Morphology of single axons of tectospinal neurons in the upper cervical spinal cord

Abstract

Morphology of single axons of tectospinal (TS) neurons was investigated by intraaxonal injection of horseradish peroxidase (HRP) at the upper cervical spinal cord of the cat. TS axons were electrophysiologically identified by their direct responses to stimulation of the contralateral superior colliculus (SC). None of these axons responded to thoracic stimulation at Th2. Three-dimensional reconstructions of the axonal trajectories were made from 20 well-stained TS axons at C1-C3. Cell bodies of these axons were located in the intermediate or deep layers of the caudal two-thirds of the SC. Usually, TS axons had multiple axon collaterals, and up to seven collaterals were given off per stem axon [2.7 +/- 1.6 (mean +/- S.D.); n = 20]. Collaterals had simple structures and ramified a few times mainly in the transverse plane. The number of terminals for each collateral was small. These collaterals terminated in the lateral parts of laminae V-IX, mainly in laminae VI, VII, and VIII. There were usually gaps free from terminal arborizations between adjacent collaterals, because the rostrocaudal spread of each collateral (mean = 700 microns) was narrower than the intercollateral interval (mean = 2,500 microns). Seven of the 19 TS axons had terminals in the lateral parts of laminae V-VIII, with little projection to lamina IX, and the other 12 axons had terminals in lamina IX besides the projection to the lateral parts of laminae V-VIII. Axon terminals in lamina IX did not appear to make contacts with the somata or proximal dendrites of retrogradely labeled motoneurons, but contacts were found with the somata of counterstained interneurons in the lateral parts of laminae V-VIII. Three spinal interneurons (two in lamina VIII and one in lamina V at C1) that received monosynaptic excitation from the SC were stained, and their axonal trajectories were reconstructed. They had multiple axon collaterals at C1-C2 and mainly projected to laminae VIII and IX, with smaller projections to lamina VII. Many axon terminals of the interneurons were found in multiple neck motor nuclei, where some of them made contacts with retrogradely labeled motoneurons. The present finding provides evidence that the direct TS projection to the spinal cord may influence activities of multiple neck muscles, mainly via spinal interneurons, and may play an important role in control of head movement in parallel with the tectoreticulospinal system.

Patterns of axonal branching of neurons of the substantia nigra pars reticulata and pars lateralis in the rat

“…Physiologically, the deep layers of the SC are responsible for the generation of directed orienting movements, which in cats and rats involve not only eye‐head movements but also movements of the entire body (Syka and Radil‐Weiss, 1971; Harris, 1980; McHaffie and Stein, 1982; Northmore et al, 1988; Dean et al, 1989). These orienting responses can be promoted by neurons of the deep SC through their connections with motor‐related structures in the brainstem, spinal cord, and diencephalon (Chevalier and Deniau, 1984; Redgrave et al, 1986; Yamasaki et al, 1986; Cowie et al, 1994; Muto et al, 1996). In this study, we showed that the type II SNr axons that provide collaterals to the SC also yielded collaterals to the PPTg, suggesting a close functional relationship between these two mesencephalic structures.…”

Neural Organization From the Superior Colliculus to Motoneurons in the Horizontal Oculomotor System of the Cat

“…In the present study, ϳ60% (27/46) of tectoreticular neurons projecting to the contralateral PPRF were found to send their axons to the spinal cord. Our recent morphological study showed that tectospinal neurons emit multiple axon collaterals in the cervical cord, and spinal interneurons receiving monosynaptic excitation from the contralateral SC directly terminate on neck motoneurons (Muto et al 1996). Therefore the SC could influence neck muscles through such tectoreticulospinal neurons as well as reticulospinal neurons that receive monosynaptic input from the SC (Kakei et al 1994;Sasaki 1992).…”

“…The SC of the cat can be divided into three anteroposterior zones from a functional point of view; the anterior, intermediate, and posterior zones (Guitton et al 1980). Tectal output neurons projecting to the spinal cord predominantly exist in the intermediate zone (Muto et al 1996). Therefore tectoreticulospinal neurons in this zone contribute to gaze control by a large-amplitude eye movement and synchronous neck movement to fixate a visual target in the periphery of the visual field (Guitton et al 1980).…”

Role of the Basal Ganglia in the Control of Purposive Saccadic Eye Movements

“…All of these sensory signals converge onto the SC in a topographical manner, forming a spatial map (319). The output of the SC is then led to the motor networks in the spinal cord for head and trunk movements to produce the orienting response (226,264). In mammals, the SC output is now connected to the brain stem networks for quick phases (46,102).…”