Head-unrestrained Gaze Shifts Research Articles

Dynamic control of eye-head gaze shifts by a spiking neural network model of the superior colliculus.

To reorient gaze (the eye's direction in space) towards a target is an overdetermined problem, as infinitely many combinations of eye- and head movements can specify the same gaze-displacement vector. Yet, behavioral measurements show that the primate gaze-control system selects a specific contribution of eye- and head movements to the saccade, which depends on the initial eye-in-head orientation. Single-unit recordings in the primate superior colliculus (SC) during head-unrestrained gaze shifts have further suggested that cells may encode the instantaneous trajectory of a desired straight gaze path in a feedforward way by the total cumulative number of spikes in the neural population, and that the instantaneous gaze kinematics are thus determined by the neural firing rates. The recordings also indicated that the latter is modulated by the initial eye position. We recently proposed a conceptual model that accounts for many of the observed properties of eye-head gaze shifts and on the potential role of the SC in gaze control. Here, we extend and test the model by incorporating a spiking neural network of the SC motor map, the output of which drives the eye-head motor control circuitry by linear cumulative summation of individual spike effects of each recruited SC neuron. We propose a simple neural mechanism on SC cells that explains the modulatory influence of feedback from an initial eye-in-head position signal on their spiking activity. The same signal also determines the onset delay of the head movement with respect to the eye. Moreover, the downstream eye- and head burst generators were taken to be linear, as our earlier work had indicated that much of the non-linear main-sequence kinematics of saccadic eye movements may be due to neural encoding at the collicular level, rather than at the brainstem. We investigate how the spiking activity of the SC population drives gaze to the intended target location within a dynamic local gaze-velocity feedback circuit that yields realistic eye- and head-movement kinematics and dynamic SC gaze-movement fields.

Visual-motor transformation in the multiunit activity of the frontal eye fields (FEF) during the head-unrestrained gaze shifts in rhesus monkeys

Visual-motor transformation in the multiunit activity of the frontal eye fields (FEF) during the head-unrestrained gaze shifts in rhesus monkeys

Transition from Target to Gaze Coding in Primate Frontal Eye Field during Memory Delay and Memory–Motor Transformation

The frontal eye fields (FEFs) participate in both working memory and sensorimotor transformations for saccades, but their role in integrating these functions through time remains unclear. Here, we tracked FEF spatial codes through time using a novel analytic method applied to the classic memory-delay saccade task. Three-dimensional recordings of head-unrestrained gaze shifts were made in two monkeys trained to make gaze shifts toward briefly flashed targets after a variable delay (450-1500 ms). A preliminary analysis of visual and motor response fields in 74 FEF neurons eliminated most potential models for spatial coding at the neuron population level, as in our previous study (Sajad et al., 2015). We then focused on the spatiotemporal transition from an eye-centered target code (T; preferred in the visual response) to an eye-centered intended gaze position code (G; preferred in the movement response) during the memory delay interval. We treated neural population codes as a continuous spatiotemporal variable by dividing the space spanning T and G into intermediate T–G models and dividing the task into discrete steps through time. We found that FEF delay activity, especially in visuomovement cells, progressively transitions from T through intermediate T–G codes that approach, but do not reach, G. This was followed by a final discrete transition from these intermediate T–G delay codes to a “pure” G code in movement cells without delay activity. These results demonstrate that FEF activity undergoes a series of sensory–memory–motor transformations, including a dynamically evolving spatial memory signal and an imperfect memory-to-motor transformation.

Spatial transformations between superior colliculus visual and motor response fields during head-unrestrained gaze shifts.

We previously reported that visuomotor activity in the superior colliculus (SC)--a key midbrain structure for the generation of rapid eye movements--preferentially encodes target position relative to the eye (Te) during low-latency head-unrestrained gaze shifts (DeSouza et al., 2011). Here, we trained two monkeys to perform head-unrestrained gaze shifts after a variable post-stimulus delay (400-700 ms), to test whether temporally separated SC visual and motor responses show different spatial codes. Target positions, final gaze positions and various frames of reference (eye, head, and space) were dissociated through natural (untrained) trial-to-trial variations in behaviour. 3D eye and head orientations were recorded, and 2D response field data were fitted against multiple models by use of a statistical method reported previously (Keith et al., 2009). Of 60 neurons, 17 showed a visual response, 12 showed a motor response, and 31 showed both visual and motor responses. The combined visual response field population (n = 48) showed a significant preference for Te, which was also preferred in each visual subpopulation. In contrast, the motor response field population (n = 43) showed a preference for final (relative to initial) gaze position models, and the Te model was statistically eliminated in the motor-only population. There was also a significant shift of coding from the visual to motor response within visuomotor neurons. These data confirm that SC response fields are gaze-centred, and show a target-to-gaze transformation between visual and motor responses. Thus, visuomotor transformations can occur between, and even within, neurons within a single frame of reference and brain structure.

A kinematic model for 3-D head-free gaze-shifts.

Rotations of the line of sight are mainly implemented by coordinated motion of the eyes and head. Here, we propose a model for the kinematics of three-dimensional (3-D) head-unrestrained gaze-shifts. The model was designed to account for major principles in the known behavior, such as gaze accuracy, spatiotemporal coordination of saccades with vestibulo-ocular reflex (VOR), relative eye and head contributions, the non-commutativity of rotations, and Listing's and Fick constraints for the eyes and head, respectively. The internal design of the model was inspired by known and hypothesized elements of gaze control physiology. Inputs included retinocentric location of the visual target and internal representations of initial 3-D eye and head orientation, whereas outputs were 3-D displacements of eye relative to the head and head relative to shoulder. Internal transformations decomposed the 2-D gaze command into 3-D eye and head commands with the use of three coordinated circuits: (1) a saccade generator, (2) a head rotation generator, (3) a VOR predictor. Simulations illustrate that the model can implement: (1) the correct 3-D reference frame transformations to generate accurate gaze shifts (despite variability in other parameters), (2) the experimentally verified constraints on static eye and head orientations during fixation, and (3) the experimentally observed 3-D trajectories of eye and head motion during gaze-shifts. We then use this model to simulate how 2-D eye-head coordination strategies interact with 3-D constraints to influence 3-D orientations of the eye-in-space, and the implications of this for spatial vision.

Visual-Motor Transformations Within Frontal Eye Fields During Head-Unrestrained Gaze Shifts in the Monkey.

A fundamental question in sensorimotor control concerns the transformation of spatial signals from the retina into eye and head motor commands required for accurate gaze shifts. Here, we investigated these transformations by identifying the spatial codes embedded in visually evoked and movement-related responses in the frontal eye fields (FEFs) during head-unrestrained gaze shifts. Monkeys made delayed gaze shifts to the remembered location of briefly presented visual stimuli, with delay serving to dissociate visual and movement responses. A statistical analysis of nonparametric model fits to response field data from 57 neurons (38 with visual and 49 with movement activities) eliminated most effector-specific, head-fixed, and space-fixed models, but confirmed the dominance of eye-centered codes observed in head-restrained studies. More importantly, the visual response encoded target location, whereas the movement response mainly encoded the final position of the imminent gaze shift (including gaze errors). This spatiotemporal distinction between target and gaze coding was present not only at the population level, but even at the single-cell level. We propose that an imperfect visual–motor transformation occurs during the brief memory interval between perception and action, and further transformations from the FEF's eye-centered gaze motor code to effector-specific codes in motor frames occur downstream in the subcortical areas.

Activity of long-lead burst neurons in pontine reticular formation during head-unrestrained gaze shifts

Primates explore a visual scene through a succession of saccades. Much of what is known about the neural circuitry that generates these movements has come from neurophysiological studies using subjects with their heads restrained. Horizontal saccades and the horizontal components of oblique saccades are associated with high-frequency bursts of spikes in medium-lead burst neurons (MLBs) and long-lead burst neurons (LLBNs) in the paramedian pontine reticular formation. For LLBNs, the high-frequency burst is preceded by a low-frequency prelude that begins 12-150 ms before saccade onset. In terms of the lead time between the onset of prelude activity and saccade onset, the anatomical projections, and the movement field characteristics, LLBNs are a heterogeneous group of neurons. Whether this heterogeneity is endemic of multiple functional subclasses is an open question. One possibility is that some may carry signals related to head movement. We recorded from LLBNs while monkeys performed head-unrestrained gaze shifts, during which the kinematics of the eye and head components were dissociable. Many cells had peak firing rates that never exceeded 200 spikes/s for gaze shifts of any vector. The activity of these low-frequency cells often persisted beyond the end of the gaze shift and was usually related to head-movement kinematics. A subset was tested during head-unrestrained pursuit and showed clear modulation in the absence of saccades. These "low-frequency" cells were intermingled with MLBs and traditional LLBNs and may represent a separate functional class carrying signals related to head movement.

Contribution of the frontal eye field to gaze shifts in the head-unrestrained rhesus monkey: Neuronal activity

The frontal eye field (FEF) has a strong influence on saccadic eye movements with the head restrained. With the head unrestrained, eye saccades combine with head movements to produce large gaze shifts, and microstimulation of the FEF evokes both eye and head movements. To test whether the dorsomedial FEF provides commands for the entire gaze shift or its separate eye and head components, we recorded extracellular single-unit activity in monkeys trained to make large head-unrestrained gaze shifts. We recorded 80 units active during gaze shifts, and closely examined 26 of these that discharged a burst of action potentials that preceded horizontal gaze movements. These units were movement or visuomovement related and most exhibited open movement fields with respect to amplitude. To reveal the relations of burst parameters to gaze, eye, and/or head movement metrics, we used behavioral dissociations of gaze, eye, and head movements and linear regression analyses. The burst number of spikes (NOS) was strongly correlated with movement amplitude and burst temporal parameters were strongly correlated with movement temporal metrics for eight gaze-related burst neurons and five saccade-related burst neurons. For the remaining 13 neurons, the NOS was strongly correlated with the head movement amplitude, but burst temporal parameters were most strongly correlated with eye movement temporal metrics (head–eye-related burst neurons, HEBNs). These results suggest that FEF units do not encode a command for the unified gaze shift only; instead, different units may carry signals related to the overall gaze shift or its eye and/or head components. Moreover, the HEBNs exhibit bursts whose magnitude and timing may encode a head displacement signal and a signal that influences the timing of the eye saccade, thereby serving as a mechanism for coordinating the eye and head movements of a gaze shift.

Neural mechanisms for predictive head movement strategies during sequential gaze shifts

Humans adopt very different head movement strategies for different gaze behaviors, for example, when playing sports versus watching sports on television. Such strategy switching appears to depend on both context and expectation of future gaze positions. Here, we explored the neural mechanisms for such behaviors by training three monkeys to make head-unrestrained gaze shifts toward eccentric radial targets. A randomized color cue provided predictive information about whether that target would be followed by either a return gaze shift to center or another, more eccentric gaze shift, but otherwise animals were allowed to develop their own eye-head coordination strategy. In the first two animals we then stimulated the frontal eye fields (FEF) in conjunction with the color cue, and in the third animal we recorded from neurons in the superior colliculus (SC). Our results show that 1) monkeys can optimize eye-head coordination strategies from trial to trial, based on learned associations between color cues and future gaze sequences, 2) these cue-dependent coordination strategies were preserved in gaze saccades evoked during electrical stimulation of the FEF, and 3) two types of SC responses (the saccade burst and a more prolonged response related to head movement) modulated with these cue-dependent strategies, although only one (the saccade burst) varied in a predictive fashion. These data show that from one moment to the next, the brain can use contextual sensory cues to set up internal "coordination states" that convert fixed cortical gaze commands into the brain stem signals required for predictive head motion.

Intrinsic Reference Frames of Superior Colliculus Visuomotor Receptive Fields during Head-Unrestrained Gaze Shifts

A sensorimotor neuron's receptive field and its frame of reference are easily conflated within the natural variability of spatial behavior. Here, we capitalized on such natural variations in 3-D eye and head positions during head-unrestrained gaze shifts to visual targets in two monkeys: to determine whether intermediate/deep layer superior colliculus (SC) receptive fields code visual targets or gaze kinematics, within four different frames of reference. Visuomotor receptive fields were either characterized during gaze shifts to visual targets from a central fixation position (32 U) or were partially characterized from each of three initial fixation points (31 U). Natural variations of initial 3-D gaze and head orientation (including torsion) provided spatial separation between four different coordinate frame models (space, head, eye, fixed-vector relative to fixation), whereas natural saccade errors provided spatial separation between target and gaze positions. Using a new statistical method based on predictive sum-of-squares, we found that in our population of 63 neurons (1) receptive field fits to target positions were significantly better than fits to actual gaze shift locations and (2) eye-centered models gave significantly better fits than the head or space frame. An intermediate frames analysis confirmed that individual neuron fits were distributed target-in-eye coordinates. Gaze position "gain" effects with the spatial tuning required for a 3-D reference frame transformation were significant in 23% (7/31) of neurons tested. We conclude that the SC primarily represents gaze targets relative to the eye but also carries early signatures of the 3-D sensorimotor transformation.

Influence of Static Eye and Head Position on Tone-Evoked Gaze Shifts

The auditory system represents sound-source directions initially in head-centered coordinates. To program eye-head gaze shifts to sounds, the orientation of eyes and head should be incorporated to specify the target relative to the eyes. Here we test (1) whether this transformation involves a stage in which sounds are represented in a world- or a head-centered reference frame, and (2) whether acoustic spatial updating occurs at a topographically organized motor level representing gaze shifts, or within the tonotopically organized auditory system. Human listeners generated head-unrestrained gaze shifts from a large range of initial eye and head positions toward brief broadband sound bursts, and to tones at different center frequencies, presented in the midsagittal plane. Tones were heard at a fixed illusory elevation, regardless of their actual location, that depended in an idiosyncratic way on initial head and eye position, as well as on the tone's frequency. Gaze shifts to broadband sounds were accurate, fully incorporating initial eye and head positions. The results support the hypothesis that the auditory system represents sounds in a supramodal reference frame, and that signals about eye and head orientation are incorporated at a tonotopic stage.

Interactions between gaze-evoked blinks and gaze shifts in monkeys

Rapid eyelid closure, or a blink, often accompanies head-restrained and head-unrestrained gaze shifts. This study examines the interactions between such gaze-evoked blinks and gaze shifts in monkeys. Blink probability increases with gaze amplitude and at a faster rate for head-unrestrained movements. Across animals, blink likelihood is inversely correlated with the average gaze velocity of large-amplitude control movements. Gaze-evoked blinks induce robust perturbations in eye velocity. Peak and average velocities are reduced, duration is increased, but accuracy is preserved. The temporal features of the perturbation depend on factors such as the time of blink relative to gaze onset, inherent velocity kinematics of control movements, and perhaps initial eye-in-head position. Although variable across animals, the initial effect is a reduction in eye velocity, followed by a reacceleration that yields two or more peaks in its waveform. Interestingly, head velocity is not attenuated; instead, it peaks slightly later and with a larger magnitude. Gaze latency is slightly reduced on trials with gaze-evoked blinks, although the effect was more variable during head-unrestrained movements; no reduction in head latency is observed. Preliminary data also demonstrate a similar perturbation of gaze-evoked blinks during vertical saccades. The results are compared with previously reported effects of reflexive blinks (evoked by air-puff delivered to one eye or supraorbital nerve stimulation) and discussed in terms of effects of blinks on saccadic suppression, neural correlates of the altered eye velocity signals, and implications on the hypothesis that the attenuation in eye velocity is produced by a head movement command.

Gaze shift duration, independent of amplitude, influences the number of spikes in the burst for medium-lead burst neurons in pontine reticular formation

Changes in the direction of the line of sight (gaze) allow successive sampling of the visual environment. Saccadic eye movements accomplish this goal when the head does not move. Medium-lead burst neurons (MLBs) in the paramedian pontine reticular formation (PPRF) discharge a high frequency burst of action potentials starting ~12ms before the saccade begins. A subgroup of MLBs rostral of abducens nucleus monosynaptically excites oculomotor neurons. The number of spikes in the presaccadic burst is correlated with the amplitude of the horizontal component of the saccade, and the peak discharge rate is correlated with peak eye velocity. During head-unrestrained gaze shifts, a linear relationship between the number of action potentials in MLB bursts and gaze (but not eye) amplitude has been reported. The anatomical connection of MLBs to motor neurons and the similarity between the phasic motor neuron burst and MLB discharge have raised questions about the usefulness of counting spikes in MLBs to determine their role in eye-head coordination. We investigated this issue using a behavioral technique that permits a dissociation of eye movement amplitude and duration during constant vector gaze shifts. Surprisingly, during gaze shifts of constant amplitude and direction, we observe a nearly linear, positive correlation between saccade duration and spike number associated with a negative correlation between spike number and saccade amplitude. These data constrain models of the oculomotor controller and may further define the time-dependence of hypothesized neural integration in this system.

Applying double-magnetic induction to measure head-unrestrained gaze shifts: calibration and validation in monkey

The double magnetic induction (DMI) method has successfully been used to record head-unrestrained gaze shifts in human subjects (Bremen etal., J Neurosci Methods 160:75-84, 2007a, J Neurophysiol, 98:3759-3769, 2007b). This method employs a small golden ring placed on the eye that, when positioned within oscillating magnetic fields, induces orientation-dependent voltages in a pickup coil in front of the eye. Here we develop and test a streamlined calibration routine for use with experimental animals, in particular, with monkeys. The calibration routine requires the animal solely to accurately follow visual targets presented at random locations in the visual field. Animals can readily learn this task. In addition, we use the fact that the pickup coil can be fixed rigidly and reproducibly on implants on the animal's skull. Therefore, accumulation of calibration data leads to increasing accuracy. As a first step, we simulated gaze shifts and the resulting DMI signals. Our simulations showed that the complex DMI signals can be effectively calibrated with the use of random target sequences, which elicit substantial decoupling of eye- and head orientations in a natural way. Subsequently, we tested our paradigm on three macaque monkeys. Our results show that the data for a successful calibration can be collected in a single recording session, in which the monkey makes about 1,500-2,000 goal-directed saccades. We obtained a resolution of 30 arc minutes (measurement range [-60,+60]°). This resolution compares to the fixation resolution of the monkey's oculomotor system, and to the standard scleral search-coil method.

Matching the oculomotor drive during head-restrained and head-unrestrained gaze shifts in monkey.

High-frequency burst neurons in the pons provide the eye velocity command (equivalently, the primary oculomotor drive) to the abducens nucleus for generation of the horizontal component of both head-restrained (HR) and head-unrestrained (HU) gaze shifts. We sought to characterize how gaze and its eye-in-head component differ when an "identical" oculomotor drive is used to produce HR and HU movements. To address this objective, the activities of pontine burst neurons were recorded during horizontal HR and HU gaze shifts. The burst profile recorded on each HU trial was compared with the burst waveform of every HR trial obtained for the same neuron. The oculomotor drive was assumed to be comparable for the pair yielding the lowest root-mean-squared error. For matched pairs of HR and HU trials, the peak eye-in-head velocity was substantially smaller in the HU condition, and the reduction was usually greater than the peak head velocity of the HU trial. A time-varying attenuation index, defined as the difference in HR and HU eye velocity waveforms divided by head velocity [alpha = (H(hr) - E(hu))/H] was computed. The index was variable at the onset of the gaze shift, but it settled at values several times greater than 1. The index then decreased gradually during the movement and stabilized at 1 around the end of gaze shift. These results imply that substantial attenuation in eye velocity occurs, at least partially, downstream of the burst neurons. We speculate on the potential roles of burst-tonic neurons in the neural integrator and various cell types in the vestibular nuclei in mediating the attenuation in eye velocity in the presence of head movements.

Head-free gaze shifts provide further insights into the role of the medial cerebellum in the control of primate saccadic eye movements.

This study examines how signals generated in the oculomotor cerebellum could be involved in the control of gaze shifts, which rapidly redirect the eyes from one object to another. Neurons in the caudal fastigial nucleus (cFN), the output of the oculomotor cerebellum, discharged when monkeys made horizontal head-unrestrained gaze shifts, composed of an eye saccade and a head movement. Eighty-seven percent of our neurons discharged a burst of spikes for both ipsiversive and contraversive gaze shifts. In both directions, burst end was much better timed with gaze end than was burst start with gaze start, was well correlated with eye end, and was poorly correlated with head end or the time of peak head velocity. Moreover, bursts accompanied all head-unrestrained gaze shifts whether the head moved or not. Therefore we conclude that the cFN is not part of the pathway that controls head movement. For contraversive gaze shifts, the early part of the burst was correlated with gaze acceleration. Thereafter, the burst of the neuronal population continued throughout the prolonged deceleration of large gaze shifts. For a majority of neurons, gaze duration was correlated with burst duration; for some, gaze amplitude was less well correlated with the number of spikes. Therefore we suggest that the population burst provides an acceleration boost for high acceleration (smaller) contraversive gaze shifts and helps maintain the drive required to extend the deceleration of large contraversive gaze shifts. In contrast, the ipsiversive population burst, which is less well correlated with gaze metrics but whose peak rate occurs before gaze end, seems responsible primarily for terminating the gaze shift.

3-Dimensional eye-head coordination in gaze shifts evoked during stimulation of the lateral intraparietal cortex

Coordinated eye-head gaze shifts have been evoked during electrical stimulation of the frontal cortex (supplementary eye field (SEF) and frontal eye field (FEF)) and superior colliculus (SC), but less is known about the role of lateral intraparietal cortex (LIP) in head-unrestrained gaze shifts. To explore this, two monkeys (M1 and M2) were implanted with recording chambers and 3-D eye+ head search coils. Tungsten electrodes delivered trains of electrical pulses (usually 200 ms duration) to and around area LIP during head-unrestrained gaze fixations. A current of 200 μA consistently evoked small, short-latency contralateral gaze shifts from 152 sites in M1 and 243 sites in M2 (Constantin et al., 2007). Gaze kinematics were independent of stimulus amplitude and duration, except that subsequent saccades were suppressed. The average amplitude of the evoked gaze shifts was 8.46° for M1 and 8.25° for M2, with average head components of only 0.36 and 0.62° respectively. The head's amplitude contribution to these movements was significantly smaller than in normal gaze shifts, and did not increase with behavioral adaptation. Stimulation-evoked gaze, eye and head movements qualitatively obeyed normal 3-D constraints (Donders' law and Listing's law), but with less precision. As in normal behavior, when the head was restrained LIP stimulation evoked eye-only saccades in Listing's plane, whereas when the head was not restrained, stimulation evoked saccades with position-dependent torsional components (driving the eye out of Listing's plane). In behavioral gaze-shifts, the vestibuloocular reflex (VOR) then drives torsion back into Listing's plane, but in the absence of subsequent head movement the stimulation-induced torsion was “left hanging”. This suggests that the position-dependent torsional saccade components are preprogrammed, and that the oculomotor system was expecting a head movement command to follow the saccade. These data show that, unlike SEF, FEF, and SC stimulation in nearly identical conditions, LIP stimulation fails to produce normally-coordinated eye-head gaze shifts.

A method for mapping response fields and determining intrinsic reference frames of single-unit activity: Applied to 3D head-unrestrained gaze shifts

Natural movements towards a target show metric variations between trials. When movements combine contributions from multiple body-parts, such as head-unrestrained gaze shifts involving both eye and head rotation, the individual body-part movements may vary even more than the overall movement. The goal of this investigation was to develop a general method for both mapping sensory or motor response fields of neurons and determining their intrinsic reference frames, where these movement variations are actually utilized rather than avoided. We used head-unrestrained gaze shifts, three-dimensional (3D) geometry, and naturalistic distributions of eye and head orientation to explore the theoretical relationship between the intrinsic reference frame of a sensorimotor neuron's response field and the coherence of the activity when this response field is fitted non-parametrically using different kernel bandwidths in different reference frames. We measure how well the regression surface predicts unfitted data using the PREdictive Sum-of-Squares (PRESS) statistic. The reference frame with the smallest PRESS statistic was categorized as the intrinsic reference frame if the PRESS statistic was significantly larger in other reference frames. We show that the method works best when targets are at regularly spaced positions within the response field's active region, and that the method identifies the best kernel bandwidth for response field estimation. We describe how gain-field effects may be dealt with, and how to test neurons within a population that fall on a continuum between specific reference frames. This method may be applied to any spatially coherent single-unit activity related to sensation and/or movement during naturally varying behaviors.

Head-unrestrained gaze adaptation in the rhesus macaque.

The ability to adjust the amplitude of gaze shifts in response to persistent visual errors ("gaze adaptation") has been investigated primarily by introducing visual errors at the end of saccades produced by head-restrained primates. Very little is known about the behavior and neural mechanisms underlying gaze adaptation when the head is free to move. We tested alternative hypotheses about the signals that are altered during gaze adaptation by increasing (25 degrees --> 50 degrees ; "forward adaptation") or decreasing (50 degrees --> 25 degrees ; "backward adaptation") the size of large, head-unrestrained gaze shifts. In our three rhesus monkey subjects, changes to primary gaze shift amplitude occurred regardless of the particular combinations of eye and head movements that made up the amplitude-altered gaze shifts. The relative changes to eye and head movements that occurred during adaptation could be predicted based on the magnitude of gaze adaptation and the positions of the eyes in the orbits at gaze onset. These results are consistent with the hypothesis that gaze adaptation occurs at the level of a gaze shift command and inconsistent with hypotheses based on the assumption that gaze adaptation results from alterations to eye- and/or head-specific signals.

Amplitude changes in response to target displacements during human eye–head movements

Sensorimotor adaptation, the ability to adjust motor output in response to persistent changes in sensory input, is a key function of the central nervous system. Although a great deal is known about vestibulo-ocular reflex and saccadic adaptation, relatively little is known about the behavior and neural mechanisms underlying gaze adaptation when the head is free to move. In an attempt to understand the mechanisms of gaze adaptation, and constrain hypotheses concerning the locus at which changes in gaze control may be implemented, we altered the size of large, head-unrestrained gaze shifts made to visual targets by surreptitiously moving the visual target forward (30° → 60°) or backwards (60° → 30°) during gaze shifts. In our 10 human subjects, after a few hundred back-step trials, gaze amplitudes were reduced by between 6° and 27°. Similarly, after a few hundred forward adaptation trials, our subjects increased gaze amplitude by between 0° and 26°. Changes in the amplitude of primary gaze shifts occurred regardless of the particular combinations of eye and head movements that made up the amplitude-altered gaze shifts. When gaze shifts were initiated with the eyes in systematically different positions relative to the head, the resulting changes in gaze, eye and head movement amplitudes were consistent with the hypothesis that gaze adaptation occurs at the level of a gaze shift command and not by altering separately the signals that produce eye and head movements.