Stress‐induced dynamic routing of hippocampal connectivity: A hypothesis
Abstract
Recent observations have caused a drastic shift in the conception of the hippocampus as a homogeneous structure that subserves cognitive functions, either spatial maps or short term episodic memory, to a structure that is associated with both cognitive and emotional functions. In fact, the assignment of cognitive functions to the hippocampus is restricted to its dorsal sector. In contrast, the ventral hippocampus (VH) appears to be associated with control of behavioral inhibition, stress and emotional memory, but not with strictly cognitive functions. Curiously, the VH but not the dorsal hippocampus (DH) is associated with the development of affective disorders. In line with these collective observations, we and others have found that the ability to evoke a sustained long term potentiation (LTP), a cellular correlate of learning and memory, is much lower in the VH compared to the DH. Strikingly, acute stress as well as direct exposure to corticosterone affect DH and VH in an opposite manner; causing facilitation of LTP in the VH and its suppression in the DH. This double dissociative action results from activation of different steroid receptor species in the DH and VH. Since the DH and VH differ in efferent connectivity, and since the strength of LTP can be considered as an indicator of strength of synaptic connectivity, these results suggest that stress regulates the routes by which the hippocampus is functionally linked to the rest of the brain such that under stress, the ventral route to the amygdala is enabled while the dorsal route to the neocortex is suppressed. This selective routing may underlie the complex outcome of stress on hippocampal and amygdala physiology and behavior. © 2009 Wiley‐Liss, Inc.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Stress and glucocorticoids affect synaptic plasticity differentially along the hippocampal dorsoventral axis, impairing long-term potentiation in dorsal hippocampus but enhancing it in ventral hippocampus.
“In addition, stress and glucocorticoids affect synaptic plasticity differentially along the hippocampal dorsoventral axis, impairing long-term potentiation in dorsal hippocampus, but enhancing this process in ventral hippocampus.15,49,118”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [49]
Cites
LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS
Scoville, W. B., & Milner, B. (1957) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.20.1.11 · Cited by 7,322 · 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
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat
O'Keefe, J., & Dostrovsky, J. (1971) · Brain Research · doi:10.1016/0006-8993(71)90358-1 · Cited by 6,151 · see citing works
Genome-wide atlas of gene expression in the adult mouse brain
Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., et al. (2007) · Nature · doi:10.1038/nature05453 · Cited by 5,572 · see citing works
Joëls, M., & Baram, T. Z. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2632 · Cited by 1,521 · see citing works
Regional dissociations within the hippocampus-memory and anxiety
Bannerman, D. M., Rawlins, J. N. P., McHugh, S. B., Deacon, R. M. J., Yee, B. K., Bast, T., Zhang, W.-N., Pothuizen, H. H. J., & Feldon, J. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.03.004 · Cited by 1,462 · see citing works
Knowing Where and Getting There: A Human Navigation Network
Maguire, E. A., Burgess, N., Donnett, J. G., Frackowiak, R. S. J., Frith, C. D., & O'Keefe, J. (1998) · Science · doi:10.1126/science.280.5365.921 · Cited by 1,303 · see citing works
The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network
van Strien, N. M., Cappaert, N. L. M., & Witter, M. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2614 · Cited by 1,041 · see citing works
Learning under stress: how does it work?
Joëls, M., Pu, Z., Wiegert, O., Oitzl, M. S., & Krugers, H. J. (2006) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2006.02.002 · Cited by 947 · see citing works
Moser, E., Moser, M. ‐., & Andersen, P. N. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03916.1993 · Cited by 916 · see citing works
Reduced fear expression after lesions of the ventral hippocampus
Kjelstrup, K. G., Tuvnes, F. A., Steffenach, H.-A., Murison, R., Moser, E. I., & Moser, M.-B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152112399 · Cited by 912 · see citing works
Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat
Jung, M. W., Wiener, S. I., & McNaughton, B. L. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-12-07347.1994 · Cited by 818 · see citing works
Karst, H., Berger, S., Turiault, M., Tronche, F., Schütz, G., & Joëls, M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507572102 · Cited by 774 · see citing works
Finite scale of spatial representation in the hippocampus
Kjelstrup, K. B., Solstad, T., Brun, V. H., Hafting, T., Leutgeb, S., Witter, M. P., Moser, E. I., & Moser, M.-B. (2008) · Science · doi:10.1126/science.1157086 · Cited by 760 · see citing works
Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., de Kloet, E. R., Joels, M., & Krugers, H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0526-08.2008 · Cited by 661 · see citing works
Ventral hippocampal lesions affect anxiety but not spatial learning
Bannerman, D. M., Grubb, M., Deacon, R. M. J., Yee, B. K., Feldon, J., & Rawlins, J. N. P. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00268-1 · Cited by 530 · see citing works
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
Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation.
Kim, J. J., Foy, M. R., & Thompson, R. F. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.10.4750 · Cited by 435 · see citing works
Corticosteroid effects in the brain: U-shape it
Joëls, M. (2006) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2006.03.007 · Cited by 408 · see citing works
Genomic–anatomic evidence for distinct functional domains in hippocampal field CA1
Dong, H., Swanson, L. W., Chen, L., Fanselow, M. S., & Toga, A. W. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812608106 · Cited by 361 · see citing works
Maroun, M., & Richter-Levin, G. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-11-04406.2003 · Cited by 293 · see citing works
Self-citationExposing 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
Alfarez, D. N., Joëls, M., & Krugers, H. J. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02622.x · Cited by 258 · see citing works
Learning During Stressful TimesPreprint
Shors, T. J. (2004) · Learning & Memory · doi:10.1101/lm.66604 · Cited by 245 · see citing works
Maggio, N., & Segal, M. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0155-07.2007 · Cited by 230 · see citing works
Self-citationNaber, P. A., & Witter, M. P. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980413)393:3 · Cited by 219 · see citing works
Functional actions of corticosteroids in the hippocampus
Joëls, M. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.064 · Cited by 209 · see citing works
Stress Impairs LTP and Hippocampal‐Dependent Memorya
Diamond, D. M., & ROSE, G. M. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb39271.x · Cited by 195 · see citing works
Herman, J. P., Dolgas, C. M., & Carlson, S. L. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00055-4 · Cited by 193 · see citing works
From Rapid Place Learning to Behavioral Performance: A Key Role for the Intermediate Hippocampus
Bast, T., Wilson, I. A., Witter, M. P., & Morris, R. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000089 · Cited by 189 · see citing works
Karst, H., & Joëls, M. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00143.2005 · Cited by 183 · see citing works
Trivedi, M. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.02.005 · Cited by 179 · see citing works
Wiegert, O., Joëls, M., & Krugers, H. (2006) · Learning & Memory · doi:10.1101/lm.87706 · Cited by 162 · see citing works
Anxiety is functionally segregated within the septo-hippocampal system
Degroot, A., & Treit, D. (2004) · Brain Research · doi:10.1016/j.brainres.2003.10.065 · Cited by 153 · cited 1× · see citing works
“Also, lesions of the VH in young animals serves as a model system for affective disorders (Kjelstrup et al., 2002; Bannerman et al., 2003; Degroot and Treit, 2004; Trivedi and Coover, 2004).”
BackgroundKavushansky, A., Vouimba, R., Cohen, H., & Richter‐Levin, G. (2006) · Hippocampus · doi:10.1002/hipo.20130 · Cited by 141 · see citing works
Self-citationSmythe, J. W., Murphy, D., Timothy, C., & Costall, B. (1997) · Pharmacology, Biochemistry and Behavior · doi:10.1016/s0091-3057(96)00244-4 · Cited by 127 · see citing works
Degroot, A., & Treit, D. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02965-7 · Cited by 121 · see citing works
Decreased ability of rat temporal hippocampal CA1 region to produce long-term potentiation
Papatheodoropoulos, C., & Kostopoulos, G. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(99)01002-2 · Cited by 120 · see citing works
Maggio, N., & Segal, M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1901-09.2009 · Cited by 119 · see citing works
Self-citationVouimba, R., Yaniv, D., Diamond, D., & Richter‐Levin, G. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03294.x · Cited by 114 · see citing works
Self-citationLong‐term potentiation is impaired in rat hippocampal slices that produce spontaneous sharp waves
Colgin, L. L., Kubota, D., Jia, Y., Rex, C. S., & LYNCH, G. S. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.068080 · Cited by 112 · see citing works
Chameau, P. J. P., Qin, Y., Spijker, S., Smit, G., & Joëls, M. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00821.2006 · Cited by 107 · see citing works
Maruki, K., Izaki, Y., Nomura, M., & Yamauchi, T. (2001) · Hippocampus · doi:10.1002/hipo.1080 · Cited by 102 · see citing works
Unique regulation of long term potentiation in the rat ventral hippocampus
Maggio, N., & Segal, M. (2007) · Hippocampus · doi:10.1002/hipo.20237 · Cited by 100 · see citing works
Self-citationStress, hippocampal plasticity, and spatial learning
Garcia, R. (2001) · Synapse · doi:10.1002/syn.1040 · Cited by 97 · see citing works
Brain-corticosteroid hormone dialogue: Slow and persistent
de Kloet, E. R., Rots, N. Y., & Cools, A. R. (1996) · Cellular and Molecular Neurobiology · doi:10.1007/bf02088100 · Cited by 96 · see citing works
Regulation of corticosteroid receptors in the rat brain: the role of serotonin and stress
Robertson, D. A. F., Beattie, J., Reid, I., & Balfour, D. J. K. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03990.x · Cited by 84 · see citing works
Physiological Dissociation in Hippocampal Subregions in Response to Amygdala Stimulation
Vouimba, R., & Richter‐Levin, G. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi058 · Cited by 80 · see citing works
Self-citationPu, Z., Krugers, H. J., & Joëls, M. (2007) · Learning & Memory · doi:10.1101/lm.527207 · Cited by 72 · see citing works
Vouimba, R., Yaniv, D., & Richter‐Levin, G. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.07.007 · Cited by 70 · see citing works
Self-citationYamada, K., McEwen, B. S., & Pavlides, C. (2003) · Experimental Brain Research · doi:10.1007/s00221-003-1519-0 · Cited by 57 · see citing works
Bramham, C. R., Southard, T. L., Ahlers, S. T., & Sarvey, J. M. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01265-1 · Cited by 54 · see citing works
Papatheodoropoulos, C., & Kostopoulos, G. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00738-9 · Cited by 48 · see citing works
Bechterew, W. V. (1996) · Neurocase · doi:10.1093/neucas/2.4.259-b · Cited by 41 · see citing works
Activation pattern of the limbic system following spatial learning under stress
Kogan, I., & Richter‐Levin, G. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06034.x · Cited by 34 · see citing works
Self-citationAzmitia, E. C., & Liao, B. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb39232.x · Cited by 20 · see citing works
O'Keefe, J. M., & Gaffan, D. (1971) · Brain Research · doi:10.1016/0006-8993(71)90207-1 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Child development in the context of adversity: Experiential canalization of brain and behavior.
Blair, C., & Raver, C. C. (2012) · American Psychologist · doi:10.1037/a0027493 · Cited by 799 · see citing works
The hippocampus in aging and disease: From plasticity to vulnerability
Bartsch, T., & Wulff, P. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.07.084 · Cited by 466 · see citing works
Brain circuit dysfunction in post-traumatic stress disorder: from mouse to man
Fenster, R. J., Lebois, L. A. M., Ressler, K. J., & Suh, J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0039-7 · Cited by 456 · see citing works
Roth, T. L., Zoladz, P. R., Sweatt, J. D., & Diamond, D. M. (2011) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2011.01.013 · Cited by 321 · see citing works
Kutlu, M. G., & Gould, T. J. (2016) · Learning & Memory · doi:10.1101/lm.042192.116 · Cited by 324 · see citing works
Traveling Theta Waves along the Entire Septotemporal Axis of the Hippocampus
Patel, J., Fujisawa, S., Berényi, A., Royer, S., & Buzsáki, G. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.015 · Cited by 306 · see citing works
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
Andero, R., Choi, D. C., & Ressler, K. J. (2014) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-420170-5.00006-4 · Cited by 182 · see citing works
Local Generation and Propagation of Ripples along the Septotemporal Axis of the Hippocampus
Patel, J., Schomburg, E. W., Berényi, A., Fujisawa, S., & Buzsáki, G. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2036-13.2013 · Cited by 167 · see citing works
Floriou‐Servou, A., von Ziegler, L., Stalder, L., Sturman, O., Privitera, M., Rassi, A., Cremonesi, A., Thöny, B., & Bohacek, J. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.02.003 · Cited by 126 · see citing works
Tuning synaptic transmission in the hippocampus by stress: the CRH system
Chen, Y., Andres, A. L., Frotscher, M., & Baram, T. Z. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00013 · Cited by 133 · see citing works
Bartsch, T., & Butler, C. (2013) · Nature Reviews Neurology · doi:10.1038/nrneurol.2012.264 · Cited by 131 · see citing works
Chen, Y., Kramár, E. A., Chen, L. Y., Babayan, A. H., Andres, A. L., Gall, C. M., Lynch, G., & Baram, T. Z. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.17 · Cited by 115 · see citing works
Maras, P. M., Molet, J., Chen, Y., Rice, C., Ji, S. G., Solodkin, A., & Baram, T. Z. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.12 · Cited by 118 · see citing works
Stress and excitatory synapses: From health to disease
Timmermans, W., Xiong, H., Hoogenraad, C. C., & Krugers, H. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.05.043 · Cited by 118 · see citing works
Could adult hippocampal neurogenesis be relevant for human behavior?
Snyder, J. S., & Cameron, H. A. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.06.024 · Cited by 113 · see citing works
Molet, J., Maras, P. M., Kinney‐Lang, E., Harris, N. G., Rashid, F. M., Ivy, A. S., Solodkin, A., Obenaus, A., & Baram, T. Z. (2016) · Hippocampus · doi:10.1002/hipo.22661 · Cited by 112 · see citing works
Rodent models of social stress and neuronal plasticity: Relevance to depressive-like disorders
Patel, D., Kas, M. J., Chattarji, S., & Buwalda, B. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.111900 · Cited by 105 · see citing works
Late Maturation of Adult-Born Neurons in the Temporal Dentate Gyrus
Snyder, J. S., Ferrante, S. C., & Cameron, H. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048757 · Cited by 98 · see citing works
McClelland, S., Kőrösi, A., Cope, J. L., Ivy, A. S., & Baram, T. Z. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.02.008 · Cited by 96 · see citing works
Distinct hippocampal functional networks revealed by tractography-based parcellation
Adnan, A., Barnett, A. J., Moayedi, M., McCormick, C., Cohn, M., & McAndrews, M. P. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1084-x · Cited by 94 · see citing works
Ritov, G., Boltyansky, B., & Richter-Levin, G. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.169 · Cited by 92 · see citing works
Self-citationHippocampal Regulation of Aversive Memories
Goosens, K. A. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.04.003 · Cited by 95 · see citing works
Ardi, Z., Albrecht, A., Richter-Levin, A., Saha, R., & Richter-Levin, G. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.01.012 · Cited by 83 · see citing works
Self-citationHippocampal network oscillations at the interplay between innate anxiety and learned fear
Çalışkan, G., & Stork, O. (2019) · Psychopharmacology · doi:10.1007/s00213-018-5109-z · Cited by 72 · see citing works
Zoladz, P. R., Park, C. R., Halonen, J. D., Salim, S., Alzoubi, K. H., Srivareerat, M., Fleshner, M., Alkadhi, K. A., & Diamond, D. M. (2011) · Hippocampus · doi:10.1002/hipo.20922 · Cited by 79 · see citing works
Dorey, R., Piérard, C., Chauveau, F., David, V., & Béracochéa, D. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.170 · Cited by 79 · see citing works
Major Depression: A Role for Hippocampal Neurogenesis?
Lee, M. M., Reif, A., & Schmitt, A. G. (2012) · Current topics in behavioral neurosciences · doi:10.1007/7854_2012_226 · Cited by 75 · see citing works
Bast, T. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.01.003 · Cited by 72 · see citing works
Maggio, N., & Segal, M. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.11.026 · Cited by 72 · see citing works
Self-citationDifferential impact of chronic stress along the hippocampal dorsal–ventral axis
Pinto, V., Costa, J. C., Morgado, P. F., Mota, C., Miranda, A. M., Bravo, F. V., Oliveira, T. G., Cerqueira, J., & Sousa, N. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0713-0 · Cited by 71 · see citing works
Multiomic profiling of the acute stress response in the mouse hippocampus
von Ziegler, L., Floriou‐Servou, A., Waag, R., Gupta, R. R. D., Sturman, O., Gapp, K., Maat, C. A., Kockmann, T., Lin, H.-Y., Duss, S. N., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29367-5 · Cited by 66 · see citing works
Felice, D. F., O'Leary, O., Pizzo, R., & Cryan, J. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.066 · Cited by 70 · see citing works
O’Leary, O. F., O’Connor, R. M., & Cryan, J. F. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.07.015 · Cited by 64 · see citing works
Neurobiological consequences of juvenile stress: A GABAergic perspective on risk and resilience
Albrecht, A., Müller, I., Ardi, Z., Çalışkan, G., Gruber, D., Ivens, S., Segal, M., Behr, J., Heinemann, U., Stork, O., et al. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.005 · Cited by 63 · see citing works
Self-citationSteroid modulation of hippocampal plasticity: switching between cognitive and emotional memories
Maggio, N., & Segal, M. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00012 · Cited by 60 · see citing works
Self-citationStress modulation of hippocampal activity – Spotlight on the dentate gyrus
Fa, M., Li, X., Anunu, R., Kehat, O., Kriebel, M., Volkmer, H., & Richter‐Levin, G. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.04.008 · Cited by 58 · see citing works
Self-citationDorey, R., Piérard, C., Shinkaruk, S., Tronche, C., Chauveau, F., Baudonnat, M., & Béracochéa, D. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.152 · Cited by 59 · see citing works
Karabeg, M. M., Grauthoff, S., Kollert, S. Y., Weidner, M., Heiming, R. S., Jansen, F., Popp, S., Kaiser, S., Lesch, K.-P., Sachser, N., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078238 · Cited by 56 · see citing works
Bambico, F. R., & Belzung, C. (2012) · Current topics in behavioral neurosciences · doi:10.1007/7854_2012_234 · Cited by 57 · see citing works
Differential lipid composition and regulation along the hippocampal longitudinal axis
Miranda, A. M., Bravo, F. V., Chan, R., Sousa, N., Paolo, G. D., & Oliveira, T. G. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0478-6 · Cited by 54 · see citing works
Dubovyk, V., & Manahan‐Vaughan, D. (2017) · Hippocampus · doi:10.1002/hipo.22816 · Cited by 54 · see citing works
Changes in Task Demands Alter the Pattern of z if268 Expression in the Dentate Gyrus
Satvat, E., Schmidt, B., Argraves, M., Marrone, D. F., & Markus, E. J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0094-11.2011 · Cited by 54 · see citing works
Region‐specific response of the hippocampus to chronic unpredictable stress
Hawley, D. F., & Leasure, J. L. (2011) · Hippocampus · doi:10.1002/hipo.20970 · Cited by 51 · see citing works
Targeting metaplasticity mechanisms to promote sustained antidepressant actions
Brown, K. A., & Gould, T. D. (2024) · Molecular Psychiatry · doi:10.1038/s41380-023-02397-1 · Cited by 49 · see citing works
Marcelin, B., Lugo, J. N., Brewster, A. L., Liu, Z., Lewis, A. S., McClelland, S., Chetkovich, D. M., Baram, T. Z., Anderson, A. E., Becker, A. J., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.c112.367110 · Cited by 49 · see citing works
Gulyaeva, N. V., Onufriev, M. V., & Moiseeva, Y. V. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.781964 · Cited by 52 · see citing works
Selective facilitation of LTP in the ventral hippocampus by calcium stores
Grigoryan, G., Korkotian, E., & Segal, M. (2012) · Hippocampus · doi:10.1002/hipo.22000 · Cited by 47 · see citing works
Self-citationJuvenile stress alters LTP in ventral hippocampal slices: Involvement of noradrenergic mechanisms
Grigoryan, G., Ardi, Z., Albrecht, A., Richter‐Levin, G., & Segal, M. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.09.047 · Cited by 46 · see citing works
Self-citationEnhancing memory with stress: Progress, challenges, and opportunities
Goldfarb, E. V. (2018) · Brain and Cognition · doi:10.1016/j.bandc.2018.11.009 · Cited by 46 · see citing works
Ritov, G., Ardi, Z., & Richter‐Levin, G. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00018 · Cited by 44 · see citing works
Self-citationDominguez, G., Dagnas, M., Decorte, L., Vandesquille, M., Belzung, C., Béracochéa, D., & Mons, N. E. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0941-3 · Cited by 43 · see citing works
Identification of dorsal–ventral hippocampal differentiation in neonatal rats
O’Reilly, K. C., Flatberg, A., Islam, S., Olsen, L. C., Kruge, I. U., & Witter, M. P. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0831-8 · Cited by 39 · see citing works
Regulation of excitatory synapses and fearful memories by stress hormones
Krugers, H. J. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00062 · Cited by 40 · see citing works
Cocaine‐ or stress‐induced metaplasticity of LTP in the dorsal and ventral hippocampus
Keralapurath, M. M., Clark, J. K., Hammond, S., & Wagner, J. J. (2014) · Hippocampus · doi:10.1002/hipo.22250 · Cited by 37 · see citing works
Functional inactivation of the rat hippocampus disrupts avoidance of a moving object
Telenský, P., Svoboda, J., Blahna, K., Bureš, J., Kubík, Š., & Stuchlı́k, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102525108 · Cited by 37 · see citing works
The impact of stress on the hippocampal spatial code
Tomar, A., & McHugh, T. J. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.11.005 · Cited by 35 · see citing works
Enhanced cortisol secretion in acute transient global amnesia
Griebe, M., Ebert, A., Nees, F., Katic, K., Gerber, B. R., & Szabo, K. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.08.033 · Cited by 35 · see citing works
Christensen, T. T., Bisgaard, C. F., Nielsen, H. B., & Wiborg, O. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.07.016 · Cited by 35 · see citing works
Long-Term Impact of Early-Life Stress on Hippocampal Plasticity: Spotlight on Astrocytes
Çalışkan, G., Müller, A., & Albrecht, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21144999 · Cited by 32 · see citing works
Croston, R., Branch, C. L., Kozlovsky, D. Y., Roth, T. C., LaDage, L. D., Freas, C. A., & Витальевич, П. В. (2015) · Integrative and Comparative Biology · doi:10.1093/icb/icv029 · Cited by 33 · see citing works
Prenatal stress alters noradrenergic modulation of LTP in hippocampal slices
Grigoryan, G., & Segal, M. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00834.2012 · Cited by 32 · see citing works
Self-citationHippocampus-Anterior Hypothalamic Circuit Modulates Stress-Induced Endocrine and Behavioral Response
Bang, J. Y., Zhao, J., Rahman, M. F., St-Cyr, S., McGowan, P. O., & Kim, J. C. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.894722 · Cited by 32 · see citing works
Moreno, E., Vaz, S. H., Cai, N.-S., Ferrada, C., Quiroz, C., Barodia, S. K., Kabbani, N., Canela, E. I., McCormick, P. J., Lluı́s, C., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0191-11.2011 · Cited by 31 · see citing works
Sarabdjitsingh, R. A., Zhou, M., Yau, J. L. W., Webster, S. P., Walker, B. R., Seckl, J. R., Joëls, M., & Krugers, H. J. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.01.042 · Cited by 31 · see citing works
Hippocampal Mechanisms Support Cortisol-Induced Memory Enhancements
Sherman, B. E., Harris, B. B., Turk‐Browne, N. B., Sinha, R., & Goldfarb, E. V. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0916-23.2023 · Cited by 30 · see citing works
Katsouli, S., Stamatakis, A., Giompres, P., Kouvelas, E. D., Stylianopoulou, F., & Mitsacos, A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.10.073 · Cited by 29 · see citing works
Vouimba, R., & Richter‐Levin, G. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00080 · Cited by 27 · see citing works
Self-citationDanan, D., Todder, D., Zohar, J., & Cohen, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22116050 · Cited by 26 · see citing works
Sadler, T. R., Nguyen, P. T., Yang, J., Givrad, T. K., Mayer, E. A., Maarek, J. I., Hinton, D. R., & Holschneider, D. P. (2011) · Brain Research · doi:10.1016/j.brainres.2011.01.104 · Cited by 26 · see citing works
Ischemic LTP : NMDA ‐dependency and dorso/ventral distribution within the hippocampus
Maggio, N., Stein, E. S., & Segal, M. (2015) · Hippocampus · doi:10.1002/hipo.22467 · Cited by 26 · see citing works
Self-citationA Theoretically and Ethically Grounded Approach to Mindfulness Practices in the Primary Grades
Moreno, A. J. (2017) · Childhood Education · doi:10.1080/00094056.2017.1300487 · Cited by 26 · see citing works
Hadad-Ophir, O., Ardi, Z., Brande-Eilat, N., Kehat, O., Anunu, R., & Richter‐Levin, G. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.06.009 · Cited by 23 · see citing works
Self-citationDominguez, 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
Mennesson, M., & Revest, J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054496 · Cited by 27 · see citing works
Vafaei, A. A., Nasrollahi, N., Kashefi, A., Raise‐Abdullahi, P., & Rashidy‐Pour, A. (2023) · Neuroscience Letters · doi:10.1016/j.neulet.2023.137302 · Cited by 21 · see citing works
Müller, M., Faber‐Zuschratter, H., Yanagawa, Y., Stork, O., Schwegler, H., & Linke, R. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0326-9 · Cited by 21 · see citing works
Chronic stress alters the expression levels of longevity-related genes in the rat hippocampus
Sánchez-Hidalgo, A. C., Muñoz, M., Herrera, A. J., Espinosa‐Oliva, A. M., Stowell, R. D., Ayala, A., Machado, A., Venero, J. L., & de Pablos, R. M. (2016) · Neurochemistry International · doi:10.1016/j.neuint.2016.04.009 · Cited by 22 · see citing works
Nguyen, P., & Gelinas, J. N. (2018) · Journal of Neurogenetics · doi:10.1080/01677063.2018.1497630 · Cited by 22 · see citing works
Sood, R., Ritov, G., Richter‐Levin, G., & Barki‐Harrington, L. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.11.009 · Cited by 21 · see citing works
Self-citationGruber, D., Gilling, K. E., Albrecht, A., Bartsch, J., Çalışkan, G., Richter‐Levin, G., Stork, O., Heinemann, U., & Behr, J. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.02.050 · Cited by 20 · see citing works
Self-citationStress and corticosteroid modulation of seizures and synaptic inhibition in the hippocampus
Maggio, N., & Segal, M. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.12.035 · Cited by 20 · see citing works
Self-citationBartsch, J., von Cramon, M., Gruber, D., Heinemann, U., & Behr, J. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.658465 · Cited by 19 · see citing works
Çalışkan, G., Raza, S. A., Demiray, Y. E., Kul, E., Sandhu, K. V., & Stork, O. (2019) · Nutritional Neuroscience · doi:10.1080/1028415x.2019.1698826 · Cited by 17 · see citing works
Pre-trauma Methylphenidate in rats reduces PTSD-like reactions one month later
Ritov, G., & Richter‐Levin, G. (2017) · Translational Psychiatry · doi:10.1038/tp.2016.277 · Cited by 17 · see citing works
Self-citationKida, H., Nakajima, S., Shikimoto, R., Ochi, R., Noda, Y., Tsugawa, S., Fujii, S., Takayama, M., Mimura, M., & Niimura, H. (2020) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12981 · Cited by 18 · see citing works
Freiman, S. V., Onufriev, M. V., Stepanichev, M. Y., Moiseeva, Y. V., Лазарева, Н. А., & Gulyaeva, N. V. (2016) · Neurochemical Journal · doi:10.1134/s1819712416020033 · Cited by 16 · see citing works
Stress and Corticosteroids Modulate Muscarinic Long Term Potentiation (mLTP) in the Hippocampus
Stein, E. S., Hayosh, Z. I., Vlachos, A., & Maggio, N. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00299 · Cited by 17 · see citing works
Self-citationLarger bilateral amygdalar volumes are associated with affective loss experiences
Acosta, H., Jansen, A., & Kircher, T. T. J. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24835 · Cited by 16 · see citing works
Tripathi, K. K., Demiray, Y. E., Kliche, S., Jing, L., Hazra, S., Hazra, J. D., Richter‐Levin, G., & Stork, O. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100350 · Cited by 16 · see citing works
Self-citationAnteroposterior perfusion heterogeneity in human hippocampus measured by arterial spin labeling MRI
Li, X., Sarkar, S. N., Purdy, D. E., Spence, J. S., Haley, R. W., & Briggs, R. W. (2013) · NMR in Biomedicine · doi:10.1002/nbm.2898 · Cited by 16 · see citing works
Ivens, S., Çalışkan, G., Papageorgiou, I. E., Cesetti, T., Malich, A., Kann, O., Heinemann, U., Stork, O., & Albrecht, A. (2019) · Glia · doi:10.1002/glia.23683 · Cited by 16 · see citing works
MacDougall, M. J., & Howland, J. G. (2013) · Physiological Reports · doi:10.1002/phy2.35 · Cited by 15 · see citing works
Sanna, M. D., Quattrone, A., & Galeotti, N. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.04.001 · Cited by 15 · see citing works
Li, Z., & Richter‐Levin, G. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.03.059 · Cited by 15 · see citing works
Self-citationPyka, M., Klatt, S., & Cheng, S. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00091 · Cited by 14 · see citing works
Barr, J. L., Bray, B., & Forster, G. L. (2018) · InTech eBooks · doi:10.5772/intechopen.70854 · Cited by 13 · see citing works
Long‐Term Potentiation: The Accidental Discovery
Lømo, T. (2024) · Hippocampus · doi:10.1002/hipo.23664 · Cited by 13 · see citing works
Piérard, C., Dorey, R., Henkous, N., Mons, N. E., & Béracochéa, D. (2017) · Hippocampus · doi:10.1002/hipo.22748 · Cited by 13 · see citing works
Tabassum, H., & Frey, J. U. (2013) · Hippocampus · doi:10.1002/hipo.22166 · Cited by 13 · see citing works
- Authors
- Segal, M., Richter‐Levin, G., & Maggio, N.
- Affiliations
- Weizmann Institute of Science (IL)
- University of Haifa (IL)
- Sheba Medical Center (IL)
- Corresponding author
- Segal, Menahem
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2010-11-24
- Volume
- 20
- Issue
- 12
- Pages
- 1332-1338
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W1979019518
- Cited by
- 146
- References
- 58
- Citations by year
- 2025: 2 · 2024: 3 · 2023: 6 · 2022: 2 · 2021: 13 · 2020: 8 · 2019: 6 · 2018: 13 · 2017: 11 · 2016: 7 · 2015: 6 · 2014: 18 · 2013: 15 · 2012: 15
- FWCI
- 9.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- 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
- hippocampal connectivity, ventral hippocampus, dorsal hippocampus, acute stress, corticosterone, long-term potentiation, steroid hormone receptors, amygdala, neocortex, emotional memory, behavioral inhibition, mood disorders
- MeSH terms
- Amygdala, Animals, Corticosterone, Hippocampus, Nerve Net, Neuronal Plasticity, Stress, Psychological
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
