David L. Sparks

Size and distribution of movement fields in the monkey superior colliculus

A gradient of response magnitude was observed across the movement fields (the range of eye movements which alter the discharge frequency of a nueron) of neurons in the intermediate and deeper layers of the superior colliculus. A vigorous discharge preceded movements with a particular direction and amplitude but reduced responses preceded movements which deviated from this direction and/or amplitude. Movement field size is a function of the amplitude of the optimal movement. Neurons discharging prior to small saccades have small and sharply tuned fields. Neurons discharging prior to large saccades have large movement fields and tuning is relatively coarse. Movement fields are topographically organized within the superior colliculus. Neurons discharging prior to small saccades are located anteriorly; neurons firing before large saccades are found caudally. Neurons near the midline discharge prior to up movements and neurons located laterally fire before downward movements. Movement fields of superior colliculus neurons are also characterized by a temporal gradient. The interval between spike discharge and the onset of a saccade is greater for movements near the center of the movement field than for movements to the periphery of the field. Results are interpreted as supporting the foveation hypothesis of superior colliculus function. It is suggested that precise saccadic movements are not produced by the discharge of a small population of finely tuned neurons but result from the weighted sum of the simultaneous movement tendencies produced by the activity of a large population of less finely tuned neurons.

Functional properties of neurons in the monkey superior colliculus: coupling of neuronal activity and saccade onset.

One class of superior colliculus neuron was isolated which meets two criteria for participation in the initiation of visually elicited saccades. First, the pulse of spike activity recorded from these neurons was tightly coupled to saccade onset, preceding the onset of eye movements by approximately 20 msec. Secondly, if a visual stimulus sometimes elicited a saccade and sometimes failed to elicit a saccade, the occurrence of the spike pulse was highly correlated with saccade occurrence. For these neurons, there was a clear distinction between the most vigorous neuronal activity occurring in the absence of a saccade and the least vigorous activity accompanying appropriate saccades. These findings are consistent with views which attribute to the superior colliculus a role in the initiation of visually elicited saccades.

Movement fields of saccade-related burst neurons in the monkey superior colliculus

The presaccadic burst of superior colliculus (SC) neurons was examined in detail to determine whether or not information concerning the vector components (amplitude and direction) of a saccade is contained within the burst. Results indicate that the pattern of spike activity originating from a single saccade-related burst neuron in the SC does not encode saccade direction or amplitude. Identical discharges may precede a wide range of saccades. Neither the magnitude, configuration nor timing of the discharge are related in any unique way to the duration of the saccade alone or the amplitude of the saccade alone. Furthermore, it is unlikely that information concerning saccade amplitude or direction is encoded by different types of signals originating from different SC neurons. For different neurons, there is no consistent relationship between the parameters of the burst and the optimal saccade amplitude or direction. It is suggested that the discharge of saccade-related burst neurons of the SC serves as a trigger input to pontine circuitry generating the required saccadic burst signals. Information concerning saccade direction and amplitude is not contained within the trigger signal, but must be extracted from the spatial distribution of SC activity.

Cerebellotectal pathways in the macaque : implications for collicular generation of saccades

The cerebellum is thought to modulate saccadic activity in the primate in order to maintain targeting accuracy, and the cerebellotectal pathway has been posited to play a role in this modulation. However, anatomical descriptions of this pathway in primates are sketchy and conflicting. To determine whether the organization of the cerebellotectal projection in primates is similar to that found in other species, neuroanatomical tracer transport techniques were utilized in two species of macaque monkey to label cerebellotectal somata and fiber terminations. Two pathways were found. One, the fastigiotectal pathway, is derived from cells in the caudal fastigial nucleus and projects bilaterally to the rostral end of the intermediate gray layer. The other pathway is derived from cells in the posterior interposed nucleus and the adjacent posterior wing of the dentate nucleus, and it terminates contralaterally throughout the ventral half of the intermediate gray and the deep gray layers. Both of these pathways terminate within the layers of the superior colliculus containing premotor, saccade-related neurons, but the differences in the distribution of their terminals and cells of origin suggest that these two pathways have different functions. Furthermore, the pattern of connections of these two pathways indicates that they do not function as a traditional feedback circuit. We suggest that the cerebellotectal pathways may instead modulate collicular activity in a more complex manner. For example, it may provide signals necessary for corrective saccades or for maintaining spatial registry between the different sensory representations supplied to the superior colliculus and its presaccadic output, which is organized into a motor map.

Neural cartography: sensory and motor maps in the superior colliculus.

The sudden onset of a novel or behaviorally significant stimulus usually triggers responses that orient the eyes, external ears, head and/or body toward the source of the stimulus. As a consequence, the reception of additional signals originating from the source and the sensory guidance of appropriate limb and body movements are facilitated. Converging lines of evidence, derived from anatomical, electrophysiological and lesion experiments, indicate that the superior colliculus is an important part of the neural substrate responsible for the generation of orienting responses. This paper briefly reviews the functional organization of the mammalian superior colliculus and discusses possible linkages between the sensory and motor maps observed in this structure. The hypothesis is advanced that the sensory maps are organized in motor (not sensory) coordinates and that the maps of sensory space are dynamic, shifting with relative movements of the eyes, head and body.

Sensory and motor maps in the mammalian superior colliculus

Abstract The sudden onset of a novel or behaviorally significant stimulus usually triggers responses that orient the eyes, external ears, head and/or body toward the source of the stimulus. As a consequence, the reception of additional signals originating from the source, and the sensory guidance of appropriate limb and body movements are facilitated. Converging lines of evidence, derived from anatomical, electrophysiological and lesion experiments, indicate that the superior colliculus (SC) is an important part of the neural substrate for the generation of orienting responses, involved in both the localization of sensory stimuli and the initiation of orienting responses 1 .

Selective retrograde transneuronal transport of wheat germ agglutinin-conjugated horseradish peroxidase in the oculomotor system

SummaryThe fate of wheat germ agglutinin-conjugated horseradish peroxidase (WGA/HRP) subsequent to its uptake and retrograde axonal transport in abducens motoneurons of the monkey was studied using histochemical localization of WGA/HRP reaction product and light microscopy. Injections of WGA/HRP into monkey lateral rectus muscles produced a pattern of labelled motoneurons like that obtained with native HRP. In contrast to the native HRP data, WGA/HRP injections consistently labelled additional neuronal populations in the ipsilateral medial vestibular nucleus and contralateral dorsal medullary reticular formation. These regions correspond to those containing neurons known to make inhibitory synaptic contact with abducens motoneurons. No labelled neurons were observed in regions which contain excitatory premotor neurons. These data are consistent with the notion of retrograde transneuronal transport of WGA/HRP to premotor neurons. The specificity of the transneuronal exchange is indicated by the finding that only certain populations of premotor neurons were labelled. The precise manner by which preferential transneuronal transport of WGA/HRP is attained remains to be determined.

The Neural Control of Saccadic Eye Movements: The Role of the Superior Colliculus

Traditionally, the superior colliculus (SC) has been considered a center for producing reflexive movements of the eyes and head in response to visual stimuli. But the suggestion that the SC is a critical or necessary structure for voluntary or involuntary eye movements has been vigorously disputed (Pasik et al., 1966). In recent years, evidence has accumulated which supports earlier suggestions that the SC is involved in coding the location of an object relative to the fovea and in eliciting saccadic movements which produce foveal acquisition of the object. An alternative hypothesis, that the SC is concerned with shifting attention to specific areas of the visual field, has received experimental support as well.

Further Studies of the Neural Mechanisms of Ketamine-induced Anesthesia in the Rhesus Monkey

Bipolar stimulation of tooth pulp was used to elicit evoked potentials in the cortex, thalamus, and midbrain reticular formation (MBRF) of 4 monkeys. Averaged evoked potentials in MBRF and medial thalamic nuclei were either completely obliterated or markedly reduced in amplitude by anesthetic dosages of ketamine. In contrast, little effect was observed upon the primary response elicited in the ventrobasal complex of the thalamus. These results suggest that anesthetic doses of ketamine block afferent signals concerned with the affective-emotional components of pain perception, but conduction of signals related to the localization of somatic stimuli in time and space may be relatively unimpaired.

The functional organization of the primate superior colliculus: a motor perspective.

Publisher Summary The deeper layers of the superior colliculus (SC) are a site where visual, auditory, and somatosensory signals converge and an area that contains neurons with motor properties. Based upon such observation, many investigators have suggested that the SC may be a brain region where signals from various sensory modalities are translated into common motor commands; commands for orienting the eyes, head, and pinnae toward the source of significant or novel environmental stimuli. Results of several recent experiments can best be explained by assuming that the SC is organized in motor coordinates. Motor error is encoded anatomically; it is the site of activity within the colliculus, not discharge frequency that specifies saccade direction and amplitude. This command format imposes constraints upon the configuration of signals that can initiate saccades and determines the required transformations of sensory signals. This chapter explains what is known about the motor signals found in the SC, and based upon this information, discusses the transformations of sensory signals that are required for a sensory/ motor interface.