Cerebral adaptation to lower motor neuron injury
2021; Elsevier BV; Volume: 424; Linguagem: Inglês
10.1016/j.jns.2021.117360
ISSN1878-5883
Autores Tópico(s)Spinal Cord Injury Research
ResumoIn this edition of the Journal of the Neurological Sciences, Li Hi Shing et al. present an intriguing report of cortical reorganisation in a cohort of poliomyelitis survivors: "Increased cerebral integrity metrics in poliomyelitis survivors: putative adaptation to longstanding lower motor neuron degeneration" [ [1] Li Hi Shing S. et al. Increased cerebral integrity metrics in poliomyelitis survivors: putative adaptation to longstanding lower motor neuron degeneration. J. Neur. Sci. 2021; 424: 117361https://doi.org/10.1016/j.jns.2021.117361 Abstract Full Text Full Text PDF Scopus (6) Google Scholar ]. The authors present a comprehensive neuroimaging analysis of a group of patients who had poliomyelitis in their infancy and they not only identify increased cortical partial volumes, but also increased white matter integrity in certain tracts. The study is not only interesting because it focuses on a relatively neglected neurological condition where woefully limited research has been carried out in recent years [ [2] Li Hi Shing S. et al. Post-polio syndrome: more than just a lower motor neuron disease. Front. Neurol. 2019; 10: 773 Crossref PubMed Scopus (25) Google Scholar ]. The findings presented by the authors are conceptually important because, in many respects, PPS represents a template condition for chronic lower motor neuron (LMN) pathology. While at first glance it may seem counterintuitive to perform a dedicated cerebral imaging study in a LMN condition, the meticulous evaluation of brain changes in a cohort with longstanding spinal anterior horn injury offers ample learning opportunities. There is emerging evidence that adaptive cortical reorganisation may occur in motor neuron disease [ [3] Bede P. et al. Degenerative and regenerative processes in amyotrophic lateral sclerosis: motor reserve, adaptation and putative compensatory changes. Neural Regen. Res. 2021; 16: 1208-1209 Crossref PubMed Scopus (4) Google Scholar ]. Similarly to the findings of Prof Bede's research group in PPS, imaging studies of adult forms of spinal muscular atrophy (SMA) have also revealed increased cerebral integrity metrics in the brain with concomitant spinal cord degeneration [ [4] Querin G. et al. The spinal and cerebral profile of adult spinal-muscular atrophy: a multimodal imaging study. Neuroimage Clin. 2019; 21: 101618 Crossref PubMed Scopus (32) Google Scholar ]. Cerebral changes in lower-motor neuron predominant conditions are under evaluated, and existing reports in SMA, Kennedy's disease (SBMA) and vascular spinal injuries are conflicting [ 5 Lebouteux M.V. et al. Revisiting the spectrum of lower motor neuron diseases with snake eyes appearance on magnetic resonance imaging. Eur. J. Neurol. 2014; 21: 1233-1241 Crossref PubMed Scopus (43) Google Scholar , 6 Hardiman O. et al. Neurodegenerative Disorders: A Clinical Guide. 2016 ed. Springer Cham Heidelberg New York Dordrecht London© Springer International Publishing Switzerland 2016: Springer International Publishing, 2016: 1-336 Crossref Google Scholar , 7 Querin G. et al. Biomarkers of spinal and bulbar muscle atrophy (SBMA): a comprehensive review. Front. Neurol. 2018; 9: 844 Crossref PubMed Scopus (16) Google Scholar ]. Putative adaptive changes in the brain have not only been detected in LMN conditions [ [4] Querin G. et al. The spinal and cerebral profile of adult spinal-muscular atrophy: a multimodal imaging study. Neuroimage Clin. 2019; 21: 101618 Crossref PubMed Scopus (32) Google Scholar ], but also demonstrated in mixed LMN-UMN pathologies such as ALS [ [8] Abidi M. et al. Adaptive functional reorganization in amyotrophic lateral sclerosis: coexisting degenerative and compensatory changes. Eur. J. Neurol. 2020; 27: 121-128 Crossref PubMed Scopus (30) Google Scholar , [9] Feron M. et al. Extrapyramidal deficits in ALS: a combined biomechanical and neuroimaging study. J Neurol. 2018 Sep; 265: 2125-2136 Crossref PubMed Scopus (26) Google Scholar ]. Functional studies using motor paradigms in ALS have consistently detected supplementary motor, subcortical, cerebellar, and ipsilateral motor cortex activation which is typically interpreted as 'function reorganisation' to carry out motor tasks in the presence of primary motor cortex degeneration [ [10] Proudfoot M. Bede P. Turner M.R. Imaging cerebral activity in amyotrophic lateral sclerosis. Front. Neurol. 2018; 9: 1148 Crossref PubMed Scopus (16) Google Scholar ]. Evidence from structural studies for such compensatory processes however is scarce. A reporting bias for only presenting degenerative changes is likely to exist, and increased integrity metrics, such as increased cortical thickness, increased partial volumes, or increased fractional anisotropy is either not evaluated at all in the statistical models, or, may not be reported due to the difficulty of interpretation. This is a missed opportunity as there is ample evidence from cognitive training, repetitive physical tasks requiring dexterity such as sports and playing musical instruments that 'positive' cortical changes occur over time. In fact, the core premise of rehabilitation medicine is that such 'adaptive' brain changes may occur with sufficient training. In Li Hi Shing's paper, patients who sustained anterior horn insult in their infancy, exhibit increased corticospinal tract and cerebellar white matter integrity compared to age-matched controls decades later on imaging. It is conceivable that the young age at the time of the spinal insult may have facilitated such cerebral adaptation. The notion that adaptive brain changes occur in response to an LMN insult is difficult to unequivocally demonstrate, as ideally, combined brain-cord imaging would be required [ [11] El Mendili M.M. et al. Spinal cord imaging in amyotrophic lateral sclerosis: historical concepts-novel techniques. Front. Neurol. 2019; 10: 350 Crossref PubMed Scopus (27) Google Scholar ] and only a longitudinal study design could explicitly demonstrate the progressive adaptive changes [ [12] Chipika R.H. et al. Tracking a fast-moving disease: longitudinal markers, monitoring, and clinical trial endpoints in ALS. Front. Neurol. 2019; 10: 229 Crossref PubMed Scopus (51) Google Scholar ]. In their research paper, Li Hi Shing et al. use a cohort of ALS patients as disease controls to showcase that the very same anatomical regions which show degeneration in ALS [ [13] Schuster C. et al. The segmental diffusivity profile of amyotrophic lateral sclerosis associated white matter degeneration. Eur. J. Neurol. 2016; 23: 1361-1371 Crossref PubMed Scopus (48) Google Scholar ], show increased integrity in a chronic LMN condition. These observations confirm the central role of rehabilitation medicine in the spectrum of motor neuron diseases, from childhood LMN pathologies to progressive mixed LMN-UMN phenotypes. The findings presented by the Computational Neuroimaging Group of Trinity College Dublin also demonstrate that structural imaging metrics may capture such adaptive changes. Given the importance of this subject, large prospective studies are needed to specifically evaluate these processes in more detail.
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