Where is my hand in space? The internal model of gravity influences proprioception

Abstract

Knowing where our limbs are in space is crucial for a successful interaction with the external world. Joint position sense (JPS) relies on both cues from muscle spindles and joint mechanoreceptors, as well as the effort required to move. However, JPS may also rely on the perceived external force on the limb, such as the gravitational field. It is well known that the internal model of gravity plays a large role in perception and behaviour. Thus, we have explored whether direct vestibular-gravitational cues could influence JPS. Participants passively estimated the position of their hand while they were upright and therefore aligned with terrestrial gravity, or pitch-tilted 45° backwards from gravity. Overall participants overestimated the position of their hand in both upright and tilted postures; however, the proprioceptive bias was significantly reduced when participants were tilted. Our findings therefore suggest that the internal model of gravity may influence and update JPS in order to allow the organism to interact with the environment.

The brain-body disconnect: A somatic sensory basis for trauma-related disorders

“…This modulatory role is crucial in multisensory integration, where the balancing of interoceptive and exteroceptive sensory input is critical in creating and maintaining our perception of reality while guiding adaptive and purposeful behavior ( Harricharan et al, 2021 ). Vestibular stimulation has a modulating effect on proprioceptive ( Gallagher et al, 2021 ), tactile, nociceptive ( McGeoch et al, 2009 ; Ferrè et al, 2013 ), and visual-proprioceptive cues ( Ponzo et al, 2018 ). Further, optogenetic stimulation of the medial vestibular nuclei results in enhanced cortical activations in response to visual and auditory stimuli ( Leong et al, 2019 ), while caloric vestibular stimulation has an analgesic effect ( Ferrè and Haggard, 2015 ) in healthy individuals.…”

How is the vestibular system affected by microgravity, and what implications could this have on elderly patients with ageing-related vestibular dysfunction?

“…Sensory systems often provide ambivalent information; the brain must have neural processes to resolve these ambiguities. For example, when the head moves in gravity, the otoliths shift with the direction of gravitational acceleration so that the hair cell receptors move and signal the brain of gravity (Gallagher et al, 2021). Nevertheless, it cannot distinguish between linear acceleration and gravity.…”

“…It is believed that the brain uses internal models, defined as "a neural mechanism that imitates the movement of an object to help with sensory, motor and cognitive functioning" (Zago, Lacquaniti, 2005)) to distinguish between linear acceleration and gravity. (Merfield, 1999) The internal gravity model is a network of subcortical and cortical regions (Gallagher et al, 2021). These parts will have increased activity when seeing targets falling with normal earth gravity versus objects not accelerating according to gravity.…”

“…Eye movements are more precise when tracing objects in 'normal' gravitational conditions versus objects in microgravity or hypergravity. In addition, the interception of moving objects is also more accurate in 'normal' gravity; in microgravity, there is a significant impairment in intercepting and predicting moving objects (Gallagher, 2021). Microgravity motor responses were often too early (Zago, Lacquaniti 2005).…”

“…Together, this suggests that gravitational acceleration is considered when we interact with our world, most likely through neural systems; this indicates that the internal model of gravity exists. (Gallagher, 2021). In addition, humans show asymmetric arm movement; this means that they are probably responding to marginally different environmental conditions, suggesting that the brain's internal model of gravity controls it (Gaveau et al, 2016).…”