Head direction cell

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.{{Cite journal|last1=Yoder|first1=Ryan M.|last2=Taube|first2=Jeffrey S.|date=2014-01-01|title=The vestibular contribution to the head direction signal and navigation|journal=Frontiers in Integrative Neuroscience|volume=8|pages=32|doi=10.3389/fnint.2014.00032|pmc=4001061|pmid=24795578|doi-access=free }} 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.

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.{{Cite journal|last1=Tryon|first1=Valerie L.|last2=Kim|first2=Esther U.|last3=Zafar|first3=Talal J.|last4=Unruh|first4=April M.|last5=Staley|first5=Shelly R.|last6=Calton|first6=Jeffrey L.|date=2012-12-01|title=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|journal=Behavioral Neuroscience|volume=126|issue=6|pages=835–844|doi=10.1037/a0030248|issn=1939-0084|pmid=23025828}}

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|reason= |date=October 2016}}.

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{{typo help inline|reason=similar to postbus|date=November 2019}}-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|reason=Skaggs et al?!|date=October 2016}}.

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, including simultaneously proposed models by Zhang{{Cite journal|last=Zhang|first=K.|date=1996-03-15|title=Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory|journal=The Journal of Neuroscience|volume=16|issue=6|pages=2112–2126|issn=0270-6474|pmid=8604055|pmc=6578512|doi=10.1523/JNEUROSCI.16-06-02112.1996}} and by Redish and Touretzky.{{Cite journal |last1=Redish |first1=A David |last2=Elga |first2=Adam N |last3=Touretzky |first3=David S |date=January 1996 |title=A coupled attractor model of the rodent head direction system |url=https://www.tandfonline.com/doi/full/10.1088/0954-898X_7_4_004 |journal=Network: Computation in Neural Systems |language=en |volume=7 |issue=4 |pages=671–685 |doi=10.1088/0954-898X_7_4_004 |issn=0954-898X|url-access=subscription }} In these models, which are a type of attractor network 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 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 place cells, 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.{{Cite book |last=Redish |first=A. David |url=https://books.google.com/books?id=vrnagI06NMIC |title=Beyond the Cognitive Map: From Place Cells to Episodic Memory |date=1999 |publisher=MIT Press |isbn=978-0-262-18194-5 |language=en}} Direct evidence for such an organization in insects was recently reported:{{cite journal|last=Seelig|first=JD|date=May 14, 2015|title=Neural dynamics for landmark orientation and angular path integration|journal=Nature|volume=521|issue=7551|pages=186–191|doi=10.1038/nature14446|pmid=25971509|author2=Jayaraman V|pmc=4704792|bibcode=2015Natur.521..186S}} 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,{{Cite journal |last1=Peyrache |first1=Adrien |last2=Lacroix |first2=Marie M. |last3=Petersen |first3=Peter C. |last4=Buzsáki |first4=György |date=May 2015 |title=Internally organized mechanisms of the head direction sense |journal=Nature Neuroscience |language=en |volume=18 |issue=4 |pages=569–575 |doi=10.1038/nn.3968 |pmid=25730672 |issn=1546-1726|pmc=4376557 }} and changes during drift and reorientation.{{Cite journal |last1=Ajabi |first1=Zaki |last2=Keinath |first2=Alexandra T. |last3=Wei |first3=Xue-Xin |last4=Brandon |first4=Mark P. |date=March 2023 |title=Population dynamics of head-direction neurons during drift and reorientation |journal=Nature |language=en |volume=615 |issue=7954 |pages=892–899 |doi=10.1038/s41586-023-05813-2 |issn=1476-4687|doi-access=free |pmid=36949190 |pmc=10060160 |bibcode=2023Natur.615..892A }}

An alternative model has also been proposed by Song and Wang,{{Cite journal|last1=Song|first1=Pengcheng|last2=Wang|first2=Xiao-Jing|date=2005-01-26|title=Angular Path Integration by Moving "Hill of Activity": A Spiking Neuron Model without Recurrent Excitation of the Head-Direction System|journal=Journal of Neuroscience|volume=25|issue=4|pages=1002–1014|doi=10.1523/jneurosci.4172-04.2005|pmid=15673682|pmc=6725619}} 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,{{Cite book |last1=Eliasmith |first1=Chris |url=https://books.google.com/books?id=J6jz9s4kbfIC |title=Neural Engineering: Computation, Representation, and Dynamics in Neurobiological Systems |last2=Anderson |first2=Charles H. |date=2003 |publisher=MIT Press |isbn=978-0-262-55060-4 |language=en}} but evidence for these alternate models is lacking.

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.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. 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.{{cite journal

| last =Taube

| first =JS |author2=Muller RU |author3=Ranck JB Jr.

| title =Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis.

| journal =J. Neurosci.

| volume = 10

| pages = 420–435

| date =1 February 1990

| pmid=2303851

| issue =2

| doi =10.1523/JNEUROSCI.10-02-00420.1990 | pmc =6570151 | doi-access =free

}}{{cite journal

| last1 =Taube

| first1 =JS

| last2 = Muller |first2=RU |last3=Ranck |first3=JB

| title =Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations.

| journal =J. Neurosci.

| volume = 10

| pages = 436–447

| date =February 1990

| pmid=2303852

| pmc =6570161

| issue =2

| doi =10.1523/JNEUROSCI.10-02-00436.1990

}} 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.

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.{{cite journal

| last =Mizumori

| first =SJ

|author2=Williams JD

| title =Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats.

|journal =J. Neurosci.

| volume = 13

| pages = 4015–4028

| date = September 1, 1993 | pmid=8366357

| issue =9| doi =10.1523/JNEUROSCI.13-09-04015.1993

| pmc =6576470

| doi-access =free

}}

Two years later, Taube found HD cells in the nearby anterior thalamic nuclei.{{cite journal

| last =Taube

| first =JS

| title =Head direction cells recorded in the anterior thalamic nuclei of freely moving rats.

| journal =J. Neurosci.

| volume = 15

| pages = 70–86

| date = January 1, 1995 | pmid=7823153

| issue =1

| doi =10.1523/JNEUROSCI.15-01-00070.1995

| pmc =6578288

| doi-access =free

}} Chen et al. found limited numbers of HD cells in posterior parts of the neocortex.{{cite journal

| last =Chen

| first =LL

|author2=Lin LH |author3=Green EJ |author4=Barnes CA |author5=McNaughton BL

| title =Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation.

|journal =Exp. Brain Res.

| volume = 101

| pages = 8–23

| year =1994

| pmid=7843305

| doi =10.1007/BF00243212

| issue =1| s2cid =25125371

}} 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.{{cite journal

| last =Zhang

| first =K

| title =Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory.

|journal =J. Neurosci.

| volume = 16

| pages = 2112–2126

| date = March 15, 1996 | pmid=8604055

| issue =6| doi =10.1523/JNEUROSCI.16-06-02112.1996

| pmc =6578512

| doi-access =free

}}

HD cells have been described in many different animal species, including rats, mice, non human primates{{cite journal

| last =Robertson

| first =RG

| author2=Rolls ET| author3=Georges-François P| author4=Panzeri S| title = Head direction cells in the primate pre-subiculum.

|journal =Hippocampus

| volume = 9

| pages =206–19

| date = 1999 | pmid=10401637

| issue =3| doi=10.1002/(sici)1098-1063(1999)9:3<206::aid-hipo2>3.0.co;2-h| s2cid =13520009

}} and bats.{{cite journal

| last =Finkelstein

| first =A

| author2=Derdikman D| author3=Rubin A| author4=Foerster JN| author5=Las L| author6=Ulanovsky N

| title = Three-dimensional head-direction coding in the bat brain.

|journal =Nature

| volume = 517

| pages =159–164

| date = January 8, 2015 | pmid=25470055

| issue =7533| doi=10.1038/nature14031| bibcode =2015Natur.517..159F

| s2cid =4457477

}} In bats, the HD system is three dimensional, and not only along the horizontal plane as in rodents. An HD-like neuronal network is also present in the drosophila, in which the HD cells are anatomically arranged along a ring.

• Spatial view cells, primate hippocampal counterpart for visual field.
• List of distinct cell types in the adult human body

{{reflist}}

• {{cite journal

| last =Blair

| first =HT

|author2=Cho J |author3=Sharp PE

| title =Role of the lateral mammillary nucleus in the rat head direction circuit: a combined single unit recording and lesion study.

|journal =Neuron

| volume = 21

| pages = 1387–1397

| year =1998

| pmid=9883731

| doi =10.1016/S0896-6273(00)80657-1

| issue =6

| s2cid =848928

|ref=refBlair1998| doi-access =free

}}

• 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."

{{DEFAULTSORT:Head Direction Cells}}

Category:Neurons