Rapid Spatial Reorientation and Head Direction Cells

Abstract

It is surprising how quickly we can find our bearings when suddenly confronted with a familiar environment, for instance when the lights are turned on in a dark room. Subjectively, this appears to occur almost instantaneously, yet the neural processes permitting this rapid reorientation are unknown. A likely candidate is the head direction (HD) cell system. These limbic neurons found in several brain regions, including the thalamus and the hippocampus, discharge selectively when the head of an animal is oriented in a particular ("preferred") direction. This neuronal activity is independent of position and ongoing behavior and is thus likely to constitute a physiological basis for the sense of direction. Remarkably, although the HD cell system has properties resembling those of a compass, it is independent of geomagnetic fields. Rather, the preferred directions of the HD cells are strongly anchored to visual cues in the environment. Here, we bring evidence for the first time that a fundamental component of the capacity to rapidly reorient in a familiar environment may be brought about by updating of HD cell responses as rapidly as 80 msec after changes in the visual scene. Continuous attractor networks have been used successfully to model HD cell ensemble dynamics. The present results suggest that after large rotations of the surrounding landmarks, activity in such networks may be propagated in abrupt jumps rather than in a gradually progressive manner.