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

The head-direction (HD) cells found in the limbic system in freely mov ing rats represent the instantaneous head direction of the animal in the horizontal plane regardless of the location of the animal. The internal direction represented by these cells uses both self-motion information for inertially based updating and familiar visual landmarks for calibration. Here, a model of the dynamics of the HD cell ensemble is presented. The stability of a localized static activity profile in the network and a dynamic shift mechanism are explained naturally by synaptic weight distribution components with even and odd symmetry, respectively. Under symmetric weights or symmetric reciprocal connections, a stable activity profile close to the known directional tuning curves will emerge. By adding a slight asymmetry to the weights, the activity profile will shift continuously without disturbances to its shape, and the shift speed can be controlled accurately by the strength of the odd-weight component. The generic formulation of the shift mechanism is determined uniquely within the current theoretical framework. The attractor dynamics of the system ensures modality-independence of the internal representation and facilitates the correction for cumulative error by the putative local-view detectors. The model offers a specific one-dimensional example of a computational mechanism in which a truly world-centered representation can be derived from observer-centered sensory inputs by integrating self-motion information.