168:, were not simple sensory responses. In these models and their subsequent versions, information about changes in the animal's orientation provided by vestibular and visual motion signals were provided by off-shifted connections, while information from distal cues were provided by learned input connections. Direct evidence for such an organization in insects was recently reported: in mammals it is assumed that the "ring" is distributed, and not a geometric anatomical form. While direct anatomical evidence for such excitatory interconnections between head direction cells is lacking, several predictions from the models have been confirmed, such as how the tuning curves would change during left and right rotations, self-coherent representations during sleep, and changes during drift and reorientation.
184:, in the rat dorsal presubiculum, a structure that lies near the hippocampus on the dorsocaudal brain surface. Ranck reported his discovery in a Society for Neuroscience abstract in 1984. Jeffrey Taube, a postdoctoral fellow working in Ranck's laboratory, made these cells the subject of his research. Taube, Ranck and Bob Muller summarized their findings in a pair of papers in the Journal of Neuroscience in 1990. These seminal papers served as the foundation for all of the work that has been done subsequently. Taube, after taking a position at Dartmouth College, has devoted his career to the study of head direction cells, and been responsible for a number of the most important discoveries, as well as writing several key review papers.
121:, which signal rotations of the head. The HD system integrates the vestibular output to maintain a signal reflecting cumulative rotation. The integration is less than perfect, though, especially for slow head rotations. If an animal is placed on an isolated platform and slowly rotated in the dark, the alignment of the HD system usually shifts a little bit for each rotation. If an animal explores a dark environment with no directional cues, the HD alignment tends to drift slowly and randomly over time.
142:
animals behave like HD cells in intact animals in the absence of light. Also, only a minority of cells recorded in the postsubiculum are HD cells, and many of the others show visual responses. In familiar environments, HD cells show consistent preferred directions across time as long as there is a polarizing cue of some sort that allows directions to be identified (in a cylinder with unmarked walls and no cues in the distance, preferred directions may drift over time).
164:
multiple incoherent orientations. Thus, these cells can be conceptualized as forming an imaginary ring, with each cell exciting cells coding for its own or neighboring directions, and suppressing cells coding for other directions. A key insight provided by these models was that the topology of the orientation selectivity (the ring) came from internal connections, while external cues were associated with those internal representations. Thus head direction cells, like
101:, a brain state rich in dreaming activity in humans and whose electrical activity is virtually indistinguishable from the waking brain, this directional signal moves as if the animal is awake: that is, HD neurons are sequentially activated, and the individual neurons representing a common direction during wake are still active, or silent, at the same time.
134:
more see landmarks, the HD system usually comes rapidly back into the normal alignment. Occasionally the realignment is delayed: the HD cells may maintain an abnormal alignment for as long as a few minutes, but then abruptly snap back. Consistent with the drifting in the dark, HD cells are not sensitive to the polarity of geomagnetic fields.
196:. Chen et al. found limited numbers of HD cells in posterior parts of the neocortex. The observation in 1998 of HD cells in the lateral mammillary area of the hypothalamus completed an interesting pattern: the parahippocampus, mammillary nuclei, anterior thalamus, and retrosplenial cortex are all elements in a neural loop called the
215:
HD cells have been described in many different animal species, including rats, mice, non human primates and bats. In bats, the HD system is three dimensional, and not only along the horizontal plane as in rodents. A HD-like neuronal network is also present in the drosophila, in which the HD cells are
137:
If these sorts of misalignment experiments are done too often, the system may break down. If an animal is repeatedly disoriented, and then placed into an environment for a few minutes each time, the landmarks gradually lose their ability to control the HD system, and eventually, the system goes into
150:
The properties of the head direction system - particularly its persistence in the dark, and also the constant relationship of firing directions between cells regardless of environmental changes - suggested to early theoreticians the still-accepted notion that the cells might be organized in the form
207:
The remarkable properties of HD cells, most particularly their conceptual simplicity and their ability to maintain firing when visual cues were removed or perturbed, led to considerable interest from theoretical neuroscientists. Several mathematical models were developed, which differed on details
133:
It is possible to temporarily disrupt the alignment of the HD system, for example by turning out the lights for a few minutes. Even in the dark, the HD system continues to operate, but its alignment to the environment may gradually drift. When the lights are turned back on and the animal can once
129:
One of the most interesting aspects of head direction cells is that their firing is not fully determined by sensory features of the environment. When an animal comes into a novel environment for the first time, the alignment of the head direction system is arbitrary. Over the first few minutes of
141:
There is evidence that the visual control of HD cells is mediated by the postsubiculum. Lesions of the postsubiculum do not eliminate thalamic HD cells, but they often cause the directionality to drift over time, even when there are plenty of visual cues. Thus, HD cells in postsubiculum-lesioned
92:
Some HD cells exhibit anticipatory behaviour: the best match between HD activity and the animal's actual head direction has been found to be up to 95 ms in future. That is, activity of head direction cells predicts, 95 ms in advance, what the animal's head direction will be. This possibly reflects
163:
with pairs of cells representing nearby directions being more strongly coupled than pairs of cells representing distant orientations. With global inhibition, these interactions cause activity to stabilize, such that a representation of a single orientation is more stable than states representing
73:
A striking characteristic of HD cells is that in most brain regions they maintain the same relative preferred firing directions, even if the animal is moved to a different room, or if landmarks are moved. This has suggested that the cells interact so as to maintain a unitary stable heading signal
200:, proposed by Walter Papez in 1939 as the neural substrate of emotion. Limited numbers of robust HD cells have also been observed in the hippocampus and dorsal striatum. Recently, substantial numbers of HD cells have been found in the medial entorhinal cortex, intermingled with spatially tuned
171:
An alternative model has also been proposed by Song and Wang, in which the same attractor mechanism could be implemented with inhibitory interconnections instead. More complex connection matrices that can produce mathematically equivalent systems have also been proposed, but evidence for these
1499:
Tryon, Valerie L.; Kim, Esther U.; Zafar, Talal J.; Unruh, April M.; Staley, Shelly R.; Calton, Jeffrey L. (2012-12-01). "Magnetic field polarity fails to influence the directional signal carried by the head direction cell network and the behavior of rats in a task requiring magnetic field
187:
The postsubiculum has numerous anatomical connections. Tracing these connections led to the discovery of head direction cells in other parts of the brain. In 1993, Mizumori and
Williams reported finding HD cells in a small region of the rat thalamus called the
96:
HD cells continue to fire in an organized manner during sleep, as if animals were awake. However, instead of always pointing toward the same direction—the animals are asleep and thus immobile—the neuronal "compass needle" moves constantly. In particular, during
85:, which is mostly orientation-invariant and location-specific, whereas HD cells are mostly orientation-specific and location-invariant. However, HD cells do not require a functional hippocampus to express their head direction specificity. They depend on the
34:
found in a number of brain regions that increase their firing rates above baseline levels only when the animal's head points in a specific direction. They have been reported in rats, monkeys, mice, chinchillas and bats, but are thought to be common to all
130:
exploration, the animal learns to associate the landmarks in the environment with directions. When the animal comes back into the same environment at a later time, if the head direction system is misaligned, the learned associations serve to realign it.
74:(see "Theoretical models"). Recently, however, a subpopulation of HD neurons has been found in the dysgranular part of retrosplenial cortex that can operate independently of the rest of the network, and which seems more responsive to environmental cues.
39:, perhaps all vertebrates and perhaps even some invertebrates, and to underlie the "sense of direction". When the animal's head is facing in the cell's "preferred firing direction" these neurons fire at a steady rate (i.e., they do not show
2375:
For a review on the HD system and place field system, see Muller (1996): "A quarter of a
Century of Place Cells", Sharp et al. (2001): "The anatomical and computational basis of rat HD signal."
752:
Chen, L. L.; Lin, L. H.; Green, E. J.; Barnes, C. A.; McNaughton, B. L. (1994-01-01). "Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation".
109:
The HD network makes use of inertial and other movement-related inputs, and thus continues to operate even in the absence of light. These inertial properties are dependent on the
70:. It is thought that the cortical head direction cells process information about the environment, while the subcortical ones process information about angular head movements.
231:
2141:
Chen, LL; Lin LH; Green EJ; Barnes CA; McNaughton BL (1994). "Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation".
1344:"Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction"
43:), but firing decreases back to baseline rates as the animal's head turns away from the preferred direction (usually about 45° away from this direction).
2278:
Finkelstein, A; Derdikman D; Rubin A; Foerster JN; Las L; Ulanovsky N (January 8, 2015). "Three-dimensional head-direction coding in the bat brain".
1142:
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416:
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1910:
1653:
1852:"Angular Path Integration by Moving "Hill of Activity": A Spiking Neuron Model without Recurrent Excitation of the Head-Direction System"
1242:
Blair, H. T.; Sharp, P. E. (1996-08-01). "Visual and vestibular influences on head-direction cells in the anterior thalamus of the rat".
308:
Robertson, R. G.; Rolls, E. T.; Georges-François, P.; Panzeri, S. (1999-01-01). "Head direction cells in the primate pre-subiculum".
2248:
321:
46:
HD cells are found in many brain areas, including the cortical regions of postsubiculum (also known as the dorsal presubiculum),
1187:"Head direction cells in rats with hippocampal or overlying neocortical lesions: evidence for impaired angular path integration"
2335:"Role of the lateral mammillary nucleus in the rat head direction circuit: a combined single unit recording and lesion study"
530:
Ben-Yishay, Elhanan; Krivoruchko, Ksenia; Ron, Shaked; Ulanovsky, Nachum; Derdikman, Dori; Gutfreund, Yoram (2021-06-21).
418:"Disruption of the head direction cell signal after occlusion of the semicircular canals in the freely moving chinchilla"
1992:"Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations"
1941:"Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis"
253:"Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis"
2235:
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1085:
Jacob, Pierre-Yves; Casali, Giulio; Spieser, Laure; Page, Hector; Overington, Dorothy; Jeffery, Kate (2016-12-19).
979:"Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity"
2186:"Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory"
1545:"Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory"
98:
63:
2041:"Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats"
922:"Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats"
1925:
Ranck Jr, J. B. "Head direction cells in the deep cell layer of dorsal presubiculum in freely moving rats."
587:
Vinepinsky, Ehud; Cohen, Lear; Perchik, Shay; Ben-Shahar, Ohad; Donchin, Opher; Segev, Ronen (2020-09-08).
589:"Representation of edges, head direction, and swimming kinematics in the brain of freely-navigating fish"
208:
but had in common a dependence on mutually excitatory feedback to sustain activity patterns: a type of
93:
inputs from the motor system ("motor efference copy") preparing the network for an impending head turn.
806:; Stensola, Tor; Bonnevie, Tora; Van Cauter, Tiffany; Moser, May-Britt; Moser, Edvard I. (2014-02-03).
2287:
1796:
1682:
1287:"Head direction is coded more strongly than movement direction in a population of entorhinal neurons"
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114:
361:"Head direction cell activity in mice: robust directional signal depends on intact otolith organs"
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1087:"An independent, landmark-dominated head-direction signal in dysgranular retrosplenial cortex"
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Raudies, Florian; Brandon, Mark P.; Chapman, G. William; Hasselmo, Michael E. (2015-09-24).
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Neural
Engineering: Computation, Representation, and Dynamics in Neurobiological Systems
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717:
Taube, JS (2007). "The head direction signal: Origins and sensory-motor integration".
2382:
2092:"Head direction cells recorded in the anterior thalamic nuclei of freely moving rats"
1726:
Peyrache, Adrien; Lacroix, Marie M.; Petersen, Peter C.; Buzsáki, György (May 2015).
1155:
865:"Head direction cells recorded in the anterior thalamic nuclei of freely moving rats"
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Ajabi, Zaki; Keinath, Alexandra T.; Wei, Xue-Xin; Brandon, Mark P. (March 2023).
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1785:"Population dynamics of head-direction neurons during drift and reorientation"
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of a ring attractor, including simultaneously proposed models by Zhang and by
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a state where it shows a different, and random, alignment on each trial .
1450:"The vestibular contribution to the head direction signal and navigation"
1036:"The vestibular contribution to the head direction signal and navigation"
67:
55:
2299:
1694:
677:
2154:
1671:"Neural dynamics for landmark orientation and angular path integration"
765:
654:"Neural dynamics for landmark orientation and angular path integration"
2249:
10.1002/(sici)1098-1063(1999)9:3<206::aid-hipo2>3.0.co;2-h
322:
10.1002/(SICI)1098-1063(1999)9:3<206::AID-HIPO2>3.0.CO;2-H
1513:
36:
31:
1743:
1416:
1102:
1600:
Redish, A David; Elga, Adam N; Touretzky, David S (January 1996).
473:
Rubin, Alon; Yartsev, Michael M.; Ulanovsky, Nachum (2014-01-15).
808:"Topography of head direction cells in medial entorhinal cortex"
1602:"A coupled attractor model of the rodent head direction system"
475:"Encoding of head direction by hippocampal place cells in bats"
58:(the anterior dorsal and the lateral dorsal thalamic nuclei),
1728:"Internally organized mechanisms of the head direction sense"
1645:
Beyond the
Cognitive Map: From Place Cells to Episodic Memory
1401:"Internally organized mechanisms of the head direction sense"
532:"Directional tuning in the hippocampal formation of birds"
1399:
Peyrache, A; Lacroix MM; Petersen PC; Buzsaki G (2015).
251:
Taube, J. S.; Muller, R. U.; Ranck, J. B. (1990-02-01).
1939:
Taube, JS; Muller RU; Ranck JB Jr. (1 February 1990).
192:. Two years later, Taube found HD cells in the nearby
652:
Seelig, Johannes D.; Jayaraman, Vivek (2015-05-14).
232:
List of distinct cell types in the adult human body
228:, primate hippocampal counterpart for visual field.
1990:Taube, JS; Muller, RU; Ranck, JB (February 1990).
1448:Yoder, Ryan M.; Taube, Jeffrey S. (2014-01-01).
1034:Yoder, Ryan M.; Taube, Jeffrey S. (2014-01-01).
359:Yoder, Ryan M.; Taube, Jeffrey S. (2009-01-28).
2039:Mizumori, SJ; Williams JD (September 1, 1993).
1899:Eliasmith, Chris; Anderson, Charles H. (2003).
1850:Song, Pengcheng; Wang, Xiao-Jing (2005-01-26).
920:Mizumori, S. J.; Williams, J. D. (1993-09-01).
16:Type of neuron involved in spatial processing
8:
977:Stackman, R. W.; Taube, J. S. (1998-11-01).
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2015:
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1465:
1424:
1375:
1342:Blair, H. T.; Sharp, P. E. (1995-09-01).
1318:
1218:
1185:Golob, E. J.; Taube, J. S. (1999-08-15).
1118:
1061:
1051:
1010:
953:
896:
831:
693:
628:
555:
506:
449:
392:
284:
1669:Seelig, JD; Jayaraman V (May 14, 2015).
180:Head direction cells were discovered by
159:. In these models, which are a type of
54:, and subcortical regions including the
243:
1606:Network: Computation in Neural Systems
731:10.1146/annurev.neuro.29.051605.112854
1637:
1635:
1454:Frontiers in Integrative Neuroscience
1040:Frontiers in Integrative Neuroscience
7:
216:anatomically arranged along a ring.
2333:Blair, HT; Cho J; Sharp PE (1998).
125:Visual and other sensory influences
2203:10.1523/JNEUROSCI.16-06-02112.1996
2109:10.1523/JNEUROSCI.15-01-00070.1995
2058:10.1523/JNEUROSCI.13-09-04015.1993
2008:10.1523/JNEUROSCI.10-02-00436.1990
1958:10.1523/JNEUROSCI.10-02-00420.1990
1561:10.1523/JNEUROSCI.16-06-02112.1996
1360:10.1523/JNEUROSCI.15-09-06260.1995
1203:10.1523/JNEUROSCI.19-16-07198.1999
995:10.1523/JNEUROSCI.18-21-09020.1998
938:10.1523/JNEUROSCI.13-09-04015.1993
881:10.1523/JNEUROSCI.15-01-00070.1995
269:10.1523/JNEUROSCI.10-02-00420.1990
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1868:10.1523/jneurosci.4172-04.2005
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491:10.1523/JNEUROSCI.5393-12.2014
434:10.1523/JNEUROSCI.3450-09.2009
377:10.1523/JNEUROSCI.1679-08.2009
1:
2352:10.1016/S0896-6273(00)80657-1
2090:Taube, JS (January 1, 1995).
172:alternate models is lacking.
77:The system is related to the
1929:. Vol. 10. No. 176.12. 1984.
1156:10.1016/0006-8993(71)90358-1
2184:Zhang, K (March 15, 1996).
1549:The Journal of Neuroscience
1348:The Journal of Neuroscience
1256:10.1037/0735-7044.110.4.643
1191:The Journal of Neuroscience
983:The Journal of Neuroscience
926:The Journal of Neuroscience
869:The Journal of Neuroscience
863:Taube, J. S. (1995-01-01).
754:Experimental Brain Research
479:The Journal of Neuroscience
422:The Journal of Neuroscience
365:The Journal of Neuroscience
257:The Journal of Neuroscience
2405:
1810:10.1038/s41586-023-05813-2
613:10.1038/s41598-020-71217-1
60:lateral mammillary nucleus
1642:Redish, A. David (1999).
1618:10.1088/0954-898X_7_4_004
833:10.1016/j.cub.2013.12.002
557:10.1016/j.cub.2021.04.029
1543:Zhang, K. (1996-03-15).
1467:10.3389/fnint.2014.00032
1053:10.3389/fnint.2014.00032
194:anterior thalamic nuclei
99:rapid eye movement sleep
64:dorsal tegmental nucleus
1856:Journal of Neuroscience
1502:Behavioral Neuroscience
1244:Behavioral Neuroscience
81:system, located in the
190:lateral dorsal nucleus
105:Vestibular influences
542:(12): 2592–2602.e4.
48:retrosplenial cortex
2300:10.1038/nature14031
2292:2015Natur.517..159F
1801:2023Natur.615..892A
1732:Nature Neuroscience
1695:10.1038/nature14446
1687:2015Natur.521..186S
1091:Nature Neuroscience
824:2014CBio...24..252G
719:Annu. Rev. Neurosci
678:10.1038/nature14446
670:2015Natur.521..186S
605:2020NatSR..1014762V
548:2021CBio...31E2592B
428:(46): 14521–14533.
182:James B. Ranck, Jr.
115:semicircular canals
2155:10.1007/BF00243212
1927:Soc Neurosci Abstr
766:10.1007/bf00243212
593:Scientific Reports
226:Spatial view cells
146:Theoretical models
2286:(7533): 159–164.
1912:978-0-262-55060-4
1795:(7954): 892–899.
1681:(7551): 186–191.
1655:978-0-262-18194-5
1197:(16): 7198–7211.
989:(21): 9020–9037.
875:(1 Pt 1): 70–86.
664:(7551): 186–191.
161:attractor network
113:, especially the
111:vestibular system
87:vestibular system
52:entorhinal cortex
2396:
2372:
2354:
2345:(6): 1387–1397.
2320:
2319:
2275:
2269:
2268:
2232:
2226:
2225:
2215:
2205:
2196:(6): 2112–2126.
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2111:
2087:
2081:
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2051:(9): 4015–4028.
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1862:(4): 1002–1014.
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1555:(6): 2112–2126.
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1514:10.1037/a0030248
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1354:(9): 6260–6270.
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1024:
1014:
974:
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967:
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932:(9): 4015–4028.
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804:Giocomo, Lisa M.
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485:(3): 1067–1080.
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2143:Exp. Brain Res
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2002:(2): 436–447.
1982:
1951:(2): 420–435.
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1738:(4): 569–575.
1718:
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1612:(4): 671–685.
1592:
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1508:(6): 835–844.
1500:orientation".
1491:
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1411:(4): 569–575.
1391:
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1291:Brain Research
1277:
1250:(4): 643–660.
1234:
1177:
1150:(1): 171–175.
1144:Brain Research
1134:
1097:(2): 173–175.
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818:(3): 252–262.
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212:, as it were.
210:working memory
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20:Head direction
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2136:
2102:(1): 70–86.
2099:
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1995:
1985:
1948:
1944:
1934:
1926:
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2237:Hippocampus
2190:J. Neurosci
2149:(1): 8–23.
2096:J. Neurosci
2045:J. Neurosci
1996:J. Neurosci
1945:J. Neurosci
1297:: 355–367.
760:(1): 8–23.
725:: 181–207.
310:Hippocampus
166:place cells
83:hippocampus
238:References
202:grid cells
79:place cell
41:adaptation
1819:1476-4687
1752:1546-1726
1626:0954-898X
1569:0270-6474
1522:1939-0084
1368:0270-6474
1311:1872-6240
1264:0735-7044
1211:1529-2401
1164:0006-8993
1111:1546-1726
1003:0270-6474
946:0270-6474
889:0270-6474
842:1879-0445
774:0014-4819
686:1476-4687
621:2045-2322
566:0960-9822
499:1529-2401
442:1529-2401
385:1529-2401
330:1050-9631
277:0270-6474
157:Touretzky
119:inner ear
2383:Category
2308:25470055
2265:13520009
2257:10401637
2171:25125371
1886:15673682
1837:36949190
1828:10060160
1770:25730672
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1435:25730672
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704:25971509
639:32901058
574:33974847
517:24431464
460:19923286
403:19176815
346:13520009
338:10401637
220:See also
68:striatum
56:thalamus
2389:Neurons
2361:9883731
2316:4457477
2288:Bibcode
2222:8604055
2213:6578512
2163:7843305
2128:7823153
2119:6578288
2077:8366357
2068:6576470
2026:2303852
2017:6570161
1977:2303851
1968:6570151
1877:6725619
1797:Bibcode
1761:4376557
1704:4704792
1683:Bibcode
1587:8604055
1578:6578512
1477:4001061
1426:4376557
1386:7666208
1377:6577663
1320:4427560
1272:8864258
1220:6782884
1172:5124915
1120:5274535
1063:4001061
1021:9787007
1012:1550347
964:8366357
955:6576470
907:7823153
898:6578288
820:Bibcode
782:7843305
695:4704792
666:Bibcode
630:7479115
601:Bibcode
544:Bibcode
508:6608343
451:2821030
394:2768409
295:2303851
286:6570151
176:History
117:of the
37:mammals
32:neurons
2369:848928
2367:
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2339:Neuron
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153:Redish
50:, and
2365:S2CID
2312:S2CID
2261:S2CID
2167:S2CID
786:S2CID
342:S2CID
28:cells
2357:PMID
2304:PMID
2253:PMID
2218:PMID
2159:PMID
2124:PMID
2073:PMID
2022:PMID
1973:PMID
1907:ISBN
1882:PMID
1833:PMID
1815:ISSN
1766:PMID
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1709:PMID
1650:ISBN
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1325:PMID
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1260:ISSN
1225:PMID
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1125:PMID
1107:ISSN
1068:PMID
1017:PMID
999:ISSN
960:PMID
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903:PMID
885:ISSN
846:PMID
838:ISSN
778:PMID
770:ISSN
735:PMID
700:PMID
682:ISSN
635:PMID
617:ISSN
570:PMID
562:ISSN
513:PMID
495:ISSN
456:PMID
438:ISSN
399:PMID
381:ISSN
334:PMID
326:ISSN
291:PMID
273:ISSN
155:and
66:and
30:are
2347:doi
2296:doi
2284:517
2245:doi
2208:PMC
2198:doi
2151:doi
2147:101
2114:PMC
2104:doi
2063:PMC
2053:doi
2012:PMC
2004:doi
1963:PMC
1953:doi
1872:PMC
1864:doi
1823:PMC
1805:doi
1793:615
1756:PMC
1740:doi
1699:PMC
1691:doi
1679:521
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1058:PMC
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1007:PMC
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950:PMC
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877:doi
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762:doi
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690:PMC
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