The projection of the superior colliculus upon the inferior olivary complex of the cat: an autoradiographic and horseradish peroxidase study

The superior colliculus is a laminated midbrain structure that acts as one of the centers organizing gaze movements. This review will concentrate on sensory and motor inputs to the superior colliculus, on its internal circuitry, and on its connections with other brainstem gaze centers, as well as its extensive outputs to those structures with which it is reciprocally connected. This will be done in the context of its laminar arrangement. Specifically, the superficial layers receive direct retinal input, and are primarily visual sensory in nature. They project upon the visual thalamus and pretectum to influence visual perception. These visual layers also project upon the deeper layers, which are both multimodal, and premotor in nature. Thus, the deep layers receive input from both somatosensory and auditory sources, as well as from the basal ganglia and cerebellum. Sensory, association, and motor areas of cerebral cortex provide another major source of collicular input, particularly in more encephalized species. For example, visual sensory cortex terminates superficially, while the eye fields target the deeper layers. The deeper layers are themselves the source of a major projection by way of the predorsal bundle which contributes collicular target information to the brainstem structures containing gaze-related burst neurons, and the spinal cord and medullary reticular formation regions that produce head turning.

The anatomical, physiological, and behavioral evidence for the involvement of three regions of the cerebellum in oculomotor behavior is reviewed here: (1) the oculomotor vermis and paravermis of lobules V, IV, and VII; (2) the uvula and nodulus; (3) flocculus and ventral parafloccculus. No region of the cerebellum controls eye movements exclusively, but each receives sensory information relevant for the control of multiple systems. An analysis of the microcircuitry suggests how sagittal climbing fiber zones bring visual information to the oculomotor vermis; convey vestibular information to the uvula and nodulus, while optokinetic space is represented in the flocculus. The mossy fiber projections are more heterogeneous. The importance of the inferior olive in modulating Purkinje cell responses is discussed.

Different tracer substances were injected into the superior colliculus (CoS) in order to study its afferents and efferents with the meso-rhombencephalic tegmentum, the precerebellar nuclei and the cerebellum in the Madagascan hedgehog tenrec. The overall pattern of tectal connectivity in tenrec was similar to that in other mammals, as, e.g. the efferents to the contralateral paramedian reticular formation. Similarly the origin of the cerebello-tectal projection in mainly the lateral portions of the tenrec's cerebellar nuclear complex corresponded to the findings in species with little binocular overlap. In comparison to other mammals, however, the tenrec showed a consistent projection to the ipsilateral inferior olivary nucleus, in addition to the classical contralateral tecto-olivary projection. The tenrec's CoS also appeared to receive an unusually prominent monoaminergic input particularly from the substantia nigra, pars compacta. There was a reciprocal tecto-parabigeminal projection, a distinct nuclear aggregation of parabigeminal neurons, however, was difficult to identify. The dorsal lemniscal nucleus did not show perikaryal labeling in contrast to the paralemniscal region. Similar to the cat but unlike the rat there were a few neurons in the nucleus of the central acoustic tract. Unlike the cat, but similar to the rat there was a distinct, predominantly ipsilateral projection to the magnocellular reticular field known to project spinalward.

The motor cortex plays a crucial role in the co-ordination of movement and posture. This is possible because the pyramidal tract fibres have access both directly and through collateral branches to structures governing eye, head, neck, trunk and limb musculature. Pyramidal tract axons also directly reach the dorsal laminae of the spinal cord and the dorsal column nuclei, thus aiding in the selection of the sensory ascendant transmission. No other neurones in the brain besides pyramidal tract cells have such a wide access to different structures within the central nervous system. The majority of the pyramidal tract fibres that originate in the motor cortex and that send collateral branches to multiple supraspinal structures do not reach the spinal cord. Also, the great majority of the corticospinal neurones that emit multiple intracraneal collateral branches terminate at the cervical spinal cord level. The pyramidal tract fibres directed to the dorsal column nuclei that send collateral branches to supraspinal structures also show a clear tendency to terminate at supraspinal and cervical cord levels. These facts suggest that a substantial co-ordination between descending and ascending pathways might be produced by the same motor cortex axons at both supraspinal and cervical spinal cord sites. This may imply that the motor cortex co-ordination will be mostly directed to motor responses involving eye-neck-forelimb muscle synergies. The review makes special emphasis in the available evidence pointing to the role of the motor cortex in co-ordinating the activities of both descending and ascending pathways related to somatomotor integration and control. The motor cortex may function to co-operatively select a unique motor command by selectively filter sensory information and by co-ordinating the activities of the descending systems related to the control of distal and proximal muscles. © 1997 Elsevier Science Ltd. All Rights Reserved.

A central goal of the Neurosciences is to provide an account of how the brain works in terms of cell groups organised into pattern generating networks. This review focuses on the neural network that generates the rapid movements of the eyes that are called saccades. A brief description of the metrical and dynamical properties of saccades is provided first. Data obtained from lesion and electrical stimulation experiments are then described; these indicate that the relevant neural machinery spreads over at least 10 distinct cortical and subcortical regions of the brain. Each one of these regions harbors several distinct classes of saccade related cells (i.e. cells whose discharge encodes the metrical and often dynamical properties of saccades). The morphological and physiological properties of about 30 saccade related cell classes are described. To generate the signals they carry, and therefore saccades, distinct classes of cells influence each other in a non-random manner. Anatomical evidence is provided that indicates the existence of about 100 distinct connections established between saccade related neurons. The overall picture of the saccadic system that emerges from these studies is one of intricate complexity. In part this is due to the presence of at least 3, multiply interconnected negative feedback loops. Several computational models of the saccadic system have been proposed in an attempt to understand the functional significance of the simultaneous operation of these loops. An evaluation of these models demonstrates that besides providing a coherent summary of the data that concern it, successful models of the saccadic system generate realistic saccades (in precise quantitative psychophysical terms) when their elements are stimulated, produce abnormal saccades, reminiscent of those encountered in the clinic, when their elements are disabled, while their constituent units display realistic discharge patterns and are connected in a manner that respects anatomy.

This chapter reviews the external and internal morphology of the cerebellum. It focuses on the afferent and intrinsic connections of the cerebellum. Three layers are present in the cortex. The granular layer borders on the central white matter of the cerebellum. The Purkinje cell layer contains the cell bodies of the Purkinje cells, which are arranged in a single row. The perikarya of the Bergmann glia (the Golgi epithelial cells) are intercalated between the larger Purkinje cells. The molecular layer has a low cell content. It contains the dendritic arbors of the Purkinje cells and the Bergmann glial fibers, which run up to the pial surface where they constitute the external glial limiting membrane. Granule cells are small neurons located in cell nests in the granular layer. Cell-free spaces in the granular layer, which are known as the “protoplasmatic islands of Held,” contain the terminals of the mossy fibers.