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Dynamics of the spatial scale of visual attention revealed by brain event-related potentials
The temporal dynamics of the spatial scaling of attention during visual search were examined by recording event-related potentials (ERPs). A total of 16 young participants performed a search task in which the search array was preceded by valid cues that varied in size and hence in precision of target localization. The effects of cue size on short-latency (P1 and N1) ERP components, and the time course of these effects with variation in cue-target stimulus onset asynchrony (SOA), were examined. Reaction time (RT) to discriminate a target was prolonged as cue size increased. The amplitudes of the posterior P1 and N1 components of the ERP evoked by the search array were affected in opposite ways by the size of the precue: P1 amplitude increased whereas N1 amplitude decreased as cue size increased, particularly following the shortest SOA. The results show that when top-down information about the region to be searched is less precise (larger cues), RT is slowed and the neural generators of P1 become more active, reflecting the additional computations required in changing the spatial scale of attention to the appropriate element size to facilitate target discrimination. In contrast, the decrease in N1 amplitude with cue size may reflect a broadening of the spatial gradient of attention. The results provide electrophysiological evidence that changes in the spatial scale of attention modulate neural activity in early visual cortical areas and activate at least two temporally overlapping component processes during visual search.
Development of gravity-sensing organs in altered gravity
Experiments are described in which the development of the gravity-sensing organs was studied in newt larvae reared in microgravity on the IML-2 mission and in Aplysia embryos and larvae reared on a centrifuge at 1 to 5 g. In Aplysia embryos, the statolith (single dense mass on which gravity and linear acceleration act) was reduced in size in a graded fashion at increasing g. In early post-metamorphic Aplysia or even in isolated statocysts from such animals, the number of statoconia produced is reduced at high g. Newt larvae launched before any of the otoconia were formed and reared for 15 days in microgravity had nearly adult labyrinths at the end of the IML-2 mission. The otoliths of the saccule and utricle were the same size in flight and ground-reared larvae. However, the system of aragonitic otoconia produced in the endolymphatic sac in amphibians was much larger and developed earlier in the flight-reared larvae. At later developmental stages, the aragonitic otoconia enter and fill the saccule. One flight-reared larva was maintained for nine months post-flight and the size of the saccular otolith, as well as the volume of otoconia within the endolymphatic sac, were considerably larger than in age-matched, ground-reared newts. This suggests that rearing in microgravity initiates a process that continues for several months after introduction to 1-g, which greatly increases the volume of otoconia. The flight-reared animal had abnormal posture, pointing its head upward, whereas normal ground-reared newts always keep their head horizontal. This suggests that rearing for even a short period in microgravity can have lasting functional consequences in an animal subsequently reared in 1-g conditions on Earth.
Eye development and the appearance and maintenance of corneal transparency
Embryonic development of the eye, including the cornea, depends on the appearance and steady maintenance of intraocular pressure. The eye is a gravity-sensitive organ, as evidence by changes in pupil diameter during parabolic flight. The cornea is largely a paracrystal of extracellular matrix. The extent to which it will polymerize normally in microgravity has yet to be determined.
Spatial orientation and balance control changes induced by altered gravitoinertial force vectors
To better understand the mechanisms of human adaptation to rotating environments, we exposed 19 healthy subjects and 8 vestibular-deficient subjects ("abnormal"; four bilateral and four unilateral lesions) to an interaural centripetal acceleration of 1 g (resultant 45 degrees roll-tilt of 1.4 g) on a 0.8-m-radius centrifuge for periods of 90 min. The subjects sat upright (body z-axis parallel to centrifuge rotation axis) in the dark with head stationary, except during 4 min of every 10 min, when they performed head saccades toward visual targets switched on at 3- to 5-s intervals at random locations (within +/- 30 degrees) in the earth-horizontal plane. Eight of the normal subjects also performed the head saccade protocol in a stationary chair adjusted to a static roll-tilt angle of 45 degrees for 90 min (reproducing the change in orientation but not the magnitude of the gravitoinertial force on the centrifuge). Eye movements, including voluntary saccades directed along perceived earth- and head-referenced planes, were recorded before, during, and immediately after centrifugation. Postural center of pressure (COP) and multisegment body kinematics were also gathered before and within 10 min after centrifugation. Normal subjects overestimated roll-tilt during centrifugation and revealed errors in perception of head-vertical provided by directed saccades. Errors in this perceptual response tended to increase with time and became significant after approximately 30 min. Motion-sickness symptoms caused approximately 25% of normal subjects to limit their head movements during centrifugation and led three normal subjects to stop the test early. Immediately after centrifugation, subjects reported feeling tilted 10 degrees in the opposite direction, which was in agreement with the direction of their earth-referenced directed saccades. Postural COP, segmental body motion amplitude, and hip-sway frequency increased significantly after centrifugation. These postural effects were short-lived, however, with a recovery time of several postural test trials (minutes). There were also asymmetries in the direction of postcentrifugation COP and head tilt which depended on the subject's orientation during the centrifugation adaptation period (left ear or right ear out). The amount of total head movements during centrifugation correlated poorly or inversely with postcentrifugation postural stability, and the most unstable subject made no head movements. There was no decrease in postural stability after static tilt, although these subjects also reported a perceived tilt briefly after return to upright, and they also had COP asymmetries. Abnormal subjects underestimated roll-tilt during centrifugation, and their directed saccades revealed permanent spatial distortions. Bilateral abnormal subjects started out with poor postural control, but showed no postural decrements after centrifugation, while unilateral abnormal subjects had varying degrees of postural decrement, both in their everyday function and as a result of experiencing the centrifugation. In addition, three unilateral, abnormal subjects, who rode twice in opposite orientations, revealed a consistent orthogonal pattern of COP offsets after centrifugation. These results suggest that both orientation and magnitude of the gravitoinertial vector are used by the central nervous system for calibration of multiple orientation systems. A change in the background gravitoinertial force (otolith input) can rapidly initiate postural and perceptual adaptation in several sensorimotor systems, independent of a structured visual surround.
Hippocampal place-cell firing during movement in three-dimensional space
"Place" cells of the rat hippocampus are coupled to "head direction" cells of the thalamus and limbic cortex. Head direction cells are sensitive to head direction in the horizontal plane only, which leads to the question of whether place cells similarly encode locations in the horizontal plane only, ignoring the z axis, or whether they encode locations in three dimensions. This question was addressed by recording from ensembles of CA1 pyramidal cells while rats traversed a rectangular track that could be tilted and rotated to different three-dimensional orientations. Cells were analyzed to determine whether their firing was bound to the external, three-dimensional cues of the environment, to the two-dimensional rectangular surface, or to some combination of these cues. Tilting the track 45 degrees generally provoked a partial remapping of the rectangular surface in that some cells maintained their place fields, whereas other cells either gained new place fields, lost existing fields, or changed their firing locations arbitrarily. When the tilted track was rotated relative to the distal landmarks, most place fields remapped, but a number of cells maintained the same place field relative to the x-y coordinate frame of the laboratory, ignoring the z axis. No more cells were bound to the local reference frame of the recording apparatus than would be predicted by chance. The partial remapping demonstrated that the place cell system was sensitive to the three-dimensional manipulations of the recording apparatus. Nonetheless the results were not consistent with an explicit three-dimensional tuning of individual hippocampal neurons nor were they consistent with a model in which different sets of cells are tightly coupled to different sets of environmental cues. The results are most consistent with the statement that hippocampal neurons can change their "tuning functions" in arbitrary ways when features of the sensory input or behavioral context are altered. Understanding the rules that govern the remapping phenomenon holds promise for deciphering the neural circuitry underlying hippocampal function.
Transient cardio-respiratory responses to visually induced tilt illusions
Although the orthostatic cardio-respiratory response is primarily mediated by the baroreflex, studies have shown that vestibular cues also contribute in both humans and animals. We have demonstrated a visually mediated response to illusory tilt in some human subjects. Blood pressure, heart and respiration rate, and lung volume were monitored in 16 supine human subjects during two types of visual stimulation, and compared with responses to real passive whole body tilt from supine to head 80 degrees upright. Visual tilt stimuli consisted of either a static scene from an overhead mirror or constant velocity scene motion along different body axes generated by an ultra-wide dome projection system. Visual vertical cues were initially aligned with the longitudinal body axis. Subjective tilt and self-motion were reported verbally. Although significant changes in cardio-respiratory parameters to illusory tilts could not be demonstrated for the entire group, several subjects showed significant transient decreases in mean blood pressure resembling their initial response to passive head-up tilt. Changes in pulse pressure and a slight elevation in heart rate were noted. These transient responses are consistent with the hypothesis that visual-vestibular input contributes to the initial cardiovascular adjustment to a change in posture in humans. On average the static scene elicited perceived tilt without rotation. Dome scene pitch and yaw elicited perceived tilt and rotation, and dome roll motion elicited perceived rotation without tilt. A significant correlation between the magnitude of physiological and subjective reports could not be demonstrated.
Three-dimensional spatial selectivity of hippocampal neurons during space flight
No abstract available
Sensory processing in the vestibular nuclei during active head movements
Many secondary vestibular neurons are sensitive to head on trunk rotation during reflex-induced and voluntary head movements. During passive whole body rotation the interaction of head on trunk signals related to the vestibulo-collic reflex with vestibular signals increases the rotational gain of many secondary vestibular neurons, including many that project to the spinal cord. In some units, the sensitivity to head on trunk and vestibular input is matched and the resulting interaction produces an output that is related to the trunk velocity in space. In other units the head on trunk inputs are stronger and the resulting interaction produces an output that is larger during the reflex. During voluntary head movements, inputs related to head on trunk movement combine destructively with vestibular signals, and often cancel the sensory reafferent consequences of self-generated movements. Cancellation of sensory vestibular signals was observed in all of the antidromically identified secondary vestibulospinal units, even though many of these units were not significantly affected by reflexive head on trunk movements. The results imply that the inputs to vestibular neurons related to head on trunk rotation during reflexive and voluntary movements arise from different sources. We suggest that the relative strength of reflexive head on trunk input to different vestibular neurons might reflect the different functional roles they have in controlling the posture of the neck and body.
Relationship between selected orientation rest frame, circular vection and space motion sickness
Space motion sickness (SMS) and spatial orientation and motion perception disturbances occur in 70-80% of astronauts. People select "rest frames" to create the subjective sense of spatial orientation. In microgravity, the astronaut's rest frame may be based on visual scene polarity cues and on the internal head and body z axis (vertical body axis). The data reported here address the following question: Can an astronaut's orientation rest frame be related and described by other variables including circular vection response latencies and space motion sickness? The astronaut's microgravity spatial orientation rest frames were determined from inflight and postflight verbal reports. Circular vection responses were elicited by rotating a virtual room continuously at 35 degrees/s in pitch, roll and yaw with respect to the astronaut. Latency to the onset of vection was recorded from the time the crew member opened their eyes to the onset of vection. The astronauts who used visual cues exhibited significantly shorter vection latencies than those who used internal z axis cues. A negative binomial regression model was used to represent the observed total SMS symptom scores for each subject for each flight day. Orientation reference type had a significant effect, resulting in an estimated three-fold increase in the expected motion sickness score on flight day 1 for astronauts who used visual cues. The results demonstrate meaningful classification of astronauts' rest frames and their relationships to sensitivity to circular vection and SMS. Thus, it may be possible to use vection latencies to predict SMS severity and duration.
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 degrees) 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.
Response properties of pigeon otolith afferents to linear acceleration
In the present study, the sensitivity to sinusoidal linear accelerations in the plane of the utricular macula was tested in afferents. The head orientation relative to the translation axis was varied in order to determine the head position that elicited the maximal and minimal responses for each afferent. The response gain and phase values obtained to 0.5-Hz and 2-Hz linear acceleration stimuli were then plotted as a function of head orientation and a modified cosine function was fit to the data. From the best-fit cosine function, the predicted head orientations that would produce the maximal and minimal response gains were estimated. The estimated maximum response gains to linear acceleration in the utricular plane for the afferents varied between 75 and 1420 spikes s-1 g-1. The mean maximal gains for all afferents to 0.5-Hz and 2-Hz sinusoidal linear acceleration stimuli were 282 and 367 spikes s-1 g-1, respectively. The minimal response gains were essentially zero for most units. The response phases always led linear acceleration and remained constant for each afferent, regardless of head orientation. These response characteristics indicate that otolith afferents are cosine tuned and behave as one-dimensional linear accelerometers. The directions of maximal sensitivity to linear acceleration for the afferents varied throughout the plane of the utricle; however, most vectors were directed out of the opposite ear near the interaural axis. The response dynamics of the afferents were tested using stimulus frequencies ranging between 0.25 Hz and 10 Hz (0.1 g peak acceleration). Across stimulus frequencies, most afferents had increasing gains and constant phase values. These dynamic properties for individual afferents were fit with a simple transfer function that included three parameters: a mechanical time constant, a gain constant, and a fractional order distributed adaptation operator.
Kinematic principles of primate rotational vestibulo-ocular reflex. I. Spatial organization of fast phase velocity axes
The spatial organization of fast phase velocity vectors of the vestibulo-ocular reflex (VOR) was studied in rhesus monkeys during yaw rotations about an earth-horizontal axis that changed continuously the orientation of the head relative to gravity ("barbecue spit" rotation). In addition to a velocity component parallel to the rotation axis, fast phases also exhibited a velocity component that invariably was oriented along the momentary direction of gravity. As the head rotated through supine and prone positions, torsional components of fast phase velocity axes became prominent. Similarly, as the head rotated through left and right ear-down positions, fast phase velocity axes exhibited prominent vertical components. The larger the speed of head rotation the greater the magnitude of this fast phase component, which was collinear with gravity. The main sequence properties of VOR fast phases were independent of head position. However, peak amplitude as well as peak velocity of fast phases were both modulated as a function of head orientation, exhibiting a minimum in prone position. The results suggest that the fast phases of vestibulo-ocular reflexes not only redirect gaze and reposition the eye in the direction of head motion but also reorient the eye with respect to earth-vertical when the head moves relative to gravity. As further elaborated in the companion paper, the underlying mechanism could be described as a dynamic, gravity-dependent modulation of the coordinates of ocular rotations relative to the head.
Fingertip contact influences human postural control
Touch and pressure stimulation of the body surface can strongly influence apparent body orientation, as well as the maintenance of upright posture during quiet stance. In the present study, we investigated the relationship between postural sway and contact forces at the fingertip while subjects touched a rigid metal bar. Subjects were tested in the tandem Romberg stance with eyes open or closed under three conditions of fingertip contact: no contact, touch contact (< 0.98 N of force), and force contact (as much force as desired). Touch contact was as effective as force contact or sight of the surroundings in reducing postural sway when compared to the no contact, eyes closed condition. Body sway and fingertip forces were essentially in phase with force contact, suggesting that fingertip contact forces are physically counteracting body sway. Time delays between body sway and fingertip forces were much larger with light touch contact, suggesting that the fingertip is providing information that allows anticipatory innervation of musculature to reduce body sway. The results are related to observations on precision grip as well as the somatosensory, proprioceptive, and motor mechanisms involved in the reduction of body sway.
Encoding of head acceleration in vestibular neurons. I. Spatiotemporal response properties to linear acceleration
1. Extracellular recordings were made in and around the medial vestibular nuclei in decerebrated rats. Neurons were functionally identified according to their semicircular canal input on the basis of their responses to angular head rotations around the yaw, pitch, and roll head axes. Those cells responding to angular acceleration were classified as either horizontal semicircular canal-related (HC) or vertical semicircular canal-related (VC) neurons. The HC neurons were further characterized as either type I or type II, depending on the direction of rotation producing excitation. Cells that lacked a response to angular head acceleration, but exhibited sensitivity to a change in head position, were classified as purely otolith organ-related (OTO) neurons. All vestibular neurons were then tested for their response to sinusoidal linear translation in the horizontal head plane. 2. Convergence of macular and canal inputs onto central vestibular nuclei neurons occurred in 73% of the type I HC, 79% of the type II HC, and 86% of the VC neurons. Out of the 223 neurons identified as receiving macular input, 94 neurons were further studied, and their spatiotemporal response properties to sinusoidal stimulation with pure linear acceleration were quantified. Data were obtained from 33 type I HC, 22 type II HC, 22 VC, and 17 OTO neurons. 3. For each neuron the angle of the translational stimulus vector was varied by 15, 30, or 45 degrees increments in the horizontal head plane. In all tested neurons, a direction of maximum sensitivity was identified. An interesting difference among neurons was their response to translation along the direction perpendicular to that that produced the maximum response ("null" direction). For the majority of neurons tested, it was possible to evoke a nonzero response during stimulation along the null direction always had response phases that varied as a function of stimulus direction. 4. These spatiotemporal response properties were quantified in two independent ways. First, the data were evaluated on the basis of the traditional one-dimensional principle governed by the "cosine gain rule" and constant response phase at different stimulus orientations. Second, the response gain and phase values that were empirically determined for each orientation of the applied linear stimulus vector were fitted on the basis of a newly developed formalism that treats neuronal responses as exhibiting two-dimensional spatial sensitivity. Thus two response vectors were determined for each neuron on the basis of its response gain and phase at different stimulus directions in the horizontal head plane.(ABSTRACT TRUNCATED AT 400 WORDS).
Two-dimensional spatiotemporal coding of linear acceleration in vestibular nuclei neurons
Response properties of vertical (VC) and horizontal (HC) canal/otolith-convergent vestibular nuclei neurons were studied in decerebrate rats during stimulation with sinusoidal linear accelerations (0.2-1.4 Hz) along different directions in the head horizontal plane. A novel characteristic of the majority of tested neurons was the nonzero response often elicited during stimulation along the "null" direction (i.e., the direction perpendicular to the maximum sensitivity vector, Smax). The tuning ratio (Smin gain/Smax gain), a measure of the two-dimensional spatial sensitivity, depended on stimulus frequency. For most vestibular nuclei neurons, the tuning ratio was small at the lowest stimulus frequencies and progressively increased with frequency. Specifically, HC neurons were characterized by a flat Smax gain and an approximately 10-fold increase of Smin gain per frequency decade. Thus, these neurons encode linear acceleration when stimulated along their maximum sensitivity direction, and the rate of change of linear acceleration (jerk) when stimulated along their minimum sensitivity direction. While the Smax vectors were distributed throughout the horizontal plane, the Smin vectors were concentrated mainly ipsilaterally with respect to head acceleration and clustered around the naso-occipital head axis. The properties of VC neurons were distinctly different from those of HC cells. The majority of VC cells showed decreasing Smax gains and small, relatively flat, Smin gains as a function of frequency. The Smax vectors were distributed ipsilaterally relative to the induced (apparent) head tilt. In type I anterior or posterior VC neurons, Smax vectors were clustered around the projection of the respective ipsilateral canal plane onto the horizontal head plane. These distinct spatial and temporal properties of HC and VC neurons during linear acceleration are compatible with the spatiotemporal organization of the horizontal and the vertical/torsional ocular responses, respectively, elicited in the rat during linear translation in the horizontal head plane. In addition, the data suggest a spatially and temporally specific and selective otolith/canal convergence. We propose that the central otolith system is organized in canal coordinates such that there is a close alignment between the plane of angular acceleration (canal) sensitivity and the plane of linear acceleration (otolith) sensitivity in otolith/canal-convergent vestibular nuclei neurons.
Horizontal angular VOR, nystagmus dumping, and sensation duration in spacelab SLS-1 crewmembers
In 1G, the apparent time constant (Td) of postrotatory SPV decay with the head tilted face down is 55% of that with head erect (Te). This phenomenon is called "nystagmus dumping" and has been attributed to G effects on VOR velocity storage. Similarly, postrotatory sensation duration with head tilted (Dd) is 32% of that when head erect (De). In parabolic flight, Te and De are 70% of 1-G values, but a pitch back dumping movement produces no further change. Te, Td, and Dd have not previously been measured in orbital flight. VOR and sensation duration was tested in 4 crewmembers in 4 preflight, 1 inflight (days 4 or 5) and 4 post flight sessions. Bitemporal EOG was recorded with eyes open in darkness. Instructions were to "gaze straight ahead," and indicate when "rotation sensation disappears or becomes ambiguous". Subjects were rotated CW and CCW head erect for 1 min at 120 degrees/s, stopped, and EOG was recorded for another 1 min. This procedure was then used to study dumping, except that immediately after chair stop, subjects pitched their head forward 90 degrees. SPV was calculated using order statistic filtering, and dropouts removed using an iterative model fitting method. Te and Td were determined by logarithmic linear regression of mean SPV for each subject. In orbit, 90 degrees pitch movement produced rapid subjective dumping, but not nystagmus dumping. Dd was noticeably shorter ("almost instantaneous") compared to preflight Dd. Te and Td in orbit were similar to preflight Te for 3/4 subjects (rather than to preflight Td as expected). No consistent VOR gain changes were seen in orbit. Although Te is known to decrease acutely in parabolic flight, a longer time constant was measured in 3/4 subjects after 4-5 days adaptation to weightlessness, suggesting a return of angular velocity storage.
A multidimensional model of the effect of gravity on the spatial orientation of the monkey
A "sensory conflict" model of spatial orientation was developed. This mathematical model was based on concepts derived from observer theory, optimal observer theory, and the mathematical properties of coordinate rotations. The primary hypothesis is that the central nervous system of the squirrel monkey incorporates information about body dynamics and sensory dynamics to develop an internal model. The output of this central model (expected sensory afference) is compared to the actual sensory afference, with the difference defined as "sensory conflict." The sensory conflict information is, in turn, used to drive central estimates of angular velocity ("velocity storage"), gravity ("gravity storage"), and linear acceleration ("acceleration storage") toward more accurate values. The model successfully predicts "velocity storage" during rotation about an earth-vertical axis. The model also successfully predicts that the time constant of the horizontal vestibulo-ocular reflex is reduced and that the axis of eye rotation shifts toward alignment with gravity following postrotatory tilt. Finally, the model predicts the bias, modulation, and decay components that have been observed during off-vertical axis rotations (OVAR).