Body-tilt and visual verticality perception during multiple cycles of roll rotation

To assess the effects of degrading canal cues for dynamic spatial orientation in human observers, we tested how judgments about visual-line orientation in space (subjective visual vertical task, SVV) and estimates of instantaneous body tilt (subjective body-tilt task, SBT) develop in the course of three cycles of constant-velocity roll rotation. These abilities were tested across the entire tilt range in separate experiments. For comparison, we also obtained SVV data during static roll tilt. We found that as tilt increased, dynamic SVV responses became strongly biased toward the head pole of the body axis (A-effect), as if body tilt was underestimated. However, on entering the range of near-inverse tilts, SVV responses adopted a bimodal pattern, alternating between A-effects (biased toward head-pole) and E-effects (biased toward feet-pole). Apart from an onset effect, this tilt-dependent pattern of systematic SVV errors repeated itself in subsequent rotation cycles with little sign of worsening performance. Static SVV responses were qualitatively similar and consistent with previous reports but showed smaller A-effects. By contrast, dynamic SBT errors were small and unimodal, indicating that errors in visual-verticality estimates were not caused by errors in body-tilt estimation. We discuss these results in terms of predictions from a canal-otolith interaction model extended with a leaky integrator and an egocentric bias mechanism. We conclude that the egocentric-bias mechanism becomes more manifest during constant velocity roll-rotation and that perceptual errors due to incorrect disambiguation of the otolith signal are small despite the decay of canal signals.     

Interpretation of a discontinuity in the sense of verticality at large body tilt

Results of earlier spatial-orientation studies focusing on the sense of verticality have emphasized an intriguing paradox. Despite evidence that nearly veridical signals for gravicentric head orientation and egocentric visual stimulus orientation are available, roll-tilted subjects err in the direction of the long body axis when adjusting a visual line to vertical in darkness (Aubert effect). This has led to the suggestion that a central egocentric bias signal with fixed strength and direction acts to pull the perceived vertical to the subjects' zenith (M-model). In the present study, the subjective visual vertical (SVV) was tested in six human subjects, across the entire 360 degrees range. For comparison, body-tilt estimates from four subjects where collected in a separate series of experiments. For absolute tilts up to approximately 135 degrees, SVV responses showed a gradually increasing Aubert effect that could not be attributed to errors in perceived body tilt but was nicely in line with the M-model. At larger absolute tilts, SVV errors abruptly reversed sign, now showing a pattern concordant with errors in body-tilt estimates but incompatible with the M-model. These results suggest that, in the normal working range, the perception of external space and the perception of body posture are based on different processing of body-tilt signals. Beyond this range, both spatial-orientation tasks seem to rely mainly on a common tilt signal.     

Reference frames in saccadic targeting

 We attempt to determine the egocentric reference frame used in directing saccades to remembered targets when landmark-based (exocentric) cues are not available. Specifically, we tested whether memory-guided saccades rely on a retina-centered frame, which must account for eye movements that intervene during the memory period (thereby accumulating error) or on a head-centered representation that requires knowledge of the position of the eyes in the head. We also examined the role of an exocentric reference frame in saccadic targeting since it would not need to account for intervening movements. We measured the precision of eye movements made by human observers to target locations held in memory for a few seconds. A variable number of saccades intervened between the visual presentation of a target and a later eye movement to its remembered location. A visual landmark that allowed for exocentric encoding of the memory target appeared in half the trials. Variable error increased slightly with a greater number of intervening saccades. The landmark aided targeting precision, but did not eliminate the increase in variable error with additional intervening saccades. We interpret these results as evidence for a representation that relies on knowledge of eye position with respect to the head and not one that relies solely on updating in a retina-centered frame. Our results allow us to set an upper bound on the standard deviation of an eye position signal available to the saccadic system during short memory periods at 1.4° for saccades of about 10°. Received: 7 February 1995 / Accepted: 4 October 1996     

Effects of external feedback about body tilt: Influence on the Subjective Proprioceptive Horizon

The present study investigated a cognitive aspect upon spatial perception, namely the impact of a true or false verbal feedback (FB) about the magnitude of body tilt on Subjective Proprioceptive Horizon (SPH) estimates. Subjects were asked to set their extended arm normal to gravity for different pitch body tilts up to 9 degrees . True FB were provided at all body tilt angles, whereas false FB were provided only at 6 degrees backward and 6 degrees forward body tilts for half of the trials. Our data confirmed previous results about the egocentric influence of body tilt itself upon SPH: estimates were linearly lowered with forward tilts and elevated with backward tilts. In addition, results showed a significant effect of the nature of the external FB provided to the subjects. When subjects received a false FB inducing a 3 degrees forward bias relative to physical body tilt, they set their SPH consequently higher than when they received a false FB inducing a 3 degrees backward bias. These findings clearly indicated that false cognitive information about body tilt might significantly modify the judgement of a geocentric direction of space, such as the SPH. This may have deleterious repercussions in aeronautics when pilots have to localize external objects relative to earth-based directions in darkened environments.     

Pitch body orientation influences the perception of self-motion direction induced by optic flow

We studied the effect of static pitch body tilts on the perception of self-motion direction induced by a visual stimulus. Subjects were seated in front of a screen on which was projected a 3D cluster of moving dots visually simulating a forward motion of the observer with upward or downward directional biases (relative to a true earth horizontal direction). The subjects were tilted at various angles relative to gravity and were asked to estimate the direction of the perceived motion (nose-up, as during take-off or nose-down, as during landing). The data showed that body orientation proportionally affected the amount of error in the reported perceived direction (by 40% of body tilt magnitude in a range of ±20°) and these errors were systematically recorded in the direction of body tilt. As a consequence, a same visual stimulus was differently interpreted depending on body orientation. While the subjects were required to perform the task in a geocentric reference frame (i.e., relative to a gravity-related direction), they were obviously influenced by egocentric references. These results suggest that the perception of self-motion is not elaborated within an exclusive reference frame (either egocentric or geocentric) but rather results from the combined influence of both.     

Cognitive allocentric representations of visual space shape pointing errors

Subjects reached in three-dimensional space to a set of remembered targets whose position was varied randomly from trial to trial, but always fell along a "virtual" line (line condition). Targets were presented briefly, one-by-one and in an empty visual field. After a short delay, subjects were required to point to the remembered target location. Under these conditions, the target was presented in the complete absence of allocentric visual cues as to its position in space. However, because the subjects were informed prior to the experiment that all targets would fall on a straight line, they could conceivably imagine each point target as belonging to a single rigid object with a particular geometry and orientation in space, although this virtual object was never explicitly shown to the subjects. We compared the responses to repeated measurements of each target with those measured for targets presented in a directionally neutral configuration (sphere condition), and used the variable errors to infer the putative reference frames underlying the corresponding sensorimotor transformation. Performance in the different tasks was compared under two different lighting conditions (dim light or total darkness) and two memory delays (0.5 or 5 s). The pattern of variable errors differed significantly between the sphere condition and the line condition. In the former case, the errors were always accounted for by egocentric reference frames. By contrast the errors in the line condition revealed both egocentric and allocentric components, consistent with the hypothesis that target information can be defined concurrently in both egocentric and allocentric frames of reference, resulting in two independent coexisting representations. Electronic Publication     

Accuracy of saccades to remembered targets as a function of body orientation in space

A vertical asymmetry in memory-guided saccadic eye movements has been previously demonstrated in humans and in rhesus monkeys. In the upright orientation, saccades generally land several degrees above the target. The origin of this asymmetry has remained unknown. In this study, we investigated whether the asymmetry in memory saccades is dependent on body orientation in space. Thus animals performed memory saccades in four different body orientations: upright, left-side-down (LSD), right-side-down (RSD), and supine. Data in all three rhesus monkeys confirm previous observations regarding a significant upward vertical asymmetry. Saccade errors made from LSD and RSD postures were partitioned into components made along the axis of gravity and along the vertical body axis. Up/down asymmetry persisted only in body coordinates but not in gravity coordinates. However, this asymmetry was generally reduced in tilted positions. Therefore the upward bias seen in memory saccades is egocentric although orientation in space might play a modulatory role.     

Haptic spatial matching in near peripersonal space

Research has shown that haptic spatial matching at intermanual distances over 60 cm is prone to large systematic errors. The error pattern has been explained by the use of reference frames intermediate between egocentric and allocentric coding. This study investigated haptic performance in near peripersonal space, i.e. at intermanual distances of 60 cm and less. Twelve blindfolded participants (six males and six females) were presented with two turn bars at equal distances from the midsagittal plane, 30 or 60 cm apart. Different orientations (vertical/horizontal or oblique) of the left bar had to be matched by adjusting the right bar to either a mirror symmetric (/ \) or parallel (/ /) position. The mirror symmetry task can in principle be performed accurately in both an egocentric and an allocentric reference frame, whereas the parallel task requires an allocentric representation. Results showed that parallel matching induced large systematic errors which increased with distance. Overall error was significantly smaller in the mirror task. The task difference also held for the vertical orientation at 60 cm distance, even though this orientation required the same response in both tasks, showing a marked effect of task instruction. In addition, men outperformed women on the parallel task. Finally, contrary to our expectations, systematic errors were found in the mirror task, predominantly at 30 cm distance. Based on these findings, we suggest that haptic performance in near peripersonal space might be dominated by different mechanisms than those which come into play at distances over 60 cm. Moreover, our results indicate that both inter-individual differences and task demands affect task performance in haptic spatial matching. Therefore, we conclude that the study of haptic spatial matching in near peripersonal space might reveal important additional constraints for the specification of adequate models of haptic spatial performance.     

Double dissociation of egocentric and allocentric space following medial prefrontal and parietal cortex lesions in the rat

Animals with medial prefrontal cortex or parietal cortex lesions and sham-operated and non-operated controls were tested for the acquisition of an adjacent arm task that accentuated the importance of egocentric spatial localization and a cheese board task that accentuated the importance of allocentric spatial localization. Results indicated that relative to controls, animals with medial-prefrontal cortex lesions are impaired on the adjacent arm task but displayed facilitation on the cheese board task. In contrast, relative to controls, rats with parietal cortex lesions are impaired on the cheese board task but show no impairment on the adjacent arm task. The data suggest a double dissociation of function between medial prefrontal cortex and parietal cortex in terms of coding of egocentric versus allocentric spatial information.     

Allocentrically implied target locations are updated in an eye-centred reference frame

When reaching to remembered target locations following an intervening eye movement a systematic pattern of error is found indicating eye-centred updating of visuospatial memory. Here we investigated if implicit targets, defined only by allocentric visual cues, are also updated in an eye-centred reference frame as explicit targets are. Participants viewed vertical bars separated by varying distances, and horizontal lines of equivalently varying lengths, implying a “target” location at the midpoint of the stimulus. After determining the implied “target” location from only the allocentric stimuli provided, participants saccaded to an eccentric location, and reached to the remembered “target” location. Irrespective of the type of stimulus reaching errors to these implicit targets are gaze-dependent, and do not differ from those found when reaching to remembered explicit targets. Implicit target locations are coded and updated as a function of relative gaze direction with respect to those implied locations just as explicit targets are, even though no target is specifically represented.     

Dynamics of maculo-ocular reflexes in the frog

Compensatory torsional and vertical eye movements were recorded in the frog during sinusoidal linear acceleration along the longitudinal and transverse body axes, respectively. Stimulus frequencies ranged between 0.1 and 1.0 Hz and peak accelerations from 0.01 g to 0.1 g corresponding to body tilts ranging from 0.57 to 5.7 degrees. In addition, static compensatory eye movements were studied during fore-and-aft and lateral body tilt over ranges of +/- 10 degrees. The evoked eye movements were generally quite small (+/- 0.5 degree). Dynamic gain (rotation of the eye/apparent rotation of gravity direction) was 0.10-0.20 at 0.1 Hz and decreased to about 0.05 at 1.0 Hz. The gain of vertical eye movements was somewhat higher than that of torsional eye movements. Phase lag relative to peak accelerations increased from about 10 degrees to about 45 degrees over the same frequency range. Static compensatory eye movements evoked by nose-up and ipsilateral side-up tilt were larger in amplitude than those evoked by nose-down and ipsilateral side-down tilt. Static gain (rotation of the eye/tilt of the whole body) was about 0.10 for vertical and about 0.06 for torsional eye movements. No consistent eye movements could be evoked by vertical sinusoidal accelerations (maximal modulation amplitudes +/- 0.025 g). The results indicate that, as in other vertebrates, maculo-ocular reflexes contribute to gaze stabilization in the frog mainly during low frequency and static head and body tilts.     

Assessment of the perception of verticality and horizontality with self-paced saccades

We investigated the ability of human subjects (Ss) to make self-paced saccades in the earth-vertical and horizontal directions (space-referenced task) and in the direction of the head-vertical and horizontal axis (self-referenced task) during whole body tilts of 0°, 22.5°, 45° and 90° in the frontal (roll) plane. Saccades were recorded in the dark with computerised video-oculography. During space-referenced tasks, the saccade vectors did not fully counter-rotate to compensate for larger angles of body tilt. This finding is in agreement with the ’A’ effect reported for the visual vertical. The error was significantly larger for saccades intended to be space-horizontal than space-vertical. This vertico-horizontal dissociation implies greater difficulty in defining horizontality than verticality with the non-visual motor task employed. In contrast, normal Ss (and an alabyrinthine subject tested) were accurate in orienting saccades to their own (cranio-centric) vertical and horizontal axes regardless of tilt indicating that cranio-centric perception is robust and apparently not affected by gravitational influences. Received: 9 October 1996 / Accepted: 23 January 1998     

Allocentric lock in anorexia nervosa: new evidences from neuroimaging studies

Individuals with anorexia nervosa (AN) have a disturbance in the way in which their body is experienced and tend to evaluate negatively their own body and body parts. It is controversial whether these symptoms are secondary to dysfunctions in the neuronal processes related to appetite and emotional regulation or reflect a primary disturbance in the way the body is experienced and remembered. According to the "Allocentric Lock Hypothesis--ALH" (http://dx.doi.org/10.1016/j.mehy.2011.10.039) individuals with AN may be locked to an allocentric (observer view) negative memory of the body that is no more updated by contrasting egocentric representations driven by perception. Recent neuroimaging studies are showing several structural and functional alterations in frame- and memory-related body-image-processing brain circuits that may support ALH.     

Human updating of visual motion direction during head rotations

Previous studies have demonstrated that human subjects update the location of visual targets for saccades after head and body movements and in the absence of visual feedback. This phenomenon is known as spatial updating. Here we investigated whether a similar mechanism exists for the perception of motion direction. We recorded eye positions in three dimensions and behavioral responses in seven subjects during a motion task in two different conditions: when the subject's head remained stationary and when subjects rotated their heads around an anteroposterior axis (head tilt). We demonstrated that after head-tilt subjects updated the direction of saccades made in the perceived stimulus direction (direction of motion updating), the amount of updating varied across subjects and stimulus directions, the amount of motion direction updating was highly correlated with the amount of spatial updating during a memory-guided saccade task, subjects updated the stimulus direction during a two-alternative forced-choice direction discrimination task in the absence of saccadic eye movements (perceptual updating), perceptual updating was more accurate than motion direction updating involving saccades, and subjects updated motion direction similarly during active and passive head rotation. These results demonstrate the existence of an updating mechanism for the perception of motion direction in the human brain that operates during active and passive head rotations and that resembles the one of spatial updating. Such a mechanism operates during different tasks involving different motor and perceptual skills (saccade and motion direction discrimination) with different degrees of accuracy.     

Judging hand laterality from my or your point of view: Interactions between motor imagery and visual perspective

Motor imagery tasks (hand laterality judgment) are usually performed with respect to a self-body (egocentric) representation, but manipulations of stimulus features (hand orientation) can induce a shift to other's body (allocentric) reference frame. Visual perspective taking tasks are also performed in self-body perspective but a shift to an allocentric frame can be triggered by manipulations of context features (e.g., another person present in the to-be-judged scene). Combining hand laterality task and visual perspective taking, we demonstrated that both stimulus and context features can modulate motor imagery performance. In Experiment 1, participants judged laterality of a hand embedded in a human or non-human silhouette. Results showed that observing a human silhouette interfered with judgments on “egocentric hand stimuli” (right hand, fingers up). In Experiment 2, participants were explicitly required to judge laterality of a hand embedded in a human silhouette from their own (egocentric group) or from the silhouette's perspective (allocentric group). Consistent with previous results, the egocentric group was significantly faster than the allocentric group in judging fingers-up right hand stimuli. These findings showed that concurrent activation of egocentric and allocentric frames during mental transformation of body parts impairs participants’ performance due to a conflict between motor and visual mechanisms.     

Allocentric versus egocentric spatial memory after unilateral temporal lobectomy in humans

Thirty patients who had undergone either a right or left unilateral temporal lobectomy (14 RTL; 16 LTL) and 16 control participants were tested on a computerized human analogue of the Morris Water Maze. The procedure was designed to compare allocentric and egocentric spatial memory. In the allocentric condition, participants searched for a target location on the screen, guided by object cues. Between trials, participants had to walk around the screen, which disrupted egocentric memory representation. In the egocentric condition, participants remained in the same position, but the object cues were shifted between searches to prevent them from using allocentric memory. Only the RTL group was impaired on the allocentric condition, and neither the LTL nor RTL group was impaired on additional tests of spatial working memory or spatial manipulation. The results support the notion that the right anterior temporal lobe stores long-term allocentric spatial memories.     

Roles of gravitational cues and efference copy signals in the rotational updating of memory saccades

Primates are able to localize a briefly flashed target despite intervening movements of the eyes, head, or body. This ability, often referred to as updating, requires extraretinal signals related to the intervening movement. With active roll rotations of the head from an upright position it has been shown that the updating mechanism is 3-dimensional, robust, and geometrically sophisticated. Here we examine whether such a rotational updating mechanism operates during passive motion both with and without inertial cues about head/body position in space. Subjects were rotated from either an upright or supine position, about a nasal-occipital axis, briefly shown a world-fixed target, rotated back to their original position, and then asked to saccade to the remembered target location. Using this paradigm, we tested subjects' abilities to update from various tilt angles (0, +/-30, +/-45, +/-90 degrees), to 8 target directions and 2 target eccentricities. In the upright condition, subjects accurately updated the remembered locations from all tilt angles independent of target direction or eccentricity. Slopes of directional errors versus tilt angle ranged from -0.011 to 0.15, and were significantly different from a slope of 1 (no compensation for head-in-space roll) and a slope of 0.9 (no compensation for eye-in-space roll). Because the eyes, head, and body were fixed throughout these passive movements, subjects could not use efference copies or neck proprioceptive cues to assess the amount of tilt, suggesting that vestibular signals and/or body proprioceptive cues suffice for updating. In the supine condition, where gravitational signals could not contribute, slopes ranged from 0.60 to 0.82, indicating poor updating performance. Thus information specifying the body's orientation relative to gravity is critical for maintaining spatial constancy and for distinguishing body-fixed versus world-fixed reference frames.     

Memory for visuospatial location following selective hippocampal sclerosis: the use of different coordinate systems

This study addressed the role of the medial temporal lobe regions and, more specifically, the contribution of the human hippocampus in memory for body-centered (egocentric) and environment-centered (allocentric) spatial location. Twenty-one patients with unilateral atrophy of the hippocampus secondary to long-standing epilepsy (left, n = 7; right, n = 14) and 15 normal control participants underwent 3 tasks measuring recall of egocentric or allocentric spatial location. Patients with left hippocampal sclerosis were consistently impaired in the allocentric conditions of all 3 tasks but not in the egocentric conditions. Patients with right hippocampal sclerosis were impaired to a lesser extent and in only 2 of the 3 tasks. It was concluded that hippocampal structures are crucial for allocentric, but not egocentric, spatial memory.     

Prefrontal serotonin depletion impairs egocentric, but not allocentric working memory in rats

Working memory is a cognitive ability chiefly organized by the prefrontal cortex. Working memory tests may be resolved based on allocentric or egocentric spatial strategies. Serotonergic neurotransmission is closely involved in working memory, but its role in spatial strategies for working memory performance is unknown. To address this issue, prefrontal serotonin depletion was induced to adult male rats, and three days after the behavioral expression of both allocentric and egocentric strategies were evaluated in the "Y" maze and in a crossed-arm maze, respectively. Serotonin depletion caused no effects on allocentric-related behavioral performance, but lesioned rats performed deficiently when the egocentric working memory was evaluated. These results suggest that serotonin may be more closely related with the organization of working memory that uses own movement-guided responses than with that involving the use of external visuospatial signals. Further neurochemical studies are needed to elucidate possible interactions between serotonergic activity and other neurotransmitter systems in the organization of working memory-related allocentric and egocentric strategies.     

Spatial coding of eye movements relative to perceived earth and head orientations during static roll tilt

This purpose of this study was to examine the spatial coding of eye movements during static roll tilt (up to ±45°) relative to perceived earth and head orientations. Binocular videographic recordings obtained in darkness from eight subjects allowed us to quantify the mean deviations in gaze trajectories along both horizontal and vertical coordinates relative to the true earth and head orientations. We found that both variability and curvature of gaze trajectories increased with roll tilt. The trajectories of eye movements made along the perceived earth-horizontal (PEH) were more accurate than movements along the perceived head-horizontal (PHH). The trajectories of both PEH and PHH saccades tended to deviate in the same direction as the head tilt. The deviations in gaze trajectories along the perceived earth-vertical (PEV) and perceived head-vertical (PHV) were both similar to the PHH orientation, except that saccades along the PEV deviated in the opposite direction relative to the head tilt. The magnitude of deviations along the PEV, PHH, and PHV corresponded to perceptual overestimations of roll tilt obtained from verbal reports. Both PEV gaze trajectories and perceptual estimates of tilt orientation were different following clockwise rather than counterclockwise tilt rotation; however, the PEH gaze trajectories were less affected by the direction of tilt rotation. Our results suggest that errors in gaze trajectories along PEV and perceived head orientations increase during roll tilt in a similar way to perceptual errors of tilt orientation. Although PEH and PEV gaze trajectories became nonorthogonal during roll tilt, we conclude that the spatial coding of eye movements during roll tilt is overall more accurate for the perceived earth reference frame than for the perceived head reference frame. Received: 22 April 1997 / Accepted: 18 December 1997