Vertical gaze angle as a distance cue for programming reaching: insights from visual form agnosia II (of III)

It has been shown that a patient with visual form agnosia (DF) relies predominantly on vergence information when gauging target distance in an open-loop pointing task. This finding suggested that the programming of prehension might be severely disrupted if DF viewed target objects through ophthalmic prisms. An initial experiment showed that this prediction was not upheld; DF was able to programme reasonably accurate movements to objects located on a tabletop despite large changes in vergence angle. A second experiment, however, showed that placing the target objects at eye height whilst manipulating vergence angle caused gross disruption to prehension, with DF mis-programming the reach component in a predictable manner. Notably, the evidence for DF's reliance on vergence distance information was obtained in a task where the targets were viewed at eye height. These experiments indicate that DF uses vertical gaze angle to gauge target distance in normal prehension and suggest that this extra-retinal cue may be a useful source of distance information for the human nervous system, especially where pictorial cues are impoverished. Electronic Publication     

Contribution of eye positioning to control of the upside-down standing posture

Summary The present study attempts to clarify the relationship between eye and body positioning during an upside-down standing posture on the hands. In this posture the head was observed to be stable and the eyes were anchored to an earth-fixed target. We measured the variations of body sway when subjects displaced their gaze upward or downward from their anchoring position. They did this voluntarily under instruction, and involuntarily by means of base-down or base-up wedge prisms. Results show that the anchoring point chosen by the subjects corresponds to a perceived limit of their body sway. They suggest that vision is also used to convey the desired optimal zone for the center of gravity in cases where fine balance is required.     

Cerebellar inactivation impairs memory of learned prism gaze-reach calibrations

Three monkeys performed a visually guided reach-touch task with and without laterally displacing prisms. The prisms offset the normally aligned gaze/reach and subsequent touch. Naive monkeys showed adaptation, such that on repeated prism trials the gaze-reach angle widened and touches hit nearer the target. On the first subsequent no-prism trial the monkeys exhibited an aftereffect, such that the widened gaze-reach angle persisted and touches missed the target in the direction opposite that of initial prism-induced error. After 20-30 days of training, monkeys showed long-term learning and storage of the prism gaze-reach calibration: they switched between prism and no-prism and touched the target on the first trials without adaptation or aftereffect. Injections of lidocaine into posterolateral cerebellar cortex or muscimol or lidocaine into dentate nucleus temporarily inactivated these structures. Immediately after injections into cortex or dentate, reaches were displaced in the direction of prism-displaced gaze, but no-prism reaches were relatively unimpaired. There was little or no adaptation on the day of injection. On days after injection, there was no adaptation and both prism and no-prism reaches were horizontally, and often vertically, displaced. A single permanent lesion (kainic acid) in the lateral dentate nucleus of one monkey immediately impaired only the learned prism gaze-reach calibration and in subsequent days disrupted both learning and performance. This effect persisted for the 18 days of observation, with little or no adaptation.     

Effects of distance and gaze position on postural stability in young and old subjects

Visual stabilization of posture is known to improve when the distance to target fixation decreases; this is attributed to increased angular size of retinal slip induced by body sway. At near distance, however, the eyes converge and efferent or afferent oculomotor signals could also be involved in posture stabilization. The goal of this study is to test whether the distance effect exists for both young and elderly and to test the role of vergence itself and of gaze position. Eighteen young (25.3 years) and 17 elderly (61.6 years) subjects were asked to fixate a target in quiet stance presented either at close (40 cm) or at far distance (200 cm); the vergence angle was 9° and 2°, respectively. For each distance, three gaze positions were studied straight-ahead (0°), 15° up or down. We found a decrease in the surface of center of pressure (CoP), of standard deviation of antero-posterior and lateral body sway and of speed variance at near distance that occurs for both young and elderly. At far distance, the surface of CoP is smaller for 15° up or down gaze in comparison with straight-ahead position, but at near distance there is no such gaze position effect. In an additional experiment, subjects fixated a target at far distance (200 cm) but prisms were used to cause the eyes to converge by an amount similar to that required for 40 cm viewing distance. The use of prisms decreased surface of CoP to values similar to those for natural near viewing distance. The effect of gaze position and of convergence (experiment with prisms) leads us to suggest that in addition to retinal slip, the ocular motor signals and perhaps related neck muscle activity are involved in postural stabilization. Finally, the elderly presented higher speed variance of CoP than the young subjects even though the surface itself was similar to adult values. We suggest that increment of speed variance is the first sign of senescence in postural control.     

Identifying visual-vestibular contributions during target-directed locomotion

The purpose of this experiment was to examine the potential interaction between visual and vestibular inputs as participants walked towards 1 of 3 targets located on a barrier 5m away. Visual and vestibular inputs were perturbed with displacing prisms and galvanic vestibular stimulation (GVS), respectively. For each target there were three vision conditions (no prisms, prisms left, and prisms right), and three GVS conditions (no GVS, anode left, and anode right). Participants were instructed to start with eyes closed, and to open the eyes at heel contact of the first step. GVS and target illumination were triggered by the first heel contact. This ensured that the upcoming visual condition and target were unknown and that both sensory perturbations occurred simultaneously. Lateral displacement was determined every 40 cm. Irrespective of target or direction, GVS or prism perturbation alone resulted in similar lateral deviations. When combined, the GVS and prism perturbations that had similar singular effects led to significantly larger deviations in the direction of the perturbations. The deviations were approximately equal to the sum of the single deviations indicating that the combined effects were additive. Conflicting GVS and prism perturbations led to significantly smaller deviations that were close to zero, indicating that opposite perturbations cancelled each other. These results show that when both visual and vestibular information remain important during task performance, the nervous system integrates the inputs equally.     

Prism adaptation of underhand throwing: Rotational inertia and the primary and latent aftereffects

The effect of prism adaptation on movement is typically reduced when movement at test (with prisms removed) is different from movement at training. Previous research [J. Fernández-Ruiz, C. Hall-Haro, R. Díaz, J. Mischner, P. Vergara, J. C. Lopez-Garcia, Learning motor synergies makes use of information on muscular load, Learning & Memory 7 (2000) 193–198] suggests, however, that some adaptation is latent and only revealed through further testing in which the movement at training is fully reinstated. Movement in their training trials was throwing overhand to a vertical target with a mass attached to the arm. The critical test trials involved the same act initially without the attached mass and then with the attached mass. In replication, we studied throwing underhand to a horizontal target with left shifting prisms and a dissociation of the throwing arm's mass and moment of inertia. The two main results were that the observed latent aftereffect (a) depended on the similarity of training and test moments of inertia, and (b) combined with the primary aftereffect to yield a condition-independent sum. Discussion focused on a parallel between prism adaptation and principles governing recall highlighted in investigations of implicit memory: whether given training (study) conditions lead to good or poor persistence of adaptation (memory performance) at test depends on the conditions at test relative to the conditions at training (study).     

Vergence-dependent adaptation of the vestibulo-ocular reflex

The gain of the vestibulo-ocular reflex (VOR) normally depends on the distance between the subject and the visual target, but it remains uncertain whether vergence angle can be linked to changes in VOR gain through a process of context-dependent adaptation. In this study, we examined this question with an adaptation paradigm that modified the normal relationship between vergence angle and retinal image motion. Subjects were rotated sinusoidally while they viewed an optokinetic (OKN) stimulus through either diverging or converging prisms. In three subjects the diverging prisms were worn while the OKN stimulus moved out of phase with the head, and the converging prisms were worn when the OKN stimulus moved in-phase with the head. The relationship between the vergence angle and OKN stimulus was reversed in the fourth subject. After 2 h of training, the VOR gain at the two vergence angles changed significantly in all of the subjects, evidenced by the two different VOR gains that could be immediately accessed by switching between the diverged and converged conditions. The results demonstrate that subjects can learn to use vergence angle as the contextual cue that retrieves adaptive changes in the angular VOR.     

The effects of inverting prisms on the horizontal–vertical illusion: a systematic effect of downward gaze

The purpose of this work is to compare the relative contributions from the extraocular and sensory systems on the magnitude of the horizontal–vertical illusion (HVI). The visual HVI refers to the general tendency to overestimate vertical extensions of small-scale lines on a picture plane relative to the horizontal by 4–16% depending on the method of measurement. The HVI line stimuli consisted of luminous vertical and horizontal lines forming “L-profiles” located in the frontoparallel plane at a 45 cm viewing distance, collinearly with a binocular gaze. The home position of gaze was aligned to the center of the screen with the ear–eye angle concordant with the environmental horizontal. Illusion strength was quantified when subjects fixated the HVI line stimuli in four quadrants of the visual field. The HVI was also viewed through prism lenses that inverted the retinal images by 180°, thereby dissociating the sensory “up-down” direction from the oculomotor up-down frame of reference. The results revealed a systematically lower magnitude of the HVI in the bottom visual field regardless of whether subjects fixated the HVI with the distorting prisms or without. Taken together, these results suggest that the HVI is sensitive to small-angle gaze shifts. In agreement with several recent findings, these results are interpreted as implying that the brain imposes an enhanced analytic structure on the ascending sensory information during downward gaze. Hans O. Richter and Jaanus Raudsepp contributed equally to this work.     

Primacy of the negative aftereffect over positive adaptation in prism adaptation with newly hatched chicks

Negative afteraffects (NAE) to prism displacement should not exist without prior positive adaptation (PA) during initial prism exposure. In 4 experiments, chicks wearing hoods containing 8.5° wedge prisms from the day of hatching showed: (a) significant NAE (pecking overcompensation in the direction opposite to their initial displacement error when matched O-degree clear plates were substituted for the prisms), but not significant PA (reduction in the lateral error of pecking while wearing the prisms) at the sixth day; (b) NAE exceeding the theoretically predicted PA on the sixteenth day; (c) significant short and long duration NAE, and significant short and long duration reversal overcompensation effects (ROE) (left-right pecking asymmetry following reversal of the prism base directions) on the seventh and eighth days, without prior PA on the seventh day; (d) neither significant NAE nor significant PA on the fourth day. Both significant NAE and significant PA had been reported previously on the eighth day. Geometrical analyses suggest that variables latent in unrestricted application of adult sensory rearrangement techniques to rapidly growing chicks of low sensory-motor plasticity produce an ontogenetic-development-related reciprocity paradox.     

The orientation of prisms in the dental enamel of human permanent teeth

Enamel of human permanent teeth was sectioned and ground with 2 planes perpendicular to each other extending centrifugally from the dentino-enamel-junction to the crown surface. Prisms were made visible by acid etching before evaluation under the SEM. In the vicinity of the dentino-enamel-junction more prisms were found to be cut longitudinally, while close to the crown surface more prisms were cut transversely. In the perpendicularly ground plane the corresponding prisms were seen to deviate the more from the centrifugal orientation the more close they came to the crown surface. In a geometric model the angle under which the prisms deviate from the centrifugal orientation was calculated in dependence from the distance to the dentino-enamel-junction. The results correspond with the SEM-findings. We conclude that--since the prism diameter is today known to be constant--the form of the enamel mantle is created by a specific orientation of the prisms: They stand perpendicular at the dentino-enamel-junction, and the farther away they run towards the periphery the more they deviate from the perpendicular path. By this increasingly oblique orientation of the prisms the volume increment of the enamel mantle is created. The maximal angle of deviation is found morphologically and mathematically between 60 degrees-70 degrees at the crown surface. This arrangement of the prisms demonstrated by us is now seen to be the reason for erroneous assumptions about an increase of the prism diameter when ground sections were used. Because the prisms are oriented more and more oblique towards the periphery, correspondingly larger effective diameters must be produced while making ground sections tangential to the crown surface.     

The anti-orienting phenomenon revisited: effects of gaze cues on antisaccade performance

When the eye gaze of a face is congruent with the direction of an upcoming target, saccadic eye movements of the observer towards that target are generated more quickly, in comparison with eye gaze incongruent with the direction of the target. This work examined the conflict in an antisaccade task, when eye gaze points towards the target, but the saccadic eye movement should be triggered in the opposite direction. In a gaze cueing paradigm, a central face provided an attentional gaze cue towards the target or away from the target. Participants (N = 38) generated pro- and antisaccades to peripheral targets that were congruent or incongruent with the previous gaze cue. Paradoxically, facilitatory effects of a gaze cue towards the target were observed for both the pro- and antisaccade tasks. The results are consistent with the idea that eye gaze cues are processed in the task set that is compatible with the saccade programme. Thus, in an antisaccade paradigm, participants may anti-orient with respect to the gaze cue, resulting in faster saccades on trials when the gaze cue is towards the target. The results resemble a previous observation by Fischer and Weber (Exp Brain Res 109:507–512, 1996) using low-level peripheral cues. The current study extends this finding to include central socially communicative cues.     

How far ahead do we look when required to step on specific locations in the travel path during locomotion?

Spatial-temporal gaze behaviour patterns were analysed as normal participants wearing a mobile eye tracker were required to step on 17 footprints, regularly or irregularly spaced over a 10-m distance, placed in their travel path. We examined the characteristics of two types of gaze fixation with respect to the participants' stepping patterns: footprint fixation; and travel fixation when the gaze is stable and travelling at the speed of whole body. The results showed that travel gaze fixation is a dominant gaze behaviour occupying over 50% of the travel time. It is hypothesised that this gaze behaviour would facilitate acquisition of environmental and self-motion information from the optic flow that is generated during locomotion: this in turn would guide movements of the lower limbs to the appropriate landing targets. When participants did fixate on the landing target they did so on average two steps ahead, about 800–1,000 ms before the limb is placed on the target area. This would allow them sufficient time to successfully modify their gait patterns. None of the gaze behaviours was influenced by the placement (regularly versus irregularly spaced) of the footprints or repeated exposures to the travel path. Rather visual information acquired during each trial was used "de novo" to modulate gait patterns. This study provides a clear temporal link between gaze and stepping pattern and adds to our understanding of how vision is used to regulate locomotion. Electronic Publication     

Relative contributions of visual and vestibular information on the trajectory of human gait

Seven healthy individuals were recruited to examine the interaction between visual and vestibular information on locomotor trajectory during walking. Subjects wore goggles that either contained a clear lens or a prism that displaced the visual scene either 20° to the left or right. A 5-s bipolar, binaural galvanic stimulus (GVS) was also applied at three times the subject's individual threshold (ranged between 1.2 to 1.5 mA). Subjects stood with their eyes closed and walked forward at a casual pace. At first heel contact, subjects opened their eyes and triggered the galvanic stimulus by foot switches positioned underneath a board. Reflective markers were placed bilaterally on the shoulders as the walking trajectory was captured using a camera mounted on the ceiling above the testing area. Twelve conditions were randomly assigned that combined four visual conditions (eyes closed, eyes open, left prism, right prism) and three GVS conditions (no GVS, GVS anode left, GVS anode right). As subjects walked forward, there was a tendency to deviate in the direction of the prisms. During GVS trials, subjects deviated towards the anode while walking, with the greatest deviations occurring with the eyes closed. However, when GVS was presented with the prisms, subjects always deviated to the side of the prisms, regardless of the position of the anode. Furthermore, the visual-vestibular conditions produced a larger lateral deviation than those observed in the prisms-only trials. This suggests that the nervous system examines the sensory inputs and takes into account the most reliable and relevant sensory input.     

Visual exteroceptive information provided during obstacle crossing did not modify the lower limb trajectory

The roles of visual exteroception (information regarding environmental characteristics) and exproprioception (the relation of body segments to the environment) during gait adaptation are not fully understood. The purpose of this study was to determine how visual exteroception regarding obstacle characteristics provided during obstacle crossing modified foot elevation and placement with and without lower limb-obstacle visual exproprioception (manipulated with goggles). Visual exteroceptive information was provided by an obstacle cue - a second obstacle identical to the obstacle that was stepped over - which was visible during crossing. Ten subjects walked over obstacles under four visual conditions: full vision with no obstacle height cue, full vision with an obstacle height cue, goggles with no obstacle height cue and goggles with an obstacle height cue. Obstacle heights were 2, 10, 20 and 30 cm. The presence of goggles increased horizontal distance (distance between foot and obstacle at foot placement), toe clearance and toe clearance variability. The presence of the obstacle height cue did not alter horizontal distance, toe clearance or toe clearance variability. These observations strengthen the argument that it is the visual exproprioceptive information, not visual exteroceptive information, that is used on-line to fine tune the lower limb trajectory during obstacle avoidance.     

Contributions of visual and proprioceptive information to travelled distance estimation during changing sensory congruencies

Recent research has provided evidence that visual and body-based cues (vestibular, proprioceptive and efference copy) are integrated using a weighted linear sum during walking and passive transport. However, little is known about the specific weighting of visual information when combined with proprioceptive inputs alone, in the absence of vestibular information about forward self-motion. Therefore, in this study, participants walked in place on a stationary treadmill while dynamic visual information was updated in real time via a head-mounted display. The task required participants to travel a predefined distance and subsequently match this distance by adjusting an egocentric, in-depth target using a game controller. Travelled distance information was provided either through visual cues alone, proprioceptive cues alone or both cues combined. In the combined cue condition, the relationship between the two cues was manipulated by either changing the visual gain across trials (0.7×, 1.0×, 1.4×; Exp. 1) or the proprioceptive gain across trials (0.7×, 1.0×, 1.4×; Exp. 2). Results demonstrated an overall higher weighting of proprioception over vision. These weights were scaled, however, as a function of which sensory input provided more stable information across trials. Specifically, when visual gain was constantly manipulated, proprioceptive weights were higher than when proprioceptive gain was constantly manipulated. These results therefore reveal interesting characteristics of cue-weighting within the context of unfolding spatio-temporal cue dynamics.     

Balance affects prism adaptation: evidence from the latent aftereffect

In prism adaptation experiments, the effect on throwing to a target is reduced (primary aftereffect is smaller) when the throwing condition with prisms removed (first test phase) is different from the throwing condition with prisms (the training phase). The missing adaptation, however, can be revealed through further testing (second test phase) in which the throwing condition during training is fully reinstated. We studied throwing underhand to a target flush with the floor. During training, participants wore left-shifting prism glasses while standing on the floor (Group 1) or on a balance board (Groups 2 and 3). Tests 1 and 2 following training involved the same underhand throwing. For Group 2, Test 1 was on the balance board and Test 2 on the ground; for Group 3, the order was reversed; and for Group 1, both tests were on the ground. The Group 3 Test 1 aftereffect was smaller, and the Test 2 aftereffect was larger than the respective tests for Groups 1 and 2, with the aftereffect sum the same for all three groups. A parallel was noted between prism adaptation and implicit memory: whether given training (study) conditions lead to better or poorer persistence of adaptation (memory performance) at test depends on the fit between the conditions at test relative to the conditions at training (study). In the general memory case, those conditions will involve nonobvious contributors to memory performance, analogous to the support for upright standing in the adaptation of the visual system to prismatic distortion investigated in the present research.     

Population density and food dispersion on the development of prism-induced aftereffects in newly hatched chicks

Newly hatched Leghorn cockerels (124) wearing hoods containing 8.5° prisms were reared in large or small groups and with high or low ratios of spatially distributed seeds on a sand filler. Only chicks reared in large groups demonstrated negative aftereffects when O° plates were substituted for the prisms on the seventh day. For large groups, high seed density resulted in smaller lateral pecking errors with prism displacement but larger negative aftereffect errors without displacement than did low seed density. For small groups, however, high seed density produced a reversal of negative aftereffect directions. High group density was necessary for negative aftereffect development, probably by its influence on socially mediated pecking rates.     

Human gaze stabilization during active head translations.

This study investigated how binocular gaze is controlled to compensate for self-generated translational movements of the head where geometric requirements dictate that the ideal gaze signal needs to be modulated by the inverse of target distance. Binocular gaze (eye plus head) was measured for visual and remembered targets at various distances in six human subjects during active head translations at frequencies of 0.25, 0.5, 1.0, and 1.5 Hz. We found that, during head translations, gaze changes were achieved by a combination of eye and head rotations. Accordingly, stabilization performance was characterized by the gaze response parameters sensitivity and phase, where sensitivity is defined as the ratio of gaze velocity and translational eye velocity and where phase refers to the phase delay of gaze velocity relative to translational eye velocity. In the analysis, we used a binocular coordinate system yielding a version and a vergence component. We examined how frequency and target distance, estimated from the vergence angle, affected sensitivity and phase of the version component of the gaze signal and compared the results to the requirements for ideal performance. The relation between gaze sensitivity and the inverse of distance was characterized by a linear regression analysis. The ratio of the slope of the linear regression and the slope required for ideal stabilization provided a measure for the degree of "distance compensation." The results show that distance compensation was better for a visual target than for remembered targets in darkness, and behaved according to low-pass characteristics in both target conditions. It declined from 1.00 to 0.84 for visual targets and from 0.87 to 0.57 for remembered targets in the frequency range 0.25-1.5 Hz. The intercept obtained from the regression yielded the gaze response at zero vergence and specified a "default sensitivity" of gaze compensation. Default sensitivity increased with frequency from 0.02 at 0.25 Hz to 0.10 degrees/cm at 1.5 Hz for visual targets and from 0.04 to 0.16 degrees/cm in darkness. The phase delays of the gaze response increased on average from 2 to 7 degrees in the frequency range 0.25-1.5 Hz. In comparison with earlier passive studies, active translation compensation in the dark is superior at all frequencies where comparison was possible. We conclude that a nonvestibular signal with low-pass characteristics contributes to gaze during active head translations.     

Incomplete inactivation and rapid recovery of voltage-dependent sodium channels during high-frequency firing in cerebellar Purkinje neurons

The ability of individuals to adapt locomotion to constraints associated with the complex environments normally encountered in everyday life is paramount for survival. Here, we tested the ability of 24 healthy young adults to adapt to a rightward prism shift (～11.3°) while either walking and stepping to targets (i.e., precision stepping task) or stepping over an obstacle (i.e., obstacle avoidance task). We subsequently tested for generalization to the other locomotor task. In the precision stepping task, we determined the lateral end-point error of foot placement from the targets. In the obstacle avoidance task, we determined toe clearance and lateral foot placement distance from the obstacle before and after stepping over the obstacle. We found large, rightward deviations in foot placement on initial exposure to prisms in both tasks. The majority of measures demonstrated adaptation over repeated trials, and adaptation rates were dependent mainly on the task. On removal of the prisms, we observed negative aftereffects for measures of both tasks. Additionally, we found a unilateral symmetric generalization pattern in that the left, but not the right, lower limb indicated generalization across the 2 locomotor tasks. These results indicate that the nervous system is capable of rapidly adapting to a visuomotor mismatch during visually demanding locomotor tasks and that the prism-induced adaptation can, at least partially, generalize across these tasks. The results also support the notion that the nervous system utilizes an internal model for the control of visually guided locomotion.     

A neural network model of flexible spatial updating

Neurons in many cortical areas involved in visuospatial processing represent remembered spatial information in retinotopic coordinates. During a gaze shift, the retinotopic representation of a target location that is fixed in the world (world-fixed reference frame) must be updated, whereas the representation of a target fixed relative to the center of gaze (gaze-fixed) must remain constant. To investigate how such computations might be performed, we trained a 3-layer recurrent neural network to store and update a spatial location based on a gaze perturbation signal, and to do so flexibly based on a contextual cue. The network produced an accurate readout of target position when cued to either reference frame, but was less precise when updating was performed. This output mimics the pattern of behavior seen in animals performing a similar task. We tested whether updating would preferentially use gaze position or gaze velocity signals, and found that the network strongly preferred velocity for updating world-fixed targets. Furthermore, we found that gaze position gain fields were not present when velocity signals were available for updating. These results have implications for how updating is performed in the brain.