Neural network simulations of the primate oculomotor system. V. Eye-head gaze shifts.

We examined the performance of a dynamic neural network that replicates much of the psychophysics and neurophysiology of eye-head gaze shifts without relying on gaze feedback control. For example, our model generates gaze shifts with ocular components that do not exceed 35 degrees in amplitude, whatever the size of the gaze shifts (up to 75 degrees in our simulations), without relying on a saturating nonlinearity to accomplish this. It reproduces the natural patterns of eye-head coordination in that head contributions increase and ocular contributions decrease together with the size of gaze shifts and this without compromising the accuracy of gaze realignment. It also accounts for the dependence of the relative contributions of the eyes and the head on the initial positions of the eyes, as well as for the position sensitivity of saccades evoked by electrical stimulation of the superior colliculus. Finally, it shows why units of the saccadic system could appear to carry gaze-related signals even if they do not operate within a gaze control loop and do not receive head-related information.

Eye position modulates the electromyographic responses of neck muscles to electrical stimulation of the superior colliculus in the alert cat.

Rapid gaze shifts are often accomplished with coordinated movements of the eyes and head, the relative amplitude of which depends on the starting position of the eyes. The size of gaze shifts is determined by the superior colliculus (SC) but additional processing in the lower brain stem is needed to determine the relative contributions of eye and head components. Models of eye-head coordination often assume that the strength of the command sent to the head controllers is modified by a signal indicative of the eye position. Evidence in favor of this hypothesis has been recently obtained in a study of phasic electromyographic (EMG) responses to stimulation of the SC in head-restrained monkeys (Corneil et al. in J Neurophysiol 88:2000-2018, 2002b). Bearing in mind that the patterns of eye-head coordination are not the same in all species and because the eye position sensitivity of phasic EMG responses has not been systematically investigated in cats, in the present study we used cats to address this issue. We stimulated electrically the intermediate and deep layers of the caudal SC in alert cats and recorded the EMG responses of neck muscles with horizontal and vertical pulling directions. Our data demonstrate that phasic, short latency EMG responses can be modulated by the eye position such that they increase as the eye occupies more and more eccentric positions in the pulling direction of the muscle tested. However, the influence of the eye position is rather modest, typically accounting for only 10-50% of the variance of EMG response amplitude. Responses evoked from several SC sites were not modulated by the eye position.

The local loop of the saccadic system closes downstream of the superior colliculus.

Models of the saccadic system differ in several respects including the signals fed back to their comparators, as well as the location and identity of the units that could serve as comparators. Some models place the comparator in the superior colliculus while others assign this role to the reticular formation. To test the plausibility of reticular models we stimulated electrically efferent fibers of the superior colliculus (SC) of alert cats along their course through the pons, in the predorsal bundle (PDB). Our data demonstrate that electrical stimulation of the PDB evokes saccades, even with stimuli of relatively low frequency (100 Hz), which are often accompanied by slow drifts. The velocity and latency of saccades are influenced by the intensity and frequency of stimulation while their amplitude depends on the intensity of stimulation and the initial position of the eyes. The dynamics of evoked saccades are comparable to those of natural, self-generated saccades of the cat and to those evoked in response to the electrical stimulation of the SC. We also show that PDB-evoked saccades are not abolished by lesions of the SC and that therefore antidromic activation of the SC is not needed for their generation. Our data clearly demonstrate that the burst generator of the horizontal saccadic system is located downstream of the SC. If it is configured as a local loop controller, as assumed by most models of the saccadic system, our data also demonstrate that its comparator is located beyond the decussation of SC efferent fibers, in the pons.

Predictive elements in ocular interception and tracking of a moving target by untrained cats.

We presented a mechanical target moving at constant velocity to awake, nontrained, head-restrained cats, in order to study how naive animals pursue objects moving at a high speed with their gaze. Eye movements were recorded while the target was moving in different directions at a constant velocity (20-80 degrees/s) through the center of the visual field. We observed two oculomotor strategies: cats either made an interception saccade (IS) toward the target but opposite to its motion, or tracked it in the direction of motion. They used the interception strategy more frequently when the gaze position error at the onset of target motion was large, and the tracking strategy when it was small. Interception was always achieved by single saccades, which were faster than tracking saccades (TS). During tracking, cats generated sequences of two to six saccades separated by "smooth" eye movements. Tracking quality varied considerably from trial to trial. When the level of motivation was high, cats would track the target at 80 degrees/s over up to 75% of the oculomotor range, with relatively small position errors. We compared ISs and TSs with respect to their metric properties and timing. The amplitudes of ISs positively correlated with position error existing 100 ms before saccade onset, but saccade vectors were directed to a point ahead of the target along the target's track. We conclude that, in programming the ISs, target motion is used to predict the future target position so as to assure a spatial lead of the gaze at the saccade end, instead of attempting a precise capture of the target. The amplitude of TSs did not depend on preceding position errors. TSs were usually small at the onset of the first saccade, as if cats would wait till the target arrived near the line of sight. A majority of primary TSs were initiated before the target arrived near the direction of gaze. Thus they had a direction, opposite to the position error sampled 100 ms before the saccade, but the same as the direction of target motion. Prediction of the future target position from its velocity vector should therefore contribute to the programming of TSs. In addition, we observed that TSs were faster when they were initiated with a spatial lag relative to the target and they were slower if there was a spatial lead or target velocity was reduced. Such a modulation appears to be analogous to the predictive correction of the saccade amplitude during smooth pursuit in primates. Considering strong visual motion sensitivity and motor properties of output neurons of the superior colliculus, it is likely that, in cats, the colliculus makes a major contribution to the integration of eye movement-related and target motion-related signals.

Saccades and multisaccadic gaze shifts are gated by different pontine omnipause neurons in head-fixed cats.

Pontine omnipause neurons (OPNs) have so far been considered as forming a homogeneous group of neurons whose tonic firing stops during the duration of saccades, when the head is immobilized. In cats, they pause for the total duration of gaze shifts, when the head is free to move. In the present study, carried out on alert cats with fixed heads, we present observations made during self-initiated saccades and during tracking of a moving target which show that the OPN population is not homogeneous. Of the 76 OPNs we identified, 39 were found to have characteristics similar to those of previously described neurons, "saccade" (S-) OPNs: (1) the durations of their pauses were significantly correlated with the durations of saccades; (2) the discharge ceased shortly before saccade onset and resumed before saccade end; (3) visual responses to target motion were excitatory; and (4) during tracking, S-OPNs interrupted the discharge for the duration of saccades and resumed firing during perisaccadic "drifts". However, the characteristics of 37 neurons ("complex" (C-) OPNs) were different: (1) the pause duration was not correlated with the duration of self-initiated saccades; (2) time lead of pause onsets relative to saccades was, on average, longer than in the group of S-OPNs, and firing resumed after the saccade end; (3) visual target motion suppressed tonic discharges; and (4) during tracking, firing was interrupted for the total duration of gaze shifts, including not only saccades but also perisaccadic "drifts". We conclude that cat OPNs can be subdivided into two main groups. The first comprises neurons whose firing patterns are compatible with gating individual saccades ("saccade" OPNs). The second group consists of "complex" OPNs whose firing characteristics are appropriate to gate total gaze displacements rather than individual saccades. The function of these neurons may be to disinhibit pontobulbar circuits participating in the generation of saccade sequences and associated perisaccadic drifts.

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.

Orienting-related eye-neck neurons of the medial ponto-bulbar reticular formation do not participate in horizontal canal-dependent vestibular reflexes of alert cats.

Ponto-bulbar reticular formation neurons, including identified reticulospinal neurons, were studied in alert, head-fixed cats. Orienting-related neurons of "eye-neck" type (ENNs) were selected on the basis of qualitative correlations of their discharges with visually triggered eye saccades and electromyographic activity (EMG) of dorsal neck muscles. It was tested whether ENNs participate both in visually triggered gaze shifts requiring eye-head coordination and in gaze-stabilizing movements, such as vestibulo-ocular and vestibulo-collic reflexes (VOR, VCR). Firing patterns were studied during passive sinusoidal rotation (0.2-1.0 Hz; 2.0-21.5 deg peak-to-peak) in the horizontal plane. Responses to electrical stimulation of the superior colliculus and the vestibular nerve were recorded to assess the convergence of tectal and vestibular synaptic inputs. The same methods were applied to a control sample of neurons with discharges apparently "unrelated" to orienting movements. ENNs did not show any modulation of firing rate correlated to compensatory VOR or VCR during passive sinusoidal rotations. Among "unrelated" cells, the fraction of modulated units was close to that reported for reticular neurons projecting in the medial reticulospinal tract. Phasic and sustained components of ENN bursts were associated with anticompensatory movements induced by rotation, such as quick phases, ocular beating field shift, and the increase of EMG activity in neck muscles acting in the direction of passive rotation. Monosynaptic excitation from the contralateral superior colliculus was observed in 92.3% of ENNs, but only 2 out of 17 tested showed an excitatory response to vestibular nerve stimulation. In the control group of "unrelated" neurons the proportions of monosynaptic tectal and excitatory vestibular nerve inputs were, respectively, 75.6 and 71.4%. It is concluded that ENNs are specifically related to active gaze shifts, derived from either visual or from head velocity inputs. Rhombencephalic connections of vestibular nuclei to these neurons appear to be quite weak. Parallel inputs from the mid- or forebrain must be assumed to explain their firing patterns during rotation-induced anticompensatory gaze shifts. Within the studied range of frequencies and amplitudes of passive rotation, ENNs did not participate in the vestibulo-collic reflex. It is therefore unlikely that reticular neurons controlling orienting eye-neck synergies act also as a premotor pathway for gaze-stabilizing movements.

Post-spike facilitation of neck EMG by cat tectoreticulospinal neurones during orienting movements.

1. The activity of fourteen tectoreticulospinal neurones (TRSNs) was recorded intraaxonally in the caudal pons of alert cats during orienting movements towards visual stimuli. TRSN spikes were used to compute the spike-triggered average (STA) of rectified EMG of dorsal neck muscles. 2. Eight TRSNs for which 400-2532 spikes were available were analysed with the STA technique. When the STA was computed from all spikes, significant post-spike facilitation (PSF) was obtained for six of eighteen cell-muscle pairs investigated (5 TRSNs). The mean relative amplitude of PSFs was 7.4% (S.D. 3.7). The onset latencies ranged from 1.1 to 5.0 ms and mean duration was 11.4 +/- 3.1 ms (mean +/- S.D.). 3. Interspike interval distributions were unimodal, with modes between 2.7 and 12.7 ms. Spike trains of TRSNs that produced significant PSFs contained 5-13% of the interspike intervals < or = 5 ms and 22-37% of the intervals < or = 10 ms. To evaluate the contribution of short intervals to PSF, STAs were computed separately for spikes preceded by 'short' (< or = 5 or < or = 10 ms) and 'long' (> 5 or > 10 ms) intervals. 4. When computed from spikes preceded by 'long' intervals, PSF amplitudes were small (mean +/- S.D., 5.3 +/- 2.7%) and onset latencies measured by cusum ranged between 2.4 and 5.4 ms. This is longer than the estimated minimal latency of monosynaptic facilitatory effect on neck EMG (1.9-2.1 ms). 5. Relative amplitudes of PSF obtained with spikes preceded by 'short' intervals were much larger (mean +/- S.D., 14.8 +/- 7.4%), but cusums indicated negative latencies for four of six PSFs. The unrealistically short onset latencies could be accounted for by the summation of facilitation from the trigger spike with that of the preceding spikes. In four of five TRSNs a large increase of PSF amplitude (from 3.2 to 7.2 times the amplitude obtained from 'long' intervals) suggests the presence of frequency-dependent potentiation of synaptic transmission. 6. This study unequivocally demonstrates that some TRSNs produce significant post-spike facilitation of neck motoneurones. This facilitation could be mediated by monosynaptic tectomotoneuronal connections although a contribution by disynaptic connections cannot be definitively ruled out. The high instantaneous firing rates of TRSNs produce a potentiation of the otherwise weak facilitatory action of TRSNs that presumably contributes to a rapid recruitment of motoneurones during initiation of head orienting movements.

Anatomical evidence for ipsilateral collicular projections to the spinal cord in the cat.

Injections of WGA-HRP were made within the C1 segment of spinal cord in cats with a midsagittal section of the midbrain. A small number of labelled cells were found in the latero-caudal part of the deeper layers of the superior colliclus (SC) ipsilateral to the injection sites. Because of the complete section of the dorsal tegmental decussation, these results definitively demonstrate the existence of an ipsilateral tecto-spinal pathway projecting to upper cervical segments in the cat. Ipsilaterally projecting tecto-reticulo-spinal neurons represent about 5% of the total population of tecto-spinal neurons. They were exclusively located in the deeper collicular layers and most of them were found in the latero-caudal part of the SC. Comparison with our previous studies suggests that more ipsilateral tecto-spinal projections that found after the section of the dorsal tegmental decussation probably exist. They may arise from tecto-reticulo-spinal neurons recrossing the midline in the brainstem or in the rostral part of C1. By analogy with the cortico-spinal tract, we suggest that the existence of an ipsilateral tecto-spinal pathway can be regarded as evidence for a substantial development of the cat tecto-spinal system as compared with other mammals.

Tracing premotor brain stem networks of orienting movements.

Methods allowing a direct matching of movement-related firing patterns and connectivity of individual neurons have been used in the analysis of premotor networks controlling orienting movements. Advances have been made in the description of coding properties of orienting-related tectal output neurons, as well as in specifying their distributed connections in the brain stem and possible modes of coupling to saccadic pattern generators in the reticular formation. New data on the properties of signals and connectivity patterns have also been obtained for the tecto-recipient reticulo-spinal neurons. At least a small portion of the network performing the spatio-temporal transformations of orienting-related tectal efferent signals can now be described both in functional and in morphological terms.

The control of slow orienting eye movements by tectoreticulospinal neurons in the cat: behavior, discharge patterns and underlying connections.

The activity of tectoreticulospinal neurons (TRSN) during orienting gaze shifts was studied in alert, head-fixed cats by intra-axonal recordings. The scope of the study was to evaluate the role of this class of superior colliculus neurons in the generation of slow eye movements (drifts) which often follow main-sequence saccades and sometimes appear as an independent motor event of orienting. The parameters of such movements are described in the first part of the paper. The organization of underlying pathways in the lower brainstem has been studied by intra-axonal horseradish peroxidase (HRP) tracing. The mean amplitude of postsaccadic drifts (PSD) is 1.21 degrees (SD 0.63), but it can eventually reach 6-8 degrees. PSDs have mean velocity of 14.9 degrees/s (SD 4.28) and mean duration of 104.2 ms (SD 50.8). These two parameters are positively correlated with PSD amplitude. The presence of PSDs is usually associated with an increased neck muscle activity on the side toward which the eyes move. The durations of these two motor events show a reliable positive correlation. PSDs appear to occur when gaze error persists after a saccade and a correction is attempted by means of a slow eye movement and a head turn. The durations of TRSN bursts are, on average, longer than the sum of the lead time and the saccade duration. Bursts associated with combinations of saccades and PSD are significantly longer than those recorded in the absence of PSDs. The probability of occurrence of PSDs is higher when firing of TRSNs continues after saccade termination. Such prolonged discharges usually coincide with a combination of PSDs and phasic activation of the neck electromyogram. The mean firing rate of TRSNs during PSDs is 62% of that during saccade-related portions of the burst and declines to 45% after the end of PSDs. According to its timing and intensity, postsaccadic firing of TRSNs is appropriate as a signal underlying slow, corrective eye movements and later portions of phasic neck muscle contractions during orienting. Intra-axonal HRP labeling showed that visuomotor TRSNs of the X type (n = 3) terminate in the abducens nucleus, with 145-331 boutons terminaux and en passant. Average bouton densities in the nucleus are lower than in the periabducens reticular formation, but higher than in more rostral paramedian pontine reticular formation (PPRF) regions. Terminal fields in the PPRF match the locations of "eye-neck' reticulospinal neurons (RSNs) and exitatory burst neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Rostrocaudal and lateromedial density distributions of superior colliculus neurons projecting in the predorsal bundle and to the spinal cord: a retrograde HRP study in the cat.

Efferent neurons of the cat superior colliculus (SC) which project in the predorsal bundle (PDB) and to the spinal cord (PDB neurons) form a major pathway by which the SC controls the changes of the direction of gaze in response to stimuli of visual and other modalities. Knowledge of rostrocaudal and lateromedial density distributions of different groups of PDB neurons within the SC is necessary to analyse their relationships with the topography of sensory and motor maps. Density gradients may also bear on the efficacy of connections originating from topographically different collicular regions. In the present study, large injections of HRP/WGA-HRP were made in the C1 segment of the spinal cord and in the pontobulbar tegmentum. Judged by several morphological criteria, axons of passage, including those not subjected to a direct mechanical damage, were participating in the uptake of tracers. Therefore, labeled SC neurons corresponded to the nearly total populations of contralaterally projecting tectospinal neurons (TSNs) and neurons projecting in the PDB, respectively. Subtraction of the TSN density map from that of the whole PDB population was used to infer the distribution of tectal neurons terminating in the rhombencephalic tegmentum (TRhN). This subtotal labeling method proved useful in resolving the contradictions between the earlier HRP studies on the TSN and TRhN topography. The following density distributions were obtained for different groups of PDB neurons: 1) The mean TSN density is more than two times higher in the lateral half of the SC, representing the lower visual field. In this region the density remains constant from rostral to caudal, i.e., from the representation of vertical meridian to large contralateral azimuths. In the medial half, the average density decreases from rostral to caudal. Consequently, TSNs do not show the caudalward increment predicted by the higher efficacy of caudal stimulation points in eliciting head movements. 2) The distribution of PDB neurons is symmetrical with respect to the representation of the horizontal meridian. It is close to homogeneous at all azimuths of the retinotopic map and within the zone limited by small (10-15 degrees) upward and downward elevations.(ABSTRACT TRUNCATED AT 400 WORDS)

How visual inputs to the ponto-bulbar reticular formation are used in the synthesis of premotor signals during orienting.

The primate superior colliculus (SC) is known as a structure subserving the transformation of visual information into "commands" for orienting eye movements. Collicular burst neurons discharging with short lead times in relation to visually triggered or spontaneous saccades are supposed to be the output elements linking the SC to immediately premotor pattern generators. In this paper we summarize some data available for the cat's SC neurones, identified as tecto-reticulo-spinal projection cells (TRSN), and reticulospinal neurones (RSN), identified as receiving excitatory collicular input. Some TRSNs respond to visual stimuli in the absence of orienting movements and, hence, their signals cannot be regarded as motor "commands", in spite of their proven connections with premotor pools in the brain stem and with the spinal cord. Moreover, a small fraction of RSNs belonging to polysynaptic descending collicular pathways also displays visual responses dissociated from movement, in addition to discharges related to the performance of orienting eye-head synergies. The processes of visual to motor transformation, assumed by current models as being definitively accomplished in the SC, appear thus to be partially performed in the reticular network incorporating the overlapping collaterals of tectal projection cells and their target neurons in the reticular core. It is concluded that, at least as for visuomotor transformations underlying orienting movements in the cat, the deep division of the SC and the brain stem reticular formation represent an ensemble, rather than a sequence of hierarchically arranged levels of processing.

Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. I. Behavioral properties.

The activity of 24 reticulo-spinal neurons (RSN) identified by antidromic stimulation at the C1-C2 level has been recorded intra-axonally in the pons of alert head-fixed cats during spontaneous gaze shifts and orienting towards novel targets. Relationship of neuronal discharge to saccadic eye movements, positions of fixation and EMG of dorsal neck muscles were analysed. The present report describes behavioral properties of a group of 14 RSN showing similar types of correlations with motor parameters during eye-head synergies. These "eye-neck" RSN (EN-RSN) generate bursts in synchrony with phasic components of ipsilateral neck EMG and leading ipsiversive saccades by a variable lead time. Bursts are followed by a prolonged discharge whose frequency decays even when eccentric eye position is maintained constant and accompanied by sustained neck muscle activity. The firing rate of EN-RSNs depends on eye position: they are silent with saccades in their ON-direction when the eyes are deviated towards the contralateral half of the oculomotor range and the ipsilateral neck muscles are relaxed. When the eyes cross the vertical meridian, the frequency of phasic and tonic components related to eye-head synergies increase proportionally to ipsilateral eye position. Ten of the 14 EN-RSNs, located in the pontine reticular formation, received monosynaptic input from the contralateral superior colliculus. Two were labeled by intra-axonal injection of HRP which revealed extensive branching in the abducens, facial, medial and lateral vestibular, prepositus and intercalatus nuclei and in the caudal pontine and bulbar reticular formation. It is concluded that the caudal pontine tegmentum, including the region just anterior to the abducens nucleus, contains RSNs whose signals seem appropriate to control phasic neck muscle activity and which also project to structures related to ocular and facial movements. Comparisons with the perisaccadic activity of tectal neurons projecting in the predorsal bundle reveals a profound transformation of the descending signal at the level of EN-RSNs which represent first order relay neurons of the tecto-reticulo-spinal pathway.

Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. II. Morphological properties as revealed by intra-axonal injections of horseradish peroxidase.

Previously we described physiological properties of pontine reticulo-spinal neurons which generate bursts and decaying tonic discharges related to eye movements and neck muscle activity during ipsiversive gaze shifts (Grantyn and Berthoz 1987). Two of these "eye-neck reticulo-spinal neurons" (EN-RSN) were labeled by intra-axonal injections of HRP. The present report provides a detailed description of their morphology with an emphasis on the topography of axon collaterals, bouton numbers, and the structure of preterminal ramifications in different target areas. The cell bodies of labeled EN-RSNs were located rostro-ventrally to the abducens nucleus. Their descending axons issued 8 and 13 collaterals (left and right EN-RSN, respectively) at different rostro-caudal levels, between the abducens nucleus and the pyramidal decussation. On the basis of the size of their cell bodies, the isodendritic type of dendritic branching and their multiple collateralization, EN-RSNs correspond to the class of "generalized" reticular neurons, often referred to as The Scheibels' neurons. Collaterals of EN-RSNs terminated in the following structures: the abducens and facial nuclei, the medial and lateral vestibular nuclei, the nn. prepositus and intercalatus, and the bulbar reticular formation. As judged from bouton numbers, the strongest connection of both neurons was with the abducens nuclei. Terminations in the rostral part of the medial vestibular and prepositus nuclei indicate that EN-RSNs may also influence oculomotor output activity through these indirect routes. In the facial nucleus, a majority of terminations was found in its medial subdivision containing motoneurons of ear muscles. However, other subdivisions were also contacted by EN-RSNs. Most terminations in the rostral bulbar reticular formation are distributed to the dorsal, gigantocellular field. Within this field, there is a substantial contribution to the zone characterized by the highest density of reticulo-spinal neurons projecting directly to neck motoneurons. Other target areas which may participate in the modulation of spinal cord activity by EN-RSNs are the ventral reticular nucleus in the caudal medulla and the lateral vestibular nucleus. EN-RSNs also establish connections with precerebellar structures: the prepositus and the paramedian reticular nuclei. The numbers of boutons on collaterals issued within 6 mm of the injection site varied between 37 and 469. The occurrence of presumed axo-somatic contacts was low (0-8.2%) and not characteristic for any particular target area. Local accumulations of boutons in the form of small and large field clusters was a common observation.(ABSTRACT TRUNCATED AT 400 WORDS)

Some collicular efferent neurons code saccadic eye velocity.

The activity of identified tecto-reticulo-spinal neurons (TRSNs) was studied in alert head-fixed cats during orienting towards moving visual stimuli. Eye movements and dorsal neck muscle activity were recorded simultaneously. Burst parameters of TRSNs showing visuomotor properties were analysed quantitatively. It could be demonstrated that some neurons generate presaccadic bursts whose instantaneous frequency profile is closely correlated with the profile of saccadic eye velocity. This correlation could be revealed only under conditions in which cats made orienting saccades to 'catch' a target moving in the preferred direction of the neuron's visual receptive field. Latency between bursts and saccades varied depending upon the degree of attention toward the target and saccade direction.

Burst activity of identified tecto-reticulo-spinal neurons in the alert cat.

Activity of tecto-reticulo-spinal neurons (TRSN), identified electrophysiologically and/or by intra-axonal HRP injections, was studied in alert cats during presentation of moving visual stimuli. A majority of TRSNs showed complex visuomotor properties: directionally selective visual responses in the absence of motor counterparts of orienting, enhanced bursting when stimuli triggered saccades, and no activation for spontaneous saccades. Highest intraburst frequencies were observed during active orienting towards novel, "interesting" objects. The more vigorous bursts usually contained repetitive grouped discharges attaining instantaneous frequencies up to 700 imp/s but average firing rates remained in the range of 120-300 imp/s. Intra-axonal HRP injections confirmed terminations of TRSN collaterals in the premotor areas of the lower brain stem, including the abducens nucleus, but also disclosed differences in the details of collateralization between neurons showing different types of visuo-motor activity.