2 A unique feature of the vestibular system: The representation of absolute self-motion and orientation

As mentioned by Alsmith, the vestibular system, unlike other sensory systems, does not code unique properties of sensory inputs such as loudness or hue. Yet, as already argued in the target article, the coding of absolute self-motion in space and self-orientation within gravity-related space is unique to the vestibular system. While relative (self-) motion and orientation can be detected by other sensory systems (e.g., vision and proprioception), gravity itself is not directly visible to these senses.[3] Because vestibular organs contain gravito-inertial sensors, they provide a coding of body translations and rotations that is independent from external references (unlike visual, auditory, and somatosensory coding of whole-body motions). For this reason, vestibular organs code self-motion even when the eyes are closed, while we are jumping on a trampoline, or swimming in the sea.

Figure 1: A) Crise de désinvolture (2003) an artwork by Philippe Ramette. Copyrights: © 2015, ProLitteris, Zurich. All rights are reserved. Reproduction and any other use without permission - except for the individual and private use - is prohibited. B) Drawing of the “haunting sway”, a “gravity-defying” device that was originally developed in the US in the 1890s for amusement parks. The visitors had the impression that they were turning with the sway, while actually the room was turning around them.

With these properties the vestibular system, especially otolith signaling, also gives us the sensation of an “up” and a “down” by encoding gravitational acceleration. This process might be less accessible to consciousness in normal circumstances, as gravitational pull is constantly acting on vestibular mechanoreceptors. However, there is a large body of data showing that an “internal model of gravity” (predicting how objects move in the physical world according to Newton’s laws; McIntyre et al. 2001) which is strongly based on otolith processing, shapes at a preconscious level several aspects of the visual perception of objects, body movements, and structure (e.g., Indovina et al. 2005; Lacquaniti et al. 2013; Lopez et al. 2009; Maffei et al. 2015; Yamamoto & Yamamoto 2006). A further illustration of the importance of the coding of body orientation in a gravity-centered space can be provided by the “tilted room illusion,” in which the furniture is aligned in a way that is incongruent with gravitational vertical (see figure 1A for an example by the French artist Philippe Ramette[4]), which has been used in a moving version as well in theme parks (the haunting swing, a “gravity-defying” ride, see figure 1B). Experiments conducted in this type of tilted environment have shown that the participant’s perception and posture are biased by tilted visual references, but not totally (Jenkin et al. 2003; Oman 2003). Merleau-Ponty has nicely noted the ambiguity of space-coding regarding the experience of up and down: “A direction can only exist for a subject who traces it out, and although a constituting mind eminently has the power to trace out all directions in space, in the present moment this mind has no direction and, consequently, it has no space, for it is lacking an actual starting point or an absolute here that could gradually give a direction to all determinations of space” (2012). It is interesting to note Merleau-Ponty’s claim that what is missing for the experience of up and down is an “absolute”. Merleau-Ponty also explains that “[w]e cannot, then, understand the experience of space through the consideration of the contents, nor through that of a pure activity of connecting, and we are confronted by that ‘third spatiality’ that we foreshadowed above, which is neither the spatiality of things in space, nor that of spatializing space […] We need an ‘absolute within the relative’, a space that does not skate over appearances, that is anchored in them and depends upon them” (2012, p. 296–297; our italics). Although Merleau-Ponty did not mention the vestibular system when he described the necessity of a “third spatiality,” we now know that the otolithic system provides the “absolute within the relative” he mentions and allows the coding of absolute self-orientation in space (see also Berthoz 2011 for a detailed account).