Where is My Hand in Space? The Internal Model of Gravity Influences Proprioception

Overview

Journal Biol Lett

Specialty Biology

Date 2021 Jun 1

PMID 34062087

Citations 7

Authors

Maria Gallagher

Breanne Kearney

Elisa Raffaella Ferre

Affiliations

Soon will be listed here.

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.

Citing Articles

Instilling the perception of weight in augmented reality using minimal haptic feedback.

Watkins A, Ghosh R, Ullal A, Sarkar N Sci Rep. 2024; 14(1):24894.

PMID: 39438622 PMC: 11496738. DOI: 10.1038/s41598-024-75596-7.

Invariant representations in abstract concept grounding - the physical world in grounded cognition.

Friedrich J, Fischer M, Raab M Psychon Bull Rev. 2024; 31(6):2558-2580.

PMID: 38806790 PMC: 11680661. DOI: 10.3758/s13423-024-02522-3.

Mental Gravity: Depression as Spacetime Curvature of the Self, Mind, and Brain.

Kent L Entropy (Basel). 2023; 25(9).

PMID: 37761574 PMC: 10528036. DOI: 10.3390/e25091275.

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

Kearney B, Lanius R Front Neurosci. 2022; 16:1015749.

PMID: 36478879 PMC: 9720153. DOI: 10.3389/fnins.2022.1015749.

Perceptual Biases as the Side Effect of a Multisensory Adaptive System: Insights from Verticality and Self-Motion Perception.

Cuturi L Vision (Basel). 2022; 6(3).

PMID: 36136746 PMC: 9502132. DOI: 10.3390/vision6030053.

References

Zu Eulenburg P, Caspers S, Roski C, Eickhoff S . Meta-analytical definition and functional connectivity of the human vestibular cortex. Neuroimage. 2012; 60(1):162-9. DOI: 10.1016/j.neuroimage.2011.12.032. View

Gallagher M, Kearney B, Ferre E . Where is my hand in space? The internal model of gravity influences proprioception. Biol Lett. 2021; 17(6):20210115. PMC: 8169209. DOI: 10.1098/rsbl.2021.0115. View

Moscatelli A, Lacquaniti F . The weight of time: gravitational force enhances discrimination of visual motion duration. J Vis. 2011; 11(4). DOI: 10.1167/11.4.5. View

Trousselard M, Barraud P, Nougier V, Raphel C, Cian C . Contribution of tactile and interoceptive cues to the perception of the direction of gravity. Brain Res Cogn Brain Res. 2004; 20(3):355-62. DOI: 10.1016/j.cogbrainres.2004.03.008. View

Bretas R, Taoka M, Suzuki H, Iriki A . Secondary somatosensory cortex of primates: beyond body maps, toward conscious self-in-the-world maps. Exp Brain Res. 2020; 238(2):259-272. PMC: 7007896. DOI: 10.1007/s00221-020-05727-9. View

Alberts B, Selen L, Bertolini G, Straumann D, Medendorp W, Tarnutzer A . Dissociating vestibular and somatosensory contributions to spatial orientation. J Neurophysiol. 2016; 116(1):30-40. PMC: 4961747. DOI: 10.1152/jn.00056.2016. View

Indovina I, Maffei V, Bosco G, Zago M, Macaluso E, Lacquaniti F . Representation of visual gravitational motion in the human vestibular cortex. Science. 2005; 308(5720):416-9. DOI: 10.1126/science.1107961. View

Maffei V, Mazzarella E, Piras F, Spalletta G, Caltagirone C, Lacquaniti F . Processing of visual gravitational motion in the peri-sylvian cortex: Evidence from brain-damaged patients. Cortex. 2016; 78:55-69. DOI: 10.1016/j.cortex.2016.02.004. View

Allen M, Poggiali D, Whitaker K, Marshall T, van Langen J, Kievit R . Raincloud plots: a multi-platform tool for robust data visualization. Wellcome Open Res. 2023; 4:63. PMC: 6480976. DOI: 10.12688/wellcomeopenres.15191.2. View

10.

Harris L, Jenkin M, Dyde R, Jenkin H . Enhancing visual cues to orientation: suggestions for space travelers and the elderly. Prog Brain Res. 2011; 191:133-42. DOI: 10.1016/B978-0-444-53752-2.00008-4. View

11.

Deecke L, Schwarz D, FREDRICKSON J . Vestibular responses in the rhesus monkey ventroposterior thalamus. II. Vestibulo-proprioceptive convergence at thalamic neurons. Exp Brain Res. 1977; 30(2-3):219-32. DOI: 10.1007/BF00237252. View

12.

Barra J, Perennou D, Thilo K, Gresty M, Bronstein A . The awareness of body orientation modulates the perception of visual vertical. Neuropsychologia. 2012; 50(10):2492-8. DOI: 10.1016/j.neuropsychologia.2012.06.021. View

13.

Gallagher M, Torok A, Klaas J, Ferre E . Gravity prior in human behaviour: a perceptual or semantic phenomenon?. Exp Brain Res. 2020; 238(9):1957-1962. PMC: 7438378. DOI: 10.1007/s00221-020-05852-5. View

14.

Vimal V, DiZio P, Lackner J . Learning dynamic balancing in the roll plane with and without gravitational cues. Exp Brain Res. 2017; 235(11):3495-3503. DOI: 10.1007/s00221-017-5068-3. View

15.

Miller W, Maffei V, Bosco G, Iosa M, Zago M, Macaluso E . Vestibular nuclei and cerebellum put visual gravitational motion in context. J Neurophysiol. 2007; 99(4):1969-82. DOI: 10.1152/jn.00889.2007. View

16.

Lacquaniti F, Bosco G, Gravano S, Indovina I, La Scaleia B, Maffei V . Multisensory integration and internal models for sensing gravity effects in primates. Biomed Res Int. 2014; 2014:615854. PMC: 4100343. DOI: 10.1155/2014/615854. View

17.

Gentili R, Cahouet V, Papaxanthis C . Motor planning of arm movements is direction-dependent in the gravity field. Neuroscience. 2007; 145(1):20-32. DOI: 10.1016/j.neuroscience.2006.11.035. View

18.

Schmidt L, Artinger F, Stumpf O, Kerkhoff G . Differential effects of galvanic vestibular stimulation on arm position sense in right- vs. left-handers. Neuropsychologia. 2013; 51(5):893-9. DOI: 10.1016/j.neuropsychologia.2013.02.013. View

19.

Knox J, Coppieters M, Hodges P . Do you know where your arm is if you think your head has moved?. Exp Brain Res. 2006; 173(1):94-101. DOI: 10.1007/s00221-006-0368-z. View

20.

Jorges B, Lopez-Moliner J . Gravity as a Strong Prior: Implications for Perception and Action. Front Hum Neurosci. 2017; 11:203. PMC: 5408029. DOI: 10.3389/fnhum.2017.00203. View