Lack of somatotopy in the macaque lateral corticospinal tract: implications for understanding of human incomplete spinal injury

Neurophysiological Bases of Human Movement (King's College London, UK) (2023) Proc Physiol Soc 55, C33

Poster Communications: Lack of somatotopy in the macaque lateral corticospinal tract: implications for understanding of human incomplete spinal injury

Roger Lemon1, Kimberley Stilwell-Morecraft1, Ge Jizhi1, Robert Morecraft1, Alexander Kraskov1,

1Queen Square Institute of Neurology UCL London United Kingdom, 2Division of Basic Biomedical Sciences, Laboratory of Neurological Sciences, University of South Dakota Vermillion United States, 3Biosciences Institute, Faculty of Medical Sciences, Newcastle University Newcastle-upon-Tyne United Kingdom,

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In some cases of incomplete cervical spinal cord injury (iSCI) there is marked paresis and dysfunction of upper extremity movement, but not of the lower extremity. A persistent explanation of such symptoms is a somatotopic organization of corticospinal tract (CST) fibres passing through the decussation of the pyramidal tract (PT) at the craniovertebral junction (CVJ) and lateral corticospinal tract (LCST). In Central Cord Syndrome, it has been repeatedly suggested that traumatic injury to the core of the cervical spinal cord may include selective damage to medially-located arm/hand LCST fibres, without compromising laterally-located leg fibres.

To investigate whether somatotopic organization exists in the primate PT, CVJ or LCST, and with

approval of the USD IACUC, we made a systematic investigation using localised injection of high-resolution anterograde tracers into physiologically-characterised cortical representations of 17 anaesthetised macaque monkeys. We thereby defined the course of the corticospinal projection (CSP) through the PT, CVJ and LCST from sensorimotor areas of the frontal and parietal lobe contributing to the corticospinal tract, including the arm/hand, shoulder and leg areas of primary motor cortex (M1), dorsal and ventral premotor cortex, SMA, rostral and caudal cingulate motor areas, S1 arm and leg areas, and parietal area PE. The approach used labels CST fibres of all sizes, large and small. We found no evidence for somatotopic organization of CST fibres passing through the CVJ or contralateral LCST.  Fibre labelling from each cortical representation was widespread throughout the PT, CVJ and LCST, and overlapped extensively with fibres from other representations. Fibres from some of the parietal areas tended to cluster in one particular region of the PT, but again overlapped with fibres from other areas. Area S1 leg and arm projections were completely overlapping.

Stereological analysis of tissue from PT and two different spinal levels (C5, C8) from 8 cases revealed no significant difference in the number of labelled M1 arm/hand fibres in different medio-lateral sectors across PT and LCST. This was assessed from the slope of the line regressing labelled fibre numbers in medial, ventral and lateral sectors of PT/LCST (p range 0.16 – 0.80). A similar result was found for fibres labelled from the M1 leg area (0.6-0.22) and shoulder (0.08-0.60) area.

Our investigation firmly rejects the concept of somatotopy amongst CST fibres passing through the PT, CVJ and LCST. All CST fibres in the LCST, regardless of their cortical origin, would thus appear to be equally susceptible to focal or diffuse injury. The disproportionate impairment of arm/hand movement after iSCI must therefore be due to other factors. One is the greater dependence of hand/arm movements on the integrity of the CST, when compared with lower limb function,  and particularly on the fast-conducting cortico-motoneuronal input to hand and digit muscles. The dispersed and commixed nature of frontal and parietal CST fibres is clearly a fundamental principle of corticospinal organization and may be important in motor recovery after cervical iSCI in humans. Textbooks and teaching explaining the effects of iSCI should be revised in the light of these new findings.



Where applicable, experiments conform with Society ethical requirements.

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