Body, action, and space representations in people affected by spinal cord injuries

Introduction

Anecdotical reports concerning modifications of the perception of the body, space, and action following a spinal cord injury (SCI) are well known to professionals that have experienced with these patients as they can report body misperceptions (e.g., phantom limb or body loss), misrepresentations of space (e.g., body or limbs position, distance lengthening), changes in action representation (e.g., illusionary and phantom limb movement leading to muscular fatigue) ( ; ; ; ). These sensations, linked to pain, the level of the lesion and the time passed since the lesion onset ( ), are symptoms of neuroplastic changes in areas related to the body, space, and action representation.

A spinal cord interruption, especially when this is not developmental but acquired, abruptly changes the brain–body communication. This modification alters the balance between the body sensorial inputs, the signals sent toward it, and the brain activity, leading to abnormalities in cortical and subcortical activity. Consequently, the brain neuroplastically changes itself ( ) into brain networks that are involved in body, space, and action representations. Therefore, modifications in these cognitive functions are likely to occur.

This chapter is organized as: a first section reviewing the main literature concerning neuroplastic modifications in SCI individuals, underlying those related to the body, space, or action representations, the following three sections will show the experimental outcomes from studies concerning these representations in SCI individuals, and a fourth section will highlight the experimental results showing the effects of rehabilitative trainings on these representations.

Finally, a concluding section will present the main findings, interpretations, and connections.

The neuroplasticity following SCI and the networks involved in the body, space, and action representations

Neuroplasticity mechanisms have been recently investigated in SCI. Different levels of activation in the sensory and motor cortices have shown, particularly a reduction of activity in areas corresponding to paralyzed limbs ( ) along with increased activation in areas corresponding to spared body parts ( ; ).

Other studies ( ) showed the expansion of the cortical hand area toward the leg area during upper limbs movements. An enlargement of the face representation in the surrounding areas in monkeys after SCI was observed in the primary and nonprimary somatosensory cortices ( ).

Other works found a general reorganization of somatotopic areas ( ; ) and their degeneration over time ( ).

All these neuroplastic changes relate to the body, space, and action representations; indeed, all the somatotopic areas are involved in BR ( ). Moreover, in BR, the posterior parietal cortex, integrating multisensory inputs and outputs has a fundamental role ( ) as this brain area is directly involved in the neuroplasticity following SCI, because of the sensorial modifications.

The understanding of others’ actions and space representations rely also on somatosensory cortices. In fact, the fronto-parietal “mirror” network ( ) includes the ventral premotor cortex and the inferior frontal gyrus. Space perception involves the intraparietal sulcus, the lateral occipital complex, and the premotor cortex ( ; ) in the peripersonal space representation, while the extrapersonal space perception is linked to an occipito-parietal circuit, a parieto-prefrontal pathway, and a parieto-premotor one ( ).

The unbalance between the somatosensory and other sensory feedbacks, causing fundamental changes in the neurological system after SCI, might cause of maladaptive neuroplasticity in these cognitive representations, causing modifications that may be subtle, or evident like phantom sensations ( ) and neuropathic pain ( ).

The body representations

Body ownership is an important aspect of our body representations (BR) and can be defined as the sensation that a bodily part is part of our body. Relevant disturbances can lead to Asomatognosia ( ), namely abnormalities in various facets of body ownership such as the experienced existence, visual self-recognition, and sense of belonging to contralesional body parts.

This facet of BR, investigated by the rubber-hand paradigm, appears to be modified according to neuroplastic cortical modifications. In the commonest version of the rubber-hand illusion (see Fig. 1 , ), participants observe a rubber-hand, i n a congruent position with their own body, synchronously touched with their hand, hidden from sight ( ). An asynchronous rubber-hand/real-hand touch should not elicit a body ownership sensation and, therefore, is used as control condition ( ).

In hand representation-deprived tetraplegics, the ownership sensation toward a rubber hand can be elicited by the synchronous tactile stimulation of the left cheek and the rubber hand (see Fig. 2 ; ). This is probably caused by the overlapping of the cheek somatic and motor representations over the representation of the hand that are normally contiguously represented ( ). A similar result with synchronous visuo-tactile stimulation of the upper back and rubber legs in SCI individuals with complete paraplegia was found ( ). Moreover, the subjective verbal report of the sensation of body ownership toward a body part seems to be captured by the mere vision of the body part, especially when there is a total lack of tactile sensations (lower limbs in people affected by complete paraplegia: ; rubber hand in a patient affected by tetraplegia: ).

A further, implicit paradigm to study body ownership relies on the body-view enhancement effect. This task exploits the effect of visual stimuli appearing on our body that evoke faster reactions than visual stimuli appearing on the same space location, but on a neutral surface ( ). By a modified version of this paradigm, it was observed that individuals affected by complete paraplegia feel body ownership for the parts of the body that have spared sensory and motor functions, but also the same level of body ownership for their wheelchair, while the lower limbs show no body ownership ( ). Interestingly, the same task executed with the SCI participant seated in a different, never used before, wheelchair shows that this redefines their whole BR: there is no body ownership toward the new wheelchair, the lower limbs, nor for the part of the body that has spared motor and sensory functions ( ).

The notion of body schema dates back to the seminal work of and can be nowadays defined as the dynamic representation of body parts and their movements, which derives from multiple sensory and motor inputs (e.g., proprioceptive, vestibular, tactile, visual, efference copy). Patients with an impaired body schema are not able to distinguish the position of their arm when their eyes are closed.

A popular experimental paradigm investigating this aspect is the Mental Body Rotation paradigm ( ). According to this, individuals are asked to identify the laterality of a hand or a foot presented on screen at different rotations. The underlying mechanisms of decision imply that participants rotate the bodily stimuli congruent with their body and, therefore, response times (RTs), required to align series of gradually more rotated images to the vertical congruent with the body position, are slower. This leads to a typical RTs pattern, characteristic of a normal body schema representation, called bio-mechanical effect ( ).

Mental Body Rotation paradigm confirms that complete SCI disrupts the influence of postural changes on the representation of the deafferented body parts (feet, but not hands) and, regardless the posture, whole-BR progressively deteriorates proportionally to SCI completeness ( ), as a direct effect of the somato-sensation lack in the affected body-parts in SCI individuals.

Indeed, in SCI participants, the misproprioception of the paralyzed body parts is not uncommon (77% of cases) and it is present in all people affected by complete tetraplegia ( ).

Also Disownership-like and Somatoparaphrenia-like sensations (sensations of not owning their own limbs, even attributing them to someone else, as in the latter case) are often reported (48% and 46%, respectively), altogether to illusory motion of paralyzed body parts (51%).

In all these cases, these bodily illusions are connected to the time since the lesion onset, the level of injury, and the presence of pain ( ).

Interestingly, these bodily illusions are less evident in presence of neuropathic and visceral pain. This apparently counterintuitive result addresses toward the fact that, in a deafferented/deefferented body, a pain sensation coming from the impaired body part is used by our cognitive system as a surrogate BR.