Biomedical subjects

J Douglas Crawford

Publications and source records attributed to J Douglas Crawford.

At least 19 recordsLinked to original sources

PubMed2007

Three-dimensional eye-head coordination after injection of muscimol into the interstitial nucleus of Cajal (INC).

The interstitial nucleus of Cajal (INC) is thought to be the "neural integrator" for torsional/vertical eye position and head posture. Here, we investigated the coordination of eye and head movements after reversible INC inactivation. Three-dimensional (3-D) eye-head movements were recorded in three head-unrestrained monkeys using search coils. INC sites were identified by unit recording/electrical stimulation and then reversibly inactivated by 0.3 mul of 0.05% muscimol injection into 26 INC sites. After muscimol injection, the eye and head 1) began to drift (an inability to maintain stable fixation) torsionally: clockwise (CW)/counterclockwise (CCW) after left/right INC inactivation respectively. 2) The eye and head tilted torsionally CW/CCW after left/right INC inactivation, respectively. Horizontal gaze/head drifts were inconsistently present and did not result in considerable position offsets. Vertical eye drift was dependent on both vertical eye position and the magnitude of the previous vertical saccade, as in head-fixed condition. This correlation was smaller for gaze and head drift, suggesting that the gaze and head deficits could not be explained by a first-order integrator model. Ocular counterroll (OC) was completely disrupted. The gain of torsional vestibuloocular reflex (VOR) during spontaneous eye and head movements was reduced by 22% in both CW/CCW directions after either left or right INC inactivation. Our results suggest a complex interdependence of eye and head deficits after INC inactivation during fixation, gaze shifts, and VOR. Some of our results resemble the symptoms of spasmodic torticollis (ST).

Animals↗

PubMed2007

Human parietal "reach region" primarily encodes intrinsic visual direction, not extrinsic movement direction, in a visual motor dissociation task.

Posterior parietal cortex (PPC) participates in the planning of visuospatial behaviors, including reach movements, in gaze-centered coordinates. It is not known if these representations encode the visual goal in retinal coordinates, or the movement direction relative to gaze. Here, by dissociating the intrinsic retinal stimulus from the extrinsic direction of movement, we show that PPC employs a visual code. Using delayed pointing and event-related functional magnetic resonance imaging, we identified a cluster of PPC regions whose activity was topographically (contralaterally) related to the direction of the planned movement. We then switched the normal visual-motor spatial relationship by adapting subjects to optical left/right reversing prisms. With prisms, movement-related PPC topography reversed, remaining tied to the retinal image. Thus, remarkably, the PPC region in each hemisphere now responded more for planned ipsilateral pointing movements. Other non-PPC regions showed the opposite world- or motor-fixed pattern. These findings suggest that PPC primarily encodes not motor commands but movement goals in visual coordinates.

Adult↗

PubMed2007

Functional organization within a neural network trained to update target representations across 3-D saccades.

The goal of this study was to understand how neural networks solve the 3-D aspects of updating in the double-saccade task, where subjects make sequential saccades to the remembered locations of two targets. We trained a 3-layer, feed-forward neural network, using back-propagation, to calculate the 3-D motor error the second saccade. Network inputs were a 2-D topographic map of the direction of the second target in retinal coordinates, and 3-D vector representations of initial eye orientation and motor error of the first saccade in head-fixed coordinates. The network learned to account for all 3-D aspects of updating. Hidden-layer units (HLUs) showed retinal-coordinate visual receptive fields that were remapped across the first saccade. Two classes of HLUs emerged from the training, one class primarily implementing the linear aspects of updating using vector subtraction, the second class implementing the eye-orientation-dependent, non-linear aspects of updating. These mechanisms interacted at the unit level through gain-field-like input summations, and through the parallel "tweaking" of optimally-tuned HLU contributions to the output that shifted the overall population output vector to the correct second-saccade motor error. These observations may provide clues for the biological implementation of updating.

Animals↗

PubMed2006

Optimal inference explains dimension-specific contractions of spatial perception.

It is known that people misperceive scenes they see during rapid eye movements called saccades. It has been suggested that some of these misperceptions could be an artifact of neurophysiological processes related to the internal remapping of spatial coordinates during saccades. Alternatively, we have recently suggested, based on a computational model, that transsaccadic misperceptions result from optimal inference. As one of the properties of the model, sudden object displacements that occur in sync with a saccade should be perceived as contracted in a non-linear fashion. To explore this model property, here we use computer simulations and psychophysical methods first to test how robust the model is to close-to-optimal approximations and second to test two model predictions: (a) contracted transsaccadic perception should be dimension-specific with more contraction for jumps parallel to the saccade than orthogonal to it, and (b) contraction should rise as a function of visuomotor noise. Our results are consistent with these predictions. They support the idea that human transsaccadic integration is governed by close-to-optimal inference.

Adult↗

PubMed2006

Interstitial nucleus of cajal encodes three-dimensional head orientations in Fick-like coordinates.

Two central, related questions in motor control are 1) how the brain represents movement directions of various effectors like the eyes and head and 2) how it constrains their redundant degrees of freedom. The interstitial nucleus of Cajal (INC) integrates velocity commands from the gaze control system into position signals for three-dimensional eye and head posture. It has been shown that the right INC encodes clockwise (CW)-up and CW-down eye and head components, whereas the left INC encodes counterclockwise (CCW)-up and CCW-down components, similar to the sensitivity directions of the vertical semicircular canals. For the eyes, these canal-like coordinates align with Listing's plane (a behavioral strategy limiting torsion about the gaze axis). By analogy, we predicted that the INC also encodes head orientation in canal-like coordinates, but instead, aligned with the coordinate axes for the Fick strategy (which constrains head torsion). Unilateral stimulation (50 microA, 300 Hz, 200 ms) evoked CW head rotations from the right INC and CCW rotations from the left INC, with variable vertical components. The observed axes of head rotation were consistent with a canal-like coordinate system. Moreover, as predicted, these axes remained fixed in the head, rotating with initial head orientation like the horizontal and torsional axes of a Fick coordinate system. This suggests that the head is ordinarily constrained to zero torsion in Fick coordinates by equally activating CW/CCW populations of neurons in the right/left INC. These data support a simple mechanism for controlling head orientation through the alignment of brain stem neural coordinates with natural behavioral constraints.

Animals↗

PubMed2005

Cross-coupled adaptation of eye and head position commands in the primate gaze control system.

Primates orient visual gaze using different eye-head coordination strategies. To test how these strategies are formed, we trained a macaque monkey to perform 'head-only' gaze shifts looking through a 10 degrees head-fixed aperture. When we suddenly relocated this aperture 15 degrees downward, the animal could orient initial eye position toward the new aperture, but during large gaze saccades the eye was mistakenly driven back to the original (now occluded) aperture. More importantly, this was accompanied by an opposite head movement, such that gaze (although blocked) pointed correctly. We conclude that the gaze control system acquires new strategies through separate but interdependent eye-head controllers, designed primarily to ensure that gaze is placed in the correct direction.

Acclimatization↗

PubMed2005

Impairment of gaze-centered updating of reach targets in bilateral parietal-occipital damaged patients.

Recent studies have suggested that internal updating of visuospatial targets in humans occurs in gaze-centered coordinates and takes place in the parietal and extrastriate cortices. We explored how information for reaching is updated in two patients with bilateral lesions in these areas. Subjects performed two visuomotor tasks: (i) a fixation reaching task, which began with the appearance of one of five fixation positions (varying eye positions) followed by a central reaching target. Subjects reached to the target while fixating on the presented fixation position (relative to gaze the target was always presented in the periphery); and (ii) a saccade reaching task, in which subjects foveated on the central reaching target, then made a saccade to the presented fixation position before reaching to the central target. In both tasks, subjects reached to targets after a 500 or 5000 ms delay. Gaze-centered updating predicts similarities in reaching errors between fixation and saccade trials. Control subjects showed evidence for gaze-centered updating during both 500 and 5000 ms delay conditions. In contrast, patient AT, who had extensive occipital-parietal damage, only showed signs of gaze-centered representation after 5 s. Patient IG, with a more focal lesion in the parietal cortices, showed partial updating in gaze-centered coordinates when reaching with the small memory delay but recovered a complete gaze-centered representation after the longer delay. This suggests that patients with bilateral occipital-parietal lesions may rely on non-gaze-centered frames to store immediate target locations in reaching space but, given enough time, this information may be rerouted to access other gaze-centered motor cortical mechanisms.

Adult↗

PubMed2004

Frames of reference for eye-head gaze commands in primate supplementary eye fields.

The supplementary eye field (SEF) is a region within medial frontal cortex that integrates complex visuospatial information and controls eye-head gaze shifts. Here, we test if the SEF encodes desired gaze directions in a simple retinal (eye-centered) frame, such as the superior colliculus, or in some other, more complex frame. We electrically stimulated 55 SEF sites in two head-unrestrained monkeys to evoke 3D eye-head gaze shifts and then mathematically rotated these trajectories into various reference frames. Each stimulation site specified a specific spatial goal when plotted in its intrinsic frame. These intrinsic frames varied site by site, in a continuum from eye-, to head-, to space/body-centered coding schemes. This variety of coding schemes provides the SEF with a unique potential for implementing arbitrary reference frame transformations.

Animals↗

PubMed2004

Distributed population mechanism for the 3-D oculomotor reference frame transformation.

Human saccades require a nonlinear, eye orientation-dependent reference frame transformation to transform visual codes to the motor commands for eye muscles. Primate neurophysiology suggests that this transformation is performed between the superior colliculus and brain stem burst neurons, but provides little clues as to how this is done. To understand how the brain might accomplish this, we trained a 3-layer neural net to generate accurate commands for kinematically correct 3-D saccades. The inputs to the network were a 2-D, eye-centered, topographic map of Gaussian visual receptive fields and an efference copy of eye position in 6-dimensional, push-pull "neural integrator" coordinates. The output was an eye orientation displacement command in similar coordinates appropriate to drive brain stem burst neurons. The network learned to generate accurate, kinematically correct saccades, including the eye orientation-dependent tilts in saccade motor error commands required to match saccade trajectories to their visual input. Our analysis showed that the hidden units developed complex, eye-centered visual receptive fields, widely distributed fixed-vector motor commands, and "gain field"-like eye position sensitivities. The latter evoked subtle adjustments in the relative motor contributions of each hidden unit, thereby rotating the population motor vector into the correct correspondence with the visual target input for each eye orientation: a distributed population mechanism for the visuomotor reference frame transformation. These findings were robust; there was little variation across networks with between 9 and 49 hidden units. Because essentially the same observations have been reported in the visuomotor transformations of the real oculomotor system, as well as other visuomotor systems (although interpreted elsewhere in terms of other models) we suggest that the mechanism for visuomotor reference frame transformations identified here is the same solution used in the real brain.

Feedback↗

PubMed2004

Task-specific sensorimotor adaptation to reversing prisms.

We tested between three levels of visuospatial adaptation (global map, parallel feature modules, and parallel sensorimotor transformations) by training subjects to reach and grasp virtual objects viewed through a left-right reversing prism, with either visual location or orientation feedback. Even though spatial information about the global left-right reversal was present in every training session, subjects trained with location feedback reached to the correct location but with the wrong (reversed) grasp orientation. Subjects trained with orientation feedback showed the opposite pattern. These errors were task-specific and not feature-specific; subjects trained to correctly grasp visually reversed-oriented bars failed to show knowledge of the reversal when asked to point to the end locations of these bars. These results show that adaptation to visuospatial distortion--even global reversals--is implemented through learning rules that operate on parallel sensorimotor transformations (e.g., reach vs. grasp).

Adaptation, Physiological↗

PubMed2004

Integration of target and effector information in human posterior parietal cortex for the planning of action.

Recently, using event-related functional MRI (fMRI), we located a bilateral region in the human posterior parietal cortex (retIPS) that topographically represents and updates targets for saccades and pointing movements in eye-centered coordinates. To generate movements, this spatial information must be integrated with the selected effector. We now tested whether the activation in retIPS is dependent on the hand selected. Using 4-T fMRI, we compared the activation produced by movements, using either eyes or the left or right hand, to targets presented either leftward or rightward of central fixation. The majority of the regions activated during saccades were also activated during pointing movements, including occipital, posterior parietal, and premotor cortex. The topographic retIPS region was activated more strongly for saccades than for pointing. The activation associated with pointing was significantly greater when pointing with the unseen hand to targets ipsilateral to the hand. For example, although there was activation in the left retIPS when pointing to targets on the right with the left hand, the activation was significantly greater when using the right hand. The mirror symmetric effect was observed in the right retIPS. Similar hand preferences were observed in a nearby anterior occipital region. This effector specificity is consistent with previous clinical and behavioral studies showing that each hand is more effective in directing movements to targets in ipsilateral visual space. We conclude that not only do these regions code target location, but they also appear to integrate target selection with effector selection.

Adult↗

PubMed2004

Role of superior colliculus in adaptive eye-head coordination during gaze shifts.

The goal of this study was to determine which aspects of adaptive eye-head coordination are implemented upstream or downstream from the motor output layers of the superior colliculus (SC). Two monkeys were trained to perform head-free gaze shifts while looking through a 10 degrees aperture in opaque, head-fixed goggles. This training produced context-dependent alterations in eye-head coordination, including a coordinated pattern of saccade-vestibuloocular reflex (VOR) eye movements that caused eye position to converge toward the aperture, and an increased contribution of head movement to the gaze shift. One would expect the adaptations that were implemented downstream from the SC to be preserved in gaze shifts evoked by SC stimulation. To test this, we analyzed gaze shifts evoked from 19 SC sites in monkey 1 and 38 sites in monkey 2, both with and without goggles. We found no evidence that the goggle paradigm altered the basic gaze position-dependent spatial coding of the evoked movements (i.e., gaze was still coded in an eye-centered frame). However, several aspects of the context-dependent coordination strategy were preserved during stimulation, including the adaptive convergence of final eye position toward the goggles aperture, and the position-dependent patterns of eye and head movement required to achieve this. For example, when initial eye position was offset from the learned aperture location at the time of stimulation, a coordinated saccade-VOR eye movement drove it back to the original aperture, and the head compensated to preserve gaze kinematics. Some adapted amplitude-velocity relationships in eye, gaze, and head movement also may have been preserved. In contrast, context-dependent changes in overall eye and head contribution to gaze amplitude were not preserved during SC stimulation. We conclude that 1) the motor output command from the SC to the brain stem can be adapted to produce different position-dependent coordination strategies for different behavioral contexts, particularly for eye-in-head position, but 2) these brain stem coordination mechanisms implement only the default (normal) level of head amplitude contribution to the gaze shift. We propose that a parallel cortical drive, absent during SC stimulation, is required to adjust the overall head contribution for different behavioral contexts.

Animals↗

PubMed2003

Motion parallax is computed in the updating of human spatial memory.

As we move through space, stationary objects around us show motion parallax: their directions relative to us change at different rates, depending on their distance. Does the brain incorporate parallax when it updates its stored representations of space? We had subjects fixate a distant target and then we flashed lights, at different distances, onto the retinal periphery. Subjects translated sideways while keeping their gaze on the distant target, and then they looked to the remembered location of the flash. Their responses corrected almost perfectly for parallax: they turned their eyes farther for nearer targets, in the predicted nonlinear patterns. Computer simulations suggest a neural mechanism in which feedback about self-motion updates remembered locations of objects within an internal map of three-dimensional visual space.

Adult↗

PubMed2003

Gaze-centered updating of visual space in human parietal cortex.

Single-unit recordings have identified a region in the posterior parietal cortex (PPC) of the monkey that represents and updates visual space in a gaze-centered frame. Here, using event-related functional magnetic resonance imaging, we identified an analogous bilateral region in the human PPC that shows contralateral topography for memory-guided eye movements and arm movements. Furthermore, when eye movements reversed the remembered horizontal target location relative to the gaze fixation point, this PPC region exchanged activity across the two cortical lobules. This shows that the human PPC dynamically updates the spatial goals for action in a gaze-centered frame.

Adult↗

PubMed2003

Optimal transsaccadic integration explains distorted spatial perception.

We scan our surroundings with quick eye movements called saccades, and from the resulting sequence of images we build a unified percept by a process known as transsaccadic integration. This integration is often said to be flawed, because around the time of saccades, our perception is distorted and we show saccadic suppression of displacement (SSD): we fail to notice if objects change location during the eye movement. Here we show that transsaccadic integration works by optimal inference. We simulated a visuomotor system with realistic saccades, retinal acuity, motion detectors and eye-position sense, and programmed it to make optimal use of these imperfect data when interpreting scenes. This optimized model showed human-like SSD and distortions of spatial perception. It made new predictions, including tight correlations between perception and motor action (for example, more SSD in people with less-precise eye control) and a graded contraction of perceived jumps; we verified these predictions experimentally. Our results suggest that the brain constructs its evolving picture of the world by optimally integrating each new piece of sensory or motor information.

Humans↗

PubMed2003

Electrical stimulation of the supplementary eye fields in the head-free macaque evokes kinematically normal gaze shifts.

The supplementary eye fields (SEFs), located on the dorsomedial surface of the frontal cortex, are involved in high-level aspects of saccade generation. Some reports suggest that the same area could also be involved in the generation of motor commands for the head. If so, it is important to establish whether this structure encodes eye and head commands separately or gaze commands that give rise to coordinated eye-head movements. Here we systematically stimulated (50 microA, 300 Hz, 200 ms) the SEF of two head-free (head unrestrained) macaques while recording three-dimensional eye and head rotations. A total of 55 sites were found to consistently elicit saccade-like gaze movements, always in the contralateral direction with variable vertical components, and ranging in average amplitude from 5 to 60 degrees. These movements were always a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between these movements and natural gaze shifts. The kinematics of the elicited movements (i.e., their temporal structure, their velocity-amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were indistinguishable from those of natural gaze shifts. Additionally, they obeyed the same three-dimensional constraints as natural gaze shifts (i.e., eye-in-head movements obeyed Listing's law, whereas head- and eye-in-space movements obeyed Donders' law). In summary, gaze movements evoked by stimulating the SEF were indistinguishable from natural coordinated eye-head gaze shifts. Based on this we conclude that the SEF explicitly encodes gaze and that the kinematics aspects of eye-head coordination are implicitly specified by mechanisms downstream from the SEF.

Animals↗

PubMed2003

Coordinating one hand with two eyes: optimizing for field of view in a pointing task.

We previously found that subjects switched 'ocular dominance' as a function of horizontal gaze direction in a reaching task [Vision Res. 41 (14) (2001) 1743]. Here we extend these findings to show that when subjects pointed to targets across the horizontal binocular field, they aligned the fingertip with a vertical plane located between the eyes and the target. This eye-target plane gradually shifted from aligning with the left eye (leftward targets) to between the two eyes (intermediate targets) to the right eye (rightward targets). We suggest that this occurs to optimize eye-hand alignment towards the eye with the best overall field of view.

Adult↗

PubMed2003

Neural control of 3-D gaze shifts in the primate.

The neural mechanisms that specify target locations for gaze shifts and then convert these into desired patterns of coordinated eye and head movements are complex. Much of this complexity is only revealed when one takes a realistic three-dimensional (3-D) view of these processes, where fundamental computational problems such as kinematic redundancy, reference-frame transformations, and non-commutativity emerge. Here we review the underlying mechanisms and solutions for these problems, starting with a consideration of the kinematics of 3-D gaze shifts in human and non-human primates. We then consider the neural mechanisms, including cortical representation of gaze targets, the nature of the gaze motor command used by the superior colliculus, and how these gaze commands are decomposed into brainstem motor commands for the eyes and head. A general conclusion is that fairly simple coding mechanisms may be used to represent gaze at the cortical and collicular level, but this then necessitates complexity for the spatial updating of these representations and in the brainstem sensorimotor transformations that convert these signals into eye and head movements.

Animals↗