In the previous sections I have provided theoretical considerations and empirical evidence assigning a critical role to multisensory spatial processing in the neural computations underlying representations of the bodily self and social cognition. This section will further examine the multisensory mechanisms relating the space of the bodily self to other individuals and the external world. I propose that important contributions to the brain’s multisensory spatial coding might come from a particular sensory system, i.e., the vestibular system, which has often been neglected in studies of higher brain functions related to subjectivity and intersubjectivity. I will ask: What might be the functional contribution of the vestibular system to pre-reflective representations of the bodily self and social cognition? How does the human vestibular cortex relate to the neural networks of the bodily self and social cognition?
The vestibular system consists of sensory organs in the inner ear that sense accelerations of the head in space, including rotational and linear movement of the head and whole body and the constant acceleration of gravity on earth (Day & Fitzpatrick 2005). Vestibular signals are processed by subcortical and cortical structures (Angelaki & Cullen 2008; Cullen 2012; Lopez & Blanke 2011). Research initially focused on subcortical processing as related to gaze control, postural stabilization, and neural computations of head motion directions (Fernandez & Goldberg 1971; Goldberg & Fernandez 1971). More recently, studies have revealed the contribution of vestibular cortical processing to spatial cognition, body perception, and the bodily self (see Lenggenhager & Lopez this collection; Lopez & Blanke 2011; Pfeiffer et al. 2014 for reviews). These studies show that vestibular cortical processing is based on a neural network of distinct, distributed, and multisensory cortical regions. In distinction from any other sensory modality, there is no primary vestibular cortex that processes purely vestibular signals. Instead, a core vestibular cortical input region, the human parieto-insular vestibular cortex (PIVC; Lopez et al. 2012; zu Eulenburg et al. 2012), processes vestibular, somatosensory, and visual signals and is connected to a number of multisensory brain regions in the parietal, temporal, cingulate, and frontal regions (figure 1c).
The vestibular system contributes to spatial aspects of the bodily self. For instance, OBEs were associated with vestibular sensation, such as floating in elevation (Blanke et al. 2004; Blanke & Mohr 2005; Blanke et al. 2002), and vestibular sensations preceded OBEs in persons with sleep paralysis (Cheyne & Girard 2009). Other studies presented conflicting visual and vestibular signals about earth gravity during the full-body illusion and induced changes in the subjectively-experienced spatial direction of the first-person perspective and self-location (Ionta et al. 2011; Pfeiffer et al. 2013). Thus, it has been argued that vestibular cortical processing does not merely signal the motions of the own body and the external world, but is also constitutive of spatial aspects of the bodily self (Lopez et al. 2008; Pfeiffer et al. 2014).
Previously, Lopez et al. (2013), Deroualle & Lopez (2014), and Lenggenhager & Lopez (this collection) have argued that the vestibular system probably contributes to social cognition. I will briefly summarize their main arguments and complement them with own points:
First, because the human species evolved under the steady influence of the earth’s gravitational field, adaptation to gravity also framed and affected action, perception, and social interaction. More recently, research has shown that the brain hosts internal models of gravity, representing the effects of gravity on the motion of objects under the influence of gravity, of self-motion, of bodily actions, and of the direction of the gravitational acceleration. Those internal models of gravity strongly overlap with the vestibular cortex (Indovina et al. 2005; Indovina et al. 2013; McIntyre et al. 2001; Sciutti et al. 2012). More evidence for a vestibular contribution to social perception comes from studies showing the effects of gravitational signals on the perception of emotional faces (Thompson 1980) and the perception of the spatial orientation of bodies (Lopez et al. 2009).
Second, the vestibular system might contribute to social cognition because it detects head motions in space and hence directly enables us, when compared to other sensory signals, to discern movements made by our own body from motions of other individuals and motions of the external environment (Deroualle & Lopez 2014).
Third, mental spatial transformation of the own visual viewpoint to that of another person presents an important underlying cognitive aspect of social cognition (Furlanetto 2013; Hamilton 2009; Newen & Vogeley 2003; also cited by Gallese & Cuccio this collection, pp. 9–11). More direct evidence supporting this hypothesis comes from a recent study that showed that physical whole-body rotations, which stimulate the vestibular sensory organs, affected the ability of participants to perform mental spatial transformations (van Elk & Blanke 2013).
Fourth, I have argued in previous sections of this commentary that multisensory spatial coding is a critical prerequisite that underlies pre-reflective brain mechanisms of the bodily self and social cognition. Because the vestibular cortical processing has been strongly associated with multisensory integration (for review see Lopez & Blanke 2011), it is likely that vestibular signals shape multisensory spatial coding relevant to the bodily self and social cognition (Deroualle & Lopez 2014; Pfeiffer et al. 2014).
Fifth, the distributed multisensory vestibular cortical network clearly overlaps with the neural structures involved in social cognition and the bodily self, which suggests that there is a functional contribution on the part of vestibular processing to these phenomena (compare figure 1c to 1a and 1b; compare also to Deroualle & Lopez 2014).
Together, these five points suggest that the vestibular system may be a promising candidate for future studies of the sensorimotor mechanisms of social cognition, which should motivate research on the intersection of vestibular cortical processing, mirror mechanisms, and intersubjectivity. These studies may, for instance, question how vestibular stimulation affects our ability to reconstruct the process of attention of another person, a function critical in the AS framework. Although the vestibular system is related to reflexive motor control, it is not clear whether it also affects motor resonance (see Deroualle & Lopez 2014 for a related proposal). One might ask whether vestibular processing facilitates or inhibits motor resonance and our understanding of intentional action observed in others. How about vestibular contributions to theory of mind and reasoning? On the other hand, does social interaction modulate vestibular functions, such as self-motion perception, postural stabilization, and gaze control? These questions address the role of vestibular processing in functional mechanisms relevant to the AS and ES frameworks. Furthermore, empirical research addressing the causal relationship between the AS and ES brain mechanisms and the bodily self and social cognition are needed, for instance by brain lesion analysis or direct brain stimulation.