Vestibular and attractor network basis of the head direction cell signal in subcortical circuits

Abstract

Accurate navigation depends on a network of neural systems that encode the moment-to-moment changes in an animal's directional orientation and location in space. Within this navigation system are head direction (HD) cells, which fire persistently when an animal's head is pointed in a particular direction (Sharp et al., 2001a; Taube, 2007). HD cells are widely thought to underlie an animal's sense of spatial orientation, and research over the last 25+ years has revealed that this robust spatial signal is widely distributed across subcortical and cortical limbic areas. The purpose of the present review is to summarize some of the recent studies arguing that the origin of the HD signal resides subcortically, specifically within the reciprocal connections of the dorsal tegmental and lateral mammillary nuclei. Furthermore, we review recent work identifying “bursting” cellular activity in the HD cell circuit after lesions of the vestibular system, and relate these observations to the long held view that attractor network mechanisms underlie HD signal generation. Finally, we summarize anatomical and physiological work suggesting that this attractor network architecture may reside within the tegmento-mammillary circuit.

The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

“…Regardless, it is likely that a subset of the inputs to the DTN, primarily from the SGN, is unaffected by the photoinhibition of NPH. This point helps to explain the difference between our results and the results of previous work with lesions or knockouts of vestibular inputs, which recorded completely non-directional bursts of firing instead of HD cells [26,40]. Because of the subtler optogenetic methods employed in this study, we also were able to examine the gradual accumulation of error in the HD network more closely.…”

“…This ring attractor organization is thought to be generated by reciprocal activity between the lateral mammillary nucleus and dorsal tegmental nucleus (DTN) [23,24]. Damage to areas upstream from these nuclei produces a bursting pattern of firing in ADN cells that resembles HD cells that are disconnected from the animal's heading [25,26]. This tegmento-mammillary circuit receives its inputs from two brainstem nuclei, the supragenual nucleus and the nucleus prepositus hypoglossi (NPH) (see Fig.…”

Amplitude and dynamics of polarization-plane signaling in the central complex of the locust brain

“…Previous work (Heinze and Homberg 2007) has drawn an analogy between polarization-sensitive compass neurons in the locust central complex and vertebrate head-direction (HD) cells, discovered in rats by Ranck (1984) and studied in detail by Taube and colleagues (Clark and Taube 2012;Taube 2007). Rat HD cells refer to visual landmarks that signal heading direction in local sceneries; they are low in OA and fire to their preferred stationary HD (⌽ max,stationary ) with a Gaussianshaped tuning covering ϳ90°centered to ⌽ max,stationary .…”

Spatial representation in the hippocampal formation: a history

“…Today, more than 20 years after its proposal, the key concepts of the ring-attractor model for head direction cells remain unchallenged, which is remarkable for theoretical models in systems neuroscience, and no competing models have surfaced. In mammals, the reciprocally connected network of the dorsal tegmental nucleus and lateral mammillary area has been proposed as a location for the ring attractor 235 , and in Drosophila, the concept of a ring attractor for directional tuning has received its first experimental support in studies of central body neurons, where a circular anatomical arrangement has been shown to identity information is added after the fact, possibly from LEC 129,130,211,212 . Like rate remapping in place cells 216 , at least some of the CA1 object vector cells appear to require extended experience 214 .…”