Can maladaptive cortical plasticity form new sensory experiences? Revisiting phantom pain

Abstract

Phantom pain has become an influential example of maladaptive cortical plasticity. According to this model, sensory deprivation following limb amputation allows for intra-regional invasion of neighbouring cortical representations into the former hand area of the primary sensorimotor cortex, which gives rise to pain sensations. Over the years, this model was extended to explain other disorders of pain, motor control and tinnitus, and has inspired rehabilitation strategies. Yet, other research, demonstrating that phantom hand representation is maintained in the sensorimotor system, and that phantom pain can be triggered by bottom-up aberrant inputs, may call this model to question. Using fMRI, we identified the cortical area representing the missing hand in a group of 18 arm amputees. This allowed us to directly study changes in the ‘phantom’ cortex associated with chronic phantom pain, using functional connectivity and voxel-based morphometry. We show that, while loss of sensory input is generally characterized by structural degeneration of the deprived sensorimotor cortex, the experience of persistent pain was associated with preserved intra-regional structure and functional organization. Furthermore, consistent with the dissociative nature of phantom sensations from other sensory experiences, phantom pain is also associated with reduced long-range inter-regional functional connectivity. We propose that this disrupted inter-regional connectivity may be consequential, rather than causal, of the retained yet isolated local representation of phantom pain. We therefore propose that, contrary to the maladaptive model, cortical plasticity occurs when powerful and long-lasting subjective sensory experience, most likely due to peripheral inputs, is decoupled from the external sensory environment.