Head direction cells

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Head direction (HD) cells are neurons 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,[1] monkeys,[2] mice,[3] chinchillas[4] and bats,[5] but are thought to be common to all mammals, perhaps all vertebrates and perhaps even some invertebrates,[6] 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 adaptation), 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).[7]

HD cells are found in many brain areas, including the cortical regions of postsubiculum (also known as the dorsal presubiculum), retrosplenial cortex,[8] and entorhinal cortex,[9] and subcortical regions including the thalamus (the anterior dorsal[10] and the lateral dorsal[11] thalamic nuclei), lateral mammillary nucleus,[12] dorsal tegmental nucleus and striatum. It is thought that the cortical head direction cells process information about the environment, while the subcortical ones process information about angular head movements.[13]

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 (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.[14]

The system is related to the place cell system, located in the hippocampus,[15] 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.[16] They depend on the vestibular system,[17] and the firing is independent of the position of the animal's body relative to its head.[18]

Some HD cells exhibit anticipatory behaviour:[19] 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 inputs from the motor system ("motor efference copy") preparing the network for an impending head turn.

HD cells continue to fire in an organized manner during sleep, as if animals were awake.[20] 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 rapid eye movement sleep, 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.

Vestibular influences[edit]

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 vestibular system, especially the semicircular canals of the inner ear, which signal rotations of the head.[21] 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.

Visual and other sensory influences[edit]

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 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.

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 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.[22]

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 a state where it shows a different, and random, alignment on each trial[citation needed].

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 postsub-lesioned 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)[citation needed].

Theoretical models[edit]

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 of a ring attractor,[23] which is a type of attractor network. In an attractor network, interactions between neurons cause activity to stabilize, such that one state is preferred and other states suppressed. In the case of head direction, the cells are 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. Direct evidence for such an organization in insects was recently reported:[24] in mammals it is assumed that the "ring" is distributed, and not a geometric anatomical form. However, anatomical evidence for such excitatory interconnections between head direction cells is lacking. An alternative model was proposed by Song and Wang,[25] in which the same attractor mechanism could be implemented with inhibitory interconnections instead. There is currently little experimental evidence for either mechanism, and the attractor hypothesis is still just a hypothesis.

History[edit]

Head direction cells were discovered by James B. Ranck, Jr., 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.[26] 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.[27][28] 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.

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 lateral dorsal nucleus.[29] Two years later, Taube found HD cells in the nearby anterior thalamic nuclei.[30] Chen et al. found limited numbers of HD cells in posterior parts of the neocortex.[31] 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 Papez circuit, 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 grid cells.

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 but had in common a dependence on mutually excitatory feedback to sustain activity patterns: a type of working memory, as it were.[32]

HD cells have been described in many different animal species, including rats, mice, non human primates[33] and bats.[34] 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 anatomically arranged along a ring.

References[edit]

  1. ^ Taube, J. S.; Muller, R. U.; Ranck, J. B. (1990-02-01). "Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis". The Journal of Neuroscience. 10 (2): 420–435. ISSN 0270-6474. PMID 2303851. 
  2. ^ Robertson, R. G.; Rolls, E. T.; Georges-François, P.; Panzeri, S. (1999-01-01). "Head direction cells in the primate pre-subiculum". Hippocampus. 9 (3): 206–219. doi:10.1002/(SICI)1098-1063(1999)9:3<206::AID-HIPO2>3.0.CO;2-H. ISSN 1050-9631. PMID 10401637. 
  3. ^ Yoder, Ryan M.; Taube, Jeffrey S. (2009-01-28). "Head direction cell activity in mice: robust directional signal depends on intact otolith organs". The Journal of Neuroscience. 29 (4): 1061–1076. doi:10.1523/JNEUROSCI.1679-08.2009. ISSN 1529-2401. PMC 2768409Freely accessible. PMID 19176815. 
  4. ^ Muir, Gary M.; Brown, Joel E.; Carey, John P.; Hirvonen, Timo P.; Della Santina, Charles C.; Minor, Lloyd B.; Taube, Jeffrey S. (2009-11-18). "Disruption of the head direction cell signal after occlusion of the semicircular canals in the freely moving chinchilla". The Journal of Neuroscience. 29 (46): 14521–14533. doi:10.1523/JNEUROSCI.3450-09.2009. ISSN 1529-2401. PMC 2821030Freely accessible. PMID 19923286. 
  5. ^ Rubin, Alon; Yartsev, Michael M.; Ulanovsky, Nachum (2014-01-15). "Encoding of head direction by hippocampal place cells in bats". The Journal of Neuroscience. 34 (3): 1067–1080. doi:10.1523/JNEUROSCI.5393-12.2014. ISSN 1529-2401. PMID 24431464. 
  6. ^ Seelig, Johannes D.; Jayaraman, Vivek (2015-05-14). "Neural dynamics for landmark orientation and angular path integration". Nature. 521 (7551): 186–191. doi:10.1038/nature14446. ISSN 1476-4687. PMC 4704792Freely accessible. PMID 25971509. 
  7. ^ Taube, JS (2007). "The head direction signal: Origins and sensory-motor integration". Annu. Rev. Neurosci. 30: 181–207. doi:10.1146/annurev.neuro.29.051605.112854. PMID 17341158. 
  8. ^ 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". Experimental Brain Research. 101 (1): 8–23. doi:10.1007/bf00243212. ISSN 0014-4819. PMID 7843305. 
  9. ^ Giocomo, Lisa M.; Stensola, Tor; Bonnevie, Tora; Van Cauter, Tiffany; Moser, May-Britt; Moser, Edvard I. (2014-02-03). "Topography of head direction cells in medial entorhinal cortex". Current Biology. 24 (3): 252–262. doi:10.1016/j.cub.2013.12.002. ISSN 1879-0445. PMID 24440398. 
  10. ^ Taube, J. S. (1995-01-01). "Head direction cells recorded in the anterior thalamic nuclei of freely moving rats". The Journal of Neuroscience. 15 (1 Pt 1): 70–86. ISSN 0270-6474. PMID 7823153. 
  11. ^ Mizumori, S. J.; Williams, J. D. (1993-09-01). "Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats". The Journal of Neuroscience. 13 (9): 4015–4028. ISSN 0270-6474. PMID 8366357. 
  12. ^ Stackman, R. W.; Taube, J. S. (1998-11-01). "Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity". The Journal of Neuroscience. 18 (21): 9020–9037. ISSN 0270-6474. PMC 1550347Freely accessible. PMID 9787007. 
  13. ^ Yoder, Ryan M.; Taube, Jeffrey S. (2014-01-01). "The vestibular contribution to the head direction signal and navigation". Frontiers in Integrative Neuroscience. 8: 32. doi:10.3389/fnint.2014.00032. PMC 4001061Freely accessible. PMID 24795578. 
  14. ^ Jacob, Pierre-Yves; Casali, Giulio; Spieser, Laure; Page, Hector; Overington, Dorothy; Jeffery, Kate (2016-12-19). "An independent, landmark-dominated head-direction signal in dysgranular retrosplenial cortex". Nature Neuroscience. 20: 173–175. doi:10.1038/nn.4465. ISSN 1546-1726. PMC 5274535Freely accessible. PMID 27991898. 
  15. ^ O'Keefe, J.; Dostrovsky, J. (1971-11-01). "The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat". Brain Research. 34 (1): 171–175. doi:10.1016/0006-8993(71)90358-1. ISSN 0006-8993. PMID 5124915. 
  16. ^ Golob, E. J.; Taube, J. S. (1999-08-15). "Head direction cells in rats with hippocampal or overlying neocortical lesions: evidence for impaired angular path integration". The Journal of Neuroscience. 19 (16): 7198–7211. ISSN 1529-2401. PMID 10436073. 
  17. ^ Blair, H. T.; Sharp, P. E. (1996-08-01). "Visual and vestibular influences on head-direction cells in the anterior thalamus of the rat". Behavioral Neuroscience. 110 (4): 643–660. doi:10.1037/0735-7044.110.4.643. ISSN 0735-7044. PMID 8864258. 
  18. ^ Raudies, Florian; Brandon, Mark P.; Chapman, G. William; Hasselmo, Michael E. (2015-09-24). "Head direction is coded more strongly than movement direction in a population of entorhinal neurons". Brain Research. 1621: 355–367. doi:10.1016/j.brainres.2014.10.053. ISSN 1872-6240. PMC 4427560Freely accessible. PMID 25451111. 
  19. ^ Blair, H. T.; Sharp, P. E. (1995-09-01). "Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction". The Journal of Neuroscience. 15 (9): 6260–6270. ISSN 0270-6474. PMID 7666208. 
  20. ^ Peyrache, A; Lacroix MM; Petersen PC; Buzsaki G (2015). "Internally organized mechanisms of the head direction sense". Nat. Neurosci. 18: 569–575. doi:10.1038/nn.3968. PMC 4376557Freely accessible. PMID 25730672. 
  21. ^ Yoder, Ryan M.; Taube, Jeffrey S. (2014-01-01). "The vestibular contribution to the head direction signal and navigation". Frontiers in Integrative Neuroscience. 8: 32. doi:10.3389/fnint.2014.00032. PMC 4001061Freely accessible. PMID 24795578. 
  22. ^ 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 orientation". Behavioral Neuroscience. 126 (6): 835–844. doi:10.1037/a0030248. ISSN 1939-0084. PMID 23025828. 
  23. ^ Zhang, K. (1996-03-15). "Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory". The Journal of Neuroscience. 16 (6): 2112–2126. ISSN 0270-6474. PMID 8604055. 
  24. ^ Seelig, JD; Jayaraman V (May 14, 2015). "Neural dynamics for landmark orientation and angular path integration". Nature. 521 (7551): 186–191. doi:10.1038/nature14446. PMC 4704792Freely accessible. PMID 25971509. 
  25. ^ Song, Pengcheng; Wang, Xiao-Jing (2005-01-26). "Angular Path Integration by Moving "Hill of Activity": A Spiking Neuron Model without Recurrent Excitation of the Head-Direction System". Journal of Neuroscience. 25 (4): 1002–1014. doi:10.1523/jneurosci.4172-04.2005. 
  26. ^ Ranck Jr, J. B. "Head direction cells in the deep cell layer of dorsal presubiculum in freely moving rats." Soc Neurosci Abstr. Vol. 10. No. 176.12. 1984.
  27. ^ Taube, JS; Muller RU; Ranck JB Jr. (1 February 1990). "Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis." J. Neurosci. 10 (2): 420–435. PMID 2303851. 
  28. ^ Taube, JS; Muller, RU; Ranck, JB (February 1990). "Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations". J. Neurosci. 10 (2): 436–447. PMID 2303852. 
  29. ^ Mizumori, SJ; Williams JD (September 1, 1993). "Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats". J. Neurosci. 13 (9): 4015–4028. PMID 8366357. 
  30. ^ Taube, JS (January 1, 1995). "Head direction cells recorded in the anterior thalamic nuclei of freely moving rats". J. Neurosci. 15 (1): 70–86. PMID 7823153. 
  31. ^ 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.". Exp. Brain Res. 101 (1): 8–23. doi:10.1007/BF00243212. PMID 7843305. 
  32. ^ Zhang, K (March 15, 1996). "Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory". J. Neurosci. 16 (6): 2112–2126. PMID 8604055. 
  33. ^ Robertson, RG; Rolls ET; Georges-François P; Panzeri S (1999). "Head direction cells in the primate pre-subiculum". Hippocampus. 9 (3): 206–19. doi:10.1002/(sici)1098-1063(1999)9:3<206::aid-hipo2>3.0.co;2-h. PMID 10401637. 
  34. ^ Finkelstein, A; Derdikman D; Rubin A; Foerster JN; Las L; Ulanovsky N (January 8, 2015). "Three-dimensional head-direction coding in the bat brain". Nature. 517 (7533): 159–164. doi:10.1038/nature14031. PMID 25470055. 

Further reading[edit]

  • Blair, HT; Cho J; Sharp PE (1998). "Role of the lateral mammillary nucleus in the rat head direction circuit: a combined single unit recording and lesion study". Neuron. 21 (6): 1387–1397. doi:10.1016/S0896-6273(00)80657-1. PMID 9883731. 
  • 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."