Skip to main content Accessibility help
×
Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-10T10:22:26.389Z Has data issue: false hasContentIssue false

Chapter 18 - The Thalamus in Navigation

from Section 7: - Cognition

Published online by Cambridge University Press:  12 August 2022

Michael M. Halassa
Affiliation:
Massachusetts Institute of Technology
Get access

Summary

The three anterior thalamic nuclei and the nucleus reuniens are essential for spatial navigation, yet their exact role in this function remains elusive. Specifically, it remains to be answered whether the thalamus acts a simple relay of spatial and executive signals or whether it critically operates on its inputs to convey processed signals to its cortical targets. The anterior thalamus and nucleus reuniens are at the center stage of anatomical networks that share one common aspect: their association with the hippocampus. Here, I review the large body of literature, starting from the classic Papez circuits, which describe how these thalamic nuclei are interconnected with subcortical, medial cortex, and parahippocampal regions, as well as their neuromodulatory inputs. I then provide an overview of the spatial and other electrophysiological correlates of anterior thalamic and reuniens neurons and of how their firing and oscillatory properties depend on ongoing behavior. Finally, I discuss the clinical and experimental evidence pointing to the role of the thalamus in navigation and, specifically, how spatial and executive signals are processed in thalamocortical loops. I conclude by discussing how the same thalamic circuits may be at play in the processing of episodic memories during sleep.

Type
Chapter
Information
The Thalamus , pp. 340 - 360
Publisher: Cambridge University Press
Print publication year: 2022

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aggleton, J.P., Brown, M.W., 1999. Episodic memory, amnesia, and the hippocampal–anterior thalamic axis. Behav. Brain Sci. 22, 425444.Google Scholar
Aggleton, J.P., Hunt, P.R., Nagle, S., Neave, N., 1996. The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat. Behav. Brain Res. 81, 189198. https://doi.org/10.1016/S0166-4328(96)89080–2Google Scholar
Aggleton, J.P., Keith, A.B., Sahgal, A., 1991. Both fornix and anterior thalamic, but not mammillary, lesions disrupt delayed non-matching-to-position memory in rats. Behav. Brain Res. 44, 151161. https://doi.org/10.1016/S0166-4328(05)80020–8Google Scholar
Aggleton, J.P., Nelson, A.J.D., 2015. Why do lesions in the rodent anterior thalamic nuclei cause such severe spatial deficits? Neurosci. Biobehav. Rev. 54, 131144. https://doi.org/10.1016/j.neubiorev.2014.08.013Google Scholar
Alexander, A.S., Carstensen, L.C., Hinman, J.R., Raudies, F., Chapman, G.W., Hasselmo, M.E., 2020. Egocentric boundary vector tuning of the retrosplenial cortex. Sci. Adv. 6, eaaz2322. https://doi.org/10.1126/sciadv.aaz2322Google Scholar
Allen, G.V., Hopkins, D.A., 1989. Mamillary body in the rat: Topography and synaptology of projections from the subicular complex, prefrontal cortex, and midbrain tegmentum. J. Comp. Neurol. 286, 311336. https://doi.org/10.1002/cne.902860303Google Scholar
Alonso, A., Llinás, R.R., 1989. Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342, 175177. https://doi.org/10.1038/342175a0Google Scholar
Amaral, D.G., Cowan, W.M., 1980. Subcortical afferents to the hippocampal formation in the monkey. J. Comp. Neurol. 189, 573591. https://doi.org/10.1002/cne.901890402Google Scholar
Andersen, P., Curtis, D.R., 1964. The excitation of thalamic neurones by acetylcholine. Acta Physiol. Scand. 61, 8599. https://doi.org/10.1111/j.1748-1716.1964.tb02945.xGoogle Scholar
Angelaki, D.E., Cullen, K.E., 2008. Vestibular system: the many facets of a multimodal sense. Annu. Rev. Neurosci. 31, 125150. https://doi.org/10.1146/annurev.neuro.31.060407.125555Google Scholar
Arcelli, P., Frassoni, C., Regondi, M.C., Biasi, S.D., Spreafico, R., 1997. GABAergic neurons in mammalian thalamus: a marker of thalamic complexity? Brain Res. Bull. 42, 2737. https://doi.org/10.1016/S0361-9230(96)00107–4Google Scholar
Bagur, S., Benchenane, K., 2018. Taming the oscillatory zoo in the hippocampus and neo-cortex: a review of the commentary of Lockmann and Tort on Roy et al. Brain Struct. Funct. 223, 59. https://doi.org/10.1007/s00429-017-1569-xGoogle Scholar
Banino, A., Barry, C., Uria, B., Blundell, C., Lillicrap, T., Mirowski, P., Pritzel, A., Chadwick, M.J., Degris, T., Modayil, J., Wayne, G., Soyer, H., Viola, F., Zhang, B., Goroshin, R., Rabinowitz, N., Pascanu, R., Beattie, C., Petersen, S., Sadik, A., Gaffney, S., King, H., Kavukcuoglu, K., Hassabis, D., Hadsell, R., Kumaran, D., 2018. Vector-based navigation using grid-like representations in artificial agents. Nature 557, 429433. https://doi.org/10.1038/s41586-018-0102-6Google Scholar
Barry, C., Lever, C., Hayman, R., Hartley, T., Burton, S., O’Keefe, J., Jeffery, K., Burgess, N., 2006. The boundary vector cell model of place cell firing and spatial memory. Rev. Neurosci. 17, 7197. https://doi.org/10.1515/revneuro.2006.17.1-2.71Google Scholar
Bassant, M.-H., Poindessous‐Jazat, F., 2001. Ventral tegmental nucleus of Gudden: a pontine hippocampal theta generator? Hippocampus 11, 809813. https://doi.org/10.1002/hipo.1096Google Scholar
Bassett, J.P., Wills, T.J., Cacucci, F., 2018. Self-organized attractor dynamics in the developing head direction circuit. Curr. Biol. 28, 609–615.e3. https://doi.org/10.1016/j.cub.2018.01.010CrossRefGoogle ScholarPubMed
Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P.L., Gioanni, Y., Battaglia, F.P., Wiener, S.I., 2010. Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 66, 921936. https://doi.org/10.1016/j.neuron.2010.05.013Google Scholar
Berthoz, A., Viaud-Delmon, I., 1999. Multisensory integration in spatial orientation. Curr. Opin. Neurobiol. 9, 708712. https://doi.org/10.1016/S0959-4388(99)00041–0Google Scholar
Bertram, E.H., Zhang, D.X., 1999. Thalamic excitation of hippocampal CA1 neurons: a comparison with the effects of CA3 stimulation. Neuroscience 92, 1526. https://doi.org/10.1016/S0306-4522(98)00712-XGoogle Scholar
Bicanski, A., Burgess, N., 2020. Neuronal vector coding in spatial cognition. Nat. Rev. Neurosci. 21, 453470. https://doi.org/10.1038/s41583-020–0336-9Google Scholar
Birrell, J.M., Brown, V.J., 2000. Medial frontal cortex mediates perceptual attentional set shifting in the rat. J. Neurosci. 20, 4320.Google Scholar
Blair, H.T., Cho, J., Sharp, P.E., 1998. Role of the lateral mammillary nucleus in the rat head direction circuit: a combined single unit recording and lesion study. Neuron 21, 13871397.Google Scholar
Blair, H.T., Cho, J., Sharp, P.E., 1999. The anterior thalamic head-direction signal is abolished by bilateral but not unilateral lesions of the lateral mammillary nucleus. J. Neurosci. 19, 66736683.Google Scholar
Blair, H.T., Sharp, P.E., 1995. Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction. J. Neurosci. 15, 6260.Google Scholar
Boucetta, S., Cissé, Y., Mainville, L., Morales, M., Jones, B.E., 2014. Discharge profiles across the sleep–waking cycle of identified cholinergic, GABAergic, and glutamatergic neurons in the pontomesencephalic tegmentum of the rat. J. Neurosci. 34, 47084727. https://doi.org/10.1523/JNEUROSCI.2617–13.2014Google Scholar
Brandon, M.P., Bogaard, A.R., Andrews, C.M., Hasselmo, M.E., 2012. Head direction cells in the postsubiculum do not show replay of prior waking sequences during sleep. Hippocampus 22, 604618. https://doi.org/10.1002/hipo.20924Google Scholar
Brandon, M.P., Bogaard, A.R., Libby, C.P., Connerney, M.A., Gupta, K., Hasselmo, M.E., 2011. Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332, 595599. https://doi.org/10.1126/science.1201652Google Scholar
Brandon, M.P., Bogaard, A.R., Schultheiss, N.W., Hasselmo, M.E., 2013. Segregation of cortical head direction cell assemblies on alternating theta cycles. Nat. Neurosci. 16, 739748. https://doi.org/10.1038/nn.3383Google Scholar
Burak, Y., Fiete, I.R., 2009. Accurate path integration in continuous attractor network models of grid cells. PLOS Comput. Biol. 5, e1000291. https://doi.org/10.1371/journal.pcbi.1000291Google Scholar
Burgess, N., Barry, C., O’Keefe, J., 2007. An oscillatory interference model of grid cell firing. Hippocampus 17, 801812. https://doi.org/10.1002/hipo.20327CrossRefGoogle ScholarPubMed
Buzsáki, G., 2002. Theta oscillations in the hippocampus. Neuron 33, 325340.Google Scholar
Buzsáki, G., 2015. Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning. Hippocampus 25, 10731188. https://doi.org/10.1002/hipo.22488Google Scholar
Buzsáki, G., Moser, E.I., 2013. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16, 130138. https://doi.org/10.1038/nn.3304Google Scholar
Byatt, G., Dalrymple-Alford, J.C., 1996. Both anteromedial and anteroventral thalamic lesions impair radial-maze learning in rats. Behav. Neurosci. 110, 13351348. https://doi.org/10.1037//0735-7044.110.6.1335Google Scholar
Cacucci, F., Lever, C., Wills, T.J., Burgess, N., O’Keefe, J., 2004. Theta-modulated place-by-direction cells in the hippocampal formation in the rat. J. Neurosci. 24, 82658277. https://doi.org/10.1523/JNEUROSCI.2635-04.2004Google Scholar
Calton, J.L., Stackman, R.W., Goodridge, J.P., Archey, W.B., Dudchenko, P.A., Taube, J.S., 2003. Hippocampal place cell instability after lesions of the head direction cell network. J. Neurosci. 23, 97199731.CrossRefGoogle ScholarPubMed
Carlén, M., 2017. What constitutes the prefrontal cortex? Science 358, 478482. https://doi.org/10.1126/science.aan8868Google Scholar
Carlesimo, G.A., Lombardi, M.G., Caltagirone, C., 2011. Vascular thalamic amnesia: A reappraisal. Neuropsychologia 49, 777789. https://doi.org/10.1016/j.neuropsychologia.2011.01.026Google Scholar
Carvalho, M.M., Tanke, N., Kropff, E., Witter, M.P., Moser, M.-B., Moser, E.I., 2020. A brainstem locomotor circuit drives the activity of speed cells in the medial entorhinal cortex. Cell Rep. 32, 108123. https://doi.org/10.1016/j.celrep.2020.108123CrossRefGoogle ScholarPubMed
Chaudhuri, R., Gercek, B., Pandey, B., Peyrache, A., Fiete, I., 2019. The intrinsic attractor manifold and population dynamics of a canonical cognitive circuit across waking and sleep. Nat. Neurosci. 22, 15121520.Google Scholar
Chen, L.L., Lin, L.H., Green, E.J., Barnes, C.A., McNaughton, B.L., 1994. Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp. Brain Res. 101, 823.Google Scholar
Christiansen, K., Dillingham, C.M., Wright, N.F., Saunders, R.C., Vann, S.D., Aggleton, J.P., 2016. Complementary subicular pathways to the anterior thalamic nuclei and mammillary bodies in the rat and macaque monkey brain. Eur. J. Neurosci. 43, 10441061. https://doi.org/10.1111/ejn.13208CrossRefGoogle Scholar
Cissé, Y., Toossi, H., Ishibashi, M., Mainville, L., Leonard, C.S., Adamantidis, A., Jones, B.E., 2018. Discharge and role of acetylcholine pontomesencephalic neurons in cortical activity and sleep-wake states examined by optogenetics and juxtacellular recording in mice. eNeuro 5. https://doi.org/10.1523/ENEURO.0270-18.2018CrossRefGoogle ScholarPubMed
Clark, B.J., Harvey, R.E., 2016. Do the anterior and lateral thalamic nuclei make distinct contributions to spatial representation and memory? Neurobiol. Learn. Mem. 133, 6978. https://doi.org/10.1016/j.nlm.2016.06.002Google Scholar
Claudi, F., Tyson, A.L., Branco, T., 2020. Brainrender. A Python-based software for visualisation of neuroanatomical and morphological data. bioRxiv 2020.02.23.961748. https://doi.org/10.1101/2020.02.23.961748CrossRefGoogle Scholar
Cornwall, J., Cooper, J.D., Phillipson, O.T., 1990. Projections to the rostral reticular thalamic nucleus in the rat. Exp. Brain Res. 80. https://doi.org/10.1007/BF00228857Google Scholar
Cruce, J.A.F., 1975. An autoradiographic study of the projections of the mammillothalamic tract in the rat. Brain Res. 85, 211219. https://doi.org/10.1016/0006-8993(75)90072-4Google Scholar
Curro Dossi, R., Pare, D., Steriade, M., 1991. Short-lasting nicotinic and long-lasting muscarinic depolarizing responses of thalamocortical neurons to stimulation of mesopontine cholinergic nuclei. J. Neurophysiol. 65, 393406. https://doi.org/10.1152/jn.1991.65.3.393Google Scholar
Dalley, J.W., Cardinal, R.N., Robbins, T.W., 2004. Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci. Biobehav. Rev. 28, 771784. https://doi.org/10.1016/j.neubiorev.2004.09.006Google Scholar
DeCoteau, W.E., Thorn, C., Gibson, D.J., Courtemanche, R., Mitra, P., Kubota, Y., Graybiel, A.M., 2007. Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task. Proc. Natl. Acad. Sci. 104, 5644.Google Scholar
Diekelmann, S., Born, J., 2010. The memory function of sleep. Nat. Rev. Neurosci. 11, 114126. https://doi.org/10.1038/nrn2762Google Scholar
Dolleman-van der Weel, M.J., Lopes da Silva, F.H., Witter, M.P., 2017. Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat. Brain Struct. Funct. 222, 24212438. https://doi.org/10.1007/s00429-016-1350-6Google Scholar
Dragoi, G., Buzsáki, G., 2006. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50, 145157.Google Scholar
Dudai, Y., 2004. The neurobiology of consolidations, or, how stable is the engram? Annu. Rev. Psychol. 55, 5186. https://doi.org/10.1146/annurev.psych.55.090902.142050Google Scholar
Ego‐Stengel, V., Wilson, M.A., 2007. Spatial selectivity and theta phase precession in CA1 interneurons. Hippocampus 17, 161174. https://doi.org/10.1002/hipo.20253Google Scholar
Ego‐Stengel, V., Wilson, M.A., 2010. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20, 110. https://doi.org/10.1002/hipo.20707Google Scholar
Etienne, A.S., Jeffery, K.J., 2004. Path integration in mammals. Hippocampus 14, 180192. https://doi.org/10.1002/hipo.10173Google Scholar
Euston, D.R., Gruber, A.J., McNaughton, B.L., 2012. The tole of medial prefrontal cortex in memory and decision making. Neuron 76, 10571070. https://doi.org/10.1016/j.neuron.2012.12.002Google Scholar
Euston, D.R., Tatsuno, M., McNaughton, B.L., 2007. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318, 11471150. https://doi.org/10.1126/science.1148979Google Scholar
Fernandez, L.M.J., Lüthi, A., 2019. Sleep spindles: mechanisms and functions. Physiol. Rev. 100, 805868. https://doi.org/10.1152/physrev.00042.2018Google Scholar
Frankland, P.W., Bontempi, B., 2005. The organization of recent and remote memories. Nat. Rev. Neurosci. 6, 119130. https://doi.org/10.1038/nrn1607Google Scholar
Fuhs, M.C., Touretzky, D.S., 2006. A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 26, 42664276. https://doi.org/10.1523/JNEUROSCI.4353-05.2006Google Scholar
Fujisawa, S., Buzsáki, G., 2011. A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron 72, 153165. https://doi.org/10.1016/j.neuron.2011.08.018Google Scholar
Gallistel, C.R., 1989. Animal cognition: the representation of space, time and number. Annu. Rev. Psychol. 40, 155189. https://doi.org/10.1146/annurev.ps.40.020189.001103Google Scholar
Gent, T.C., Bandarabadi, M., Herrera, C.G., Adamantidis, A.R., 2018. Thalamic dual control of sleep and wakefulness. Nat. Neurosci. 21, 974. https://doi.org/10.1038/s41593-018-0164-7Google Scholar
Girardeau, G., Benchenane, K., Wiener, S.I., Buzsáki, G., Zugaro, M.B., 2009. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12, 12221223. https://doi.org/10.1038/nn.2384Google Scholar
Gofman, X., Tocker, G., Weiss, S., Boccara, C.N., Lu, L., Moser, M.-B., Moser, E.I., Morris, G., Derdikman, D., 2019. Dissociation between postrhinal cortex and downstream parahippocampal regions in the representation of egocentric boundaries. Curr. Biol. 29, 2751–2757.e4. https://doi.org/10.1016/j.cub.2019.07.007CrossRefGoogle ScholarPubMed
Gonzalo-Ruiz, A., Lieberman, A.R., 1995. Topographic organization of projections from the thalamic reticular nucleus to the anterior thalamic nuclei in the rat. Brain Res. Bull. 37, 1735. https://doi.org/10.1016/0361-9230(94)00252-5Google Scholar
Goodridge, J.P., Taube, J.S., 1997. Interaction between the postsubiculum and anterior thalamus in the generation of head direction cell activity. J. Neurosci. 17, 93159330.Google Scholar
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., Moser, E.I., 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801806. https://doi.org/10.1038/nature03721Google Scholar
Halassa, M.M., Acsády, L., 2016. Thalamic inhibition: diverse sources, diverse scales. Trends Neurosci. 39, 680693. https://doi.org/10.1016/j.tins.2016.08.001Google Scholar
Harding, A., Halliday, G., Caine, D., Kril, J., 2000. Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. Brain 123, 141154. https://doi.org/10.1093/brain/123.1.141Google Scholar
Harland, B., Grieves, R.M., Bett, D., Stentiford, R., Wood, E.R., Dudchenko, P.A., 2017. Lesions of the head direction cell system increase hippocampal place field repetition. Curr. Biol. 27, 27062712. https://doi.org/10.1016/j.cub.2017.07.071Google Scholar
Harris, K.D., Csicsvari, J., Hirase, H., Dragoi, G., Buzsaki, G., 2003. Organization of cell assemblies in the hippocampus. Nature 424, 552556. https://doi.org/10.1038/nature01834Google Scholar
Hasselmo, M.E., 2006. The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 16, 710715. https://doi.org/10.1016/j.conb.2006.09.002Google Scholar
Heckers, S., Geula, C., Mesulam, M.-M., 1992. Cholinergic innervation of the human thalamus: dual origin and differential nuclear distribution. J. Comp. Neurol. 325, 6882. https://doi.org/10.1002/cne.903250107Google Scholar
Herkenham, M., 1978. The connections of the nucleus reuniens thalami: evidence for a direct thalamo-hippocampal pathway in the rat. J. Comp. Neurol. 177, 589609. https://doi.org/10.1002/cne.901770405Google Scholar
Hulse, B.K., Jayaraman, V., 2020. Mechanisms underlying the neural computation of head direction. Annu. Rev. Neurosci. 43, 3154. https://doi.org/10.1146/annurev-neuro-072116-031516Google Scholar
Ito, H.T., Zhang, S.-J., Witter, M.P., Moser, E.I., Moser, M.-B., 2015. A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation. Nature 522, 5055. https://doi.org/10.1038/nature14396Google Scholar
Jacob, P.-Y., Casali, G., Spieser, L., Page, H., Overington, D., Jeffery, K., 2017. An independent, landmark-dominated head-direction signal in dysgranular retrosplenial cortex. Nat. Neurosci. 20, 173175. https://doi.org/10.1038/nn.4465Google Scholar
Jankowski, M.M., Islam, M.N., Wright, N.F., Vann, S.D., Erichsen, J.T., Aggleton, J.P., O’Mara, S.M., 2014. Nucleus reuniens of the thalamus contains head direction cells. eLife 3, e03075. https://doi.org/10.7554/eLife.03075Google Scholar
Jankowski, M.M., Passecker, J., Islam, M.N., Vann, S., Erichsen, J.T., Aggleton, J.P., O’Mara, S.M., 2015. Evidence for spatially-responsive neurons in the rostral thalamus. Front. Behav. Neurosci. 9. https://doi.org/10.3389/fnbeh.2015.00256CrossRefGoogle ScholarPubMed
Jay, T.M., Glowinski, J., Thierry, A.-M., 1989. Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res. 505, 337340. https://doi.org/10.1016/0006-8993(89)91464–9Google Scholar
Johnson, A., Redish, A.D., 2007. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27, 12176.Google Scholar
Jones, B.E., 1993. The organization of central cholinergic systems and their functional importance in sleep-waking states. Prog. Brain Res. 98, 6171. https://doi.org/10.1016/s0079-6123(08)62381-xGoogle Scholar
Jones, E.G., 2007. The Thalamus. Cambridge University Press.Google Scholar
Jones, M.W., Wilson, M.A., 2005. Theta rhythms coordinate hippocampal–prefrontal interactions in a spatial memory task. PLOS Biol. 3, e402. https://doi.org/10.1371/journal.pbio.0030402Google Scholar
Kaitz, S.S., Robertson, R.T., 1981. Thalamic connections with limbic cortex. II. Corticothalamic projections. J. Comp. Neurol. 195, 527545. https://doi.org/10.1002/cne.901950309Google Scholar
Kay, K., Chung, J.E., Sosa, M., Schor, J.S., Karlsson, M.P., Larkin, M.C., Liu, D.F., Frank, L.M., 2020. Constant sub-second cycling between representations of possible futures in the hippocampus. Cell 180, 552–567.e25. https://doi.org/10.1016/j.cell.2020.01.014Google Scholar
Knierim, J.J., Kudrimoti, H.S., McNaughton, B.L., 1995. Place cells, head direction cells, and the learning of landmark stability. J. Neurosci. 15, 16481659.Google Scholar
Kocsis, B., Prisco, G.V.D., Vertes, R.P., 2001. Theta synchronization in the limbic system: the role of Gudden’s tegmental nuclei. Eur. J. Neurosci. 13, 381388. https://doi.org/10.1111/j.1460-9568.2001.tb01708.xGoogle Scholar
Koenig, J., Linder, A.N., Leutgeb, J.K., Leutgeb, S., 2011. The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332, 592595. https://doi.org/10.1126/science.1201685Google Scholar
Kornienko, O., Latuske, P., Bassler, M., Kohler, L., Allen, K., 2018. Non-rhythmic head-direction cells in the parahippocampal region are not constrained by attractor network dynamics. eLife 7, e35949. https://doi.org/10.7554/eLife.35949Google Scholar
Kuypers, H.G., Bentivoglio, M., Catsman-Berrevoets, C.E., Bharos, A.T., 1980. Double retrograde neuronal labeling through divergent axon collaterals, using two fluorescent tracers with the same excitation wavelength which label different features of the cell. Exp. Brain Res. 40, 383392. https://doi.org/10.1007/BF00236147Google Scholar
LaChance, P.A., Todd, T.P., Taube, J.S., 2019. A sense of space in postrhinal cortex. Science 365, eaax4192. https://doi.org/10.1126/science.aax4192Google Scholar
Lee, A.K., Wilson, M.A., 2002. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 11831194.Google Scholar
Leutgeb, S., Leutgeb, J.K., Treves, A., Moser, M.-B., Moser, E.I., 2004. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305, 12951298. https://doi.org/10.1126/science.1100265Google Scholar
Lever, C., Burton, S., Jeewajee, A., O’Keefe, J., Burgess, N., 2009. Boundary vector cells in the subiculum of the hippocampal formation. J. Neurosci. 29, 97719777. https://doi.org/10.1523/JNEUROSCI.1319-09.2009Google Scholar
Levey, A.I., Hallanger, A.E., Wainer, B.H., 1987. Choline acetyltransferase immunoreactivity in the rat thalamus. J. Comp. Neurol. 257, 317332. https://doi.org/10.1002/cne.902570302Google Scholar
Lozsádi, D.A., 1995. Organization of connections between the thalamic reticular and the anterior thalamic nuclei in the rat. J. Comp. Neurol. 358, 233246. https://doi.org/10.1002/cne.903580206Google Scholar
Maisson, D.J.-N., Gemzik, Z.M., Griffin, A.L., 2018. Optogenetic suppression of the nucleus reuniens selectively impairs encoding during spatial working memory. Neurobiol. Learn. Mem. 155, 7885. https://doi.org/10.1016/j.nlm.2018.06.010Google Scholar
Markus, E.J., Qin, Y.L., Leonard, B., Skaggs, W.E., McNaughton, B.L., Barnes, C.A., 1995. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J. Neurosci. 15, 70797094. https://doi.org/10.1523/JNEUROSCI.15-11-07079.1995Google Scholar
Mathiasen, M.L., Amin, E., Nelson, A.J.D., Dillingham, C.M., O’Mara, S.M., Aggleton, J.P., 2019. Separate cortical and hippocampal cell populations target the rat nucleus reuniens and mammillary bodies. Eur. J. Neurosci. 49, 16491672. https://doi.org/10.1111/ejn.14341Google Scholar
Maurer, A.P., Cowen, S.L., Burke, S.N., Barnes, C.A., McNaughton, B.L., 2006. Phase precession in hippocampal interneurons showing strong functional coupling to individual pyramidal cells. J. Neurosci. 26, 1348513492. https://doi.org/10.1523/JNEUROSCI.2882–06.2006Google Scholar
McKenna, J.T., Vertes, R.P., 2004. Afferent projections to nucleus reuniens of the thalamus. J. Comp. Neurol. 480, 115142. https://doi.org/10.1002/cne.20342Google Scholar
McNaughton, B.L., Barnes, C.A., Gerrard, J.L., Gothard, K., Jung, M.W., Knierim, J.J., Kudrimoti, H., Qin, Y., Skaggs, W.E., Suster, M., Weaver, K.L., 1996. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J. Exp. Biol. 199, 173.Google Scholar
McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I., Moser, M.-B., 2006. Path integration and the neural basis of the “cognitive map.” Nat. Rev. Neurosci. 7, 663678. https://doi.org/10.1038/nrn1932Google Scholar
Mei, H., Logothetis, N.K., Eschenko, O., 2018. The activity of thalamic nucleus reuniens is critical for memory retrieval, but not essential for the early phase of “off-line” consolidation. Learn. Mem. 25, 129137. https://doi.org/10.1101/lm.047134.117Google Scholar
Meibach, R.C., Siegel, A., 1977. Efferent connections of the hippocampal formation in the rat. Brain Res. 124, 197224. https://doi.org/10.1016/0006-8993(77)90880-0Google Scholar
Mitchell, A.S., Dalrymple-Alford, J.C., Christie, M.A., 2002. Spatial working memory and the brainstem cholinergic innervation to the anterior thalamus. J. Neurosci. 22, 19221928. https://doi.org/10.1523/JNEUROSCI.22-05-01922.2002Google Scholar
Mittelstaedt, M.L., Mittelstaedt, H., 1980. Homing by path integration in a mammal. Naturwissenschaften 67, 566567. https://doi.org/10.1007/bf00450672Google Scholar
Mizumori, S.J., Williams, J.D., 1993. Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J. Neurosci. 13, 40154028.Google Scholar
Moruzzi, G., Magoun, H.W., 1949. Brain stem reticular formation and activation of the EEG. Electroencephalogr. Clin. Neurophysiol. 1, 455473. https://doi.org/10.1016/0013-4694(49)90219-9Google Scholar
Muir, G.M., Brown, J.E., Carey, J.P., Hirvonen, T.P., Santina, C.C.D., Minor, L.B., Taube, J.S., 2009. Disruption of the head direction cell signal after occlusion of the semicircular canals in the freely moving chinchilla. J. Neurosci. 29, 1452114533. https://doi.org/10.1523/JNEUROSCI.3450-09.2009Google Scholar
Muller, R.U., Bostock, E., Taube, J.S., Kubie, J.L., 1994. On the directional firing properties of hippocampal place cells. J. Neurosci. 14, 72357251.Google Scholar
Muller, R.U., Kubie, J.L., 1987. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 19511968.Google Scholar
Musil, S.Y., Olson, C.R., 1988. Organization of cortical and subcortical projections to anterior cingulate cortex in the cat. J. Comp. Neurol. 272, 203218. https://doi.org/10.1002/cne.902720205Google Scholar
Nadel, L., Moscovitch, M., 1997. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol. 7, 217227. https://doi.org/10.1016/s0959-4388(97)80010-4Google Scholar
Nelson, A.J.D., Kinnavane, L., Amin, E., O’Mara, S.M., Aggleton, J.P., 2020. Deconstructing the direct reciprocal hippocampal-anterior thalamic pathways for spatial learning. J. Neurosci. 40, 69786990. https://doi.org/10.1523/JNEUROSCI.0874-20.2020Google Scholar
Niimi, M., 1978. Cortical projections of the anterior thalamic nuclei in the cat. Exp. Brain Res. 31, 403416. https://doi.org/10.1007/BF00237298Google Scholar
Oda, S., Kuroda, M., Chen, S.Y., Shinkai, M., Kishi, K., 1996. Ultrastructure and distribution of axon terminals from the reticular thalamic nucleus to the anteroventral thalamic nucleus of the rat. J. Hirnforsch. 37, 459466.Google Scholar
O’Keefe, J., 1976. Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51, 78109. https://doi.org/10.1016/0014–4886(76)90055–8Google Scholar
O’Keefe, J., Burgess, N., 1996. Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425428. https://doi.org/10.1038/381425a0Google Scholar
O’Keefe, J., Dostrovsky, J., 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171175.CrossRefGoogle ScholarPubMed
O’Keefe, J., Nadel, L., 1978. The Hippocampus as a Cognitive Map. Clarendon Press Oxford.Google Scholar
O’Keefe, J., Recce, M.L., 1993. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317330. https://doi.org/10.1002/hipo.450030307Google Scholar
Papez, J.W., 1937. A proposed mechanism of emotion. Arch. Neurol. Psychiatry 38, 725743. https://doi.org/10.1001/archneurpsyc.1937.02260220069003Google Scholar
Pare, D., Steriade, M., Deschênes, M., Bouhassira, D., 1990. Prolonged enhancement of anterior thalamic synaptic responsiveness by stimulation of a brain-stem cholinergic group. J. Neurosci. 10, 2033. https://doi.org/10.1523/JNEUROSCI.10-01-00020.1990Google Scholar
Perry, B.A.L., Mercer, S.A., Barnett, S.C., Lee, J., Dalrymple‐Alford, J.C., 2018. Anterior thalamic nuclei lesions have a greater impact than mammillothalamic tract lesions on the extended hippocampal system. Hippocampus 28, 121135. https://doi.org/10.1002/hipo.22815Google Scholar
Perry, B.A.L., Mitchell, A.S., 2019. Considering the evidence for anterior and laterodorsal thalamic nuclei as higher order relays to cortex. Front. Mol. Neurosci. 12. https://doi.org/10.3389/fnmol.2019.00167Google Scholar
Petrof, I., Sherman, S.M., 2009. Synaptic properties of the mammillary and cortical afferents to the anterodorsal thalamic nucleus in the mouse. J. Neurosci. 29, 78157819. https://doi.org/10.1523/JNEUROSCI.1564-09.2009Google Scholar
Peyrache, A., Battaglia, F.P., Destexhe, A., 2011. Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs. Proc. Natl. Acad. Sci. 108, 1720717212. https://doi.org/10.1073/pnas.1103612108Google Scholar
Peyrache, A., Duszkiewicz, A.J., Viejo, G., Angeles-Duran, S., 2019. Thalamocortical processing of the head-direction sense. Prog. Neurobiol. 183, 101693. https://doi.org/10.1016/j.pneurobio.2019.101693Google Scholar
Peyrache, A., Khamassi, M., Benchenane, K., Wiener, S.I., Battaglia, F.P., 2009. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat. Neurosci. 12, 919926. https://doi.org/10.1038/nn.2337Google Scholar
Peyrache, A., Lacroix, M.M., Petersen, P.C., Buzsáki, G., 2015. Internally organized mechanisms of the head direction sense. Nat. Neurosci. 18, 569575. https://doi.org/10.1038/nn.3968Google Scholar
Peyrache, A., Schieferstein, N., Buzsáki, G., 2017. Transformation of the head-direction signal into a spatial code. Nat. Commun. 8, 1752. https://doi.org/10.1038/s41467-017-01908-3Google Scholar
Peyrache, A., Seibt, J., 2020. A mechanism for learning with sleep spindles. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190230. https://doi.org/10.1098/rstb.2019.0230Google Scholar
Phillips, J.W., Schulmann, A., Hara, E., Winnubst, J., Liu, C., Valakh, V., Wang, L., Shields, B.C., Korff, W., Chandrashekar, J., Lemire, A.L., Mensh, B., Dudman, J.T., Nelson, S.B., Hantman, A.W., 2019. A repeated molecular architecture across thalamic pathways. Nat. Neurosci. 22, 19251935. https://doi.org/10.1038/s41593-019-0483-3Google Scholar
Pisokas, I., Heinze, S., Webb, B., 2020. The head direction circuit of two insect species. eLife 9, e53985. https://doi.org/10.7554/eLife.53985Google Scholar
Powell, T.P.S., Cowan, W.M., 1954. The origin of the mamillo-thalamic tract in the rat. J. Anat. 88, 489497.Google Scholar
Preuss, T.M., 1995. Do rats have prefrontal cortex? The Rose-Woolsey-Akert Program reconsidered. J. Cogn. Neurosci. 7, 124. https://doi.org/10.1162/jocn.1995.7.1.1Google Scholar
Ranck, J.B., 1985. Head direction cells in the deep cell layer of dorsal presubiculum in freely moving rats. In: Buzsáki, G., Vanderwolf, C. H. (Eds.), Electrical Activity of Archicortex. Akademiai Kiado, pp. 217220.Google Scholar
Raudies, F., Brandon, M.P., Chapman, G.W., Hasselmo, M.E., 2015. Head direction is coded more strongly than movement direction in a population of entorhinal neurons. Brain Res. 1621, 355367. https://doi.org/10.1016/j.brainres.2014.10.053Google Scholar
Redish, A.D., 2016. Vicarious trial and error. Nat. Rev. Neurosci. 17, 147159. https://doi.org/10.1038/nrn.2015.30CrossRefGoogle ScholarPubMed
Redish, A.D., Elga, A.N., Touretzky, D.S., 1996. A coupled attractor model of the rodent head direction system. Netw. Comput. Neural Syst. 7, 671685. https://doi.org/10.1088/0954-898X_7_4_004Google Scholar
Robertson, R.T., Kaitz, S.S., 1981. Thalamic connections with limbic cortex. I. Thalamocortical projections. J. Comp. Neurol. 195, 501525. https://doi.org/10.1002/cne.901950308Google Scholar
Rosene, D.L., Hoesen, G.V., 1977. Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 198, 315317. https://doi.org/10.1126/science.410102Google Scholar
Rosenstock, J., Field, T.D., Greene, E., 1977. The role of mammillary bodies in spatial memory. Exp. Neurol. 55, 340352. https://doi.org/10.1016/0014-4886(77)90005-XGoogle Scholar
Roy, A., Svensson, F.P., Mazeh, A., Kocsis, B., 2017. Prefrontal-hippocampal coupling by theta rhythm and by 2–5 Hz oscillation in the delta band: the role of the nucleus reuniens of the thalamus. Brain Struct. Funct. 222, 28192830. https://doi.org/10.1007/s00429-017-1374-6Google Scholar
Samsonovich, A., McNaughton, B.L., 1997. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17, 5900.Google Scholar
Sargolini, F., Fyhn, M., Hafting, T., McNaughton, B.L., Witter, M.P., Moser, M.-B., Moser, E.I., 2006. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758762. https://doi.org/10.1126/science.1125572Google Scholar
Satoh, K., Fibiger, H.C., 1986. Cholinergic neurons of the laterodorsal tegmental nucleus: Efferent and afferent connections. J. Comp. Neurol. 253, 277302. https://doi.org/10.1002/cne.902530302Google Scholar
Savelli, F., Yoganarasimha, D., Knierim, J.J., 2008. Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18, 12701282. https://doi.org/10.1002/hipo.20511Google Scholar
Scoville, W.B., Milner, B., 1957. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 1121.Google Scholar
Seidenbecher, T., 2003. Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301, 846850. https://doi.org/10.1126/science.1085818Google Scholar
Seki, M., Zyo, K., 1984. Anterior thalamic afferents from the mamillary body and the limbic cortex in the rat. J. Comp. Neurol. 229, 242256. https://doi.org/10.1002/cne.902290209Google Scholar
Sharp, P.E., 1996. Multiple spatial/behavioral correlates for cells in the rat postsubiculum: multiple regression analysis and comparison to other hippocampal areas. Cereb. Cortex 6, 238259.Google Scholar
Sharp, P.E., Blair, H.T., Cho, J., 2001. The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci. 24, 289294.Google Scholar
Sherman, S.M., Guillery, R.W., 2002. The role of the thalamus in the flow of information to the cortex. Philos. Trans. R. Soc. B Biol. Sci. 357, 16951708. https://doi.org/10.1098/rstb.2002.1161Google Scholar
Shibata, H., 1992. Topographic organization of subcortical projections to the anterior thalamic nuclei in the rat. J. Comp. Neurol. 323, 117127. https://doi.org/10.1002/cne.903230110Google Scholar
Shibata, H., 1993a. Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat. J. Comp. Neurol. 337, 431445. https://doi.org/10.1002/cne.903370307Google Scholar
Shibata, H., 1993b. Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat. J. Comp. Neurol. 330, 533542. https://doi.org/10.1002/cne.903300409Google Scholar
Shibata, H., Kato, A., 1993. Topographic relationship between anteromedial thalamic nucleus neurons and their cortical terminal fields in the rat. Neurosci. Res. 17, 6369. https://doi.org/10.1016/0168–0102(93)90030-tGoogle Scholar
Siapas, A.G., Lubenov, E.V., Wilson, M.A., 2005. Prefrontal phase locking to hippocampal theta oscillations. Neuron 46, 141151. https://doi.org/10.1016/j.neuron.2005.02.028Google Scholar
Siapas, A.G., Wilson, M.A., 1998. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21, 11231128.Google Scholar
Sikes, R.W., Vogt, B.A., 1987. Afferent connections of anterior thalamus in rats: sources and association with muscarinic acetylcholine receptors. J. Comp. Neurol. 256, 538551. https://doi.org/10.1002/cne.902560406Google Scholar
Sirota, A., Csicsvari, J., Buhl, D., Buzsáki, G., 2003. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. U.S.A. 100, 2065.Google Scholar
Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M., Buzsaki, G., 2008. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60, 683697. https://doi.org/10.1016/j.neuron.2008.09.014Google Scholar
Skaggs, W.E., McNaughton, B.L., 1996. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271, 18701873.Google Scholar
Solstad, T., Boccara, C.N., Kropff, E., Moser, M.-B., Moser, E.I., 2008. Representation of geometric borders in the entorhinal cortex. Science 322, 18651868. https://doi.org/10.1126/science.1166466Google Scholar
Squire, L.R., 1992. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195231. https://doi.org/10.1037/0033-295x.99.2.195Google Scholar
Sripanidkulchai, K., Wyss, J.M., 1986. Thalamic projections to retrosplenial cortex in the rat. J. Comp. Neurol. 254, 143165. https://doi.org/10.1002/cne.902540202Google Scholar
Stackman, R.W., Taube, J.S., 1998. Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity. J. Neurosci. 18, 90209037.Google Scholar
Stark, E., Eichler, R., Roux, L., Fujisawa, S., Rotstein, H.G., Buzsáki, G., 2013. Inhibition-induced theta resonance in cortical circuits. Neuron 80, 12631276. https://doi.org/10.1016/j.neuron.2013.09.033Google Scholar
Steriade, M., McCormick, D.A., Sejnowski, T.J., 1993. Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679685.Google Scholar
Sutherland, R.J., Rodriguez, A.J., 1989. The role of the fornix/fimbria and some related subcortical structures in place learning and memory. Behav. Brain Res. 32, 265277. https://doi.org/10.1016/S0166-4328(89)80059–2Google Scholar
Swanson, L.W., Cowan, W.M., 1977. An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. Comp. Neurol. 172, 4984. https://doi.org/10.1002/cne.901720104Google Scholar
Swanson, L.W., Cowan, W.M., 1979. The connections of the septal region in the rat. J. Comp. Neurol. 186, 621655. https://doi.org/10.1002/cne.901860408Google Scholar
Sziklas, V., Petrides, M., 1998. Memory and the region of the mammillary bodies. Prog. Neurobiol. 54, 5570. https://doi.org/10.1016/S0301-0082(97)00064-6Google Scholar
Taube, J.S., 1995. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 15, 7086.Google Scholar
Taube, J.S., 2007. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181207. https://doi.org/10.1146/annurev.neuro.29.051605.112854Google Scholar
Taube, J.S., Bassett, J.P., 2003. Persistent neural activity in head direction cells. Cereb. Cortex 13, 11621172. https://doi.org/10.1093/cercor/bhg102Google Scholar
Taube, J.S., Muller, R.U., Ranck, J.B., 1990a. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420435.Google Scholar
Taube, J.S., Muller, R.U., Ranck, J.B., Jr, 1990b. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 10, 436447.Google Scholar
Touretzky, D.S., Redish, A.D., 1996. Theory of rodent navigation based on interacting representations of space. Hippocampus 6, 247270. https://doi.org/10.1002/(SICI)1098-1063(1996)6:3%3C247::aid-hipo4%3E3.0.CO;2-KGoogle Scholar
Tsanov, M., Chah, E., Vann, S.D., Reilly, R.B., Erichsen, J.T., Aggleton, J.P., O’Mara, S.M., 2011. Theta-modulated head direction cells in the rat anterior thalamus. J. Neurosci. 31, 94899502. https://doi.org/10.1523/JNEUROSCI.0353-11.2011Google Scholar
Tsanov, M., Wright, N., Vann, S.D., Erichsen, J.T., Aggleton, J.P., O’Mara, S.M., 2011. Hippocampal inputs mediate theta-related plasticity in anterior thalamus. Neuroscience 187, 5262. https://doi.org/16/j.neuroscience.2011.03.055Google Scholar
Uylings, H., Groenewegen, H.J., Kolb, B., 2003. Do rats have a prefrontal cortex? Behav. Brain Res. 146, 317.Google Scholar
Valerio, S., Taube, J.S., 2012. Path integration: how the head direction signal maintains and corrects spatial orientation. Nat. Neurosci. 15, 14451453. https://doi.org/10.1038/nn.3215Google Scholar
van der Meer, M.A.A., Knierim, J.J., Yoganarasimha, D., Wood, E.R., van Rossum, M.C.W., 2007. Anticipation in the rodent head direction system can be explained by an interaction of head movements and vestibular firing properties. J. Neurophysiol. 98, 18831897. https://doi.org/10.1152/jn.00233.2007Google Scholar
van Groen, T., Kadish, I., Wyss, J.M., 1999. Efferent connections of the anteromedial nucleus of the thalamus of the rat. Brain Res. Rev. 30, 126. https://doi.org/10.1016/s0165-0173(99)00006-5Google Scholar
van Groen, T., Kadish, I., Wyss, J.M., 2002. Role of the anterodorsal and anteroventral nuclei of the thalamus in spatial memory in the rat. Behav. Brain Res. 132, 1928. https://doi.org/10.1016/S0166-4328(01)00390-4Google Scholar
van Groen, T., Wyss, J.M., 1995. Projections from the anterodorsal and anteroventral nucleus of the thalamus to the limbic cortex in the rat. J. Comp. Neurol. 358, 584604. https://doi.org/10.1002/cne.903580411Google Scholar
Vanderwolf, C.H., 1969. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407418. https://doi.org/10.1016/0013-4694(69)90092-3Google Scholar
Vann, S.D., Aggleton, J.P., 2004. The mammillary bodies: two memory systems in one? Nat. Rev. Neurosci. 5, 3544. https://doi.org/10.1038/nrn1299Google Scholar
Vann, S.D., Brown, M.W., Aggleton, J.P., 2000. Fos expression in the rostral thalamic nuclei and associated cortical regions in response to different spatial memory tests. Neuroscience 101, 983991. https://doi.org/10.1016/s0306-4522(00)00288-8Google Scholar
Vantomme, G., Rovó, Z., Cardis, R., Béard, E., Katsioudi, G., Guadagno, A., Perrenoud, V., Fernandez, L.M.J., Lüthi, A., 2020. A thalamic reticular circuit for head direction cell tuning and spatial navigation. Cell Rep. 31, 107747. https://doi.org/10.1016/j.celrep.2020.107747Google Scholar
Varela, C., Kumar, S., Yang, J.Y., Wilson, M.A., 2014. Anatomical substrates for direct interactions between hippocampus, medial prefrontal cortex, and the thalamic nucleus reuniens. Brain Struct. Funct. 219, 911929. https://doi.org/10.1007/s00429-013-0543-5Google Scholar
Varela, C., Wilson, M.A., 2020. mPFC spindle cycles organize sparse thalamic activation and recently active CA1 cells during non-REM sleep. eLife 9, e48881. https://doi.org/10.7554/eLife.48881Google Scholar
Veazey, R.B., Amaral, D.G., Cowan, W.M., 1982. The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). II. Efferent connections.J. Comp. Neurol. 207, 135156. https://doi.org/10.1002/cne.902070204Google Scholar
Vertes, R.P., Albo, Z., Prisco, Viana Di, G., 2001. Theta-rhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez’s circuit. Neuroscience 104, 619625. https://doi.org/10.1016/S0306-4522(01)00131-2Google Scholar
Vertes, R.P., Hoover, W.B., Szigeti-Buck, K., Leranth, C., 2007. Nucleus reuniens of the midline thalamus: Link between the medial prefrontal cortex and the hippocampus. Brain Res. Bull. 71, 601609.Google Scholar
Viejo, G., Cortier, T., Peyrache, A., 2018. Brain-state invariant thalamo-cortical coordination revealed by non-linear encoders. PLOS Comput. Biol. 14, e1006041. https://doi.org/10.1371/journal.pcbi.1006041Google Scholar
Viejo, G., Peyrache, A., 2020. Precise coupling of the thalamic head-direction system to hippocampal ripples. Nat. Commun. 11, 2524. https://doi.org/10.1038/s41467-020-15842-4Google Scholar
Walz, N., Mühlberger, A., Pauli, P., 2016. A human open field test reveals thigmotaxis related to agoraphobic fear. Biol. Psychiatry 80, 390397. https://doi.org/10.1016/j.biopsych.2015.12.016Google Scholar
Wang, B., Gonzalo-Ruiz, A., Sanz, J.M., Campbell, G., Lieberman, A.R., 1999. Immunoelectron microscopic study of gamma-aminobutyric acid inputs to identified thalamocortical projection neurons in the anterior thalamus of the rat. Exp. Brain Res. 126, 369382. https://doi.org/10.1007/s002210050744Google Scholar
Watanabe, K., Kawana, E., 1980. A horseradish peroxidase study on the mammillothalamic tract in the rat. Cells Tissues Organs 108, 394401. https://doi.org/10.1159/000145322Google Scholar
Weel, M.J.D.-V. der, Silva, F.H.L. da, Witter, M.P., 1997. Nucleus reuniens thalami modulates activity in hippocampal field CA1 through excitatory and inhibitory mechanisms. J. Neurosci. 17, 56405650. https://doi.org/10.1523/JNEUROSCI.17-14-05640.1997Google Scholar
Welday, A.C., Shlifer, I.G., Bloom, M.L., Zhang, K., Blair, H.T., 2011. Cosine directional tuning of theta cell burst frequencies: evidence for spatial coding by oscillatory interference. J. Neurosci. 31, 1615716176. https://doi.org/10.1523/JNEUROSCI.0712-11.2011Google Scholar
Wierzynski, C.M., Lubenov, E.V., Gu, M., Siapas, A.G., 2009. State-dependent Spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 61, 587596. https://doi.org/10.1016/j.neuron.2009.01.011Google Scholar
Wilson, M.A., McNaughton, B.L., 1994. Reactivation of hippocampal ensemble memories during sleep. Science 265, 676.Google Scholar
Wiltschko, A.B., Johnson, M.J., Iurilli, G., Peterson, R.E., Katon, J.M., Pashkovski, S.L., Abraira, V.E., Adams, R.P., Datta, S.R., 2015. Mapping sub-second structure in mouse behavior. Neuron 88, 11211135. https://doi.org/10.1016/j.neuron.2015.11.031Google Scholar
Wimmer, R.D., Schmitt, L.I., Davidson, T.J., Nakajima, M., Deisseroth, K., Halassa, M.M., 2015. Thalamic control of sensory selection in divided attention. Nature 526, 705709. https://doi.org/10.1038/nature15398Google Scholar
Winter, S.S., Clark, B.J., Taube, J.S., 2015. Disruption of the head direction cell network impairs the parahippocampal grid cell signal. Science 347, 870874. https://doi.org/10.1126/science.1259591Google Scholar
Wood, E.R., Dudchenko, P.A., Robitsek, R.J., Eichenbaum, H., 2000. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623633. https://doi.org/10.1016/S0896-6273(00)00071-4Google Scholar
Wright, N.F., Erichsen, J.T., Vann, S.D., O’Mara, S.M., Aggleton, J.P., 2010. Parallel but separate inputs from limbic cortices to the mammillary bodies and anterior thalamic nuclei in the rat. J. Comp. Neurol. 518, 23342354. https://doi.org/10.1002/cne.22336Google Scholar
Wright, N.F., Vann, S.D., Erichsen, J.T., O’Mara, S.M., Aggleton, J.P., 2013. Segregation of parallel inputs to the anteromedial and anteroventral thalamic nuclei of the rat. J. Comp. Neurol. 521, 29662986. https://doi.org/10.1002/cne.23325Google Scholar
Xu, W., Südhof, T.C., 2013. A neural circuit for memory specificity and generalization. Science 339, 12901295. https://doi.org/10.1126/science.1229534Google Scholar
Yoder, R.M., Taube, J.S., 2011. Projections to the anterodorsal thalamus and lateral mammillary nuclei arise from different cell populations within the postsubiculum: Implications for the control of head direction cells. Hippocampus 21, 10621073. https://doi.org/10.1002/hipo.20820Google Scholar
Yoganarasimha, D., Yu, X., Knierim, J.J., 2006. Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J. Neurosci. 26, 622631. https://doi.org/10.1523/JNEUROSCI.3885-05.2006Google Scholar
Zugaro, M.B., Berthoz, A., Wiener, S.I., 2001. Background, but not foreground, spatial cues are taken as references for head direction responses by rat anterodorsal thalamus neurons. J. Neurosci. 21, RC154.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×