Skilled digit movements in feline and primate – recovery after selective spinal cord lesions

Abstract

Recovery of voluntary movements after partial spinal cord injury depends, in part, on a take-over of function via unlesioned pathways. Using precise forelimb movements in the cat as model, spinal pathways contributing to motor restitution have been investigated in more detail. The food-taking movement by which the cat graSPS a morsel of food with the digits and brings it to the mouth is governed by interneurones in the forelimb segments (C6-Th1) and is normally controlled via the cortico- and rubrospinal tracts. Food-taking disappears after transection of these pathways in the dorsal part of the lateral funiculus (DLF) in C5/C6, but then recovers during a period of 2-3 weeks. Experiments with double lesions showed that the recovery depends on a take-over via ipsilateral ventral systems; a ventrally descending pathway, most probably cortico-reticulospinal, and a pathway via propriospinal neurones in the C3-C4 segments. It is postulated that the recovery involves a plastic reorganization of these systems. Dexterous finger movements in the macaque monkey are generally considered to depend on the monosynaptic cortico-motoneuronal (CM) connexion, which is lacking in the cat. Such movements are abolished after pyramidotomy at the level of the trapezoid body. However, experiments with transection of the corticospinal tract in the DLF and partly ventral part of the lateral funiculus in C5, showed a fast (1-28 days) recovery of precision grip and, to some extent, independent finger movements. Deficits in preshaping during the final approach to the morsel as well as lack of force were observed. A C5 DLF lesion spares corticofugal pathways to the brainstem and upper cervical segments. It is suggested that indirect corticomotoneuronal pathways may provide for recovery of dexterous finger movements and that the role of CM pathways for such movements should be broadened to include not only the monosynaptic connexion.

Chondroitinase Combined with Rehabilitation Promotes Recovery of Forelimb Function in Rats with Chronic Spinal Cord Injury

“…BDA ϩve axons were seen extensively at 1.5 mm rostral to lesion (k); however, fewer were seen at 0.5 mm rostral to the lesion (l) and at the lesion site (m). Scale bar, 200 m. (Whishaw et al, 1993(Whishaw et al, , 1998Basso et al, 1996;McKenna and Whishaw, 1999;Starkey et al, 2005;Pettersson et al, 2007). After injury, animals recover most gross motor functions rapidly, but show a sustained deficit in skilled paw reaching (Bradbury et al, 2002;García-Alías et al, 2008.…”

Organization of pontine reticulospinal inputs to motoneurons controlling axial and limb muscles in the neonatal mouse

“…Thus we distinguish two pontine reticulospinal pathways to spinal MNs, one uncrossed and the other crossed, of which the uncrossed pathway transmits more faithfully and appears to be more direct. motor control; descending pathways; brain stem; spinal cord; trunk; limb THE MAMMALIAN RETICULOSPINAL system, consisting of the mesencephalic, pontine, and medullary reticulospinal pathways, is crucial for the control of skeletal musculature (Baker 2011;Kuypers 1964;Lemon 2008;Perreault and Glover 2013;Peterson 1979;Pettersson et al 2007), but the neural mechanisms by which it initiates and regulates movement are far from understood.Electrical stimulation has been a key method in studying the organization of the mammalian reticulospinal system, revealing excitatory reticulospinal connections (mono-and polysynaptic) with axial motoneurons (MNs), proximal and distal limb MNs, and digit MNs in a variety of species (monkey: Davidson and Buford 2006;Riddle et al 2009; cat: Drew and Rossignol 1990b;Galea et al 2010;Grillner et al 1968;Jankowska et al 2003;Lloyd 1941;Peterson et al 1979;Sprague and Chambers 1954;Wilson and Yoshida 1969; rat: Bolzoni et al 2013; Floeter and Lev-Tov 1993;Umeda et al 2010; and mouse: Alstermark and Ogawa 2004;Szokol et al 2008). However, many studies have not differentiated among different areas of the reticular formation (RF) that project to the spinal cord.…”

“…Thus we distinguish two pontine reticulospinal pathways to spinal MNs, one uncrossed and the other crossed, of which the uncrossed pathway transmits more faithfully and appears to be more direct. motor control; descending pathways; brain stem; spinal cord; trunk; limb THE MAMMALIAN RETICULOSPINAL system, consisting of the mesencephalic, pontine, and medullary reticulospinal pathways, is crucial for the control of skeletal musculature (Baker 2011;Kuypers 1964;Lemon 2008;Perreault and Glover 2013;Peterson 1979;Pettersson et al 2007), but the neural mechanisms by which it initiates and regulates movement are far from understood.…”

Dynamic Motor Compensations with Permanent, Focal Loss of Forelimb Force after Cervical Spinal Cord Injury

“…It must be emphasized, however, that the single damage of the CPPS is not expected to produce permanent locomotor impairments, because the takeover of foreleg motor function by other tracts is common after selective cervical spinal cord lesions. 17,32,79 Hence, the permanent deficits were very likely caused by damage of brain descending axons together with damage of axons of the CPPS.…”

“…10 The loss and recovery of forelimb motor function has been studied in several models of cervical SCI in rats, 4,[11][12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27] cats, [28][29][30] and primates. [31][32][33][34][35] All those studies demonstrated some extent of spontaneous motor function recovery, albeit with persisting deficits as a consequence of interruption of descending axonal tracts or segmental neuronal death. Despite these advances, there is still a need of cervical SCI models in which motor performance is comprehensively assessed in the long term to determine the motor components that show recovery and to link the chronic deficits with the neuroanatomical damage.…”