A. Lundberg

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.

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.

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.

Control of claw movements in cats

In cats with the distal paw shaved and the claws painted with nail varnish, claw movements were recorded during the approach to a morsel of food with a conventional video camera; supplementary results were obtained with a high frequency video system. The claws can be protruded in two directions, either ventrally or more dorsalwards. Measurements of the outer contour of the paw suggest that these two modes are not due to differences in angular movements in the proximal interphalangeal joints; it is suggested that they depend on some (so far unknown) function in the distal interphalangeal joints. Differential movements of the claws of the different digits suggest some degree of individual control of the digits.

Control of digits via C3-C4 propriospinal neurones in cats; recovery after lesions.

C3-C4 propriospinal neurones (C3-C4 PNs) transmit the command for forelimb target-reaching in cats, while the command for food-taking is mediated by interneurones in the forelimb segments. The ability of the C3-C4 PNs to control digits has now been reinvestigated with combined lesions in dorsal C5 (transecting the cortico- and rubrospinal tracts) and ventral C2 (transecting reticulospinal tracts) leaving the C3-C4 PNs in sole control of the forelimb. Components of food-taking like flexion in the proximal interphalangeal joints were found in half of the cats. Supination and terminal flexion of the metacarpophalangeal joints by which normal cats bring the morsel of food to the mouth were lacking in all cats.

Food-taking in the cat investigated with transection of the rubro- and corticospinal tracts.

In cats with the distal paw shaved food-taking from a horizontally or vertically placed tube was recorded with a video camera, supplementary results were obtained with a high frequency video system. Measurements were made of the dorsal contour of the digits to investigate angular movement in the proximal interphalangeal (PIP) joint and withdrawal of the paw before and after complete transection of the rubro- and corticospinal tracts just rostral to the forelimb segments. In the preoperative state PIP flexion occurs before withdrawal of the paw in the large majority of cats. Postsurgically the main part of PIP flexion is made during withdrawal of the paw. It is suggested that PIP flexion before withdrawal allows for accurate manipulative placement of the digits on the target which depends on the rubro- and corticospinal tracts, while PIP flexion during withdrawal, which may favour speed at the expense of accuracy, can be made without the rubro-and corticospinal tracts.

The pathway from Ia forelimb afferents to the motor cortex: a new hypothesis.

Forelimb target-reaching and food-taking in cats depend on different interneuronal circuitry in the spinal cord. On the basis of previous findings regarding the effect of transection of the corticospinal tract in the spinal cord, of high dorsal column (DC) transection, of low pyramidotomy and of pyramidotomy after previous DC transection, it is proposed that the food-taking movement is temporally linked to target-reaching as follows: During target-reaching, the position of the paw is signalled by the pathway from forelimb proprioceptors (mainly Ia) to the motor cortex with a relay in the main cuneate nucleus. The command for food-taking is issued by the motor cortex only when the pathway from the forelimb signals that the paw approaches the target correctly, as may be determined by a comparison of the information from the forelimb with an efference copy of the motor program for target-reaching. The hypothesis is based on previous results regarding the organization of the pathway from the forelimb to area 3a and the motor cortex, and regarding the cortico-cuneate pathway with selective projection from area 3a and motor cortex to the basal caudal part of the cuneate nucleus, where the proprioceptive information from the forelimb is relayed. Results relevant to the present hypothesis regarding responses of precentral neurones during active and passive movements in awake animals are briefly discussed.