Cues to move increased information in superior colliculus tuning curves

Shifts in the location of spatial attention produce increases in the gain and sensitivity of neuronal responses to sensory stimuli. Cues to shift the line of sight have the same effect on sensory responses in a motor area involved in the control of eye movements, the superior colliculus. Evidence has shown that shifts of gaze and shifts of attention are linked, suggesting there may be similar underlying mechanisms. Here, we report on a novel way in which cues to move the eyes (top-down signals) can influence sensory responses of neurons by altering the variability of their discharge rate. We measured the spatial tuning of superior colliculus neuronal activity in trials with cues to either make or withhold saccadic eye movements. We found that tuning curve widths both increased and decreased, but that the information conveyed by the neuronal discharge about the stimulus increased with a cue to make a saccade. The increase in information resulted partly from a decrease in trial-to-trial variability of neuronal discharges for stimuli located at the flanks of the tuning curves rather than from increases in the discharge rate for stimuli located at the peak of the tuning curves. This result is consistent with theoretical work and provides a novel way for cognitive signals to influence sensory responses within motor regions of the brain.     

Human eye-head coordination in two dimensions under different sensorimotor conditions

 The coordination between eye and head movements during a rapid orienting gaze shift has been investigated mainly when subjects made horizontal movements towards visual targets with the eyes starting at the centre of the orbit. Under these conditions, it is difficult to identify the signals driving the two motor systems, because their initial motor errors are identical and equal to the coordinates of the sensory stimulus (i.e. retinal error). In this paper, we investigate head-free gaze saccades of human subjects towards visual as well as auditory stimuli presented in the two-dimensional frontal plane, under both aligned and unaligned initial fixation conditions. Although the basic patterns for eye and head movements were qualitatively comparable for both stimulus modalities, systematic differences were also obtained under aligned conditions, suggesting a task-dependent movement strategy. Auditory-evoked gaze shifts were endowed with smaller eye-head latency differences, consistently larger head movements and smaller concomitant ocular saccades than visually triggered movements. By testing gaze control for eccentric initial eye positions, we found that the head displacement vector was best related to the initial head motor-error (target-re-head), rather than to the initial gaze error (target-re-eye), regardless of target modality. These findings suggest an independent control of the eye and head motor systems by commands in different frames of reference. However, we also observed a systematic influence of the oculomotor response on the properties of the evoked head movements, indicating a subtle coupling between the two systems. The results are discussed in view of current eye-head coordination models. Received: 24 April 1996 / Accepted: 25 October 1996     

Sensorimotor integration in the primate superior colliculus. I. Motor convergence

Orienting movements of the eyes and head are made to both auditory and visual stimuli even though in the primary sensory pathways the locations of auditory and visual stimuli are encoded in different coordinates. This study was designed to differentiate between two possible mechanisms for sensory-to-motor transformation. Auditory and visual signals could be translated into common coordinates in order to share a single motor pathway or they could maintain anatomically separate sensory and motor routes for the initiation and guidance of orienting eye movements. The primary purpose of the study was to determine whether neurons in the superior colliculus (SC) that discharge before saccades to visual targets also discharge before saccades directed toward auditory targets. If they do, this would indicate that auditory and visual signals, originally encoded in different coordinates, have been converted into a single coordinate system and are sharing a motor circuit. Trained monkeys made saccadic eye movements to auditory or visual targets while the activity of visual-motor (V-M) cells and saccade-related burst (SRB) cells was monitored. The pattern of spike activity observed during trials in which saccades were made to visual targets was compared with that observed when comparable saccades were made to auditory targets. For most (57 of 59) V-M cells, sensory responses were observed only on visual trials. Auditory stimuli originating from the same region of space did not activate these cells. Yet, of the 72 V-M and SRB cells studied, 79% showed motor bursts prior to saccades to either auditory or visual targets. This finding indicates that visual and auditory signals, originally encoded in retinal and head-centered coordinates, respectively, have undergone a transformation that allows them to share a common efferent pathway for the generation of saccadic eye movements. Saccades to auditory targets usually have lower velocities than saccades of the same amplitude and direction made to acquire visual targets. Since fewer collicular cells are active prior to saccades to auditory targets, one determinant of saccadic velocity may be the number of collicular neurons discharging before a particular saccade.     

Role of the monkey substantia nigra pars reticulata in orienting behaviour and visually triggered arm movements

The role of the substantia nigra pars reticulata (SNpr) has been studied in the head-free monkey during orienting behaviour in response to visual instruction signals triggering head positioning and conditioned arm movement. During the behavioural responses we recorded the electromyographic activities of neck muscles and triceps brachii, head movement, horizontal electrooculogram and single unit activity of SNpr neurons. Activity of 38 neurons located in the medial part of SNpr were analysed during the visuo-motor task. Forty percent of these units showed a moderate decrease in tonic firing rate during postural preparation preceding the orientation toward eccentric visual signal. This decrease, unrelated with saccadic eye movements per se, was followed by a marked pause observed when the rewarded stimulus was switched on and the conditioned arm movement was executed to get the reward. These data suggest that the pause in discharge of these SNpr neurons are time locked with behaviourally relevant visual stimuli and/or appropriate motor responses.     

Kinematics and eye–head coordination of gaze shifts evoked from different sites in the superior colliculus of the cat

Shifting gaze requires precise coordination of eye and head movements. It is clear that the superior colliculus (SC) is involved with saccadic gaze shifts. Here we investigate its role in controlling both eye and head movements during gaze shifts. Gaze shifts of the same amplitude can be evoked from different SC sites by controlled electrical microstimulation. To describe how the SC coordinates the eye and the head, we compare the characteristics of these amplitude-matched gaze shifts evoked from different SC sites. We show that matched amplitude gaze shifts elicited from progressively more caudal sites are progressively slower and associated with a greater head contribution. Stimulation at more caudal SC sites decreased the peak velocity of the eye but not of the head, suggesting that the lower peak gaze velocity for the caudal sites is due to the increased contribution of the slower-moving head. Eye–head coordination across the SC motor map is also indicated by the relative latencies of the eye and head movements. For some amplitudes of gaze shift, rostral stimulation evoked eye movement before head movement, whereas this reversed with caudal stimulation, which caused the head to move before the eyes. These results show that gaze shifts of similar amplitude evoked from different SC sites are produced with different kinematics and coordination of eye and head movements. In other words, gaze shifts evoked from different SC sites follow different amplitude–velocity curves, with different eye–head contributions. These findings shed light on mechanisms used by the central nervous system to translate a high-level motor representation (a desired gaze displacement on the SC map) into motor commands appropriate for the involved body segments (the eye and the head).     

Firing behaviour of squirrel monkey eye movement-related vestibular nucleus neurons during gaze saccades

The firing behaviour of vestibular nucleus neurons putatively involved in producing the vestibulo-ocular reflex (VOR) was studied during active and passive head movements in squirrel monkeys. Single unit recordings were obtained from 14 position-vestibular (PV) neurons, 30 position-vestibular-pause (PVP) neurons and 9 eye-head-vestibular (EHV) neurons. Neurons were sub-classified as type I or II based on whether they were excited or inhibited during ipsilateral head rotation. Different classes of cell exhibited distinctive responses during active head movements produced during and after gaze saccades. Type I PV cells were nearly as sensitive to active head movements as they were to passive head movements during saccades. Type II PV neurons were insensitive to active head movements both during and after gaze saccades. PVP and EHV neurons were insensitive to active head movements during saccadic gaze shifts, and exhibited asymmetric sensitivity to active head movements following the gaze shift. PVP neurons were less sensitive to ondirection head movements during the VOR after gaze saccades, while EHV neurons exhibited an enhanced sensitivity to head movements in their on direction. Vestibular signals related to the passive head movement were faithfully encoded by vestibular nucleus neurons. We conclude that central VOR pathway neurons are differentially sensitive to active and passive head movements both during and after gaze saccades due primarily to an input related to head movement motor commands. The convergence of motor and sensory reafferent inputs on VOR pathways provides a mechanism for separate control of eye and head movements during and after saccadic gaze shifts.     

Serial linkage of target selection for orienting and tracking eye movements

Many natural actions require the coordination of two different kinds of movements. How are targets chosen under these circumstances: do central commands instruct different movement systems in parallel, or does the execution of one movement activate a serial chain that automatically chooses targets for the other movement? We examined a natural eye tracking action that consists of orienting saccades and tracking smooth pursuit eye movements, and found strong physiological evidence for a serial strategy. Monkeys chose freely between two identical spots that appeared at different sites in the visual field and moved in orthogonal directions. If a saccade was evoked to one of the moving targets by microstimulation in either the frontal eye field (FEF) or the superior colliculus (SC), then the same target was automatically chosen for pursuit. Our results imply that the neural signals responsible for saccade execution can also act as an internal command of target choice for other movement systems.     

Combined eye-head gaze shifts to visual and auditory targets in humans

We studied the characteristics of combined eye-head gaze shifts in human subjects to determine whether they used similar strategies when looking at visual (V), auditory (A), and combined (V+A) targets located at several target eccentricities along the horizontal meridian. Subjects displayed considerable variability in the combinations of eye and head movement used to orient to the targets, ranging from those who always aligned their head close to the target, to those who relied predominantly on eye movements and only moved their head when the target was located beyond the limits of ocular motility. For a given subject, there was almost no variability in the amount of eye and head movement in the three target conditions (V, A, V+A). The time to initiate a gaze shift was influenced by stimulus modality and eccentricity. Auditory targets produced the longest latencies when located centrally (less than 20° eccentricity), whereas visual targets evoked the longest latencies when located peripherally (greater than 40° eccentricity). Combined targets (V+A) elicited the shortest latency reaction times at all eccentricities. The peak velocity of gaze shifts was also affected by target modality. At eccentricities between 10 and 30°, peak gaze velocity was greater for movements to visual targets than for movements to auditory targets. Movements to the combined target were of comparable speed with movements to visual targets. Despite the modality-specific differences in reaction latency and peak gaze velocity, the consistency of combinations of eye and head movement within subjects suggests that visual and auditory signals are remapped into a common reference frame for controlling orienting gaze shifts. A likely candidate is the deeper layers of the superior colliculus, because visual and auditory signals converge directly onto the neurons projecting to the eye and head premotor centers.     

Visual responses of pulvinar and collicular neurons during eye movements of awake, trained macaques.

1. We recorded from single neurons in awake, trained rhesus monkeys in a lighted environment and compared responses to stimulus movement during periods of fixation with those to motion caused by saccadic or pursuit eye movements. Neurons in the inferior pulvinar (PI), lateral pulvinar (PL), and superior colliculus were tested. 2. Cells in PI and PL respond to stimulus movement over a wide range of speeds. Some of these cells do not respond to comparable stimulus motion, or discharge only weakly, when it is generated by saccadic or pursuit eye movements. Other neurons respond equivalently to both types of motion. Cells in the superficial layers of the superior colliculus have similar properties to those in PI and PL. 3. When tested in the dark to reduce visual stimulation from the background, cells in PI and PL still do not respond to motion generated by eye movements. Some of these cells have a suppression of activity after saccadic eye movements made in total darkness. These data suggest that an extraretinal signal suppresses responses to visual stimuli during eye movements. 4. The suppression of responses to stimuli during eye movements is not an absolute effect. Images brighter than 2.0 log units above background illumination evoke responses from cells in PI and PL. The suppression appears stronger in the superior colliculus than in PI and PL. 5. These experiments demonstrate that many cells in PI and PL have a suppression of their responses to stimuli that cross their receptive fields during eye movements. These cells are probably suppressed by an extraretinal signal. Comparable effects are present in the superficial layers of the superior colliculus. These properties in PI and PL may reflect the function of the ascending tectopulvinar system.     

The fixation area of the cat superior colliculus: effects of electrical stimulation and direct connection with brainstem omnipause neurons

The superior colliculus has long been recognized as an important structure in the generation of saccadic displacements of the visual axis. Neurons with presaccadic activity encoding saccade vectors are topographically organized and form a motor map. Recently, neurons with fixation-related activity have been recorded at the collicular rostral pole, at the area centralis representation or fixation area. Another collicular function which deals with the maintenance of fixation behavior by means of active inhibition of orientation commands was then suggested. We tested that hypothesis as it relates to the suppression of gaze saccades (gaze = eye in space = eye in head + head in space) in the head-free cat by increasing the activity of the fixation cells at the rostral pole with electrical microstimulation. Long stimulation trains applied before gaze saccades delayed their initiation. Short stimuli, delivered during the gaze saccades, transiently interrupted both eye and head components. These results provide further support for a role in fixation behavior for collicular fixation neurons. Brainstem omnipause neurons also exhibit fixation-related activity and have been shown to receive a direct excitatory input from the superior colliculus. To determine whether the collicular projection to omnipause neurons arises from the fixation area, the deep layers of the superior colliculus were electrically stimulated either at the rostral pole including the fixation area or in more caudal regions where stimulation evokes orienting responses. Forty-nine neurons were examined in three cats. 61% of the neurons were found to be orthodromically excited by single-pulse stimulation of the rostral pole, whereas only 29% responded to caudal stimulation. In addition, stimuli delivered to the rostral pole activated, on average, omnipause neurons at shorter latencies and with lower currents than those applied in caudal regions. These results suggest that excitatory inputs to omnipause neurons from the superior colliculus are principally provided by the fixation area, via which the superior colliculus could play a role in suppression of gaze shifts.     

Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals

Based on the findings of the preceding paper, it is known that auditory and visual signals have been translated into common coordinates at the level of the superior colliculus (SC) and share a motor circuit involved in the generation of saccadic eye movements. It is not known, however, whether the translation of sensory signals into motor coordinates occurs prior to or within the SC. Nor is it known in what coordinates auditory signals observed in the SC are encoded. The present experiment tested two alternative hypotheses concerning the frame of reference of auditory signals found in the deeper layers of the SC. The hypothesis that auditory signals are encoded in head coordinates predicts that, with the head stationary, the response of auditory neurons will not be affected by variations in eye position but will be determined by the location of the sound source. The hypothesis that auditory responses encode the trajectory of the eye movement required to look to the target (motor error) predicts that the response of auditory cells will depend on both the position of the sound source and the position of the eyes in the orbit. Extracellular single-unit recordings were obtained from neurons in the SC while monkeys made delayed saccades to auditory or visual targets in a darkened room. The coordinates of auditory signals were studied by plotting auditory receptive fields while the animal fixated one of three targets placed 24 degrees apart along the horizontal plane. For 99 of 121 SC cells, the spatial location of the auditory receptive field was significantly altered by the position of the eyes in the orbit. In contrast, the responses of five sound-sensitive cells isolated in the inferior colliculus were not affected by variations in eye position. The possibility that systematic variations in the position of the pinnae associated with different fixation positions could account for these findings was controlled for by plotting auditory receptive fields while the pinnae were mechanically restrained. Under these conditions, the position of the eyes in the orbit still had a significant effect on the responsiveness of collicular neurons to auditory stimuli. The average magnitude of the shift of the auditory receptive field with changes in eye position (12.9 degrees) did not correspond to the magnitude of the shift in eye position (24 degrees). Alternative explanations for this finding were considered. One possibility is that, within the SC, there is a gradual transition from auditory signals in head coordinates to signals in motor error coordinates.(ABSTRACT TRUNCATED AT 400 WORDS)     

Head and body movements produced by electrical stimulation of superior colliculus in rats: effects of interruption of crossed tectoreticulospinal pathway

Stimulation of the superior colliculus in rats produces movements of the head and body that resemble either orientation and approach towards a contralateral stimulus, or avoidance of, or escape from, such a stimulus. A variety of evidence indicates that the crossed descending pathway, which runs in the contralateral predorsal bundle to the pontomedullary reticular formation and the spinal cord, is involved in orienting movements. The nature of this involvement was investigated, by assessing the effects on tectally-elicited movements of midbrain knife-cuts intended to section the pathway as it crosses midline in the dorsal tegmental decussation. As expected, ipsilateral movements resembling avoidance or escape were little affected by dorsal tegmental decussation section, whereas contralateral circling movements of the body were almost abolished. However, contralateral movements of the head in response to electrical stimulation were not eliminated, nor were orienting head movements to visual or tactile stimuli. There was some suggestion that section of the dorsal tegmental decussation increased the latency of head movements from electrical stimulation at lateral sites, and decreased the accuracy of orienting movements to sensory stimuli. These results support the view that the crossed tectoreticulospinal system is concerned with approach rather than avoidance movements. However, it appears that other, as yet unidentified, tectal efferent systems are also involved in orienting head movements. It is possible that this division of labour may reflect functional differences between various kinds of apparently similar orienting responses. One suggestion is that the tectoreticulospinal system is concerned less in open-loop orienting responses (that are initiated but not subsequently guided by sensory stimuli), than in following or pursuit movements.     

Brainstem control of head movements during orienting; organization of the premotor circuits

When an object appears in the visual field, animals orient their head, eyes, and body toward it in a well-coordinated manner (orienting movement). The head movement is a major portion of the orienting movement. Interest in the neural control of head movements in the monkey and human have increased in the 1990's, however, fundamental knowledge about the neural circuits controlling the orienting head movement continues to be based on a large number of experimental studies performed in the cat. Thus, it is crucial now to summarize information that has been clarified in the cat for further advancement in understanding the neural control of head movements in different animal species. The superior colliculus (SC) has been identified as the primary brainstem center controlling the orienting. Its output signal is transmitted to neck motoneurons via two major separate pathways: one through the reticulospinal neurons (RSNs) in the pons and medulla and the other through neurons in Forel's field H (FFH) in the mesodiencephalic junction. The tecto-reticulo-spinal pathway controls orienting chiefly in the horizontal direction, while the tecto-FFH-spinal pathway controls orienting in the vertical direction. In each pathway, a subgroup of neurons functions as premotor neurons for both extraocular and neck motoneurons, while others are specified for each, which allows both coordinated and separate control of eye and head movements. Head movements almost always produce shifts in the center of gravity that might cause postural disturbances. The postural equilibrium may be maintained by transmitting the orienting command to the limb segments via descending axons of the reticulospinal and long propriospinal neurons. The SC and brainstem relay neurons receive descending inputs from higher order structures such as the cerebral cortex, cerebellum, and basal ganglia. These inputs may serve context-dependent control of orienting by modulating the activities of the primary brainstem pathways.     

Superior colliculus control of vibrissa movements

This study tested the role of the superior colliculus in generating movements of the mystacial vibrissae-whisking. First, we compared the kinematics of whisking generated by the superior colliculus with those generated by the motor cortex. We found that in anesthetized rats, microstimulation of the colliculus evoked a sustained vibrissa protraction, whereas stimulation of motor cortex produced rhythmic protractions. Movements generated by the superior colliculus are independent of motor cortex and can be evoked at lower thresholds and shorter latencies than those generated by the motor cortex. Next we tested the hypothesis that the colliculus is acting as a simple reflex loop with the neurons that drive vibrissa movement receiving sensory input evoked by vibrissa contacts. We found that most tecto-facial neurons do not receive sensory input. Not only did these neurons not spike in response to sensory stimulation, but field potential analysis revealed that subthreshold sensory inputs do not overlap spatially with tecto-facial neurons. Together these findings suggest that the superior colliculus plays a pivotal role in vibrissa movement-regulating vibrissa set point and whisk amplitude-but does not function as a simple reflex loop. With the motor cortex controlling the whisking frequency, the superior colliculus control of set point and amplitude would account for the main parameters of voluntary whisking.     

Sound localization behavior in ferrets: comparison of acoustic orientation and approach-to-target responses

Auditory localization experiments typically either require subjects to judge the location of a sound source from a discrete set of response alternatives or involve measurements of the accuracy of orienting responses made toward the source location. To compare the results obtained by both methods, we trained ferrets by positive conditioning to stand on a platform at the center of a circular arena prior to stimulus presentation and then approach the source of a broadband noise burst delivered from 1 of 12 loudspeakers arranged at 30 degrees intervals in the horizontal plane. Animals were rewarded for making a correct choice. We also obtained a non-categorized measure of localization accuracy by recording head-orienting movements made during the first second following stimulus onset. The accuracy of the approach-to-target responses declined as the stimulus duration was reduced, particularly for lateral and posterior locations, although responses to sounds presented in the frontal region of space and directly behind the animal remained quite accurate. Head movements had a latency of approximately 200 ms and varied systematically in amplitude with stimulus direction. However, the final head bearing progressively undershot the target with increasing eccentricity and rarely exceeded 60 degrees to each side of the midline. In contrast to the approach-to-target responses, the accuracy of the head orienting responses did not change much with stimulus duration, suggesting that the improvement in percent correct scores with longer stimuli was due, at least in part, to re-sampling of the acoustical stimulus after the initial head turn had been made. Nevertheless, for incorrect trials, head orienting responses were more closely correlated with the direction approached by the animals than with the actual target direction, implying that at least part of the neural circuitry for translating sensory spatial signals into motor commands is shared by these two behaviors.     

Midbrain contributions to sensorimotor decision making

Making decisions about future actions is a fundamental function of the nervous system. Classical theories hold that separate sets of brain regions are responsible for selecting and implementing an action. Traditionally, action selection has been considered the domain of high-level regions, such as the prefrontal cortex, whereas action generation is thought to be carried out by dedicated cortical and subcortical motor regions. However, increasing evidence suggests that the activity of individual neurons in cortical motor structures reflects abstract properties of "decision variables" rather than conveying simple motor commands. Less is known, though, about the role of subcortical structures in decision making. In particular, the superior colliculus (SC) is critical for planning and initiating visually guided, gaze-displacing movements and selecting visual targets, but whether and how it contributes more generally to sensorimotor decisions are unclear. Here, we show that the SC is intimately involved in orienting decisions based on odor cues, even though the SC does not explicitly process olfactory stimuli. Neurons were recorded from the intermediate and deep SC layers in rats trained to perform a delayed-response, odor-cued spatial choice task. SC neurons commonly fired well in advance of movement initiation, predicting the chosen direction nearly 1 s before movement. Moreover, under conditions of sensory uncertainty, SC activity varied with task difficulty and reward outcome, reflecting the influence of decision variables on the intercollicular competition thought to underlie orienting movements. These results indicate that the SC plays a more general role in decisions than previously appreciated, extending beyond visuomotor functions.     

Organization of the crossed tecto-reticulo-spinal projection in rat--I. Anatomical evidence for separate output channels to the periabducens area and caudal medulla.

The superior colliculus has been used to study principles of sensorimotor transformation underlying the guidance of orienting movements by multimodal sensory stimuli. We have previously suggested that there may be two different classes of mechanism which can produce orienting-like movements towards a novel event; one that locates a stimulus on the basis of remembered position, and another which uses continuous feedback relating to target velocity. The crossed descending pathway of the superior colliculus is widely considered the projection most likely to relay signals associated with the production of orienting movements. However, if different neural mechanisms are used to produce functionally distinct types of orienting, we might expect this pathway to have separate anatomical components related to function. The purpose of the present experiment was to see if collicular fibres innervating two important pre-motor targets of the crossed descending pathway, the periabducens area and the caudal medulla-spinal cord, come from the same population of tectal cells. One of the retrogradely transported fluorescent tracers (Diamidino Yellow) was injected into the periabducens area, and another (True Blue or Fast Blue) was injected into tectospinal fibres at the level of the ventromedial caudal medulla. Under these conditions we found: (i) less than 10% of labelled cells within the superior colliculus contained both tracers; (ii) the bulk of singly labelled cells projecting to the periabducens area or the caudal medulla were concentrated at different locations within the colliculus, (iii) in regions of the superior colliculus where there was overlap of singly labelled cells, neurons projecting to the periabducens area or the caudal medulla could be distinguished morphologically. These data provide three classes of evidence which indicate that the crossed descending projection in rat can be subdivided into at least two relatively independent anatomical components. This conclusion may, in part, provide an anatomical substrate for the functional dissociations proposed for orienting movements.     

Context dependence of receptive field remapping in superior colliculus

Our perception of the positions of objects in our surroundings is surprisingly unaffected by movements of the eyes, head, and body. This suggests that the brain has a mechanism for maintaining perceptual stability, based either on the spatial relationships among visible objects or internal copies of its own motor commands. Strong evidence for the latter mechanism comes from the remapping of visual receptive fields that occurs around the time of a saccade. Remapping occurs when a single neuron responds to visual stimuli placed presaccadically in the spatial location that will be occupied by its receptive field after the completion of a saccade. Although evidence for remapping has been found in many brain areas, relatively little is known about how it interacts with sensory context. This interaction is important for understanding perceptual stability more generally, as the brain may rely on extraretinal signals or visual signals to different degrees in different contexts. Here, we have studied the interaction between visual stimulation and remapping by recording from single neurons in the superior colliculus of the macaque monkey, using several different visual stimulus conditions. We find that remapping responses are highly sensitive to low-level visual signals, with the overall luminance of the visual background exerting a particularly powerful influence. Specifically, although remapping was fairly common in complete darkness, such responses were usually decreased or abolished in the presence of modest background illumination. Thus the brain might make use of a strategy that emphasizes visual landmarks over extraretinal signals whenever the former are available.     

The coordination of eye, head, and arm movements during rapid gaze orienting and arm pointing

This study aimed to investigate the coordination of multiple control actions involved in human horizontal gaze orienting or arm pointing to a common visual target. The subjects performed a visually triggered reaction time task in three conditions: (1) gaze orienting with a combined eye saccade and head rotation (EH), (2) arm pointing with gaze orienting by an eye saccade without head rotation (EA), and (3) arm pointing with gaze orienting by a combined eye saccade and head rotation (EHA). The subjects initiated eye movement first with nearly constant latencies across all tasks, followed by head movement in the EH task, by arm movement in the EA task, and by head and then arm movements in the EHA task. The differences of onset times between eye and head movements in the EH task, and between eye and arm movements in the EA task, were both preserved in the EHA task, leading to an eye-to-head-to-arm sequence. The onset latencies of eye and head in the EH task, eye and arm in the EA task, and eye, head and arm in the EHA task, were all positively correlated on a trial-by-trial basis. In the EHA task, however, the correlation coefficients of eye–head coupling and of eye–arm coupling were reduced and increased, respectively, compared to those estimated in the two-effector conditions (EH, EA). These results suggest that motor commands for different motor effectors are linked differently to achieve coordination in a task-dependent manner.     

Discharges of superior colliculus neurons during head and eye movements of the alert cat

Summary 452 single neurons from the superior colliculus were recorded in awake and non-paralysed cats. 75 neurons were obtained from cats with unrestrained horizontal head movements.228 neurons remained unaffected by saccadic eye movements. Eye movement related discharge followed the onset of saccades in 156 neurons either only in the presence of a visual pattern (92 neurons) or in darkness, too (64 neurons). The latter reaction type probably depends on eye muscle afferents.In 48 neurons eye movement related activity preceded the onset of eye movements. 12 neurons fired in synchrony with eye movements of any direction (type I). 30 neurons were excited during contralaterally directed eye versions within or into the contralateral head related hemifield. They were inhibited when the eyes moved within or into the ipsilateral head related hemifield (type II). 6 neurons with constant maintained activity during fixation were inhibited by ipsilaterally directed saccades, but remained unaffected by contralateral eye movements.Head movement related discharge followed the onset of head movements in 20 neurons only in presence of a visual pattern and also in darkness in 6 neurons. Ipsilateral head movements or postures strongly suppressed maintained activity and visual responsiveness of some neurons.15 neurons discharged in synchrony with and prior to contralateral head movements. Ipsilateral head movements inhibited these neurons. Activation or inhibition were usually related to movement and to posture, exceptionally to movement or to posture.Electrical stimulation of recording sites of these neurons through the recording microelectrode elicits contralateral head movements.