Head Direction Cells - History

History

Head direction cells were first noticed 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 brief abstract in 1984. A postdoctoral fellow working in his laboratory, Jeffrey S. Taube, made these cells the subject of his research, and summarized his 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.

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

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”.