ReviewCorticospinal tract development and its plasticity after perinatal injury
Introduction
The young human brain is highly plastic and thus brain lesions during development interfere with the innate development of architecture, connectivity and mapping of functions and trigger modifications in structure, wiring and representations (for review see (Payne and Lomber, 2001). Older concepts of developmental plasticity focused on the protective effect of a young age at the time of the brain damage (Kennard, 1936). In these views, a younger rather than an older age at onset was thought to produce fewer and/or less severe symptoms and a more rapid recovery. It is now clear that quite specific effects of early brain damage persist and produce complex and often severe patterns of impairment that are different from that observed following lesions in the adult brain. Furthermore, although an understanding of the nature of neural plasticity in response to damage is critical to those attempting to augment recovery from neurological insults, it is misleading to treat the underlying mechanisms as self-reparative. The appreciation that these mechanisms evolved as mechanism for activity-dependent fine tuning of neural circuitry during normal development and the fact that they may only be available for response to damage as an incidental side effect, can help to focus on how best to augment the desirable and avoid any undesirable effects.
In childhood the motor cortex and/or corticospinal tract is a common site of brain damage and the pre or immediately perinatal period, is the most common time for brain damage to occur. It is now increasingly appreciated that lesions at such an early stage in its development may lead to substantial reorganisation of the corticospinal system during subsequent development (Eyre, 2005; Martin, 2005; Terashima, 1995). In the mature nervous system, synaptic plasticity in pre-existing pathways and the formation of new circuits through collateral sprouting of lesioned and unlesioned fibres are the principle components of post-lesional plasticity (Raineteau and Schwab, 2001). In the developing nervous system it is clear that there is much greater potential for plasticity, which may involve plasticity not only of the ipsi-lesional cerebral cortex but also of the contra-lesional cortex and of spinal cord networks (Benecke et al., 1991; Carr et al., 1993; Cao et al., 1994; Lewine et al., 1994; Maegaki et al., 1995; Terashima, 1995; Nirkko et al., 1997; O’Sullivan et al., 1998; Balbi et al., 2000; Eyre et al., 2000a, Eyre et al., 2001a, Eyre et al., 2001b; Thickbroom et al., 2001; Staudt et al., 2004). Functional and anatomical evidence demonstrates that spontaneous plasticity can be modified by activity, as well as by specific experimental manipulations. Knowledge of the time course and processes of corticospinal system development and plasticity is essential both for a better understanding of current rehabilitation treatments and for the design of new strategies for the treatment of children who sustain damage to the corticospinal system early in life.
Section snippets
Corticospinal tract development and plasticity in sub-primate mammals
The development of the corticospinal system has been studied most extensively in the rat. In the neonatal rat the corticospinal projection originates from the whole neocortex including the visual cortex (O’Leary et al., 1992; Stanfield and O’Leary, 1985) (Fig. 1). The axons that enter the grey matter occupy a larger terminal field and contact more spinal neurones than in the adult (Curfs et al., 1994, Curfs et al., 1996, Curfs et al., 1995; Kamiyama et al., 2006). Corticospinal projections in
Corticospinal development and plasticity in subhuman primates
It has been proposed that corticospinal innervation in primates may not be governed by the same processes nor have the degree of plasticity described in sub-primate mammals (Armand et al., 1997; O’Leary et al., 1992). However, in the Macaque monkey a halving of the area of the cerebral cortex from which corticospinal axons originate has been demonstrated during the first 8 postnatal months, when brain volume overall increases by more than 30%. These changes are associated with a three-fold
Corticospinal development and plasticity in man
Human corticospinal axons reach the lower cervical spinal cord by 24 weeks post-conceptional age (Fig. 2). Following a waiting period of up to a few weeks they progressively innervate the grey matter such that there is extensive innervation of spinal neurones, including motoneurones, prior to birth (Eyre et al., 2000a, Eyre et al., 2002; Eyre, 2005) By 40 weeks post-conceptional age corticospinal axons have begun to express neurofilaments and to undergo myelination (Fig. 3). These anatomical
Corticospinal system reorganisation in man
There are now repeated observations in man that demonstrate substantial plastic reorganisation of the motor cortex and corticospinal projections following pre or perinatal lesions to the corticospinal system (Balbi et al., 2000; Benecke et al., 1991; Cao et al., 1994; Carr et al., 1993; Chu et al., 2000; Eyre et al., 2007, Eyre et al., 2000b, Eyre et al., 2001a; Graveline et al., 1998; Hertz-Pannier, 1999; Holloway et al., 1999; Lewine et al., 1994; Maegaki et al., 1995; Muller et al., 1997,
Acknowledgements
The Wellcome Trust and Action Research.
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