The first section of Alsmith’s commentary (“Structural vs. taxonomic approaches to vestibular processes”) raises an important question: is there a vestibular sense? The enduring lack of a clear answer to this seemingly simple question might stem from the old assumption that there are five and only five senses, all of which giving rise to a distinct conscious sensation. The relatively late identification of the anatomical structures that code self-motion (Wade 2003; Lopez & Blanke 2014) has probably further contributed to the neglect of the “vestibular sense” in philosophy and science. We comment below on two questions raised by Alsmith concerning this debate: (1) Are vestibular events sensory events? and (2) Are vestibular events of a specific kind, i.e., distinct from other sensations?
(1) Are vestibular events sensory events? Several criteria have been proposed to determine whether an event is sensory or not (Macpherson 2011).[1] Following this type of approach, vestibular events can be described as sensory events because a sensory organ is dedicated to coding gravito-inertial forces and because there is a phenomenal experience associated with vestibular stimulation. Indeed, there are many situations during which passive own-body motions are characterized by distinct self-motion sensations. Imagine, for example, a situation in which we are sitting with eyes closed in the train and feel the departure, or when we are standing with eyes opened in a lift and experience vertical movement of the body. In such situations visual and somatosensory signals do not (or only weakly) contribute, but changes in vestibular signaling result in the conscious perception of self-motion, i.e., of “being translated forward” or “being elevated”.
Self-motion perception due to vestibular stimulation is also testable in the laboratory using motorized motion platforms (rotating chairs or translational platforms, see Palla & Lenggenhager 2014): participants are usually tested sitting on a chair, while non-vestibular sensory signals are largely excluded by having the participant’s body strapped to the chair and stabilized with cushions, by testing participants with eyes closed, by reducing auditory cues via white noise presented in headphones, and by testing participants with gloves and long sleeves (e.g., Grabherr et al. 2008; Hartmann et al. 2013; Lopez et al. 2013; Macauda et al. 2014; Valko et al. 2012). Participants are able to accurately detect and report self-motion and its direction, which forms the basis for the measurement of vestibular thresholds, which are comparable to auditory or tactile thresholds. When accelerations are applied above the threshold of the mechanoreceptors in the inner ear (e.g., above 0.6°/s2 for rotations around the vertical axis), a motion sensation emerges in healthy participants, which in our opinion is the sensory event corresponding to the vestibular sensation “I was moved”. Such sensory events therefore constitute the basis of what has often been referred to as the “sixth sense” (Goldberg et al. 2012; Wade 2003; Berthoz 2000). Further compelling support comes from patients with dysfunctions of the peripheral vestibular apparatus like benign paroxysmal positional vertigo, vestibular neuritis, or Menière’s disease, who experience strong vestibular sensations in the form of vertigo (Brandt 1999).
We acknowledge, however, that in situations where we actively move the head with eyes opened in space, vestibular signals from self-motion do not give rise to such distinct “vestibular” sensation of self-motion. As explained in our target article, in conditions of active, self-generated head movements, vestibular signals are cancelled or strongly attenuated in the vestibular nuclei (Cullen 2011; Roy & Cullen 2004). This is probably why the vestibular sense has been termed a “silent sense” by some authors (Day & Fitzpatrick 2005).
(2) Are vestibular sensory events of a specific kind, i.e., distinct from other sensations? Vestibular sensations are sensations of own-body rotations, translations, and orientation (sensation of whole-body orientation with respect to the vertical) in space. Such sensations may in principle also emerge from the stimulation of other sensory systems, such as the visual, somatosensory and auditory systems. Impressively, illusory self-motion might be evoked by large optic flows, tactile stimulation under the feet, or displacement of auditory stimuli (Berthoz et al. 1975; Dichgans et al. 1972; Lackner & DiZio 2001, 2005; Väljamäe 2009). These findings resulted in Alsmith’s claim that “one may begin to seriously consider the possibility that vestibular processing does not constitute a form of sensory processing of its own kind ”(this collection, p. 2). Yet if vestibular processing does not constitute a distinct form of sensory perception, to which type of sensory processing does it belong? Some authors have proposed that vestibular processing might relate to proprioception (since the vestibular system detects own body motions) or to exteroception (since it detects gravitational acceleration), but these propositions link vestibular processing to a function rather than a sensory modality. As recently pointed out by Macpherson (2011), “it is not even clear which sensory modality equilibrioception should be assimilated to, if indeed it should be assimilated to any” (p. 18).
Although vestibular, visual, and somesthetic signals may all support self-motion perception, this does not mean that the phenomenal experience of self-motion based on vestibular signals is similar to the experience based on visual signals. Actually, they may strongly differ in their content since, for example, the vestibular system is specialized in coding high-frequency movements whereas the visual system is tuned to low-frequency movements (see also next paragraph).[2] And even at the neurophysiological level, vestibular signals interact very early with visual and somatosensory signals; yet this does not mean that these signals provide the exact same sensation of body motion and orientation. An analogy might be when we observe a person speaking: both auditory and visual signals from the speaker’s lip movements contribute to the experience of listening to a voice; nevertheless both signals provide clearly distinct sensations and experiences. We believe the same holds for vestibular processing. Vestibular sensations might be clearly distinct sensations, but in daily life they are often integrated with other senses, confounding a pure conscious sensation (Angelaki & Cullen 2008; Angelaki et al. 2009). Vestibular-only neurons are found in the vestibular nuclei, which are not influenced by visual signals or eye movements, suggesting that vestibular signals are not entirely fused with other sensory signals (Goldberg et al. 2012). Similarly, intracranial stimulations in epileptic patients have showed that pure vestibular sensations could be evoked during electrical stimulations of the superior temporal cortex and insula (Penfield 1957; Kahane et al. 2003; Mazzola et al. 2014).