New mechanism that accounts for position sensitivity of saccades evoked in response to stimulation of superior colliculus.

New mechanism that accounts for position sensitivity of saccades evoked in response to stimulation of superior colliculus. J. Neurophysiol. 80: 3373-3379, 1998. Electrical stimulation of the feline superior colliculus (SC) is known to evoke saccades whose size depends on the site stimulated (the "characteristic vector" of evoked saccades) and the initial position of the eyes. Similar stimuli were recently shown to produce slow drifts that are presumably caused by relatively direct projections of the SC onto extraocular motoneurons. Both slow and fast evoked eye movements are similarly affected by the initial position of the eyes, despite their dissimilar metrics, kinematics, and anatomic substrates. We tested the hypothesis that the position sensitivity of evoked saccades is due to the superposition of largely position-invariant saccades and position-dependent slow drifts. We show that such a mechanism can account for the fact that the position sensitivity of evoked saccades increases together with the size of their characteristic vector. Consistent with it, the position sensitivity of saccades drops considerably when the contribution of slow drifts is minimal as, for example, when there is no overlap between evoked saccades and short-duration trains of high-frequency stimuli.

An anatomical substrate for the spatiotemporal transformation.

The purpose of the present experiments was to test the hypothesis that the metrics of saccades caused by the activation of distinct collicular sites depend on the strength of their projections onto the burst generators. This study of morphofunctional correlations was limited to the horizontal components of saccades. We evoked saccades by stimulation of the deeper layers of the superior colliculus (SC) in alert, head-fixed cats. We used standard stimulus trains of 350 msec duration, 200 Hz pulse rate, and intensity set at two times saccade threshold in all experiments. Evoked saccades were analyzed quantitatively to determine the amplitude of the horizontal component of their "characteristic vectors". This parameter is independent of eye position and was used as the physiological, saccade-related metric of the stimulation sites. Anatomical connections arising from these sites were visualized after anterograde transport of biocytin injected through a micropipette adjoining the stimulation electrode. The stimulation and injection sites were, therefore, practically identical. We counted boutons deployed in regions of the paramedian pontine reticular formation reported to contain long-lead and medium-lead burst neurons of the horizontal burst generator. Regression analysis of the normalized bouton counts revealed a significant positive correlation with the size of the horizontal component of the characteristic vectors. This data supports a frequent modelling assumption that the spatiotemporal transformation in the saccadic system relies on the graded strength of anatomical projections of distinct SC sites onto the burst generators.

Neuronal mechanisms of two-dimensional orienting movements in the cat. I. A quantitative study of saccades and slow drifts produced in response to the electrical stimulation of the superior colliculus.

To evaluate the metrics of rapid eye movements caused by the activation of distinct collicular microzones, the superior colliculus (SC) was electrically stimulated in alert behaving cats while their heads were restrained. A quantitative study of electrically induced rapid eye movements demonstrated that their amplitude and direction depended on the intensity of stimulation, the electrode location, and the initial position of the eyes, while their duration depended on the intensity of stimulation. When detailed quantitative procedures are employed, properties of saccades produced in response to the electrical stimulation of the feline SC resemble those of saccades elicited in response to the electrical stimulation of a variety of primate brain areas. Besides saccades, electrical stimulation of the feline SC gave rise to slow drifts whose amplitude and direction was also influenced by the initial position of the eyes. Because their size depended on the frequency of stimulation and their time course reflected mechanical properties of the oculomotor plant, induced slow drifts could be due to a more or less direct projection of the SC onto extraocular motoneurons. A model that includes such a variety of connections between the SC and extraocular motoneurons is presented and is shown to produce realistic combinations of fast and slow eye movements when its input is a step function of time. The present findings support the notion that an orbital mechanical factor underlies the eye position sensitivity of slow drifts and saccades evoked in response to the electrical stimulation of the SC.

Synaptic actions of tectofugal pathways on abducens motoneurons in the cat.

Organization of pathways between the superior colliculus (CS) and abducens motoneurons (VI-MNs) was studied in cats under pentobarbital anesthesia using intracellular recordings from VI-MNs and adjacent reticular neurons. Latencies of EPSPs elicited by contralateral CS stimulation indicate that a small fraction of the excitatory pathway may be monosynaptic while its major part is disynaptic. As suggested by an analysis of synaptic responses to microstimulation of the paramedian pontine region, excitatory impulses descend in the tectobulbospinal tract after crossing at midbrain levels. An attempt was made to identify interneurons of the excitatory tectoabducens pathway in the region just ventral and rostroventral to the VI-nucleus. About one-quarter of the reticular neurons in this region received monosynaptic excitation specifically from the contralateral CS. They were acceptable as interneurons with regard to other response characteristics too. Axonal projection to, or through, the abducens nucleus was demonstrated for some of them by intranuclear microstimulation or by tracing axons after Procion yellow injections. It is suggested that "premotor" interneurons of the excitatory tectoabducens pathway are concentrated in the vicinity of the abducens nucleic. A similar investigation of inhibitory responses to ipsilateral CS-stimulation indicates that inhibitory pathways are at least disynaptic and, for the most part, contain three or more synapses. In its initial trajectory the inhibitory pathway appears to be identical with the tectobulbospinal tract,but it decussates for the second time at caudal pontine levels to reach ipsilateral VI-MNs.