of apolipoprotein E knockout mice
Grootendorst, J., Oitzl, M. S., Dalm, S., Enthoven, L., Schachner, M., de Kloet, E. R., & Sandi, C. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01766.x · Cited by 18 · see citing works
Self-citation
Noise Stress Impairs Prefrontal Cortical Cognitive Function in Monkeys: Evidence for a Hyperdopaminergic Mechanism
Arnsten, A. F. T., & Goldman-Rakic, P. S. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.4.362 · Cited by 6 · see citing works
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The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law
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“Speciﬁcally, 30 minutes of cat exposure impaired spatial memory and dramatically reduced hippocampal levels of neural cell adhesion molecules (NCAMs) (Sandi et al. [136]), which are important structural components of long-term memory storage (Sandi [297]).”
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Stress and Memory: Behavioral Effects and Neurobiological Mechanisms
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Self-citation
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Correlated memory defects and hippocampal dendritic spine loss after acute stress involve corticotropin-releasing hormone signaling
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Gascon, E., Vutskits, L., & Kiss, J. Z. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.014 · Cited by 231 · see citing works
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McCormick, C. M., & Mathews, I. Z. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.09.019 · Cited by 230 · see citing works
Stressful Experience and Learning Across the Lifespan
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Diamond, D. M., Campbell, A. M., Park, C. R., Woodson, J. C., Conrad, C. D., Bachstetter, A. D., & Mervis, R. F. (2006) · Hippocampus · doi:10.1002/hipo.20188 · Cited by 213 · see citing works
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Understanding stress: Insights from rodent models
Atrooz, F., Alkadhi, K. A., & Salim, S. (2021) · Current Research in Neurobiology · doi:10.1016/j.crneur.2021.100013 · Cited by 201 · see citing works
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Acute predator stress impairs the consolidation and retrieval of hippocampus-dependent memory in male and female ratsPreprint
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Self-citation
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Differential expression of molecular markers of synaptic plasticity in the hippocampus, prefrontal cortex, and amygdala in response to spatial learning, predator exposure, and stress‐induced amnesia
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Self-citation
Evolutionary conserved role of neural cell adhesion molecule-1 in memory
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The antidepressant agomelatine blocks the adverse effects of stress on memory and enables spatial learning to rapidly increase neural cell adhesion molecule (NCAM) expression in the hippocampus of rats
Conboy, L., Tanrıkut, C., Zoladz, P. R., Campbell, A. M., Park, C. R., Gabriel, C., Mocaër, E., Sandi, C., & Diamond, D. M. (2008) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708009255 · Cited by 66 · see citing works
Self-citation
Permissive Influence of Stress in the Expression of a U-Shaped Relationship between Serum Corticosterone Levels and Spatial Memory Errors in Rats
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Self-citation
The role of rewarding and novel events in facilitating memory persistence in a separate spatial memory taskPreprint
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Evidence for a role of GABAA receptor in the acute restraint stress-induced enhancement of spatial memory
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Molecular basis of fluoride toxicities: Beyond benefits and implications in human disorders
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Effects of letrozole on hippocampal and cortical catecholaminergic neurotransmitter levels, neural cell adhesion molecule expression and spatial learning and memory in female rats
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Stress time-dependently influences the acquisition and retrieval of unrelated information by producing a memory of its own
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Aged rats are hypo-responsive to acute restraint: implications for psychosocial stress in aging
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Self-citation
Neuronal cell adhesion molecule deletion induces a cognitive and behavioral phenotype reflective of impulsivity
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Self-citation
BT‐11 improves stress‐induced memory impairments through increment of glucose utilization and total neural cell adhesion molecule levels in rat brains
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Self-citation
Repeated stress in combination with pyridostigmine
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Pre-training administration of tianeptine, but not propranolol, protects hippocampus-dependent memory from being impaired by predator stress
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Self-citation
Imaging the immediate non-genomic effects of stress hormone on brain activity
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Zheng, G., Chen, Y., Zhang, X., Cai, T., Liu, M., Zhao, F., Luo, W., & Chen, J. (2008) · Brain Research · doi:10.1016/j.brainres.2008.08.057 · Cited by 37 · see citing works
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Goode, T. D., Leong, K.-C., Goodman, J., Maren, S., & Packard, M. G. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.02.004 · Cited by 35 · see citing works
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Learning improvement after PI3K activation correlates with de novo formation of functional small spines
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Self-citation
Effectiveness of memantine on depression-like behavior, memory deficits and brain mRNA levels of BDNF and TrkB in rats subjected to repeated unpredictable stress
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Wielgat, P., & Braszko, J. J. (2012) · Advances in Medical Sciences · doi:10.2478/v10039-012-0011-0 · Cited by 35 · see citing works
Early environmental cues affect object recognition memory in adult female but not male C57BL/6 mice
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Chronic social isolation suppresses proplastic response and promotes proapoptotic signalling in prefrontal cortex of Wistar rats
Djordjevic, A., Adzic, M., Djordjevic, J., & Radojcic, M. B. (2010) · Journal of Neuroscience Research · doi:10.1002/jnr.22403 · Cited by 31 · see citing works
The hippocampus and prefrontal cortex are differentially involved in serial memory retrieval in non-stress and stress conditions
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The corticotropin-releasing factor 1 receptor antagonist, SSR125543, and the vasopressin 1b receptor antagonist, SSR149415, prevent stress-induced cognitive impairment in mice
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Evolution of stress responses refine mechanisms of social rank
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Albrecht, A., Bergado-Acosta, J. R., Pape, H., & Stork, O. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145709991106 · Cited by 27 · see citing works
Effects of fluoxetine on plasticity and apoptosis evoked by chronic stress in rat prefrontal cortex
Djordjevic, A. D., Djordjevic, J., Elaković, I., Adžić, M., Matić, G. M., & Radojcic, M. B. (2012) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2012.07.042 · Cited by 27 · see citing works
Steroids, Learning and Memory
Dohanich, G. P., Korol, D. L., & Shors, T. J. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00015-2 · Cited by 25 · see citing works
Effects of repeated restraint stress and WiFi signal exposure on behavior and oxidative stress in rats
Othman, H., Ammari, M., Sakly, M., & Abdelmelek, H. (2017) · Metabolic Brain Disease · doi:10.1007/s11011-017-0016-2 · Cited by 25 · see citing works
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Hidese, S., Hattori, K., Sasayama, D., Miyakawa, T., Matsumura, R., Yokota, Y., Ishida, I., Matsuo, J., Noda, T., Yoshida, S., et al. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.02.016 · Cited by 24 · see citing works
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Philbert, J., Pichat, P., Palme, R., Belzung, C., & Griebel, G. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2012.05.013 · Cited by 22 · see citing works
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Dominguez, G., Faucher, P., Henkous, N., Krazem, A., Pierard, C., & Béracochéa, D. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00166 · Cited by 22 · see citing works
Mitigation of adverse behavioral impact from predator exposure by the nociceptin/orphanin FQ peptide antagonist J-113397 in rats
Genovese, R. F., & Dobre, S. (2017) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000329 · Cited by 21 · see citing works
Prefrontal cortex or basolateral amygdala lesions blocked the stress-induced inversion of serial memory retrieval pattern in mice
Chauveau, F., Piérard, C., Coutan, M., Drouet, I., Liscia, P., & Béracochéa, D. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.04.014 · Cited by 19 · see citing works
Hippocampal cytogenesis and spatial learning in senile rats exposed to chronic variable stress: effects of previous early life exposure to mild stress
Jáuregui-Huerta, F., Zhang, L., Yañez-Delgadillo, G., Hernandez-Carrillo, P., Garcı́a‐Estrada, J., & Luquı́n, S. (2015) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2015.00159 · Cited by 18 · see citing works
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Zoladz, P. R., Park, C. R., & Diamond, D. M. (2011) · Wiley eBooks · doi:10.1002/9781118083222.ch8 · Cited by 16 · see citing works
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Zoladz, P. R., Muñoz, C., & Diamond, D. M. (2010) · Pharmaceuticals · doi:10.3390/ph3103143 · Cited by 11 · see citing works
Self-citation
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Multiple presentations reduce the behavioral impact of protected predator exposure in rats
Genovese, R. F., Johnson, C. C., Tobin, C. A., & Gauchan, S. (2014) · Behavioural Processes · doi:10.1016/j.beproc.2014.09.032 · Cited by 8 · see citing works
Role of NCAM in Emotion and Learning
Conboy, L., Bisaz, R., Markram, H., & Sandi, C. (2008) · Neurochemical Research · doi:10.1007/s11064-008-9601-4 · Cited by 8 · see citing works
Self-citation
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Jeon, Y.-J., Park, J.-C., Jang, Y.-S., Kim, D.-H., Choi, B., Kim, J., Kim, J. J., & Han, J. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac381 · Cited by 7 · see citing works
Emotional Tagging and Long-Term Memory Formation
Richter-Levin, G., Kehat, O., & Anunu, R. (2015) · Springer eBooks · doi:10.1007/978-1-4939-1761-7_13 · Cited by 7 · see citing works
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Kroell, M., Winckler, C., & Hintze, S. (2025) · Animal Welfare · doi:10.1017/awf.2025.21 · Cited by 6 · see citing works
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Morroni, F., Kitazawa, M., Drago, D., Cheng, D., Medeiros, R., & LaFerla, F. M. (2011) · Journal of Behavioral and Brain Science · doi:10.4236/jbbs.2011.14027 · Cited by 5 · see citing works
Role of stress system disturbance and enhanced novelty response in spatial learning of NCAM-deficient mice
Brandewiede, J., Jakovcevski, M., Stork, O., & Schachner, M. (2013) · Stress · doi:10.3109/10253890.2013.840773 · Cited by 5 · see citing works
Impact of cold exposure duration and intensity on hippocampal tyrosine hydroxylase, brain-derived neurotrophic factor, and mitochondrial markers in mice
Dzik, K. P., Majkutewicz, I., Kołodziej, M., Gorlikowska, K., Nekrash, M., & Kaczor, J. J. (2025) · Experimental Neurology · doi:10.1016/j.expneurol.2025.115407 · Cited by 4 · see citing works
Effects of Hypoxia or Dexamethasone at Different Gestation Periods on Fear Conditioning in Adult Rats
Vataeva, L. A., Tyulkova, E. I., Alekhin, A. N., & Stratilov, V. A. (2018) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093018060030 · Cited by 4 · see citing works
Acute stress impairs intentional memory suppression through aberrant prefrontal cortex activation in high trait ruminators
Long, J., Peng, L., Li, Q., Niu, L., Dai, H., Zhang, J., Chen, K., Lee, T. M., Huang, M., & Zhang, R. (2024) · International Journal of Clinical and Health Psychology · doi:10.1016/j.ijchp.2024.100463 · Cited by 3 · see citing works

Stress-induced cognitive and psychopathological alterations : functional involvement of the neural cell adhesion molecule (NCAM)
Bisaz, R., & Sandi, C. (2009) · Infoscience (Ecole Polytechnique Fédérale de Lausanne) · doi:10.5075/epfl-thesis-4395
Self-citation
Causal evidence for the involvement of the neural cell adhesion molecule, NCAM, in chronic stress‐induced cognitive impairments
Bisaz, R., Schachner, M., & Sandi, C. (2009) · Hippocampus · doi:10.1002/hipo.20723 · Cited by 56 · see citing works
Self-citation
Stress, cognitive impairment and cell adhesion molecules
Sandi, C. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1555 · Cited by 374 · see citing works
Self-citation
Chronic stress induces opposite changes in the mRNA expression of the cell adhesion molecules NCAM and L1
Venero, C., Tilling, T., Hermans‐Borgmeyer, I., Schmidt, R., Schachner, M., & Sandi, C. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00543-2 · Cited by 104 · see citing works
Self-citation
Learning under stress: A role for the neural cell adhesion molecule NCAM
Bisaz, R., Conboy, L., & Sandi, C. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.11.003 · Cited by 83 · see citing works
Self-citation

Authors: Sandi, C., Woodson, J. C., Haynes, V. F., Park, C. R., Touyarot, K., Lopez-Fernandez, M. A., Venero, C., & Diamond, D. M.
Affiliations: École Polytechnique Fédérale de Lausanne (CH)
University of Tampa (US)
Youngstown State University (US)
United States Department of Veterans Affairs (US)
Universidad Nacional de Educación a Distancia (ES)
Corresponding author: Sandi, Carmen
ORCID: Sandi, Carmen
Park, Collin R.
Touyarot, Katia
Venero, César
Diamond, David M.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2005-04
Volume: 57
Issue: 8
Pages: 856-864
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2004.12.034
OpenAlex: W2035626388
Cited by: 122
References: 101
Citations by year: 2026: 2 · 2025: 6 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 2 · 2019: 2 · 2018: 2 · 2017: 6 · 2016: 5 · 2015: 4 · 2014: 13 · 2013: 4 · 2012: 7
FWCI: 4.67
Type: journal article
Language: en
Open access: green
infoscience.epfl.ch
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Digital Commons - University of South Florida (University of South Florida) (submittedVersion)
Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: acute stress, spatial memory, CD56, hippocampus, prefrontal cortex, predator stress, water maze, amygdala, cerebellum, stress-induced memory impairment, learning and memory
MeSH terms: Animals, Brain Chemistry, Cats, Corticosterone, Fear, Hippocampus, Male, Space Perception, Stress, Psychological, Blotting, Western, Rats, Sprague-Dawley, Prefrontal Cortex, Maze Learning, Neural Cell Adhesion Molecules, Rats

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Acute stress-induced impairment of spatial memory is associated with decreased expression of neural cell adhesion molecule in the hippocampus and prefrontal cortex

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