Head direction cells: Properties and functional significance

Current Opinion in Neurobiology

Volumn 6, Issue 2, 1996, Pages 196-206

  Muller, Robert U ^a   Ranck Jr , James B ^a   Taube, Jeffrey S ^b  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

^b Dartmouth College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN CELL; COGNITION; HIPPOCAMPUS; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW; SPATIAL DISCRIMINATION; THALAMUS;

EID: 0029979099     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(96)80073-0     Document Type: Article

References (40)

1. Muller RU, Bostock EM, Taube JS, Kubie JL: On the directional firing properties of hippocampal place cells. J Neurosci 1994, 4:7235-7251. It is shown that hippocampal place cells show virtually no directional selectivity when recorded in a cylindrical enclosure with an open floor. When recorded on an eight-arm maze, however, the same cells show significant directional selectivity. The authors argue that the omnidirectional firing in the cylinder falsifies the local view theory of place cell firing. They also conclude that directional selectivity is not a fixed feature of place cells, but is dependent on the behavioral task and the environment.
2. Taube JS, Muller RU, Ranck JB Jr: Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 1990, 10:420-435.
3. Taube JS: Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 1995, 15:70-86. The first paper to demonstrate the existence of HD cells in the anterior thalamic nuclei (ADN), as suggested by the anatomical connections between the ADN and the postsubiculum. ADN HD cells are remarkably similar to postsubicular HD cells in almost all regards. A small correlation was seen between firing rate and angular head turning speed. ADN HD cell discharge was disrupted when the rat was restrained and passively rotated, indicating active motor input is necessary to support normal firing.
4. Muller RU, Kubie JL: The effects of changes In the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 1987, 7:1951-1968.
5. Taube JS, Muller RU, Ranck JB Jr: Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci 1990, 10:436-447.
6. O'Keefe J, Nadel L: The Hippocampus as a Cognitive Map. Oxford: Clarendon; 1978.
7. Eichenbaum H, Otto T, Cohen NJ: Two functional components of the hippocampal memory system. Behav Brain Sci 1994, 17:449-518.
8. Nadel L: The hippocampus and space revisited. Hippocampus 1991, 1:221-229.
9. Muller RU, Kubie JL, Bostock EM, Taube JS, Quirk G: Spatial firing correlates of neurons in the hippocampal formation of freely moving rats. In Brain and Space. Edited by Paillard J. Oxford: Oxford University Press; 1991:296-333.
10. Muller RU, Stead M, Pach J: The hippocampus as a cognitive graph: expanded version. J Gen Physiol 1996, in press.
11. Jung MW, McNaughton BL: Spatial selectivity of unit activity In the hippocampal granular layer. Hippocampus 1993, 3:165-182.
12. Quirk GJ, Muller RU, Kubie JL, Ranck JB Jr: The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 1992, 12:1945-1963.
13. Sharp PE, Green C: Spatial correlates of firing patterns of single cells in the subiculum of freely moving rat. J Neurosci 1994, 14:2339-2356.
14. Taube JS: Place cells recorded in the parasubiculum of freely-moving rats. Hippocampus 1995, 5:569-583.
15. Ranck JB Jr: Head direction cells in the deep cell layer of dorsal presublculum in freely moving rats. In Electrical Activity of Archicortex. Edited by Buzsaki G, Vanderwolf CH. Budapest: Akademai Kiado; 1985:217-220.
16. Bingman VP: Remembering spatial cognition as a hippocampal functional component. Behav Brain Res 1994, 17:473-474.
17. Muller RU, Kubie JL, Ranck JB Jr: Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 1987, 7:1935-1950.
18. Sharp PE: Multiple spatial/behavioral correlates for cells in the rat postsubiculum: multiple regression analysis and comparison to other hippocampal areas. Cereb Cortex 1996, 6:238-259.
19. Knierim JJ, Kudrimoti HS, McNaughton BL: Place cells, head direction cells, and the learning of landmark stability. J Neurosci 1995, 15:1648-1659. Rats learned to retrieve food pellets in a cylinder with a single prominent cue in either disorientation or non-disorientation conditions. Disorientation was done by putting a rat in a box that was carried along a circuitous route into the recording room. In non-disorientation, rats could see as they were carried along a direct path into the recording room. During recordings, all rats were treated as in disorientation training. Hippocampal place cells and ADN HD cells were then simultaneously recorded. For non-disoriented rats, place cell firing fields and HD cell preferred directions were stable. Furthermore, discharge of both cell types was controlled by the cue card. In contrast, for disoriented rats, firing fields and preferred directions often rotated unpredictably during and across sessions; the cue card did not reliably control the angular position of firing fields or preferred directions. Crucially, when spontaneous rotations occurred for disoriented rats, place cells and HD cells stayed in register, suggesting a unitary navigational coordinate system. The authors suggest that the unstable behavior of cells in disoriented rats arises because the rats learned to treat landmarks as unreliable. They further argue that this cell behavior is expected of a navigational system that is using only dead reckoning.
20. Kubie JL, Ranck JB Jr: Sensory-behavioral correlates in individual hippocampal neurons in three situations: space and context. In Neurobiology of the Hippocampus. Edited by Seifert W. New York: Academic Press; 1983:433-447.
21. Wiener SI: Spatial and behavioral correlates of striatal neurons In rats performing a self-initiated navigation task. J Neurosci 1993, 13:3802-3817.
22. Mizumori SJY, Williams JD: Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J Neurosci 1993, 13:4015-4028.
23. Chen LL, Lin LH, Green EJ, Barnes CA, McNaughton BL: Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp Brain Res 1994, 101:8-23. Rats were trained on a spatial working memory task on a radial arm maze in a cue-controlled room. A small number of HD cells were identified in the retrosplenial and medial prestriate areas. The discharge of some of these HD cells was modulated by the rat's behavior; in particular, cell discharge was most affected by angular head turns of the rat. The directional signals carried by cells in posterior cortex appear to be much weaker than the signals in postsubiculum or anterior thalamic nuclei.
24. •] have few of the properties that make HD cells in ADN and the postsubiculum excellent candidates for the substrate of a navigational directional system.
25. Lavoie AM, Mizumori SJY: Spatial, movement-, and reward-sensitive discharge by medial ventral striatal neurons of rats. Brain Res 1994, 638:157-168.
26. Blair HT, Sharp PE: Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction. J Neurosci 1995, 15:6260-6270. This paper reports a key difference between postsubicular and ADN HD cells. HD cell firing was compared when the rats head was turning clockwise or counterclockwise; cell activity was further correlated with the speed of turning. ADN HD cell discharge for clockwise and counterclockwise turns are brought into register when the discharge anticipates where the rat will point its head ∼40ms in the future. In contrast, postsubicular HD cell discharge for turns in the two directions is in register when the discharge is associated with the current directional heading. It is also reported that the firing rate of HD cells is determined, in part, by the speed of the head turn.
27. ••], but the mathematical rigor distinguishes this work. In our opinion, the novel ideas raised raised by the author as well as the clarity and completeness of the dynamical exposition make this perhaps the best paper reviewed. Highly recommended reading.
28. Foster T, Castro CA, McNaughton BL: Spatial selectivity of rat hippocampal neurons: dependence on preparedness for movement Science 1989, 244:1580-1582.
29. Quirk GJ, Muller RU, Kubie JL: The firing of hippocampal place cells in the dark reflects the rat's recent experience. J Neurosci 1990, 10:2008-2017.
30. Gallistel CR: The Organization of Learning. Cambridge, Massachusetts: MIT Press; 1990.
31. McNaughton BL, Chen LL, Markus EJ: 'Dead reckoning', landmark learning, and the sense of direction: a neurophysiological and computational hypothesis. J Cogn Neurosci 1991, 3:190-202.
32. Goodridge JP, Taube JS: Preferential use of the landmark navigational system by head direction cells. Behav Neurosci 1995, 109:49-61. HD cells in the ADN and postsubiculum were recorded in a cylinder with a single cue on the wall. Rats were then removed from the apparatus, the floor paper was changed, and the cue removed. Next, rats were reintroduced into the cylinder and a second recording session was done. If the cell's preferred direction shifted by >30° from its initial orientation, the cue was replaced at its original position in full view of the rat. If the cell's preferred direction did not shift, the cue card was replaced to a 90° rotated position, again in full view of the rat. Under both conditions, the preferred direction shifted back to its original orientation with respect to the cue card. The authors concluded that stable visual landmarks preferentially exert more control over HD cell discharge than idiothetic cues derived from the rat's own movements.
33. Taube JS, Burton HL: Head direction cell activity monitored in a novel environment and during a cue conflict situation. J Neurophysiol 1995, 74:1953-1971. Postsubicular and ADN HD cells were recorded in two conditions. In the first, rats went from a familiar cylinder to a novel rectangle through a U-shaped alley; a door initially kept the rat in the cylinder. HD cells maintained their preferred direction as they went into the new alley and rectangle; the consistency is attributable perhaps to the use of idiothetic sensory information (vestibular, proprioceptive, motor efference copy). In the second condition, a salient cue in the cylinder was rotated 90° and the rat was reintroduced into the cylinder. If the preferred direction of the HD cell rotated to an extent similar to card rotation, the door was opened and the rat was allowed back into the alley and rectangle. The preferred direction of HD cells immediately shifted back to its original value when the rat entered the alley. When the rat returned to the rotated cylinder, the preferred directions either: shifted back to the direction first observed with the rotated card; remained aligned with their orientation in the rectangle; or shifted to a value in between the values seen in the rectangle and the cylinder with the cue rotated. These results imply that visual cues can override idiothetic information that asserts that the world is stable.
34. Sutherland RJ, Rodriguez AJ: The role of the fornix/fimbria and some related subcortical structures in place learning and memory. Behav Brain Res 1989, 32:265-277.
35. Taube JS, Kesslak JP, Cotman CW: Lesions of the rat postsubiculum impair performance on spatial tasks. Behav Neural Biol 1992, 57:131-143.
36. Mizumori SJY, Miya DY, Ward KE: Reversible inactivation of the lateral dorsal thalamus disrupts hippocampal place representation and impairs spatial learning. Brain Res 1994, 644:168-174.
37. Amaral DG, Witter MP: Hippocampal formation. In The Rat Nervous System, edn 2. Edited by Paxinos G. San Diego: Academic Press; 1995:443-493.
38. Skaggs WE, Knierim JJ, Kudrimoti HS, McNaughton BL: A model of the neural basis of the rat's sense of direction. In Advances in Neural Information Processing Systems, vol 7. Edited by Tesauro G, Touretzky D, Leen T. Cambridge, Massachusetts: MIT Press; 1995:173-180. A dynamical model for HD cell firing is proposed. The particular set of directional cells that is firing is stable in the absence of perturbing input because of hypothesized connections that are excitatory between cells with similar preferred directions and inhibitory between cells with quite different preferred directions. The authors proposed mechanisms for fixing the alignment of the ring of directional cells with the environment and updating the current heading with reference to environmental landmarks.
39. Blair HT: A thalamocortical circuit for computing directional heading in the rat. In Advances in Neural Information Processing Systems, vol 8. Edited by Touretzky DS, Mozer MC, Hasselmo ME. Cambridge, Massachusetts: MIT Press; 1996:in press. This article outlines a neural model for how a head directional system is able to keep continuous track of the rats heading at it moves about the environment. Experimental findings on postsubicular and anterior thalamic HD cells and on angular velocity cells in postsubiculum are incorporated. The model predicts the existence of several other neuronal types in other brain structures whose activity is correlated with aspects of the directional signal.
40. ••] is expanded to two dimensions for place cells to show how trajectories might be imparted with a property similar to inertia.