L.-G. Pettersson

Motor recovery after serial spinal cord lesions of defined descending pathways in cats

The food-taking movement by which a cat uses its forepaw to take a piece of food and bring it to its mouth normally depends on the cortico- (CS) and rubrospinal (RS) tracts and disappears when they are transected in C5; a slow reappearance over months is due to bulbospinal (BS) take-over. After complete CS transection but minimal RS transection, food-taking remains. If, one month later, the RS tract is completely transected, food-taking is not abolished as it is when transection is made in one session. It is permanently abolished after a third transection of the ventral quadrant in C2. It is suggested that the food-taking remaining after the first lesion is due to combined RS and BS activity and that the RS tract induces the BS neurones to contribute to the extent that they can take over when the RS tract is completely transected.

The C3–C4 propriospinal system in the cat and monkey: a spinal pre-motoneuronal centre for voluntary motor control

This review deals with a spinal interneuronal system, denoted the C3–C4 propriospinal system, which is unique in the sense that it so far represents the only spinal interneuronal system for which it has been possible to demonstrate a command mediating role for voluntary movements. The C3–C4 propriospinal neurones govern target reaching and can update the descending cortical command when a fast correction is required of the movement trajectory and also integrate signals generated from the forelimb to control deceleration and termination of reaching.

Motor command for precision grip in the macaque monkey can be mediated by spinal interneurons

In motor control, the general view is still that spinal interneurons mainly contribute to reflexes and automatic movements. The question raised here is whether spinal interneurons can mediate the cortical command for independent finger movements, like a precision grip between the thumb and index finger in the macaque monkey, or if this function depends exclusively on a direct corticomotoneuronal pathway. This study is a followup of a previous report (Sasaki et al. J Neurophysiol 92: 3142-3147, 2004) in which we trained macaque monkeys to pick a small piece of sweet potato from a cylinder by a precision grip between the index finger and thumb. We have now isolated one spinal interneuronal system, the C3-C4 propriospinal interneurons with projection to hand and arm motoneurons. In the previous study, the lateral corticospinal tract (CST) was interrupted in C4/C5 (input intact to the C3-C4 propriospinal interneurons), and in this study, the CST was interrupted in C2 (input abolished). The precision grip could be performed within the first 15 days after a CST lesion in C4/C5 but not in C2. We conclude that C3-C4 propriospinal interneurons also can carry the command for precision grip.

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

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.

EFFECT OF SPINAL CORD LESIONS ON FORELIMB TARGET-REACHING AND ON VISUALLY GUIDED SWITCHING OF TARGET-REACHING IN THE CAT

Cats were trained to reach to an illuminated tube placed horizontally at shoulder level and retrieve food with the forepaw. The trajectory of an infrared light emitting diode, taped to the wrist dorsum, was recorded with a SELSPOT-like recording system. Movement paths and velocity profiles were compared before and after lesions: (1) in dorsal C5, transecting cortico- and rubrospinal pathways to the forelimb segments so that the cats could only use the C3-C4 propriospinal neurones (PNs) to command reaching, (2) in the ventral part of the lateral funicle in C5, transecting the axons of C3-C4 PNs so that the cats had to use circuitry in the forelimb segments to command reaching. Comparison of trajectories and velocity profiles before and after lesion 1 did not reveal any major qualitative change. After lesion 2, the last third of the movement was fragmented with separate lifting and protraction. Switching of target-reaching occurred when illumination was shifted to another tube during the ongoing movement. The switching latency measured from the time of illumination shift to the earliest change in movement trajectory had a minimal value of 50-60 ms. Short latencies were present after lesion 1 as well as lesion 2 which suggest that fast switching mediated by the C3-C4 PNs and the interneuronal system in the forelimb segments is controlled in parallel by the brain. In order to test a hypothesis that fast switching depends on the tectospinal and tecto-reticulospinal pathways (the tecto-reticulo-spinal system) a ventral lesion was made in C2 aiming at interrupting these pathways. Large ventral C2 lesions tended to block conduction in the more dorsally located rubrospinal (less in corticospinal) axons probably due to compression during surgery. When conduction in the rubrospinal tract was completely interrupted by a ventral C2 lesion which also completely transected the axons of the tecto-reticulo-spinal system, then there was a prolongation of the switching latency with 10-20 ms. After a similar large ventral lesion with remaining conduction in the rubrospinal tract the switching latencies were unchanged. It is postulated that fast visually governed switching does not depend on the tecto-reticulo-spinal system alone but on more dorsally located pathways, presumably the rubrospinal tract, either acting alone or together with the tecto-reticulo-spinal system. It is further postulated that the delayed switching after interruption of conduction both in the rubrospinal tract and the tecto-reticulo-spinal system depends on the corticospinal tract. Visual control of rubrospinal and of corticospinal neurones is considered. It is postulated that target-reaching normally depends on signals in the cortico- and rubrospinal tracts and mechanisms for co-ordination of activity in them as required during switching is discussed in view of the findings now reported.

Effect of different spinal cord lesions on visually guided switching of target-reaching in cats

It has previously been shown that when a target is moved, cats can change the direction of ongoing target-reaching with brief latency suggesting a tectal relay. Switching of target-reaching has now been investigated after spinal lesions: (1) dorsally in C5 interrupting cortico- (CS) and rubrospinal (RS) fibres to forelimb segments; (2) more ventrally in C5 interrupting axons of the C3-C4 propriospinal neurones (PNs) to forelimb motoneurones; and (3) ventrally in C2 interrupting tectospinal and tecto-reticulospinal fibres. Short-latency switching of target-reaching remained after lesions 1 and 2. A subsequent lesion 3 after lesion 1 or 2 prolonged the switching latency. The results show that fast switching, presumably relayed in tectum, can be made when the cat utilizes C3-C4 PNs or interneurones in the forelimb segments for target-reaching. For both neuronal systems, the longer-latency switching after ventral C2 lesion is assumed to be cortically relayed and mediated by the CS and RS tracts.

Recovery of food-taking in cats after lesions of the corticospinal (complete) and rubrospinal (complete and incomplete) tracts

The food-taking movement by which a cat grasps a morsel of food and brings it to the mouth is governed by interneurones in the forelimb segments (C6-Th1) and is normally controlled by the cortico- and rubrospinal tracts. It disappears reversibly when these tracts are transected in C5. The reappearance after some time is at least in part due to a reticulospinal take-over of the command. We have compared the recovery after total transection of both tracts with that after lesions giving subtotal transection of the rubrospinal tract but total transection of the corticospinal tract. With 4-6% of the rubrospinal fibres left, the recovery of food-taking was clearly faster than after total transection.

The effect of low pyramidal lesions on forelimb movements in the cat

Complete transection of the pyramid just rostral to the crossing gave defects in forelimb target-reaching and food-taking tested with retrieval of food from a cylinder. The most marked symptoms were dysmetria, dyscoordination of movement and almost total loss of the food-taking movement. Gradual recovery occurred, but even after 3-4 months the food-taking movement was deficient. The symptoms were less severe than those previously found after a high pyramidotomy but much more pronounced than those observed after complete transection of the corticospinal tract in the spinal cord. The motor defects after a low pyramidotomy closely resemble those found after a high dorsal column transection. It is tentatively proposed that the motor defects after low pyramidotomy are largely due to transection of corticocuneate fibers which regulate the feedback pathway from forelimb afferents to the motor cortex.

Characteristics of target-reaching in cats

Trajectory formation of unrestrained forelimb target-reaching was investigated in six cats. A Selspotlike recording system was used for three-dimensional recording of the position of the wrist every 3 ms with the aid of two cameras detecting infrared light emitted from diodes taped to the wrist. These measurements allowed reconstruction of movement paths in the horizontal and sagittal planes and velocity profiles in the direction of the cartesian x, y and z co-ordinates. Horizontal movement paths were smoothly curved, segmented or almost linear. Sagittal movement paths were sigmoid. The net velocity profile was usually bell-shaped with longer deceleration than acceleration, but for some slow movements the velocity profile had a plateau. When the net velocity profile was bell-shaped, the averaged sagittal movement paths and normalized x (protraction) and z (lifting) velocity profiles were virtually superimposable for fast and slow movements: thus, movement speed was changed by parallel scaling of protraction and lifting. Comparison of movement paths and velocity profiles amongst the different cats revealed considerable differences. The ż profile was unimodal in one cat and double peaked in five cats: the second component was pronounced in two cats and small in the other three. The ż profile was unimodal and, except for one cat, it had later onset and summit than the first component of the x profile. In contrast to the interindividual differences, there was a high degree of intraindividual constancy over 6–12 months. It is postulated that the interindividual variability depends on chance differences established early during learning of the task and that the imprinted pattern remains, resulting in intra-individual constancy.

Role of claws and pads in taking and holding food in cats.

In order to investigate the role of claws and pads in taking food the planter surface of the distal forelimb paw was recorded with a conventional video camera. The claws were involved in the great majority of trials. The morsel of food may be taken by piercing with one claw (rarely two) either alone or by pressure against a digital pad; support by pressure from another claw was also common, while pressure between two claws was used more rarely. Another technique was pressure between claws (without piercing) and digital pads. The morsel was also taken without participation of claws by pressure between digital pads and the central pad and more rarely between two digital pads.