Skilled reaching and grasping in the rat: lacking effect of corticospinal lesion

Abstract

The corticospinal system is a major motor pathway in the control of skilled voluntary movements such as reaching and grasping. It has developed considerably phylogenetically to reach a peak in humans. Because rodents possess advanced forelimb movements that can be used for reaching and grasping food, it is commonly considered that the corticospinal tract (CST) is of major importance for this control also in rodents. A close homology to primate reaching and grasping has been described but with obvious limitations as to independent digit movements, which are lacking in rodents. Nevertheless, it was believed that there are, as in the primate, direct cortico-motoneuronal connections. Later, it was shown that there are no such connections. The fastest excitatory pathway is disynaptic, mediated via cortico-reticulospinal neurons and in the spinal cord the excitation is mainly polysynaptically mediated via segmental interneurons. Earlier behavioral studies have aimed at investigating the role of the CST by using pyramidotomy in the brainstem. However, in addition to interrupting the CST, a pyramidal transection abolishes the input to reticulospinal neurons. It is therefore not possible to conclude if the deficits after pyramidotomy result from interruption of the CST or the input to reticulospinal neurons or both. We have re-investigated the role of the CST by examining the effect of a CST lesion in the C1-C2 spinal segments on the success rate of reaching and grasping. This lesion spares the cortico-reticulospinal pathway. In contrast to investigations using pyramidal transections, the present study did not demonstrate marked deficits in reaching and grasping. We propose that the difference in results can be explained by the intact cortical input to reticulospinal neurons in our study and thus implicate an important role of this pathway in the control of reaching and grasping in the rat.

Keywords: corticospinal tract lesion; grasping; interneuron; motorneuron; reaching; reticulospinal; skilled forelimb movements.

Figure 1

Schematic drawing of the test box (oblique lateral view; measurements in millimeters) showing the behavioral paradigm with a vertical slit formed by glass walls. The upper part of the space between the vertical walls is covered so that the height of the slit is 20 mm.

Figure 2

Histological control. Transverse extent of spinal selective lesions in four rats (A–D) giving complete interruption of the CST but with remaining fibers in unlesioned areas of the DC. The asterisks in (A,B) show the position of a notch cut, after fixation, in the lateral funicle on one side to identify that side of each section when mounting them.

Figure 3

Electrophysiological control. (A,B), upper traces are intracellular recordings from a MN antidromically identified by stimulation of the ulnar/median nerves. Lower traces were recorded from the cord dorsum in the same segment (C7) as the intracellular recordings. The contralateral pyramid was stimulated electrically with a single pulse at 100 μA in (A) and with two pulses in (B,C), histogram of EPSP latencies measured from the second pyramidal stimulus to the onset. Arrow head indicates the arrival of the synaptic volley in C7. (D) Schematic circuit diagram of demonstrated cortico-motoneuronal pathways. ReST in green, PN pathway in blue and sINs in orange. Note that the ReST has both monosynaptic projection to MNs and disynaptic projection via PNs and sINs. The red area indicates the lesion of CST in C1–C2. Cord dorsum recordings from C1 and C4 evoked by a single stimulation in the contralateral pyramid at 100 μA.

Figure 4

Images of reaching and digit grasping movements obtained with high-speed video (250 Hz) preoperatively (A) and 8 days postoperatively (B) viewed from the lateral side and from above. Times are given in milliseconds relative to the first image. The background has been digitally retouched.