The neural encoding of self-generated and externally applied movement: implications for the perception of self-motion and spatial memory

Abstract

The vestibular system is vital for maintaining an accurate representation of self-motion. As one moves (or is moved) toward a new place in the environment, signals from the vestibular sensors are relayed to higher-order centers. It is generally assumed the vestibular system provides a veridical representation of head motion to these centers for the perception of self-motion and spatial memory. In support of this idea, evidence from lesion studies suggests that vestibular inputs are required for the directional tuning of head direction cells in the limbic system as well as neurons in areas of multimodal association cortex. However, recent investigations in monkeys and mice challenge the notion that early vestibular pathways encode an absolute representation of head motion. Instead, processing at the first central stage is inherently multimodal. This minireview highlights recent progress that has been made towards understanding how the brain processes and interprets self-motion signals encoded by the vestibular otoliths and semicircular canals during everyday life. The following interrelated questions are considered. What information is available to the higher-order centers that contribute to self-motion perception? How do we distinguish between our own self-generated movements and those of the external world? And lastly, what are the implications of differences in the processing of these active vs. passive movements for spatial memory?

Keywords: corollary discharge; efference copy; head direction cells; place cells; proprioception; self-motion; sensory coding; voluntary movement.

Figure 1

(A) Mouse vestibular afferents can be classified on the basis of their discharge regularity, and are on average 3–4 times less sensitive to head velocity when compared to monkey afferents. (B) Comparison of rotational sensitivities and mutual information density of mouse and monkey VN neurons. (Monkey data are adapted from Massot et al., 2011, 2012).

Figure 2

Vestibular pathways for spatial memory. Vestibular signals from the labyrinth of the inner ear are transferred to the VN via the vestibular afferents of the VIII nerve. In turn, the VN projects to other brain areas to: (i) control posture and balance, (ii) produce estimates of spatial orientation, and (iii) encode heading direction.