Published May 21, 2021
| Version 1
Journal article
Open
Embodying an artificial hand increases blood flow to the investigated limb
- 1. NeXT: Neurophysiology and Neuroengineering of Human-Technology Interaction Research Unit, Campus Bio-Medico University of Rome, via Alvaro del Portillo, 5, Rome, 00128, Italy
- 2. Headache and Neurosonology Unit, Neurology, Campus Bio-Medico University of Rome, via Alvaro del Portillo, 200, Rome, 00128, Italy
Description
Background: The autonomic nervous system is the main determinant of the blood flow directed towards a body part, and it is tightly connected to the representation of the body in the brain; would the experimental modulation of the sense of ownership of the limb affect its blood perfusion?
Methods: In healthy participants, we employed the rubber hand illusion paradigm to modulate limb ownership while we monitored the brachial artery blood flow and resistance of the investigated limb.
Results: In all conditions with brush-stroking, we found an initial drop in the blood flow due to tactile stimulation. Subsequently, in the illusion condition where both the rubber and real hand experience synchronous brush-stroking, the blood flow rose significantly faster and reached significantly higher values. Moreover, the increase in blood flow correlated to the embodiment level measured by questionnaires and, negatively, to the change of peripherical vascular resistance.
Conclusions: These findings demonstrate that modulating the representation of a body part impacts its blood perfusion.
Files
openreseurope-1-14712.pdf
Files
(3.0 MB)
| Name | Size | Download all |
|---|---|---|
|
md5:94628e167b8fb9ee2e1662c66a0e9a96
|
3.0 MB | Preview Download |
Additional details
References
- Critchley HD, Eccles J, Garfinkel SN (2013). Interaction between cognition, emotion, and the autonomic nervous system. Handb Clin Neurol. doi:10.1016/B978-0-444-53491-0.00006-7
- Craig AD (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci. doi:10.1038/nrn894
- Brüggemann J, Shi T, Apkarian AV (1997). Viscero-somatic neurons in the primary somatosensory cortex (SI) of the squirrel monkey. Brain Res. doi:10.1016/s0006-8993(97)00296-5
- Follett KA, Dirks B (1994). Characterization of responses of primary somatosensory cerebral cortex neurons to noxious visceral stimulation in the rat. Brain Res. doi:10.1016/0006-8993(94)91362-5
- Levinthal DJ, Strick PL (2012). The Motor Cortex Communicates with the Kidney. J Neurosci. doi:10.1523/JNEUROSCI.0406-12.2012
- Rebollo I, Devauchelle AD, Beranger B (2018). Stomach-brain synchrony reveals a novel, delayed-connectivity resting-state network in humans. Elife. doi:10.7554/eLife.33321
- Bultitude JH, Rafal RD (2010). Derangement of body representation in complex regional pain syndrome: report of a case treated with mirror and prisms. Exp Brain Res. doi:10.1007/s00221-009-2107-8
- McCabe CS, Blake DR (2008). An embarrassment of pain perceptions? Towards an understanding of and explanation for the clinical presentation of CRPS type 1. Rheumatology (Oxford). doi:10.1093/rheumatology/ken254
- AbuRahma AF, Robinson PA, Powell M (1994). Sympathectomy for reflex sympathetic dystrophy: factors affecting outcome. Ann Vasc Surg. doi:10.1007/BF02133000
- Förderreuther S, Sailer U, Straube A (2004). Impaired self-perception of the hand in complex regional pain syndrome (CRPS). Pain. doi:10.1016/j.pain.2004.05.019
- Sumitani M, Rossetti Y, Shibata M (2007). Prism adaptation to optical deviation alleviates pathologic pain. Neurology. doi:10.1212/01.wnl.0000250242.99683.57
- Pleger B, Tegenthoff M, Ragert P (2005). Sensorimotor returning in complex regional pain syndrome parallels pain reduction. Ann Neurol. doi:10.1002/ana.20394
- Maihöfner C, Handwerker HO, Neundörfer B (2003). Patterns of cortical reorganization in complex regional pain syndrome. Neurology. doi:10.1212/01.wnl.0000098939.02752.8e
- Mccabe CS, Haigh RC, Ring E (2003). A controlled pilot study of the utility of mirror visual feedback in the treatment of complex regional pain syndrome (type 1). Rheumatology (Oxford). doi:10.1093/rheumatology/keg041
- Moseley GL, Parsons TJ, Spence C (2008). Visual distortion of a limb modulates the pain and swelling evoked by movement. Curr Biol. doi:10.1016/j.cub.2008.09.031
- Ronchi R, Bernasconi F, Pfeiffer C (2017). Interoceptive signals impact visual processing: Cardiac modulation of visual body perception. Neuroimage. doi:10.1016/j.neuroimage.2017.06.064
- Aspell JE, Heydrich L, Marillier G (2013). Turning body and self inside out: visualized heartbeats alter bodily self-consciousness and tactile perception. Psychol Sci. doi:10.1177/0956797613498395
- Suzuki K, Garfinkel SN, Critchley HD (2013). Multisensory integration across exteroceptive and interoceptive domains modulates self-experience in the rubber-hand illusion. Neuropsychologia. doi:10.1016/j.neuropsychologia.2013.08.014
- Filippetti ML, Tsakiris M (2017). Heartfelt embodiment: Changes in body-ownership and self-identification produce distinct changes in interoceptive accuracy. Cognition. doi:10.1016/j.cognition.2016.11.002
- Tsakiris M, Jiménez AT-, Costantini M (2011). Just a heartbeat away from one's body: interoceptive sensitivity predicts malleability of body-representations. Proc Biol Sci. doi:10.1098/rspb.2010.2547
- Gleitman H (2004). Psychology by Gleitman Henry Fridlund Alan J Reisberg Daniel. Psychology.
- Esler M, Jennings G, Lambert G (1990). Overflow of catecholamine neurotransmitters to the circulation: source, fate, and functions. Physiol Rev. doi:10.1152/physrev.1990.70.4.963
- Blessing W, McAllen R, McKinley M (2016). Control of the Cutaneous Circulation by the Central Nervous System. Compr Physiol. doi:10.1002/cphy.c150034
- Krasnikov G, Tyurina M, Piskunova G (2020). Periodic Concentration of Mental Attention Changes the Structure of Oscillatory Processes in the Cardiovascular System. Human Physiology. doi:10.1134/S0362119720010107
- Abrahams V, Hilton S, Zbrożyna A (1964). The role of active muscle vasodilatation in the alerting stage of the defence reaction. J Physiol. doi:10.1113/jphysiol.1964.sp007371
- Kelly D (1966). Measurement of anxiety by forearm blood flow. Br J Psychiatry. doi:10.1192/bjp.112.489.789
- Rosenberg C (1970). Forearm blood flow in response to stress. J Abnorm Psychol. doi:10.1037/h0029883
- Ootsuka Y, Tanaka M (2015). Control of cutaneous blood flow by central nervous system. Temperature (Austin). doi:10.1080/23328940.2015.1069437
- Botvinick M, Cohen J (1998). Rubber hands' feel'touch that eyes see. Nature. doi:10.1038/35784
- Armel KC, Ramachandran VS (2003). Projecting sensations to external objects: evidence from skin conductance response. Proc Biol Sci. doi:10.1098/rspb.2003.2364
- Tsakiris M (2010). My body in the brain: a neurocognitive model of body-ownership. Neuropsychologia. doi:10.1016/j.neuropsychologia.2009.09.034
- Pinardi M, Ferrari F, D'Alonzo M (2020). 'Doublecheck: a sensory confirmation is required to own a robotic hand, sending a command to feel in charge of it'. Cogn Neurosci. doi:10.1080/17588928.2020.1793751
- Mioli A, D'Alonzo M, Pellegrino G (2018). Intermittent Theta Burst Stimulation Over Ventral Premotor Cortex or Inferior Parietal Lobule Does Not Enhance the Rubber Hand Illusion. Front Neurosci. doi:10.3389/fnins.2018.00870
- D'Alonzo M, Mioli A, Formica D (2019). Different level of virtualization of sight and touch produces the uncanny valley of avatar's hand embodiment. Sci Rep. doi:10.1038/s41598-019-55478-z
- Ocklenburg S, Rüther N, Peterburs J (2011). Laterality in the rubber hand illusion. Laterality. doi:10.1080/13576500903483515
- Rohde M, Di Luca M, Ernst MO (2011). The rubber hand illusion: feeling of ownership and proprioceptive drift do not go hand in hand. PLoS One. doi:10.1371/journal.pone.0021659
- Abdulkarim Z, Ehrsson HH (2016). No causal link between changes in hand position sense and feeling of limb ownership in the rubber hand illusion. Atten Percept Psychophys. doi:10.3758/s13414-015-1016-0
- Boas FE, Desser T, Kamaya A (2011). Does separating the resistive index into pre-and post-glomerular resistance and vascular compliance improve the diagnostic accuracy of renal transplant Doppler ultrasound. Am J Radiol.
- Bude RO, Rubin JM (1999). Relationship between the resistive index and vascular compliance and resistance. Radiology. doi:10.1148/radiology.211.2.r99ma48411
- Pourcelot L (1974). Velocimetrie ultrasonore doppler. Seminaire INSERM.
- D'Alonzo M (2021). Embodying an artificial hand increases blood flow to the investigated limb.
- Söderström T, Stefanovska A, Veber M (2003). Involvement of sympathetic nerve activity in skin blood flow oscillations in humans. Am J Physiol Heart Circ Physiol. doi:10.1152/ajpheart.00826.2000
- Kunkel P, Stead EA, Weiss S (1939). Blood flow and vasomotor reactions in the hand, forearm, foot, and calf in response to physical and chemical stimuli. J Clin Invest. doi:10.1172/JCI101038
- Tieri G, Gioia A, Scandola M (2017). Visual appearance of a virtual upper limb modulates the temperature of the real hand: a thermal imaging study in Immersive Virtual Reality. Eur J Neurosci. doi:10.1111/ejn.13545
- Carey M, Crucianelli L, Preston C (2019). The Effect of Visual Capture Towards Subjective Embodiment Within the Full Body Illusion. Sci Rep. doi:10.1038/s41598-019-39168-4
- Guterstam A, Larsson DEO, Zeberg H (2019). Multisensory correlations-Not tactile expectations-Determine the sense of body ownership. PLoS One. doi:10.1371/journal.pone.0213265
- Petkova VI, Ehrsson HH (2009). When right feels left: referral of touch and ownership between the hands. PLoS One. doi:10.1371/journal.pone.0006933
- Tsuji T, Yamakawa H, Yamashita A (2013). Analysis of electromyography and skin conductance response during rubber hand illusion. 2013 IEEE Workshop on Advanced Robotics and its Social Impacts. doi:10.1109/ARSO.2013.6705511
- Yuan Y, Steed A (2010). Is the rubber hand illusion induced by immersive virtual reality?. 2010 IEEE Virtual Reality Conference (VR). doi:10.1109/VR.2010.5444807
- D'Alonzo M, Mioli A, Formica D (2020). Modulation of Body Representation Impacts on Efferent Autonomic Activity. J Cogn Neurosci. doi:10.1162/jocn_a_01532
- Braithwaite JJ, Broglia E, Watson DG (2014). Autonomic emotional responses to the induction of the rubber-hand illusion in those that report anomalous bodily experiences: evidence for specific psychophysiological components associated with illusory body representations. J Exp Psychol Hum Percept Perform. doi:10.1037/a0036077
- Langley JN (1921). The autonomic nervous system (Pt. I).
- Wehrwein EA, Orer HS, Barman SM (2016). Overview of the anatomy, physiology, and pharmacology of the autonomic nervous system. Compr Physiol. doi:10.1002/cphy.c150037
- Moseley GL, Olthof N, Venema A (2008). Psychologically induced cooling of a specific body part caused by the illusory ownership of an artificial counterpart. Proc Natl Acad Sci U S A. doi:10.1073/pnas.0803768105
- Kammers MPM, Rose K, Haggard P (2011). Feeling numb: Temperature, but not thermal pain, modulates feeling of body ownership. Neuropsychologia. doi:10.1016/j.neuropsychologia.2011.02.039
- Tsakiris M, Tajadura-Jiménez A, Costantini M (2011). Just a heartbeat away from one's body: interoceptive sensitivity predicts malleability of body-representations. Proc Biol Sci. doi:10.1098/rspb.2010.2547
- van Stralen HE, van Zandvoort MJE, Kappelle LJ (2013). The Rubber Hand Illusion in a patient with hand disownership. Perception. doi:10.1068/p7583
- de Haan AM, van Stralen HE, Smit M (2017). No consistent cooling of the real hand in the rubber hand illusion. Acta Psychol (Amst). doi:10.1016/j.actpsy.2017.07.003
- Rohde M, Wold A, Karnath HO (2013). The human touch: skin temperature during the rubber hand illusion in manual and automated stroking procedures. PLoS One. doi:10.1371/journal.pone.0080688
- Chae Y, Lee IS, Jung WM (2014). Decreased peripheral and central responses to acupuncture stimulation following modification of body ownership. PLoS One. doi:10.1371/journal.pone.0109489
- Wyss CR, Brengelmann GL, Johnson JM (1974). Control of skin blood flow, sweating, and heart rate: role of skin vs. core temperature. J Appl Physiol. doi:10.1152/jappl.1974.36.6.726
- Abramson DI, Ferris EB (1940). Responses of blood vessels in the resting hand and forearm to various stimuli. Am Heart J. doi:10.1016/S0002-8703(40)90195-8
- Barnsley N, McAuley JH, Mohan R (2011). The rubber hand illusion increases histamine reactivity in the real arm. Curr Biol. doi:10.1016/j.cub.2011.10.039
- Zeller D, Friston KJ, Classen J (2016). Dynamic causal modeling of touch-evoked potentials in the rubber hand illusion. Neuroimage. doi:10.1016/j.neuroimage.2016.05.065
- Zeller D, Litvak V, Friston KJ (2015). Sensory processing and the rubber hand illusion--an evoked potentials study. J Cogn Neurosci. doi:10.1162/jocn_a_00705
- Burin D, Garbarini F, Bruno V (2017). Movements and body ownership: evidence from the rubber hand illusion after mechanical limb immobilization. Neuropsychologia. doi:10.1016/j.neuropsychologia.2017.11.004
- Gatta FD, Garbarini F, Puglisi G (2016). Decreased motor cortex excitability mirrors own hand disembodiment during the rubber hand illusion. eLife. doi:10.7554/eLife.14972
- Fossataro C, Bruno V, Giurgola S (2018). Losing my hand. Body ownership attenuation after virtual lesion of the primary motor cortex. Eur J Neurosci. doi:10.1111/ejn.14116
- Gentile G, Guterstam A, Brozzoli C (2013). Disintegration of multisensory signals from the real hand reduces default limb self-attribution: an fMRI study. J Neurosci. doi:10.1523/JNEUROSCI.1363-13.2013
- Vissing SF, Scherrer U, Victor RG (1991). Stimulation of skin sympathetic nerve discharge by central command. Differential control of sympathetic outflow to skin and skeletal muscle during static exercise. Circ Res. doi:10.1161/01.res.69.1.228
- Ferri F, Chiarelli AM, Merla A (2013). The body beyond the body: expectation of a sensory event is enough to induce ownership over a fake hand. Proc Biol Sci. doi:10.1098/rspb.2013.1140
- di Pino G, Romano D, Spaccasassi C (2020). Sensory- and Action-Oriented Embodiment of Neurally-Interfaced Robotic Hand Prostheses. Front Neurosci. doi:10.3389/fnins.2020.00389
- di Pino G, Maravita A, Zollo L (2014). Augmentation-related brain plasticity. Front Syst Neurosci. doi:10.3389/fnsys.2014.00109
- Niedernhuber M, Barone DG, Lenggenhager B (2018). Prostheses as extensions of the body: Progress and challenges. Neurosci Biobehav Rev. doi:10.1016/j.neubiorev.2018.04.020
- Moseley GL, Gallace A, Spence C (2012). Bodily illusions in health and disease: physiological and clinical perspectives and the concept of a cortical 'body matrix'. Neurosci Biobehav Rev. doi:10.1016/j.neubiorev.2011.03.013
- Blefari ML, Martuzzi R, Salomon R (2017). Bilateral Rolandic operculum processing underlying heartbeat awareness reflects changes in bodily self‐consciousness. Eur J Neurosci. doi:10.1111/ejn.13567
- Park HD, Blanke O (2019). Coupling inner and outer body for self-consciousness. Trends Cogn Sci. doi:10.1016/j.tics.2019.02.002
- Salvato G, Richter F, Sedeño L (2020). Building the bodily self-awareness: Evidence for the convergence between interoceptive and exteroceptive information in a multilevel kernel density analysis study. Hum Brain Mapp. doi:10.1002/hbm.24810