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[6][7] and perhaps even some invertebrates,[8] and to underlie the "sense of direction".
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.
If an animal explores a dark environment with no directional cues, the HD alignment tends to drift slowly and randomly over time.
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.
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.
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[25] and by Redish and Touretzky.
[27] Direct evidence for such an organization in insects was recently reported:[28] in mammals it is assumed that the "ring" is distributed, and not a geometric anatomical form.
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.
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.
In 1993, Mizumori and Williams reported finding HD cells in a small region of the rat thalamus called the lateral dorsal nucleus.
[38] 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.
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.