Head Direction Cell Activity in Mice: Robust Directional Signal Depends on Intact Otolith Organs

Abstract

The head direction (HD) cell signal is a representation of an animal's perceived directional heading with respect to its environment. This signal appears to originate in the vestibular system, which includes the semicircular canals and otolith organs. Preliminary studies indicate the semicircular canals provide a necessary component of the HD signal, but involvement of otolithic information in the HD signal has not been tested. The present study was designed to determine the otolithic contribution to the HD signal, as well as to compare HD cell activity of mice with that of rats. HD cell activity in the anterodorsal thalamus was assessed in wild-type C57BL/6J and otoconiadeficient tilted mice during locomotion within a cylinder containing a prominent visual landmark. HD cell firing properties in C57BL/6J mice were generally similar to those in rats. However, in C57BL/6J mice, landmark rotation failed to demonstrate dominant control of the HD signal in 36% of the sessions. In darkness, directional firing became unstable during 42% of the sessions, but landmark control was not associated with HD signal stability in darkness. HD cells were identified in tilted mice, but directional firing properties were not as robust as those of C57BL/6J mice. Most HD cells in tilted mice were controlled by landmark rotation but showed substantial signal degradation across trials. These results support current models that suggest otolithic information is involved in the perception of directional heading. Furthermore, compared with rats, the HD signal in mice appears to be less reliably anchored to prominent environmental cues.Key words: otolith organs; mouse; gravity; anterodorsal thalamic nucleus; navigation; head direction IntroductionAccurate navigation depends, in part, on a neural representation of directional heading, which appears to be encoded by head direction (HD) cells located throughout Papez circuit (for review, see Sharp et al., 2001a;Taube, 2007). This HD signal provides a constantly updated representation of perceived orientation in the yaw plane, regardless of the animal's position within an environment. Generation of the HD signal depends on information from the vestibular labyrinth, because damage to the vestibular labyrinth, either permanent or temporary, disrupts the HD signal and causes spatial memory impairments (Stackman and Taube, 1997;Stackman and Herbert, 2002;Wallace et al., 2002;Schautzer et al., 2003;Brandt et al., 2005). Within the vestibular labyrinth, the semicircular canals sense angular acceleration and the otolith organs sense linear acceleration, including static pitch/tilt relative to gravity (Tait and McNally, 1934;Adrian, 1943;Fernandez et al., 1972; Fernán-dez and Goldberg, 1976a,b,c). Both systems appear to be necessary for accurate perception of rotation and translation because activation of the canals occurs with respect to a head-based reference frame and the otoliths are unable to distinguish between linear acceleration and static pitch or tilt (Angelaki et al., 1999;Angelaki and Dickm...

Septal elicitation of hippocampal theta rhythm did not repair cognitive and emotional deficits resulting from vestibular lesions

“…It has also been well documented that specific vestibular information is required to maintain normal function of place cells in the hippocampus (Sharp et al, 1995;Russell et al, 2003) and the head direction cells in the anterodorsal thalamic nucleus (Muir et al, 2009;Yoder and Taube, 2009), that are thought to be crucial for accurate spatial navigation. The reinstatement of theta rhythmicity in the absence of such specific vestibular signals would certainly not be expected to restore vestibularcontrolled functions, which would be likely to include spatial working memory-and could also extend to the emotional changes assessed here, since loss of vestibular input has been reported to alter exploration and anxiety in animal models using both rats and mice Zheng et al, 2008;Avni et al, 2009).…”

Maturation of glutamatergic transmission in the vestibulo-olivary pathway impacts on the registration of head rotational signals in the brainstem of rats

“…This involves maturation of both the semicircular canals and otolith organs in the detection and transduction of head-directional signals (Muir et al 2009;Yoder and Taube 2009). In rats, a rudimentary representation of head-directional signals is decipherable in the parasubiculum and entorhinal cortex as early as 2.5 weeks after birth (Langston et al 2010;Wills et al 2010).…”

Decoding signal processing in thalamo-hippocampal circuitry: implications for theories of memory and spatial processing

“…Furthermore, firing mode strongly affects the propagation of the sensory signal (Ramcharan et al, 2000;Ramcharan et al, 2005;Sherman, 2001). Head-direction neurons in anterodorsal thalamic nucleus normally do not express bursting properties; however, such firing modes appear after disconnection of the afferent input that processes the vestibular signal (Muir et al, 2009;Stackman and Taube, 1997;Yoder and Taube, 2009) but see also (Stackman et al, 2002). The variability of the firing patterns between the head-direction neurons during tonic spiking is expressed by their inter-spike intervals (Taube, 2010) and recent data suggest that ISI variability affects the encoding of the directional signal (Tsanov et al, 2014a).…”