Anatomical substrates for direct interactions between hippocampus, medial prefrontal cortex, and the thalamic nucleus reuniens
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The reuniens nucleus in the midline thalamus projects to the medial prefrontal cortex (mPFC) and the hippocampus, and has been suggested to modulate interactions between these regions, such as spindle-ripple correlations during sleep and theta band coherence during exploratory behavior. Feedback from the hippocampus to the nucleus reuniens has received less attention but has the potential to influence thalamocortical networks as a function of hippocampal activation. We used the retrograde tracer cholera toxin B conjugated to two fluorophores to study thalamic projections to the dorsal and ventral hippocampus and to the prelimbic and infralimbic subregions of mPFC. We also examined the feedback connections from the hippocampus to reuniens. The goal was to evaluate the anatomical basis for direct coordination between reuniens, mPFC, and hippocampus by looking for double-labeled cells in reuniens and hippocampus. In confirmation of previous reports, the nucleus reuniens was the origin of most thalamic afferents to the dorsal hippocampus, whereas both reuniens and the lateral dorsal nucleus projected to ventral hippocampus. Feedback from hippocampus to reuniens originated primarily in the dorsal and ventral subiculum. Thalamic cells with collaterals to mPFC and hippocampus were found in reuniens, across its anteroposterior axis, and represented, on average, about 8 % of the labeled cells in reuniens. Hippocampal cells with collaterals to mPFC and reuniens were less common (~1 % of the labeled subicular cells), and located in the molecular layer of the subiculum. The results indicate that a subset of reuniens cells can directly coordinate activity in mPFC and hippocampus. Cells with collaterals in the hippocampus-reuniens-mPFC network may be important for the systems consolidation of memory traces and for theta synchronization during exploratory behavior.
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Anatomical interconnections are also found among the NR, perirhinal cortex and LEC.
“Anatomical interconnections are also found among the NR, perirhinal cortex and LEC”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Varela et al., 2014
A subpopulation of single NR and LEC neurons sends axonal collaterals to both mPFC and hippocampus, implicating that the NR and LEC can directly and simultaneously modulate the activities of mPFC and hippocampus.
“a subpopulation of single NR and LEC neurons sends axonal collaterals to both mPFC and hippocampus, implicating that the NR and LEC can directly and simultaneously modulate the activities of mPFC and hippocampus”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Varela et al., 2014
Other neural substrates that project to both mPFC and hippocampus include the amygdala, ventral tegmental area, MSDB, and hypothalamus.
“other neural substrates that project to both mPFC and hippocampus include the amygdala, ventral tegmental area, MSDB, and hypothalamus”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Varela et al., 2014
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Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,497 · see citing works
Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures?
Fanselow, M. S., & Dong, H.-W. (2010) · Neuron · doi:10.1016/j.neuron.2009.11.031 · Cited by 3,358 · see citing works
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · see citing works
Reactivation of hippocampal ensemble memories during sleep
Wilson, M. A., & McNaughton, B. L. (1994) · Science · doi:10.1126/science.8036517 · Cited by 3,118 · see citing works
Self-citationThe development and application of optogenetics
Fenno, L., Yizhar, O., & Deisseroth, K. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113817 · Cited by 1,822 · see citing works
Reverse replay of behavioural sequences in hippocampal place cells during the awake state
Foster, D. J., & Wilson, M. A. (2006) · Nature · doi:10.1038/nature04587 · Cited by 1,727 · see citing works
Self-citationSelective suppression of hippocampal ripples impairs spatial memory
Girardeau, G., Benchenane, K., Wiener, S. I., Buzsáki, G., & Zugaro, M. B. (2009) · Nature Neuroscience · doi:10.1038/nn.2384 · Cited by 1,560 · see citing works
Differential projections of the infralimbic and prelimbic cortex in the rat
Vertes, R. P. (2004) · Synapse · doi:10.1002/syn.10279 · Cited by 1,550 · see citing works
Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat
Hoover, W. B., & Vertes, R. P. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0150-4 · Cited by 1,365 · see citing works
The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat
Krettek, J. E., & Price, J. L. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901710204 · Cited by 1,277 · see citing works
Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep
Louie, K., & Wilson, M. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00186-6 · Cited by 1,148 · see citing works
Self-citationCoordinated interactions between hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep
Siapas, A. G., & Wilson, M. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80629-7 · Cited by 1,052 · see citing works
Self-citationTheta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task
Jones, M. W., & Wilson, M. A. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030402 · Cited by 1,036 · see citing works
Self-citationPrefrontal phase locking to hippocampal theta oscillations
Siapas, A. G., Lubenov, E. V., & Wilson, M. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.028 · Cited by 1,014 · see citing works
Self-citationVan der Werf, Y. D., Witter, M. P., & Groenewegen, H. J. (2002) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00181-9 · Cited by 994 · see citing works
Communication between neocortex and hippocampus during sleep in rodents
Sirota, A., Csicsvari, J., Buhl, D., & Buzsáki, G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437938100 · Cited by 930 · see citing works
Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat
Ego‐Stengel, V., & Wilson, M. A. (2010) · Hippocampus · doi:10.1002/hipo.20707 · Cited by 842 · see citing works
Self-citationJay, T. M., & Witter, M. P. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903130404 · Cited by 841 · see citing works
Hippocampal replay of extended experience
Davidson, T. J., Kloosterman, F., & Wilson, M. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.07.027 · Cited by 806 · cited 1× · see citing works
“In addition, ripple events can occur in groups (ripple bursts), in which ensembles of place cells represent extended exploratory behavior (Davidson et al. 2009).”
BackgroundSelf-citationVidal-Gonzalez, I., Vidal-Gonzalez, B., Rauch, S. L., & Quirk, G. J. (2006) · Learning & Memory · doi:10.1101/lm.306106 · Cited by 705 · see citing works
Impaired hippocampal–prefrontal synchrony in a genetic mouse model of schizophrenia
Sigurdsson, T., Stark, K. L., Karayiorgou, M., Gogos, J. A., & Gordon, J. A. (2010) · Nature · doi:10.1038/nature08855 · Cited by 702 · see citing works
Sites of Neocortical Reorganization Critical for Remote Spatial Memory
Maviel, T., Durkin, T., Menzaghi, F., & Bontempi, B. (2004) · Science · doi:10.1126/science.1098180 · Cited by 659 · see citing works
The deafferented reticular thalamic nucleus generates spindle rhythmicity
Steriade, M., Domich, L., Oakson, G., & Deschenes, M. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.57.1.260 · Cited by 640 · see citing works
Dynamics of Retrieval Strategies for Remote Memories
Goshen, I., Brodsky, M., Prakash, R., Wallace, J. L., Gradinaru, V., Ramakrishnan, C., & Deisseroth, K. A. (2011) · Cell · doi:10.1016/j.cell.2011.09.033 · Cited by 546 · see citing works
A direct projection from Ammon's horn to prefrontal cortex in the rat
Swanson, L. W. (1981) · Brain Research · doi:10.1016/0006-8993(81)90192-x · Cited by 533 · see citing works
Hippocampal theta activity following selective lesion of the septal cholinergic systeM
Lee, M., Chrobak, J. J., Attila Gabor, S. I. K., Wiley, R. G., & Buzsáki, G. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90341-7 · Cited by 501 · see citing works
Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat
Berendse, H. W., & Groenewegen, H. J. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90151-d · Cited by 494 · see citing works
Herkenham, M. A. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901770405 · Cited by 479 · see citing works
Efferent projections of the paraventricular thalamic nucleus in the rat
Moga, M. M., Weis, R. P., & Moore, R. Y. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903590204 · Cited by 402 · see citing works
A study of subcortical afferents to the hippocampal formation in the rat
Wyss, J. M., Swanson, L. W., & Cowan, W. M. (1979) · Neuroscience · doi:10.1016/0306-4522(79)90124-6 · Cited by 376 · see citing works
Entorhinal Cortex Layer III Input to the Hippocampus Is Crucial for Temporal Association Memory
Suh, J., Rivest, A. J., Nakashiba, T., Tominaga, T., & Tonegawa, S. (2011) · Science · doi:10.1126/science.1210125 · Cited by 352 · see citing works
Risold, P., Thompson, R. H., & Swanson, L. W. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00007-6 · Cited by 347 · see citing works
Vertes, R. P., Hoover, W. B., Szigeti‐Buck, K., & Léránth, C. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2006.12.002 · Cited by 345 · see citing works
Remote Control of Neuronal Signaling
Rogan, S. C., & Roth, B. L. (2011) · Pharmacological Reviews · doi:10.1124/pr.110.003020 · Cited by 339 · see citing works
Wouterlood, F. G., Saldana, E., & Witter, M. P. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.902960202 · Cited by 328 · see citing works
Spatial Memory in the Rat Requires the Dorsolateral Band of the Entorhinal Cortex
Steffenach, H.-A., Witter, M. P., Moser, M., & Moser, E. I. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.044 · Cited by 321 · see citing works
Hyman, J. M., Zilli, E. A., Paley, A., & Hasselmo, M. E. (2005) · Hippocampus · doi:10.1002/hipo.20106 · Cited by 313 · see citing works
Halassa, M. M., Siegle, J. H., Ritt, J. T., Ting, J. T., Feng, G., & Moore, C. I. (2011) · Nature Neuroscience · doi:10.1038/nn.2880 · Cited by 312 · see citing works
Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat
Vertes, R. P., Hoover, W. B., Valle, A. C., Sherman, A., & Rodriguez, J. J. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21135 · Cited by 305 · see citing works
Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat
Vertes, R. P., & Hoover, W. B. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21679 · Cited by 296 · see citing works
Afferent projections to nucleus reuniens of the thalamus
McKenna, J. T., & Vertes, R. P. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20342 · Cited by 272 · see citing works
Su, H., & Bentivoglio, M. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902970410 · Cited by 269 · see citing works
Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs
Peyrache, A., Battaglia, F. P., & Destexhe, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103612108 · Cited by 254 · see citing works
Hyman, J. M. (2010) · Frontiers in Integrative Neuroscience · doi:10.3389/neuro.07.002.2010 · Cited by 241 · see citing works
Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat
Shibata, H. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903300409 · Cited by 231 · see citing works
Van Groen, T., & Wyss, J. M. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903580411 · Cited by 218 · see citing works
Nyakas, C. J., Luiten, P. G. M., Spencer, D. G., & Traber, J. (1987) · Brain Research Bulletin · doi:10.1016/0361-9230(87)90117-1 · Cited by 213 · see citing works
Theta Rhythm of the Hippocampus: Subcortical Control and Functional Significance
Vertes, R. P., Hoover, W. B., & Prisco, G. V. D. (2004) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582304273594 · Cited by 213 · see citing works
Stoeckel, K., Schwab, M. E., & Thoenen, H. (1977) · Brain Research · doi:10.1016/0006-8993(77)90421-8 · Cited by 192 · see citing works
Retrograde amnesia after hippocampal damage: Recent vs. remote memories in two tasks
Sutherland, R. J., Weisend, M. P., Mumby, D. G., Astur, R. S., Hanlon, F. M., Koerner, A., Thomas, M. J., Wu, Y., Moses, S. N., Cole, C., et al. (2001) · Hippocampus · doi:10.1002/1098-1063(2001)11:1 · Cited by 190 · see citing works
Jay, T. M., Thierry, A., Wiklund, L., & Glowinski, J. (1992) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1992.tb00154.x · Cited by 187 · see citing works
Hoover, W. B., & Vertes, R. P. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0345-6 · Cited by 178 · see citing works
Gabbott, P. L. A., & Bacon, S. J. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960122)364:4 · Cited by 165 · see citing works
Analysis of direct hippocampal cortical field CA1 axonal projections to diencephalon in the rat
Cenquizca, L. A., & Swanson, L. W. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20985 · Cited by 157 · see citing works
Quinn, J. J., Ma, Q. D., Tinsley, M. R., Christof Koch, A., & Fanselow, M. S. (2008) · Learning & Memory · doi:10.1101/lm.813608 · Cited by 154 · see citing works
van Groen, T., & Wyss, J. M. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903240310 · Cited by 143 · see citing works
Loureiro, M., Cholvin, T., Lopez, J., Mérienne, N., Latreche, A., Cosquer, B., Geiger, K., Kelche, C. R., Cassel, J., & de Vasconcelos, A. P. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0410-12.2012 · Cited by 142 · see citing works
Condé, F., Audinat, É., Maire-Lepoivre, E., & Crépel, F. (1990) · Brain Research Bulletin · doi:10.1016/0361-9230(90)90088-h · Cited by 136 · see citing works
The rat perirhinal cortex: A review of anatomy, physiology, plasticity, and function
Kealy, J., & Commins, S. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.03.002 · Cited by 123 · see citing works
Endocytosis of cholera toxin into neuronal GERL.
Joseph, K. C., Kim, S. U., Stieber, A., & Gonatas, N. K. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.6.2815 · Cited by 99 · see citing works
Thompson, S. M., & Robertson, R. T. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902650203 · Cited by 98 · see citing works
Otake, K., & Nakamura, Y. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00062-1 · Cited by 73 · see citing works
Conte, W. L., Kamishina, H., & Reep, R. L. (2009) · Brain Structure and Function · doi:10.1007/s00429-009-0212-x · Cited by 65 · see citing works
Schofield, B. R., Schofield, R. M., Sorensen, K. A., & Motts, S. D. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.02.026 · Cited by 60 · see citing works
Topographical organization of subicular neurons projecting to subcortical regions
Namura, S., Takada, M., Kikuchi, H., & Mizuno, N. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90126-0 · Cited by 42 · see citing works
Yamano, M., & Luiten, P. G. M. (1989) · Brain Research Bulletin · doi:10.1016/0361-9230(89)90011-7 · Cited by 23 · see citing works
Deng, C., & Rogers, L. J. (1999) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(99)00044-8 · Cited by 15 · see citing works
Oka, H., & Yoshida, K. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90322-2 · Cited by 8 · see citing works
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Mechanisms of systems memory consolidation during sleep
Klinzing, J. G., Niethard, N., & Born, J. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0467-3 · Cited by 1,176 · see citing works
Limbic circuitry of the midline thalamus
Vertes, R. P., Linley, S. B., & Hoover, W. B. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.01.014 · Cited by 391 · see citing works
The hippocampus and related neocortical structures in memory transformation
Sekeres, M. J., Winocur, G., & Moscovitch, M. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.05.006 · Cited by 370 · see citing works
Over the river, through the woods: cognitive maps in the hippocampus and orbitofrontal cortex
Wikenheiser, A. M., & Schoenbaum, G. M. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.56 · Cited by 353 · see citing works
The Cognitive Thalamus as a Gateway to Mental Representations
Wolff, M., & Vann, S. D. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0479-18.2018 · Cited by 340 · see citing works
Interictal epileptiform discharges induce hippocampal–cortical coupling in temporal lobe epilepsy
Gelinas, J. N., Khodagholy, D., Thesen, T., Devinsky, O., & Buzsáki, G. (2016) · Nature Medicine · doi:10.1038/nm.4084 · Cited by 329 · see citing works
Prefrontal-Hippocampal Interactions in Memory and Emotion
Jin, J., & Maren, S. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00170 · Cited by 313 · see citing works
“robust projection to the mPFC, including the infralimbic (IL) and prelimbic (PL) cortices in rats (Swanson and Kohler, 1986; Jay and Witter, 1991; Thierry et al., 2000; Varela et al., 2014).”
BackgroundInfluentialO’Neill, P.-K., Gordon, J. A., & Sigurdsson, T. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2378-13.2013 · Cited by 294 · see citing works
Pavlov, V. A., & Tracey, K. J. (2015) · Immunologic Research · doi:10.1007/s12026-015-8718-1 · Cited by 254 · see citing works
Prefrontal–hippocampal pathways underlying inhibitory control over memory
Anderson, M. C., Bunce, J. G., & Barbas, H. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.11.008 · Cited by 242 · see citing works
Keiser, A. A., Turnbull, L. M., Darian, M. A., Feldman, D. E., Song, I., & Tronson, N. C. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.174 · Cited by 237 · see citing works
What happens to your brain on the way to Mars
Parihar, V. K., Allen, B., Tran, K. K., Macaraeg, T. G., Chu, E. M., Kwok, S. F., Chmielewski, N. N., Craver, B. M., Baulch, J. E., Acharya, M. M., et al. (2015) · Science Advances · doi:10.1126/sciadv.1400256 · Cited by 217 · see citing works
Cassel, J., de Vasconcelos, A. P., Loureiro, M., Cholvin, T., Dalrymple‐Alford, J. C., & Vertes, R. P. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.08.006 · Cited by 202 · see citing works
der Weel, M. J. D.-V., Griffin, A. L., Ito, H., Shapiro, M. L., Witter, M. P., Vertes, R. P., & Allen, T. A. (2019) · Learning & Memory · doi:10.1101/lm.048389.118 · Cited by 201 · see citing works
Xia, F., Richards, B. A., Tran, M. M., Josselyn, S. A., Takehara‐Nishiuchi, K., & Frankland, P. W. (2017) · eLife · doi:10.7554/elife.27868 · Cited by 202 · see citing works
Ventral Midline Thalamus Is Critical for Hippocampal-Prefrontal Synchrony and Spatial Working Memory
Hallock, H. L., Wang, A., & Griffin, A. L. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0991-16.2016 · Cited by 197 · see citing works
Chao, O. Y., de Souza Silva, M. A., Yang, Y.-M., & Huston, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.007 · Cited by 158 · see citing works
Neuronal circuitry for recognition memory of object and place in rodent models
Chao, O. Y.-H., Nikolaus, S., Yang, Y., & Huston, J. P. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104855 · Cited by 157 · see citing works
Prefrontal neuronal circuits of contextual fear conditioning
Rozeske, R. R., Valério, S., Chaudun, F., & Herry, C. (2014) · Genes Brain & Behavior · doi:10.1111/gbb.12181 · Cited by 144 · see citing works
Griffin, A. L. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00029 · Cited by 142 · see citing works
Top-down control of hippocampal signal-to-noise by prefrontal long-range inhibition
Malik, R., Li, Y., Schamiloglu, S., & Sohal, V. S. (2022) · Cell · doi:10.1016/j.cell.2022.04.001 · Cited by 138 · see citing works
Afferents to anterior cingulate areas 24a and 24b and midcingulate areas 24a′ and 24b′ in the mouse
Fillinger, C., Yalçın, İ., Barrot, M., & Veinante, P. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1290-1 · Cited by 139 · see citing works
Prefrontal projections to the thalamic nucleus reuniens mediate fear extinction
Ramanathan, K. R., Jin, J., Giustino, T. F., Payne, M. R., & Maren, S. (2018) · Nature Communications · doi:10.1038/s41467-018-06970-z · Cited by 140 · see citing works
Sampath, D., Sathyanesan, M., & Newton, S. S. (2017) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s136122 · Cited by 139 · see citing works
Dysregulation of Midbrain Dopamine System and the Pathophysiology of Schizophrenia
Sonnenschein, S. F., Gomes, F. V., & Grace, A. A. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00613 · Cited by 132 · see citing works
Separate elements of episodic memory subserved by distinct hippocampal-prefrontal connections
Barker, G. R. I., Banks, P. J., Scott, H., Ralph, G. S., Mitrophanous, K. A., Wong, L.-F., Bashir, Z. I., Uney, J. B., & Warburton, E. C. (2017) · Nature Neuroscience · doi:10.1038/nn.4472 · Cited by 124 · see citing works
Thalamic neuromodulation and its implications for executive networks
Varela, C. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00069 · Cited by 124 · see citing works
Self-citationA cFos activation map of remote fear memory attenuation
Silva, B. A., Burns, A. M., & Gräff, J. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5000-y · Cited by 118 · see citing works
How development sculpts hippocampal circuits and function
Cossart, R., & Khazipov, R. (2021) · Physiological Reviews · doi:10.1152/physrev.00044.2020 · Cited by 119 · see citing works
Hippocampal-cortical interaction in decision making
Yu, J. Y., & Frank, L. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.02.002 · Cited by 110 · see citing works
Huang, X., Huang, P., Huang, L., Hu, Z., Liu, X., Shen, J., Xi, Y., Yang, Y., Fu, Y., Tao, Q., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.10.023 · Cited by 113 · see citing works
Roy, A., Svensson, F. P., Mazeh, A., & Kocsis, B. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1374-6 · Cited by 99 · see citing works
The Neural Dynamics of Novel Scene Imagery
Barry, D. N., Barnes, G. R., Clark, I. A., & Maguire, E. A. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2497-18.2019 · Cited by 99 · see citing works
Two-photon calcium imaging of the medial prefrontal cortex and hippocampus without cortical invasion
Kondo, M., Kobayashi, K., Ohkura, M., Nakai, J., & Matsuzaki, M. (2017) · eLife · doi:10.7554/elife.26839 · Cited by 94 · see citing works
Efferents of anterior cingulate areas 24a and 24b and midcingulate areas 24aʹ and 24bʹ in the mouse
Fillinger, C., Yalçın, İ., Barrot, M., & Veinante, P. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1585-x · Cited by 97 · see citing works
The role of the hippocampus in the consolidation of emotional memories during sleep
Pronier, É., Morici, J. F., & Girardeau, G. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.08.003 · Cited by 96 · see citing works
Ferraris, M., Ghestem, A., Vicente, A. F., Nallet-Khosrofian, L., Bernard, C., & Quilichini, P. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.3058-17.2018 · Cited by 91 · see citing works
Duan, A. R., Varela, C., Zhang, Y., Shen, Y., Xiong, L. L., Wilson, M. A., & Lisman, J. E. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.01.020 · Cited by 87 · see citing works
Self-citationArdi, 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
Viena, T. D., Linley, S. B., & Vertes, R. P. (2018) · Hippocampus · doi:10.1002/hipo.22831 · Cited by 85 · see citing works
The nucleus reuniens orchestrates prefrontal-hippocampal synchrony during spatial working memory
Griffin, A. L. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.05.033 · Cited by 85 · see citing works
Major diencephalic inputs to the hippocampus
Vertes, R. P. (2015) · Progress in brain research · doi:10.1016/bs.pbr.2015.03.008 · Cited by 83 · see citing works
Ferraris, M., Cassel, J., de Vasconcelos, A. P., Stéphan, A., & Quilichini, P. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.02.025 · Cited by 85 · see citing works
Structural and functional organization of the midline and intralaminar nuclei of the thalamus
Vertes, R. P., Linley, S. B., & Rojas, A. K. P. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.964644 · Cited by 82 · see citing works
Hippocampal representations as a function of time, subregion, and brain state
Duncan, K. D., & Schlichting, M. L. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.03.006 · Cited by 78 · see citing works
Nucleus reuniens mediates the extinction of contextual fear conditioning
Ramanathan, K. R., & Maren, S. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112114 · Cited by 76 · see citing works
Maisson, D. J.-N., Gemzik, Z. M., & Griffin, A. L. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.06.010 · Cited by 74 · see citing works
Troyner, F., Bicca, M. A., & Bertoglio, L. J. (2018) · Hippocampus · doi:10.1002/hipo.22964 · Cited by 73 · see citing works
Hippocampal ripples as a mode of communication with cortical and subcortical areas
Todorova, R., & Zugaro, M. B. (2018) · Hippocampus · doi:10.1002/hipo.22997 · Cited by 54 · see citing works
Hippocampal 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
Temporal associations between sleep slow oscillations, spindles and ripples
Oyanedel, C. N., Durán, E., Niethard, N., Inostroza, M., & Born, J. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14906 · Cited by 71 · see citing works
The nonspecific thalamus: A place in a wedding bed for making memories last?
de Vasconcelos, A. P., & Cassel, J. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.021 · Cited by 68 · see citing works
Raut, S. B., Marathe, P. A., van Eijk, L., Eri, R. D., Ravindran, M., Benedek, D. M., Ursano, R. J., Canales, J. J., & Johnson, L. R. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108195 · Cited by 71 · see citing works
Zimmerman, E. C., & Grace, A. A. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1402-16.2016 · Cited by 66 · see citing works
The two faces of synaptic failure in AppNL-G-F knock-in mice
Latif‐Hernandez, A., Sabanov, V., Ahmed, T., Craessaerts, K., Saito, T., Saido, T. C., & Balschun, D. (2020) · Alzheimer s Research & Therapy · doi:10.1186/s13195-020-00667-6 · Cited by 65 · 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
Moscovitch, M., & Gilboa, A. (2021) · doi:10.31234/osf.io/yxbrs · Cited by 62 · see citing works
Hauer, B. E., Pagliardini, S., & Dickson, C. T. (2019) · eNeuro · doi:10.1523/eneuro.0365-19.2019 · Cited by 59 · see citing works
Operant Conditioning of Synaptic and Spiking Activity Patterns in Single Hippocampal Neurons
Ishikawa, D., Matsumoto, N., Sakaguchi, T., Matsuki, N., & Ikegaya, Y. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.5298-13.2014 · Cited by 55 · see citing works
Çalışkan, G., & Stork, O. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.02.022 · Cited by 55 · see citing works
Yang, M., Logothetis, N. K., & Eschenko, O. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.2107-18.2018 · Cited by 57 · see citing works
Monosynaptic Hippocampal-Prefrontal Projections Contribute to Spatial Memory Consolidation in Mice
Binder, S., Mölle, M., Lippert, M., Bruder, R., Aksamaz, S., Ohl, F. W., Wiegert, J. S., & Marshall, L. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2158-18.2019 · Cited by 55 · see citing works
Cassel, J., Ferraris, M., Quilichini, P., Cholvin, T., Boch, L., Stéphan, A., & de Vasconcelos, A. P. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.023 · Cited by 54 · see citing works
McKenzie, S., Keene, C. S., Farovik, A., Bladon, J. H., Place, R., Komorowski, R. W., & Eichenbaum, H. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.12.008 · Cited by 53 · see citing works
Differential effects of paradoxical sleep deprivation on memory and oxidative stress
Lima, Á. M. A., de Bruin, V. M. S., Rios, E. R. V., & de Bruin, P. F. C. (2014) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-013-0955-z · Cited by 53 · see citing works
Hartung, H., Brockmann, M. D., Pöschel, B., Feo, V. D., & Hanganu‐Opatz, I. L. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3232-15.2016 · Cited by 53 · see citing works
Varela, C., & Wilson, M. A. (2020) · eLife · doi:10.7554/elife.48881 · Cited by 52 · see citing works
Self-citationNucleus reuniens transiently synchronizes memory networks at beta frequencies
Jayachandran, M., Viena, T. D., Garcia, A., Veliz, A. V., Leyva, S., Roldan, V., Vertes, R. P., & Allen, T. A. (2023) · Nature Communications · doi:10.1038/s41467-023-40044-z · Cited by 53 · see citing works
der Weel, M. J. D.-V., Lopes, F. H. D. S., & Witter, M. P. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1350-6 · Cited by 46 · see citing works
Distributed interactive brain circuits for object-in-place memory: A place for time?
Aggleton, J. P., & Nelson, A. J. D. (2020) · Brain and Neuroscience Advances · doi:10.1177/2398212820933471 · Cited by 50 · see citing works
Cholvin, T., Hok, V., Giorgi, L., Chaillan, F. A., & Poucet, B. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2039-17.2017 · Cited by 50 · see citing works
Altered Hippocampal-Prefrontal Neural Dynamics in Mouse Models of Down Syndrome
Chang, P., Bush, D., Schorge, S., Good, M., Canonica, T., Shing, N., Noy, S., Wiseman, F. K., Burgess, N., Tybulewicz, V. L. J., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.065 · Cited by 47 · see citing works
Understanding the dynamic and destiny of memories
Alvares, L. D. O., & Monte, F. H. D. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.009 · Cited by 47 · see citing works
Linley, S. B., Gallo, M. M., & Vertes, R. P. (2016) · Brain Research · doi:10.1016/j.brainres.2016.08.022 · Cited by 47 · see citing works
Cell Assemblies in the Cortico-Hippocampal-Reuniens Network during Slow Oscillations
Angulo‐García, D., Ferraris, M., Ghestem, A., Nallet-Khosrofian, L., Bernard, C., & Quilichini, P. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0571-20.2020 · Cited by 46 · see citing works
Vertes, R. P., Linley, S. B., Groenewegen, H. J., & Witter, M. P. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00016-4 · Cited by 43 · see citing works
Zhu, X., Cabungcal, J.-H., Cuénod, M., Uliana, D. L., Kim, Q., & Grace, A. A. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01198-8 · Cited by 44 · see citing works
Symanski, C. A., Bladon, J. H., Kullberg, E. T., Miller, P. C., & Jadhav, S. P. (2022) · eLife · doi:10.7554/elife.79545 · Cited by 49 · see citing works
Šanda, P., Malerba, P., Jiang, X., Krishnan, G. P., González-Martínez, J., Halgren, E., & Bazhenov, M. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa228 · Cited by 42 · see citing works
Brain mechanisms underlying the inhibitory control of thought
Anderson, M. C., Crespo‐García, M., & Subbulakshmi, S. (2025) · Nature reviews. Neuroscience · doi:10.1038/s41583-025-00929-y · Cited by 44 · see citing works
Critical appraisal of pathology transmission in the α-synuclein fibril model of Lewy body disorders
Nouraei, N., Mason, D. M., Miner, K. M., Carcella, M. A., Bhatia, T. N., Dumm, B. K., Soni, D., Johnson, D. A., Luk, K. C., & Leak, R. K. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.10.017 · Cited by 40 · see citing works
Rahman, F., Nanu, R., Schneider, N. A., Katz, D. B., Lisman, J. E., & Pi, H.-J. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107396 · Cited by 40 · see citing works
Mystery of the memory engram: History, current knowledge, and unanswered questions
Lopez, M. R., Wasberg, S. M., Gagliardi, C. M., Normandin, M. E., & Muzzio, I. A. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105574 · Cited by 39 · see citing works
Afferent connections of the thalamic nucleus reuniens in the mouse
Scheel, N., Wulff, P., & Malsen, J. G. D. M. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24811 · Cited by 39 · see citing works
The neural correlates of navigation beyond the hippocampus
Dumont, J. R., & Taube, J. S. (2015) · Progress in brain research · doi:10.1016/bs.pbr.2015.03.004 · Cited by 39 · see citing works
Albrecht, A., Redavide, E., Regev-Tsur, S., Stork, O., & Richter‐Levin, G. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.11.002 · Cited by 38 · see citing works
ACC Theta Improves Hippocampal Contextual Processing during Remote Recall
Wirt, R. A., & Hyman, J. M. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.080 · Cited by 39 · see citing works
Dickerson, D. D., & Bilkey, D. K. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00217 · Cited by 38 · see citing works
Klein, M.-M., Cholvin, T., Cosquer, B., Salvadori, A., Méro, J. L., Kourouma, L., Boutillier, A., de Vasconcelos, A. P., & Cassel, J. (2019) · Brain Structure and Function · doi:10.1007/s00429-019-01865-1 · Cited by 37 · see citing works
The anterior thalamic nuclei and nucleus reuniens: So similar but so different
Mathiasen, M. L., O’Mara, S. M., & Aggleton, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.006 · Cited by 36 · see citing works
Morici, J. F., Weisstaub, N., & Zold, C. L. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2203024119 · Cited by 37 · see citing works
Wolff, A. R., Bygrave, A. M., Sanderson, D. J., Boyden, E. S., Bannerman, D. M., Kullmann, D. M., & Kätzel, D. (2018) · Scientific Reports · doi:10.1038/s41598-018-31163-5 · Cited by 36 · see citing works
Importance of the ventral midline thalamus in driving hippocampal functions
Cassel, J., & de Vasconcelos, A. P. (2015) · Progress in brain research · doi:10.1016/bs.pbr.2015.03.005 · Cited by 37 · see citing works
Heck, D. H., Fox, M. B., Chapman, B., McAfee, S. S., & Liu, Y. (2023) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2023.1126508 · Cited by 35 · see citing works
Weiss, C., & Disterhoft, J. F. (2015) · Behavioral Neuroscience · doi:10.1037/bne0000061 · Cited by 35 · see citing works
The thalamic midline nucleus reuniens: potential relevance for schizophrenia and epilepsy
der Weel, M. J. D.-V., & Witter, M. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.033 · Cited by 35 · see citing works
McGinn, R. J., Stein, E. L. V., Datta, A., Wu, T. Q., Lusk, Z., Nam, S., Dilts-Garcha, M., Fisher, R. S., Buch, V., & Parvizi, J. (2024) · Neurology · doi:10.1212/wnl.0000000000210039 · Cited by 35 · see citing works
Rossignoli, M. T., Lopes‐Aguiar, C., Ruggiero, R. N., da Silva, R. A. D. V., Bueno-Júnior, L. S., Kandratavicius, L., Peixoto-Santos, J. E., Crippa, J. A. S., Hallak, J. E. C., Zuardi, A. W., et al. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.03.019 · Cited by 34 · see citing works
The reuniens and rhomboid nuclei are necessary for contextual fear memory persistence in rats
Quet, É., Majchrzak, M. J., Cosquer, B., Morvan, T., Wolff, M., Cassel, J., de Vasconcelos, A. P., & Stéphan, A. (2020) · Brain Structure and Function · doi:10.1007/s00429-020-02048-z · Cited by 33 · see citing works
Liu, T., Lu, J., Łukasiewicz, K., Pan, B., & Zuo, Y. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100342 · Cited by 32 · see citing works
- Authors
- Varela, C., Kumar, S., Yang, J. Y., & Wilson, M. A.
- Affiliations
- Massachusetts Institute of Technology (US)
- Corresponding author
- Varela, C.
- Venue
- Brain Structure and Function
- Published
- 2013-04-10
- Volume
- 219
- Issue
- 3
- Pages
- 911-929
- ISSN
- 1863-2653 (ISSN-L)
- 1863-2661
- PMC
- PMC4179252
- OpenAlex
- W1981683953
- Cited by
- 277
- References
- 69
- Citations by year
- 2026: 21 · 2025: 18 · 2024: 25 · 2023: 16 · 2022: 29 · 2021: 34 · 2020: 27 · 2019: 18 · 2018: 26 · 2017: 23 · 2016: 16 · 2015: 13 · 2014: 7 · 2013: 4
- FWCI
- 7.28
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Brain Structure and Function (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
- PMC
- Funders
- National Institute of Mental Health (R01MH061976)
- National Institute of General Medical Sciences (R01GM104948)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- nucleus reuniens, medial prefrontal cortex, hippocampus, thalamocortical connections, dorsal hippocampus, ventral hippocampus, subiculum, prelimbic cortex, infralimbic cortex, retrograde tracing, cholera toxin B, thalamocortical network, memory consolidation, theta synchronization, sleep spindles
- MeSH terms
- Animals, Hippocampus, Male, Memory, Neural Pathways, Neurons, Thalamic Nuclei, Prefrontal Cortex, Rats, Long-Evans
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