Interacting with virtual objects via embodied avatar hands reduces pain intensity and diverts attention

Hunter G Hoffman, Hunter G Hoffman

Abstract

The current study introduces a new paradigm for exploring cognitive factors in pain. Interacting with virtual objects via embodied avatar hands increased the illusion of "being there" in the virtual world, increased VR analgesia for acute pain, and reduced accuracy on an attention demanding task. Twenty-four healthy volunteer college students participated in this within-subject randomized crossover design study. During Phase 1, each participant received brief thermal pain stimuli during interactive embodied avatar VR vs. passive VR (no avatar and no interactivity), VR treatment order randomized. After each pain stimulus, participants provided subjective 0-10 ratings of pain. Compared to the passive VR condition, during the interactive avatar VR, participants reported significant reductions in (1) worst pain, (2) pain unpleasantness, (3) time thinking about pain and (4). they had significantly more fun during the pain stimulus (p = .000 for each). During Phase 2, participants performed a divided attention task in each of the two VR conditions. Participants made significantly more errors on the divided attention task during the interactive avatar VR condition, compared to passive VR, implicating an attention mechanism for how virtual reality reduces pain and helping understand how VR influences pain perception.Trial registration: NCT04245475. Date of registration: 29/01/2020.

Conflict of interest statement

The author declares no competing interests.

Figures

Figure 1
Figure 1
Increasing the illusion of “being there” in VR may increase the amount of attention drawn into VR, leaving less attention available to process incoming nociceptive signals. If so, participants may feel less pain during Avatar VR. Copyright Hunter Hoffman, www.vrpain.com.
Figure 2
Figure 2
Participants’ enrollment flowchart.
Figure 3
Figure 3
A detailed description of the stimulus sequence. Participants are randomly assigned to either Treatment Order 1 or Treatment Order 2.
Figure 4
Figure 4
While wearing the XTAL VR helmet, any movements of the hands or fingers in the real world are seen by the participant in the virtual world (the image on the right is from the Architecture World demo by VRgineering.com). Photo and image copyrights Hunter Hoffman, U.W., vrpain.com.
Figure 5
Figure 5
Phase 1. Compared to a passive VR version of the same world, interactive avatar VR was significantly more effective at reducing pain intensity (worst pain ratings).
Figure 6
Figure 6
Boxplot showing lower quartile, median, upper quartile, and outliers for Phase 1 results. Interactive avatar VR was significantly more effective at increasing the illusion of “being there” in the virtual world.
Figure 7
Figure 7
Compared to passive VR, interactive avatar VR significantly reduced participants’ accuracy on an attention demanding task.
Figure 8
Figure 8
Phase 1. On an n = 12 side study to test important assumptions of my thermal pain paradigm, consistent with my assumptions, as predicted, no significant differences were found between No VR, passive VR on Test 1 vs. passive VR again on Test 2 reducing pain intensity (worst pain ratings).

References

    1. Keefe FJ, et al. Virtual reality for persistent pain: a new direction for behavioral pain management. Pain. 2012;153:2163–2166. doi: 10.1016/j.pain.2012.05.030.
    1. Hoffman HG, et al. Immersive virtual reality as an adjunctive non-opioid analgesic for pre-dominantly Latin American children with large severe burn wounds during burn wound cleaning in the intensive care unit: A pilot study. Front. Hum. Neurosci. 2019;13:262. doi: 10.3389/fnhum.2019.00262.
    1. Melzack R. The tragedy of needless pain. Sci. Am. 1990;262:27–33. doi: 10.1038/scientificamerican0290-27.
    1. Krane EJ, Walco GA. With apologies to Lennon and McCartney, all we need is data: Opioid concerns in pediatrics. Clin. J. Pain. 2019;35:461–462. doi: 10.1097/AJP.0000000000000699.
    1. Malchow RJ, Black IH. The evolution of pain management in the critically ill trauma patient: Emerging concepts from the global war on terrorism. Crit. Care Med. 2008;36:S346–357. doi: 10.1097/CCM.0b013e31817e2fc9.
    1. McIntyre MK, Clifford JL, Maani CV, Burmeister DM. Progress of clinical practice on the management of burn-associated pain: Lessons from animal models. Burns. 2016;42:1161–1172. doi: 10.1016/j.burns.2016.01.023.
    1. Wilson N, Kariisa M, Seth P, Smith HT, Davis NL. Drug and opioid-involved overdose deaths—United States, 2017–2018. MMWR Morb. Mortal Wkly. Rep. 2020;69:290–297. doi: 10.15585/mmwr.mm6911a4.
    1. Birnie KA, Chambers CT, Spellman CM. Mechanisms of distraction in acute pain perception and modulation. Pain. 2017;158:1012–1013. doi: 10.1097/j.pain.0000000000000913.
    1. Donnelly TJ, Palermo TM, Newton-John TRO. Parent cognitive, behavioural, and affective factors and their relation to child pain and functioning in pediatric chronic pain: A systematic review and meta-analysis. Pain. 2020;161:1401–1419. doi: 10.1097/j.pain.0000000000001833.
    1. Fields HL. How expectations influence pain. Pain. 2018;159(Suppl 1):S3–S10. doi: 10.1097/j.pain.0000000000001272.
    1. Melzack R, Wall PD. Pain mechanisms: A new theory. Science. 1965;150:971–979. doi: 10.1126/science.150.3699.971.
    1. Noel M, Rabbitts JA, Tai GG, Palermo TM. Remembering pain after surgery: A longitudinal examination of the role of pain catastrophizing in children's and parents' recall. Pain. 2015;156:800–808. doi: 10.1097/j.pain.0000000000000102.
    1. Topham L, et al. The transition from acute to chronic pain: dynamic epigenetic reprogramming of the mouse prefrontal cortex up to 1 year after nerve injury. Pain. 2020;161:2394–2409. doi: 10.1097/j.pain.0000000000001917.
    1. Hoffman HG, Patterson DR, Carrougher GJ. Use of virtual reality for adjunctive treatment of adult burn pain during physical therapy: A controlled study. Clin J Pain. 2000;16:244–250. doi: 10.1097/00002508-200009000-00010.
    1. Hoffman HG. Virtual reality: a new tool for interdisciplinary psychology research. CyberPsychol. Behav. 1998;1:195–200. doi: 10.1089/cpb.1998.1.195.
    1. Hoffman HG, Doctor JN, Patterson DR, Carrougher GJ, Furness TA., 3rd Virtual reality as an adjunctive pain control during burn wound care in adolescent patients. Pain. 2000;85:305–309. doi: 10.1016/s0304-3959(99)00275-4.
    1. Dahlquist LM, et al. Active and passive distraction using a head-mounted display helmet: Effects on cold pressor pain in children. Health Psychol. 2007;26:794–801. doi: 10.1037/0278-6133.26.6.794.
    1. Garrett B, et al. A rapid evidence assessment of immersive virtual reality as an adjunct therapy in acute pain management in clinical practice. Clin. J. Pain. 2014;30:1089–1098. doi: 10.1097/AJP.0000000000000064.
    1. Hoffman HG. Virtual-reality therapy. Sci. Am. 2004;291:58–65. doi: 10.1038/scientificamerican0804-58.
    1. Jeffs D, et al. Effect of virtual reality on adolescent pain during burn wound care. J. Burn Care Res. 2014;35:395–408. doi: 10.1097/BCR.0000000000000019.
    1. Kathner I, Bader T, Pauli P. Heat pain modulation with virtual water during a virtual hand illusion. Sci. Rep. 2019;9:19137. doi: 10.1038/s41598-019-55407-0.
    1. Khadra C, et al. Effects of a projector-based hybrid virtual reality on pain in young children with burn injuries during hydrotherapy sessions: A within-subject randomized crossover trial. Burns. 2020 doi: 10.1016/j.burns.2020.04.006.
    1. Maani CV, et al. Virtual reality pain control during burn wound debridement of combat-related burn injuries using robot-like arm mounted VR goggles. J. Trauma. 2011;71:S125–130. doi: 10.1097/TA.0b013e31822192e2.
    1. Maani CV, et al. Combining ketamine and virtual reality pain control during severe burn wound care: One military and one civilian patient. Pain Med. 2011;12:673–678. doi: 10.1111/j.1526-4637.2011.01091.x.
    1. Lier EJ, Oosterman JM, Assmann R, de Vries M, van Goor H. The effect of Virtual Reality on evoked potentials following painful electrical stimuli and subjective pain. Sci. Rep. 2020;10:9067. doi: 10.1038/s41598-020-66035-4.
    1. Trost Z, France C, Anam M, Shum C. Virtual reality approaches to pain: Toward a state of the science. Pain. 2021;162:325–331. doi: 10.1097/j.pain.0000000000002060.
    1. Hoffman HG, et al. Modulation of thermal pain-related brain activity with virtual reality: Evidence from fMRI. NeuroReport. 2004;15:1245–1248. doi: 10.1097/01.wnr.0000127826.73576.91.
    1. Hoffman HG, et al. The analgesic effects of opioids and immersive virtual reality distraction: evidence from subjective and functional brain imaging assessments. Anesth Analg. 2007;105:1776–1783. doi: 10.1213/01.ane.0000270205.45146.db.
    1. Bergstrom I, Kilteni K, Slater M. First-person perspective virtual body posture influences stress: A virtual reality body ownership study. PLoS ONE. 2016;11:e0148060. doi: 10.1371/journal.pone.0148060.
    1. Dwan K, Li T, Altman DG, Elbourne D. CONSORT 2010 statement: extension to randomised crossover trials. BMJ. 2019;366:l4378. doi: 10.1136/bmj.l4378.
    1. Hoffman HG, et al. Virtual reality hand therapy: A new tool for nonopioid analgesia for acute procedural pain, hand rehabilitation, and VR embodiment therapy for phantom limb pain. J. Hand Ther. 2020;33:254–262. doi: 10.1016/j.jht.2020.04.001.
    1. Jensen MP. The validity and reliability of pain measures in adults with cancer. J. Pain. 2003;4:2–21. doi: 10.1054/jpai.2003.1.
    1. Williamson A, Hoggart B. Pain: a review of three commonly used pain rating scales. J. Clin. Nurs. 2005;14:798–804. doi: 10.1111/j.1365-2702.2005.01121.x.
    1. Slater M, Spanlang B, Corominas D. Simulating virtual environments within virtual environments as the basis for a psychophysics of presence. ACM Trans. Graphic. 2010;29:1–9. doi: 10.1145/1778765.1778829.
    1. Slater M, Usoh M, Steed A. Depth of presence in immersive virtual environments. Presence Teleoper. Virtual Environ. 1994;3:130–144. doi: 10.1162/pres.1994.3.2.130.
    1. Slater M, Wilbur S. A framework for immersive virtual environments (FIVE): speculations on the role of presence in virtual environments. Presence Teleoper. Virtual Environ. 1997;6:603–616. doi: 10.1162/pres.1997.6.6.603.
    1. Hoffman HG, et al. Using FMRI to study the neural correlates of virtual reality analgesia. CNS Spectr. 2006;11:45–51. doi: 10.1017/s1092852900024202.
    1. Al-Ghamdi NA, et al. Virtual reality analgesia with interactive eye tracking during brief thermal pain stimuli: A randomized controlled trial (crossover design) Front. Hum. Neurosci. 2019;13:467. doi: 10.3389/fnhum.2019.00467.
    1. Hoffman HG, et al. Manipulating presence influences the magnitude of virtual reality analgesia. Pain. 2004;111:162–168. doi: 10.1016/j.pain.2004.06.013.
    1. Hoffman HG, et al. Virtual reality helmet display quality influences the magnitude of virtual reality analgesia. J. Pain. 2006;7:843–850. doi: 10.1016/j.jpain.2006.04.006.
    1. Wender R, et al. Interactivity influences the magnitude of virtual reality analgesia. J. Cyber Ther. Rehabil. 2009;2:27–33.
    1. Craik F. On the transfer of information from temporary to permanent memory. Philos. Trans. R. Soc. B. 1983;302:341–359.
    1. Hoffman HG, Garcia-Palacios A, Kapa V, Beecher J, Sharar SR. Immersive virtual reality for reducing experimental ischemic pain. Int. J. Hum. Comput. Int. 2003;15:469–486. doi: 10.1207/S15327590ijhc1503_10.
    1. Jacoby LL, Woloshyn V, Kelley C. Becoming famous without being recognized—Unconscious influences of memory produced by dividing attention. J. Exp. Psychol. Gen. 1989;118:115–125. doi: 10.1037/0096-3445.118.2.115.
    1. Iidaka T, Anderson ND, Kapur S, Cabeza R, Craik FI. The effect of divided attention on encoding and retrieval in episodic memory revealed by positron emission tomography. J. Cogn. Neurosci. 2000;12:267–280. doi: 10.1162/089892900562093.
    1. Firoozabadi R, et al. Case report: Virtual reality analgesia in an opioid sparing orthopedic outpatient clinic setting: A case study. Front. Virtual Real. 2020 doi: 10.3389/frvir.2020.553492.
    1. Slater M, Usoh M. Representations Systems, Perceptual Position, and Presence in Immersive Virtual Environments. Presence Teleoper. Virtual Environ. 1993;2:221–233. doi: 10.1162/pres.1993.2.3.221.
    1. Martini M. Real, rubber or virtual: The vision of "one's own" body as a means for pain modulation. A narrative review. Conscious Cogn. 2016;43:143–151. doi: 10.1016/j.concog.2016.06.005.
    1. Martini M, Kilteni K, Maselli A, Sanchez-Vives MV. The body fades away: investigating the effects of transparency of an embodied virtual body on pain threshold and body ownership. Sci. Rep. 2015 doi: 10.1038/srep13948.
    1. Martini M, Perez-Marcos D, Sanchez-Vives MV. What color is my arm? Changes in skin color of an embodied virtual arm modulates pain threshold. Front. Hum. Neurosci. 2013;7:438. doi: 10.3389/fnhum.2013.00438.
    1. Matamala-Gomez M, DiazGonzalez AM, Slater M, Sanchez-Vives MV. Decreasing pain ratings in chronic arm pain through changing a virtual body. Different strategies for different pain types. J. Pain. 2019;20:685–697. doi: 10.1016/j.jpain.2018.12.001.
    1. Matamala-Gomez M, et al. Changing body representation through full body ownership illusions might foster motor rehabilitation outcome in patients with stroke. Front. Psychol. 2020;11:1962. doi: 10.3389/fpsyg.2020.01962.
    1. Matamala-Gomez M, Nierula B, Donegan T, Slater M, Sanchez-Vives MV. Manipulating the perceived shape and color of a virtual limb can modulate pain responses. J. Clin. Med. 2020;9:291. doi: 10.3390/jcm9020291.
    1. Solca M, et al. Heartbeat-enhanced immersive virtual reality to treat complex regional pain syndrome. Neurology. 2018;91:e479–e489. doi: 10.1212/WNL.0000000000005905.
    1. Hoffman HG, Patterson DR, Carrougher GJ, Sharar SR. Effectiveness of virtual reality-based pain control with multiple treatments. Clin. J. Pain. 2001;17:229–235. doi: 10.1097/00002508-200109000-00007.
    1. Campbell D, Stanley JC. Experimental and Quasi-Experimental Designs for Research. Chennai: Houghton Mifflin Company; 1963. pp. 47–50.
    1. Schulz KF, Grimes DA. Blinding in randomised trials: hiding who got what. Lancet. 2002;359:696–700. doi: 10.1016/S0140-6736(02)07816-9.
    1. Hoffman HG, et al. Virtual reality analgesia for children with large severe burn wounds during burn wound debridement. Front. Virtual Real. 2020;1:602299. doi: 10.3389/frvir.2020.602299.
    1. Ballantyne JC. The brain on opioids. Pain. 2018;159(Suppl 1):S24–S30. doi: 10.1097/j.pain.0000000000001270.
    1. Kipping B, Rodger S, Miller K, Kimble RM. Virtual reality for acute pain reduction in adolescents undergoing burn wound care: A prospective randomized controlled trial. Burns. 2012;38:650–657. doi: 10.1016/j.burns.2011.11.010.
    1. McSherry T, et al. Randomized, crossover study of immersive virtual reality to decrease opioid use during painful wound care procedures in adults. J Burn Care Res. 2018;39:278–285. doi: 10.1097/BCR.0000000000000589.
    1. Matamala-Gomez M, et al. Immersive virtual reality and virtual embodiment for pain relief. Front. Hum. Neurosci. 2019;13:279. doi: 10.3389/fnhum.2019.00279.

Source: PubMed

3
Tilaa