Elsevier

Neuropsychologia

Volume 49, Issue 5, April 2011, Pages 1316-1321
Neuropsychologia

Feeling numb: Temperature, but not thermal pain, modulates feeling of body ownership

https://doi.org/10.1016/j.neuropsychologia.2011.02.039Get rights and content

Abstract

There is an important link between pain, regulation of body temperature, and body ownership. For example, an altered feeling of body ownership – due to either chronic pain or “rubber-hand illusions” (RHI) – is associated with reduced temperature of the affected limb. However, the causal relationships within this triad are not well understood. We therefore investigated whether external manipulation of body temperature can influence body ownership. We used a thermode to make the right hand of healthy participants either painfully cold, cool, neutral, warm or painfully hot. Next, we induced the RHI and investigated its effects on the perceived position of the hand, on the subjective feeling of body ownership, and on physical changes in hand temperature. We replicate previous reports that inducing the RHI produces a decrease in limb temperature. Importantly, we demonstrate for the first time a causal effect in the opposite direction. Cooling down the participant's hand increased the strength of the RHI, while warming the hand externally decreased the strength of the RHI. Finally, we show that the painful extremes of these temperatures do not modulate the RHI. Hence, while thermosensation is an important driver of body ownership, pain seems to bypass the multisensory mechanisms of embodiment.

Highlights

▸ Previous studies showed a reduction in the temperature of a disowned body part. ▸ We show an opposite causal relationship between temperature and body ownership. ▸ External hand cooling facilitates disownership while warming impedes disownership. ▸ The painful extremes of these temperatures do not change feeling of body ownership. ▸ Temperature modifies while thermal pain bypasses multisensory embodiment mechanisms.

Introduction

The word “numb” is often used to describe a lack of sensation, but it is used in two very different senses. On the one hand, parts of the body may go numb due to extreme cold. The resulting lack of sensation can produce both the feeling that the body part is no longer ours but also result in physical pain. On the other hand, emotional pain, grief or exhaustion can also make us numb, which means that both our affects and sensations are reduced. Interestingly, although both senses of numbness imply a general lack of feeling, both are clearly associated with subjective feelings of pain, and with changes in homeostatic body regulation. These interactions point to an important triadic link in neuroscience that is not yet fully understood, between feeling of body ownership, body temperature and pain.

We both feel and know that we have a body (the feeling of embodiment), that belongs uniquely to ourselves (the feeling of body ownership), and that occupies a distinctive position in space, defining a first person perspective (body localization). Indeed, “I” am always and necessarily “here” (Longo, Kammers, Gomi, Tsakiris, & Haggard, 2009). However, although we take these feelings of localization for granted, they can be selectively disturbed. For example, out of body experiences involve the feeling that the self is located outside the physical body (Blanke, Landis, Spinelli, & Seeck, 2004). In this situation, people experience and recognize their own body from a third person perspective (Lopez, Halje, & Blanke, 2008). Conversely, in sensorimotor deficits such as somatoparaphrenia, patients experience their limb as belonging to a third person (Rode et al., 1992), rather than seeing it from the normal first-person perspective.

Such experiences of altered embodiment are caused by disintegration of the normally coherent multisensory information that flows from the body to the brain. Strikingly, multisensory disintegration produces not only an alteration in bodily self-consciousness, disembodiment, or reduced feeling of body ownership, but can also lead to a strong experience of pain. For example, loss of somatosensory afferent information can trigger both reorganization of cortical body representations, and pain in a phantom limb (Ramachandran & Hirstein, 1998). Conversely, disorders such as phantom limb pain (Hill, 1999, Ramachandran and Rogers-Ramachandran, 1996), Complex Regional Pain Syndrome (CRPS) (Moseley, 2005) and chronic back pain (Moseley, 2008) can disturb the feelings of embodiment, body ownership, and body localization. Remarkably, restoration of coherent multisensory information, for example by illusory vision of the phantom limb can reduce this pain (Flor et al., 2006, Hill, 1999, Ramachandran and Rogers-Ramachandran, 1996; but see Moseley, Gallace, & Spence, 2008 for a review).

Chronic pain can also disrupt representations of the body. For example, mental hand rotation is slower for the affected hand than the unaffected hand of chronic pain patients (Moseley, 2004, Schwoebel et al., 2001). This delay is correlated with the intensity of the pain (Schwoebel, Coslett, Bradt, Friedman, & Dileo, 2002) and the duration of the symptoms (Moseley, 2004). Furthermore, chronic pain significantly increases the perceived size of the affected body part (Moseley, 2005). Manipulating the perceived size of a body part can also influence one's experience of pain. For example, manipulating the size at which Complex Regional Pain Syndrome (CRPS) patients viewed their affected hand using a combination of magnifying and reducing lenses produced directly proportional changes in pain levels (Moseley, Parsons, & Spence, 2008). Pain is thereby clearly related both to cerebral body representation and to spatial localization of the body.

Just as failure of multisensory integration in pathology produces abnormal body experiences, manipulations of multisensory input in healthy volunteers produce clear alterations in bodily awareness. For example, the Rubber Hand Illusion (RHI – Botvinick & Cohen, 1998) involves synchronous stroking of a viewed rubber hand and the participant's own unseen hand. Typically, the rubber hand is placed in a different location from the real hand. The visual-tactile correlation provided by synchronous stroking seems to be interpreted by the brain as evidence that the rubber hand and the real hand are one and the same, even though visual and proprioceptive position senses suggest they are in different locations. The brain resolves this conflict by accepting the rubber hand as part of the body and by adapting the perceived position of the real hand towards the seen location of the rubber hand (Botvinick & Cohen, 1998). That is, the representation of one's own body is spatially reorganized to integrate correlating multisensory information. The RHI can therefore be seen as acquiring a sense of ownership over the rubber hand, as well as a reciprocal disownership or disembodiment of one's own hand (Moseley, Olthof, et al., 2008). Recently, Moseley, Olthof, et al. (2008) observed a drop in temperature of the participant's own hand during the RHI, and interpreted this as a consequence of “disembodiment” associated with the illusion. Decreased limb temperature is also linked to chronic disorders of bodily awareness that involve pain, such as CRPS (Janig & Baron, 2003).

Hence, there seems to be an important triadic link relating body ownership, pain, and body temperature, though the precise relations between the three elements are not well understood. Previous studies suggested that changes in body temperature regulation are a consequence of the disembodiment triggered by the RHI (Moseley, Olthof, et al., 2008). However, the possibility of a causal link in the opposite direction has not been explored. In particular, it remains unclear whether changes in body temperature might themselves influence bodily awareness. This possibility seems plausible, given the strong links between pain and thermosensation (Craig, 2002), and also between pain and bodily awareness (Janig & Baron, 2003). The links between acute pain and body ownership also deserve further investigation. Chronic pain has been reported to change one's sense of body ownership (Moseley, 2004). Acute painful stimulation during the RHI however has been shown to have no additional effects on one's sense of body ownership over innocuous RHI stimulation (Capelari, Uribe, & Brasil-Neto, 2009). However, the effect of acute pain on the sense of body (dis)ownership has not been otherwise investigated.

In the present study we therefore investigated the interaction between body ownership, pain, and temperature using the RHI. During the experiment, we externally manipulated the temperature of the participant's hand, and then induced the RHI using the traditional visual-tactile stimulation (Botvinick & Cohen, 1998). We measured the RHI effect in three ways: (1) by asking participants to localize their unseen hand, (2) by a questionnaire investigating bodily awareness and feeling of body ownership, and (3) by measuring changes in the temperature of the participant's hand that are a consequence of the RHI (measured at a site remote from the external temperature manipulation). We particularly aimed to assess whether mild external body temperature changes and thermal pain would alter bodily awareness and whether they would do so in a similar way.

Section snippets

Participants

Ten healthy participants took part in this experiment of which 7 were female (mean age 23.9, range: 18–30). One participant was excluded from the study due to an unusually low baseline skin temperature. All participants gave written informed consent prior to the experiment. Right-handedness was assessed by the Edinburgh Inventory (mean: 89.17, range: 83.33–100). Participants were naïve to the rationale of the experiment and received a small fee for participation. The study was approved by the

Results

One of five different temperatures was applied to the palm of the participant's right hand with a large thermode (Painfully Cold, Cool, Neutral, Warm, and Painfully Hot). Next, the Rubber Hand Illusion (RHI) was induced by synchronous (Illusion condition) or asynchronous (Control condition) stroking of the dorsum of the index finger of the participant's unseen right hand and the corresponding part of the rubber hand. Three measures of the RHI were obtained: (1) perceived position of the unseen

Discussion

In the present study, we used the Rubber Hand Illusion (RHI) to investigate the interaction between thermosensation (non-painful and painful), thermoregulation, and the subjective experience of body ownership. We replicate previous reports that changes in bodily awareness influence thermoregulation (Moseley, Olthof, et al., 2008). More importantly, we demonstrate for the first time a causal effect in the opposite direction. We show that externally cooling a limb increases the strength of the

Acknowledgements

MK was supported by an ESRC-MRC Postdoctoral Fellowship (G0800056/86947). PH was supported by a Leverhulme Trust Major Research Fellowship. Additional support was provided by EU FP7 project VERE.

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