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Physiologically impossible movement of phantom limbs explained

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Nature mentioned our recent PNAS paper in their research highlights Neurology: Impossible movements:

Scientists can alter people’s perception of their bodies by playing with their sensory input, for example by using trick mirrors or touch. Now Lorimer Moseley of the Prince of Wales Medical Research Institute in Sydney, Australia, and Peter Brugger of University Hospital Zurich in Switzerland show that the sensation of having impossible bodily forms can be generated using thought alone…

The team asked seven amputees who have a phantom arm to perform a wrist movement with the phantom limb that would be impossible with an actual wrist. Four were able to learn the movement, which induced a change in body image and made some previously easy movements of the phantom arm more difficult.

“What is all this fuss about?”  Well, we reckon this paper is of fundamental relevance to how we understand ourselves. I know, it is a very big call. However, here is our pitch:

The feeling that we have of our bodies – their size, shape, position – that they belong to us, is a fundamental aspect of self-awareness. Neuroscientists, psychologists, clinicians and philosophers have long recognized that an understanding of how the brain represents the self is key to understanding how the brain produces consciousness [1-4].  There has been a great deal of interest recently in how our bodily awareness, or ‘body image’ interacts with our body.  For example, our group has shown that modifying bodily awareness of a single limb can disrupt localized blood flow and sensory processing in that single limb [5, 6].  Body image supposedly depends on an innate representation that is modified by sensory input.  Profound changes in body image can be induced by modifying sensory input. The potent influence of sensory feedback on body image is demonstrated by the induction of impossible configurations of the body image.  For example, a blind-folded participant places the palm of their own hand on their forehead.  The tendon of the muscle that straightens the elbow, is vibrated at about 70Hz, which induces the illusion in the participant that they can feel their elbow bending, which in turn feels as though the participant’s hand is moving backwards through their own head [4].

No-one has ever tested whether changes in body image can be induced without disrupting sensory input – can they be self-generated by the brain?  We have overcome the methodological barrier to asking this question by first taking a covert approach to the question, which removes participant reporting bias, and then using robust empirical data from established motor imagery tasks to corroborate participant report.

This result has implications for our understanding of self-awareness because it shows that our bodily awareness can change in a profound way by internally generated commands (ie without sensory or external feedback) and that the Newtonian principles that govern our body – that movement repertoire is limited by the biomechanical characteristics of our body parts – also govern our brain at a fundamental level, not just as a reflection of the body.

This result also has important implications for our understanding of motor learning: it has been accepted for some time that motor learning depends on proprioceptive or external feedback, yet these participants learnt an entirely new movement with neither proprioceptive or external feedback. This demonstrates that the brain is able to use the internally transformed visual image of an outcome state to compare against the predicted state generated by the motor plan.

We suspect that these results will be of interest to philosophers and scientists across the biological, consciousness, psychological and artificial intelligence sciences.

(at least this was the jist of our cover letter to the journal PNAS….)

References

1. Damasio A (2000) The feeling of what happens: body and emotion in the making of consciousness. (Vintage, London).
2. Churchland PS (2002) Self-representation in nervous systems Science 296, 308-310.
3. Ramachandran VS (1998) Consciousness and body image: lessons from phantom limbs, Capgras syndrome and pain asymbolia Philosophical Transactions of the Royal Society of London – Series B: Biological Sciences 353, 1851-1859.
4. Price EH (2006) A critical review of congenital phantom limb cases and a developmental theory for the basis of body image Consciousness and Cognition 15, 310-322.
5. Moseley GL, Olthof N, Venema A, Don S, Wijers M, Gallace A, & Spence C (2008) Psychologically induced cooling of a specific body part caused by the illusory ownership of an artificial counterpart Proc Natl Acad Sci 105, 13169-13173.
6. Moseley GL, Parsons TJ, & Spence C (2008) Visual distortion of a limb modulates the pain and swelling evoked by movement. Curr Biol 18, R1047-R1048.
7. Parsons LM (2001) Integrating cognitive psychology, neurology and neuroimaging Acta Psychol. (Amst). 107, 155-181.

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