Multisensory Integration and Internal Models for Sensing Gravity Effects in Primates

Abstract

Gravity is crucial for spatial perception, postural equilibrium, and movement generation. The vestibular apparatus is the main sensory system involved in monitoring gravity. Hair cells in the vestibular maculae respond to gravitoinertial forces, but they cannot distinguish between linear accelerations and changes of head orientation relative to gravity. The brain deals with this sensory ambiguity (which can cause some lethal airplane accidents) by combining several cues with the otolith signals: angular velocity signals provided by the semicircular canals, proprioceptive signals from muscles and tendons, visceral signals related to gravity, and visual signals. In particular, vision provides both static and dynamic signals about body orientation relative to the vertical, but it poorly discriminates arbitrary accelerations of moving objects. However, we are able to visually detect the specific acceleration of gravity since early infancy. This ability depends on the fact that gravity effects are stored in brain regions which integrate visual, vestibular, and neck proprioceptive signals and combine this information with an internal model of gravity effects.

Cerebellar Degeneration Increases Visual Influence on Dynamic Estimates of Verticality

“…Although we make the argument that participants' behavior during a dynamic subjective vertical task can be explained simply by an increase in vestibular noise, it remains unclear how cerebellar degeneration might affect other gravity-related visual processing. Recent evidence suggests that along with the temporo-parietal junction (TPJ) [39], the cerebellum and vestibular nuclei also contribute to the process of predicting visually represented gravitational acceleration [40] (for a review, see [41]). If such processing occurs downstream of verticality estimation and relies on common models of gravity or such noisy vestibular cues, we might expect them to exhibit correlated deficits.…”

Acceleration and deceleration at constant speed: systematic modulation of motion perception by kinematic sonification

“…5 Even if the theory of internal models does not focus comprehensively on modality-specific questions, internal models relyat least partially-on multimodal sensory streams and multisensory representations. [6][7][8] Extensive neurophysiological evidence on the integration of multisensory information down to the level of single neurons indicates a seamless integration of the senses, as well as a direct involvement of multisensory areas of the central nervous system (CNS) into motor regulation. [9][10][11][12] Even single multisensory convergence neurons in the deep layers of the superior colliculus integrate (afferent) visual, auditory, and proprioceptive input and affect orientation doi: 10.1111/nyas.13693 and attention behavior via (efferent) motor output, as described by Stein and Meredith 10 for cats.…”

Gravity highlights a dual role of the insula in internal models

“…Visual tasks have been shown to activate the insula. In an elegant study, Lacquaniti and colleagues, demonstrated that an internal representation of gravity is activated by visual motion that appears to be coherent with natural gravity (Indovina et al, 2005;Lacquaniti et al, 2014). The insular activation associated to neural predictive mechanisms was also observed during experiment of visual motion when comparing prediction versus perception of visual motion (Cheong et al, 2012).…”

“…The gravitational force significantly alters motion dynamics during the execution of movements. The insula, known to process the effects of gravity via a stored internal representation of gravitational acceleration, is activated for actual hand movements (Indovina et al, 2005;Lacquaniti et al, 2014;Rousseau et al, 2016). Here, we made a step forward by showing that the insula is also activated when the task mainly relied on mental predictive states.…”

“…Previous studies showed that the interaction with visual objects relies on an internal model of gravity, stored in the vestibular cortex. This internal representation of gravity is, however, only activated by visual motion that appears to be coherent with natural gravity (Indovina et al, 2005;Lacquaniti et al, 2014). Interestingly, the same authors found that mental imagery of objects' visual motion does not have access to the internal model of Earth gravity, but resorts to a simulation of visual motion compatible with a 0g environment (Gravano et al, 2017).…”