Head Direction Cell Activity Is Absent in Mice without the Horizontal Semicircular Canals

Abstract

Head direction (HD) cells fire when an animal faces a particular direction in its environment, and they are thought to represent the neural correlate of the animal's perceived spatial orientation. Previous studies have shown that vestibular information is critical for generating the HD signal but have not delineated whether information from all three semicircular canals or just the horizontal canals, which are primarily sensitive to angular head rotation in the horizontal (yaw) plane, are critical for the signal. Here, we monitored cell activity in the anterodorsal thalamus (ADN), an area known to contain HD cells, in epstatic circler (Ecl) mice, which have a bilateral malformation of the horizontal (lateral) semicircular canals. Ecl mice and their littermates that did not express the mutation (controls) were implanted with recording electrodes in the ADN. Results confirm the important role the horizontal canals play in forming the HD signal. Although normal HD cell activity (Raleigh's r Ͼ 0.4) was recorded in control mice, no such activity was found in Ecl mice, although some cells had activity that was mildly modulated by HD (0.4 Ͼ r Ͼ 0.2). Importantly, we also observed activity in Ecl mice that was best characterized as bursty-a pattern of activity similar to an HD signal but without any preferred firing direction. These results suggest that the neural structure for the HD network remains intact in Ecl mice, but the absence of normal horizontal canals results in an inability to control the network properly and brings about an unstable HD signal. Key words: anterior thalamus; navigation; orientation; place cell; spatial; vestibular IntroductionHead direction (HD) cells, first discovered in the postsubiculum (Ranck, 1984;Taube et al., 1990a), discharge when an animal is facing a specific direction, independent of its location and behavior in space. Under normal conditions, the HD signal is primarily controlled by visual landmark information (Goodridge and Taube, 1995;Goodridge et al., 1998; Yoder et al., 2011), but several studies have also shown the importance of idiothetic information (vestibular, motor, and proprioceptive cues;Taube et al., 1990b; Taube and Burton, 1995;Goodridge et al., 1998;Stackman et al., 2003;van der Meer et al., 2010;Valerio and Taube, 2012).The influence of the vestibular system on HD cell firing has been a focus of many studies (Taube et al., 1990b; McNaughton et al., 1991). Indeed, the information coded by the horizontal semicircular canals (the acceleration of rotational head movements) makes it an ideal candidate for providing information about the animal's head movements in the yaw plane. Furthermore, the anatomical projections from the vestibular nuclei to the HD network via the nucleus prepositus hypoglosis, supragenual nucleus, and dorsal tegmental nucleus (DTN) reinforced this hypothesis (Biazoli et al., 2006 Sept. 9, 2014; revised Oct. 23, 2015; accepted Nov. 16, 2015. Author contributions: S.V. and J.S.T. designed research; S.V. performed research; S.V. and J.S.T. ana...

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“…Vestibular inputs that generate the HD signal can be traced back to the contributions of individual vestibular sensory end organs. Recent experiments in transgenic mice have shown that the horizontal canals, which are mostly sensitive to angular acceleration in the yaw (horizontal) plane when the animal’s head is held in the upright position, are essential for generating the directional signal (Valerio and Taube, 2012). Yoder and Taube (2009) found that the otolith organs, which are sensitive to translational acceleration of the animal, are also known to play some role in the generation of the HD signal.…”

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“…The vestibular system comprises the semicircular canals which detect angular head acceleration in three planes, and the otolith organs which detect linear head acceleration and static head position relative to gravity. Disruption of semicircular canal function eliminates the directional tuning of head direction cells and often causes the animal to spin or circle within a limited area [20, 21]. The otolith organs also contribute to head direction cell function, but this contribution appears to be relatively less than that of the canals; otoconia-deficient mice have head direction cells that are directionally tuned, but this tuning degrades over time [22].…”

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