Abstract
Orientation in space is a fundamental cognitive process relying on brain-wide neuronal circuits. Many neurons in the presubiculum in the parahippocampal region encode head direction and each head direction cell selectively discharges when the animal faces a specific direction. Here, we attempt to link the current knowledge of afferent and efferent connectivity of the presubiculum to the processing of the head direction signal. We describe the cytoarchitecture of the presubicular six-layered cortex and the morphological and electrophysiological intrinsic properties of principal neurons and interneurons. While the presubicular head direction signal depends on synaptic input from thalamus, the intra- and interlaminar information flow in the microcircuit of the presubiculum may contribute to refine directional tuning. The interaction of a specific interneuron type, the Martinotti cells, with the excitatory pyramidal cells may maintain the head direction signal in the presubiculum with attractor-like properties.
Similar content being viewed by others
References
Abbasi S, Kumar SS (2013) Electrophysiological and morphological characterization of cells in superficial layers of rat presubiculum. J Comp Neurol 521:3116–3132
Allen GV, Hopkins DA (1989) Mamillary body in the rat: topography and synaptology of projections from the subicular complex, prefrontal cortex, and midbrain tegmentum. J Comp Neurol 286:311–336
Angevine JB, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766–768
Bartesaghi R, Gessi T, Sperti L (1988) Electrophysiological analysis of the dorsal hippocampal commissure projections to the entorhinal area. Neuroscience 26:55–67
Bassett JP, Tullman ML, Taube JS (2007) Lesions of the tegmentomammillary circuit in the head direction system disrupt the head direction signal in the anterior thalamus. J Neurosci 27:7564–7577
Bayer SA (1980) Development of the hippocampal region in the rat I. Neurogenesis examined with3H-thymidine autoradiography. J Comp Neurol 190:87–114
Bean BP (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8:451–465
Beckstead RM (1978) Afferent connections of the entorhinal area in the rat as demonstrated by retrograde cell-labeling with horseradish peroxidase. Brain Res 152:249–264
Bezdudnaya T, Keller A (2008) Laterodorsal nucleus of the thalamus: a processor of somatosensory inputs. J Comp Neurol 507:1979–1989
Bjerknes TL, Langston RF, Kruge IU, Moser EI, Moser M-B (2015) Coherence among head direction cells before eye opening in rat pups. Curr Biol 25:103–108
Blackstad TW (1956) Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J Comp Neurol 105:417–537
Blair HT (1996) Simulation of a thalamocortical circuit for computing directional heading in the rat. Adv Neural Inf Process Syst 8:152–158
Blair HT, Sharp PE (1995) Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction. J Neurosci 15:6260–6270
Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, Moser M-B (2010) Grid cells in pre- and parasubiculum. Nat Neurosci 13:987–994
Boccara CN, Kjonigsen LJ, Hammer IM, Bjaalie JG, Leergaard TB, Witter MP (2015) A three-plane architectonic atlas of the rat hippocampal region. Hippocampus 25(7):838–857
Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D, Kubie JL, Roudi Y, Moser EI, Moser M-B (2013) Grid cells require excitatory drive from the hippocampus. Nat Neurosci 16:309–317
Brodmann K (1909) Vergleichende Lokalisationslehre der Grosshirnrinde. Barth-Verlag, Leipzig. Translated version: Brodmann K, Garey L (2006) Brodmann’s Localisation in the cerebral cortex: the principles of comparative localisation in the cerebral cortex based on the cytoarchitectonics. Springer, New York
Buzsáki G, Moser EI (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16:130–138
Caballero-Bleda M, Witter MP (1993) Regional and laminar organization of projections from the presubiculum and parasubiculum to the entorhinal cortex: an anterograde tracing study in the rat. J Comp Neurol 328:115–129
Caballero-Bleda M, Witter MP (1994) Projections from the presubiculum and the parasubiculum to morphologically characterized entorhinal-hippocampal projection neurons in the rat. Exp Brain Res 101:93–108
Cajal SRY (1899) Textura del sistema nervioso del hombre y de los vertebrados. Moya, Madrid. English translation: Histology of the Nervous System of Man and Vertebrates (Oxford University Press, New York, 1995)
Calton JL, Stackman RW, Goodridge JP, Archey WB, Dudchenko PA, Taube JS (2003) Hippocampal place cell instability after lesions of the head direction cell network. J Neurosci 23:9719–9731
Canto CB, Koganezawa N, Beed P, Moser EI, Witter MP (2012) All layers of medial entorhinal cortex receive presubicular and parasubicular inputs. J Neurosci 32:17620–17631
Cenquizca LA, Swanson LW (2007) Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Neuroscience 56:1–26
Cho J, Sharp PE (2001) Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav Neurosci 115:3–25
Clark BJ, Taube JS (2012) Vestibular and attractor network basis of the head direction cell signal in subcortical circuits. Front Neural Circuits 6:7
Dillingham CM, Erichsen JT, O’Mara SM, Aggleton JP, Vann SD (2015) Fornical and nonfornical projections from the rat hippocampal formation to the anterior thalamic nuclei. Hippocampus 25:977–992
Ding S-L (2013) Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum and parasubiculum in human, monkey and rodent. J Comp Neurol 521(18):4145–4162
Ding SL, Rockland KS (2001) Modular organization of the monkey presubiculum. Exp Brain Res 139:255–265
Doeller CF, Barry C, Burgess N (2010) Evidence for grid cells in a human memory network. Nature 463:657–661
Filimonoff IN (1947) A rational subdivision of the cerebral cortex. Arch Neurol Psychiatr 58:296–311
Finkelstein A, Derdikman D, Rubin A, Foerster JN, Las L, Ulanovsky N (2015) Three-dimensional head-direction coding in the bat brain. Nature 517:159–164
Fricker D, Dinocourt C, Eugène E, Wood JN, Wood J, Miles R (2009) Pyramidal cells of rodent presubiculum express a tetrodotoxin-insensitive Na+ current. J Physiol Lond 587:4249–4264
Funahashi M, Stewart M (1997) Presubicular and parasubicular cortical neurons of the rat: functional separation of deep and superficial neurons in vitro. J Physiol Lond 501:387–403
Funahashi M, Harris E, Stewart M (1999) Re-entrant activity in a presubiculum-subiculum circuit generates epileptiform activity in vitro. Brain Res 849:139–146
Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M (2005) Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48:315–327
Golob EJ, Wolk DA, Taube JS (1998) Recordings of postsubiculum head direction cells following lesions of the laterodorsal thalamic nucleus. Brain Res 780:9–19
Gonzalez-Sulser A, Parthier D, Candela A, McClure C, Pastoll H, Garden D, Surmeli G, Nolan MF (2014) GABAergic projections from the medial septum selectively inhibit interneurons in the medial entorhinal cortex. J Neurosci 34:16739–16743
Gonzalo-Ruiz A, Alonso A, Sanz JM, Llinás RR (1992) Afferent projections to the mammillary complex of the rat, with special reference to those from surrounding hypothalamic regions. J Comp Neurol 321:277–299
Goodridge JP, Taube JS (1997) Interaction between the postsubiculum and anterior thalamus in the generation of head direction cell activity. J Neurosci 17:9315–9330
Goodridge JP, Touretzky DS (2000) Modeling attractor deformation in the rodent head-direction system. J Neurophysiol 83:3402–3410
Goodridge JP, Dudchenko PA, Worboys KA, Golob EJ, Taube JS (1998) Cue control and head direction cells. Behav Neurosci 112:749–761
Harland B, Grieves RM, Bett D, Stentiford R, Wood ER, Dudchenko PA (2017) Lesions of the head direction cell system increase hippocampal place field repetition. Curr Biol 27:2706–2712.e2
Honda Y, Ishizuka N (2004) Organization of connectivity of the rat presubiculum: I. Efferent projections to the medial entorhinal cortex. J Comp Neurol 473:463–484
Honda Y, Shibata H (2017) Organizational connectivity among the CA1, subiculum, presubiculum, and entorhinal cortex in the rabbit. J Comp Neurol 525:3705–3741
Honda Y, Umitsu Y, Ishizuka N (2008) Organization of connectivity of the rat presubiculum: II. Associational and commissural connections. J Comp Neurol 506:640–658
Honda Y, Furuta T, Kaneko T, Shibata H, Sasaki H (2011) Patterns of axonal collateralization of single layer V cortical projection neurons in the rat presubiculum. J Comp Neurol 519:1395–1412
Huang L-W, Simonnet J, Nassar M, Richevaux L, Lofredi R, Fricker D (2017) Laminar localization and projection-specific properties of presubicular neurons targeting the lateral mammillary nucleus, thalamus, or medial entorhinal cortex. Eneuro 4, ENEURO.0370-16.2017
Isaacson JS, Scanziani M (2011) How inhibition shapes cortical activity. Neuron 72:231–243
Ishihara Y, Fukuda T (2016) Immunohistochemical investigation of the internal structure of the mouse subiculum. Neuroscience 337:1–25
Ishizuka N (2001) Laminar organization of the pyramidal cell layer of the subiculum in the rat. J Comp Neurol 435:89–110
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 20:173–175
Jacobs J, Weidemann CT, Miller JF, Solway A, Burke JF, Wei X-X, Suthana N, Sperling MR, Sharan AD, Fried I, Kahana MJ (2013) Direct recordings of grid-like neuronal activity in human spatial navigation. Nat Neurosci 16:1188–1190
Jarrard LE (1993) On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 60:9–26
Jones BF, Witter MP (2007) Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat. Hippocampus 17:957–976
Killian NJ, Jutras MJ, Buffalo EA (2012) A map of visual space in the primate entorhinal cortex. Nature 491(7426):761–764
Kim Y, Spruston N (2011) Target-specific output patterns are predicted by the distribution of regular-spiking and bursting pyramidal neurons in the subiculum. Hippocampus 22(4):693–706
Knierim JJ, Zhang K (2012) Attractor dynamics of spatially correlated neural activity in the limbic system. Annu Rev Neurosci 35:267–285
Knierim JJ, Kudrimoti HS, McNaughton BL (1995) Place cells, head direction cells, and the learning of landmark stability. J Neurosci 15:1648–1659
Köhler C (1984) Morphological details of the projection from the presubiculum to the entorhinal area as shown with the novel PHA-L immunohistochemical tracing method in the rat. Neurosci Lett 45:285–290
Köhler C (1985) Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. J Comp Neurol 236:504–522
Kondo H, Witter MP (2014) Topographic organization of orbitofrontal projections to the parahippocampal region in rats. J Comp Neurol 522:772–793
Kononenko NL, Witter MP (2012) Presubiculum layer III conveys retrosplenial input to the medial entorhinal cortex. Hippocampus 22:881–895. https://doi.org/10.1002/hipo.20949
Kosel KC, Van Hoesen GW, Rosene DL (1983) A direct projection from the perirhinal cortex (area 35) to the subiculum in the rat. Brain Res 269:347–351
Lampl I, Katz Y (2017) Neuronal adaptation in the somatosensory system of rodents. Neuroscience 343:66–76
Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL, Witter MP, Moser EI, Moser M-B (2010) Development of the spatial representation system in the rat. Science 328:1576–1580
Lorente de No R (1933) Studies on the structure of the cerebral cortex. Journal für Psychologie und Neurologie Bd 45:381–438
Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RS, Frith CD (2000) Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A 97:4398–4403
Major G, Larkum ME, Schiller J (2013) Active properties of neocortical pyramidal neuron dendrites. Annu Rev Neurosci 36:1–24
McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser M-B (2006) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7:663–678
Menendez De La Prida L, Suarez F, Pozo M (2003) Electrophysiological and morphological diversity of neurons from the rat subicular complex in vitro. Hippocampus 13:728–744
Mizumori SJ, Williams JD (1993) Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J Neurosci 13:4015–4028
Muir GM, Brown JE, Carey JP, Hirvonen TP, Santina Della CC, Minor LB, Taube JS (2009) Disruption of the head direction cell signal after occlusion of the semicircular canals in the freely moving chinchilla. J Neurosci 29:14521–14533
Nassar M, Simonnet J, Lofredi R, Cohen I, Savary E, Yanagawa Y, Miles R, Fricker D (2015) Diversity and overlap of parvalbumin and somatostatin expressing interneurons in mouse presubiculum. Front Neural Circuits 9:1–19
Nassar M, Simonnet J, Huang LW, Mathon B, Cohen I, Beraneck M, Miles R, Fricker D (2018) Anterior thalamic nuclei provide excitation and PV mediated feed-forward inhibition onto presubicular layer 3 neurons. bioRxiv. https://doi.org/10.1101/243022
Nishikawa S, Goto S, Hamasaki T, Yamada K, Ushio Y (2002) Involvement of reelin and Cajal-Retzius cells in the developmental formation of vertical columnar structures in the cerebral cortex: evidence from the study of mouse presubicular cortex. Cereb Cortex 12:1024–1030
O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford
O’Mara SM, Commins S, Anderson M, Gigg J (2001) The subiculum: a review of form, physiology and function. Prog Neurobiol 64:129–155
Paxinos G, Franklin KBJ (2013) Paxinos and Franklin’s The mouse brain in stereotaxic coordinates. Academic Press, Elsevier
Peng Y, Tomás B, Federico J, Klisch C, Vida I, Geiger JR (2017) Layer-specific organization of local excitatory and inhibitory synaptic connectivity in the rat presubiculum. Cereb Cortex 27(4):2435–2452
Peyrache A, Lacroix MM, Petersen PC, Buzsáki G (2015) Internally organized mechanisms of the head direction sense. Nat Neurosci 18:569–575
Pouille F, Scanziani M (2004) Routing of spike series by dynamic circuits in the hippocampus. Nature 429:717–723
Preston-Ferrer P, Coletta S, Frey M, Burgalossi A (2016) Anatomical organization of presubicular head-direction circuits. elife 5:e14592
Rakic P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425–427
Ranck JJ (1984) Head direction cells in the deep layer of dorsal presubiculum in freely moving rats. Soc Neurosci Abstr 10:599
Ray S, Burgalossi A, Brecht M, Naumann RK (2017) Complementary modular microcircuits of the rat medial entorhinal cortex. Front Syst Neurosci 11:20. https://doi.org/10.3389/fnsys.2017.00020
Redish AD, Elga AN, Touretzky DS (1996) A coupled attractor model of the rodent head direction system. Netw Comput Neural Syst 7:671–685
Robertson RG, Rolls ET, Georges-François P, Panzeri S (1999) Head direction cells in the primate pre-subiculum. Hippocampus 9:206–219
Rose M (1926) Über das histogenetische Prinzip der Einteilung der Großhirnrinde. J Psychol Neurol 32:97–160
Rose JE, Woolsey CN (1948) Structure and relations of limbic cortex and anterior thalamic nuclei in rabbit and cat. J Comp Neurol 89:279–347
Rowland DC, Weible AP, Wickersham IR, Wu H, Mayford M, Witter MP, Kentros CG (2013) Transgenically targeted rabies virus demonstrates a major monosynaptic projection from hippocampal area CA2 to medial entorhinal layer II neurons. J Neurosci 33:14889–14898
Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser M-B, Moser EI (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758–762
Sharp PE, Blair HT, Cho J (2001a) The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci 24:289–294
Sharp PE, Tinkelman A, Cho J (2001b) Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of gudden in the rat: implications for path integration in the head direction cell circuit. Behav Neurosci 115:571–588
Shibata H (1993) Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat. J Comp Neurol 337:431–445
Shibata H, Honda Y (2012) Thalamocortical projections of the anterodorsal thalamic nucleus in the rabbit. J Comp Neurol 520:2647–2656
Shibata H, Honda Y (2015) Thalamocortical projections of the anteroventral thalamic nucleus in the rabbit. J Comp Neurol 523:726–741
Shires KL, Hawthorne JP, Hope AMJ, Dudchenko PA, Wood ER, Martin SJ (2013) Functional connectivity between the thalamus and postsubiculum: analysis of evoked responses elicited by stimulation of the laterodorsal thalamic nucleus in anesthetized rats. Hippocampus 23:559–569
Simonnet J, Eugène E, Cohen I, Miles R, Fricker D (2013) Cellular neuroanatomy of rat presubiculum. Eur J Neurosci 37:583–597
Simonnet J, Nassar M, Stella F, Cohen I, Mathon B, Boccara CN, Miles R, Fricker D (2017) Activity dependent feedback inhibition may maintain head direction signals in mouse presubiculum. Nat Comms 8:16032
Skaggs WE, Knierim JJ, Kudrimoti HS, McNaughton BL (1995) A model of the neural basis of the rat’s sense of direction. Adv Neural Inf Process Syst 7:173–180
Slomianka L, Geneser FA (1991) Distribution of acetylcholinesterase in the hippocampal region of the mouse: I. Entorhinal area, parasubiculum, retrosplenial area, and presubiculum. J Comp Neurol 303:339–354
Song P, Wang X-J (2005) Angular path integration by moving “hill of activity”: a spiking neuron model without recurrent excitation of the head-direction system. J Neurosci 25:1002–1014
Sorensen KE, Shipley MT (1979) Projections from the subiculum to the deep layers of the ipsilateral presubicular and entorhinal cortices in the guinea pig. J Comp Neurol 188:313–333
Stackman RW, Taube JS (1997) Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J Neurosci 17:4349–4358
Stackman RW, Taube JS (1998) Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity. J Neurosci 18:9020–9037
Sugar J, Witter MP (2016) Postnatal development of retrosplenial projections to the parahippocampal region of the rat. elife 5:1–58
Swanson LW, Cowan WM (1977) An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172:49–84
Tan HM, Bassett JP, O’keefe J, Cacucci F, Wills TJ (2015) The development of the head direction system before eye opening in the rat. Curr Biol 25(4):479–483
Taube JS (1995) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70–86
Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181–207
Taube JS, Muller RU (1998) Comparisons of head direction cell activity in the postsubiculum and anterior thalamus of freely moving rats. Hippocampus 8:87–108
Taube JS, Muller RU, Ranck JB (1990a) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10:420–435
Taube JS, Muller RU, Ranck JB (1990b) Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci 10:436–447
Taube JS, Kesslak JP, Cotman CW (1992) Lesions of the rat postsubiculum impair performance on spatial tasks. Behav Neural Biol 57:131–143
Tukker JJ, Tang Q, Burgalossi A, Brecht M (2015) Head-directional tuning and theta modulation of anatomically identified neurons in the presubiculum. J Neurosci 35:15391–15395
van Groen T, Wyss JM (1990a) The connections of presubiculum and parasubiculum in the rat. Brain Res 518:227–243
van Groen T, Wyss JM (1990b) The postsubicular cortex in the rat: characterization of the fourth region of the subicular cortex and its connections. Brain Res 529:165–177
van Groen T, Wyss JM (1990c) Connections of the retrosplenial granular a cortex in the rat. J Comp Neurol 300:593–606
van Groen T, Wyss JM (1992) Projections from the laterodorsal nucleus of the thalamus to the limbic and visual cortices in the rat. J Comp Neurol 324:427–448
van Groen T, Wyss JM (1995) Projections from the anterodorsal and anteroventral nucleus of the thalamus to the limbic cortex in the rat. J Comp Neurol 358:584–604
van Groen T, Kadish I, Wyss JM (1999) Efferent connections of the anteromedial nucleus of the thalamus of the rat. Brain Res Brain Res Rev 30:1–26
van Haeften T, Wouterlood FG, Jorritsma-Byham B, Witter MP (1997) GABAergic presubicular projections to the medial entorhinal cortex of the rat. J Neurosci 17:862–874
Van Strien NM, Cappaert NLM, Witter MP (2009) The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 10:272–282
Vandecasteele M, Varga V, Berenyi A, Papp E, Barthó P, Venance L, Freund TF, Buzsáki G (2014) Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus. Proc Natl Acad Sci U S A 111:13535–13540
Vogt BA, Miller MW (1983) Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J Comp Neurol 216:192–210
Wang Q, Ng L, Harris JA, Feng D, Li Y, Royall JJ, Oh SW, Bernard A, Sunkin SM, Koch C, Zeng H (2017) Organization of the connections between claustrum and cortex in the mouse. J Comp Neurol 525:1317–1346
Whitmire CJ, Stanley GB (2016) Rapid sensory adaptation redux: a circuit perspective. Neuron 92:298–315
Wiener SI, Taube JS (2005) Head direction cells and the neural mechanisms of spatial orientation. Bradford Books. The MIT Press, Cambridge
Wills TJ, Cacucci F, Burgess N, O’keefe J (2010) Development of the hippocampal cognitive map in preweanling rats. Science 328:1573–1576
Winter SS, Clark BJ, Taube JS (2015) Spatial navigation. Disruption of the head direction cell network impairs the parahippocampal grid cell signal. Science 347:870–874
Witter MP, Amaral DG (2004) The hippocampal formation. In: The rat nervous system. Elsevier, pp 635–704. https://doi.org/10.1016/B978-012547638-6/50022-5
Wolbers T, Wiener JM, Mallot HA, Buchel C (2007) Differential recruitment of the hippocampus, medial prefrontal cortex, and the human motion complex during path integration in humans. J Neurosci 27:9408–9416
Wyss JM (1981) An autoradiographic study of the efferent connections of the entorhinal cortex in the rat. J Comp Neurol 199:495–512
Wyss JM, van Groen T (1992) Connections between the retrosplenial cortex and the hippocampal formation in the rat: a review. Hippocampus 2:1–11
Yoder RM, Taube JS (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 21:1062–1073
Yoder RM, Clark BJ, Taube JS (2011) Origins of landmark encoding in the brain. Trends Neurosci 34:561–571
Yoder RM, Peck JR, Taube JS (2015) Visual landmark information gains control of the head direction signal at the lateral mammillary nuclei. J Neurosci 35:1354–1367
Yoshida M, Hasselmo ME (2009) Persistent firing supported by an intrinsic cellular mechanism in a component of the head direction system. J Neurosci 29:4945–4952
Zhang K (1996) Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 16:2112–2126
Zugaro MB, Arleo A, Berthoz A, Wiener SI (2003) Rapid spatial reorientation and head direction cells. J Neurosci 23:3478–3482
Acknowledgements
We thank Legado Cajal (Instituto Cajal, Consejo Superior de Investigaciones Científicas-CSIC/Spanish National Research Council, Madrid, Spain) for their permission for the reproduction of figure 493 (Fig. 1c). We would like to thank Yoshiko Honda, François Simon and Mathieu Beraneck for comments.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Simonnet, J., Fricker, D. Cellular components and circuitry of the presubiculum and its functional role in the head direction system. Cell Tissue Res 373, 541–556 (2018). https://doi.org/10.1007/s00441-018-2841-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-018-2841-y