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Training, transfer, and retention of three-dimensional spatial memory in virtual environments

Human orientation requires one to remember and visualize spatial arrangements of landmarks from different perspectives. Astronauts have reported difficulties remembering relationships between environmental landmarks when imagined in arbitrary 3D orientations. The present study investigated the effects of strategy training on humans' 1) ability to infer their orientation from landmarks presented ahead and below, 2) performance when subsequently learning a different array, and 3) retention of configurational knowledge over time. On the first experiment day, 24 subjects were tested in a virtual cubic chamber in which a picture of an animal was drawn on each wall. Through trial-by-trial exposures, they had to memorize the spatial relationships among the six pictures around them and learn to predict the direction to a specific picture when facing any view direction, and in any roll orientation. Half of the subjects ("strategy group") were taught methods for remembering picture groupings, while the remainder received no such training ("control group"). After learning one picture array, the procedure was repeated in a second. Accuracy (% correct) and response time learning curves were measured. Performance for the second array and configurational memory of both arrays were also retested 1, 7, and 30 days later. Results showed that subjects "learned how to learn" this generic 3D spatial memory task regardless of their relative orientation to the environment, that ability and configurational knowledge was retained for at least a month, that figure rotation ability and field independence correlate with performance, and that teaching subjects specific strategies in advance significantly improves performance. Training astronauts to perform a similar generic 3D spatial memory task, and suggesting strategies in advance, may help them orient in three dimensions.

Non-NASA Center

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.

NASA Discipline Neuroscience

Rapid motor learning in the translational vestibulo-ocular reflex

Motor learning was induced in the translational vestibulo-ocular reflex (TVOR) when monkeys were repeatedly subjected to a brief (0.5 sec) head translation while they tried to maintain binocular fixation on a visual target for juice rewards. If the target was world-fixed, the initial eye speed of the TVOR gradually increased; if the target was head-fixed, the initial eye speed of the TVOR gradually decreased. The rate of learning acquisition was very rapid, with a time constant of approximately 100 trials, which was equivalent to <1 min of accumulated stimulation. These learned changes were consolidated over >or=1 d without any reinforcement, indicating induction of long-term synaptic plasticity. Although the learning generalized to targets with different viewing distances and to head translations with different accelerations, it was highly specific for the particular combination of head motion and evoked eye movement associated with the training. For example, it was specific to the modality of the stimulus (translation vs rotation) and the direction of the evoked eye movement in the training. Furthermore, when one eye was aligned with the heading direction so that it remained motionless during training, learning was not expressed in this eye, but only in the other nonaligned eye. These specificities show that the learning sites are neither in the sensory nor the motor limb of the reflex but in the sensory-motor transformation stage of the reflex. The dependence of the learning on both head motion and evoked eye movement suggests that Hebbian learning may be one of the underlying cellular mechanisms.

Non-NASA Center

Transcriptional profiling reveals regulated genes in the hippocampus during memory formation

Transcriptional profiling (TP) offers a powerful approach to identify genes activated during memory formation and, by inference, the molecular pathways involved. Trace eyeblink conditioning is well suited for the study of regional gene expression because it requires the hippocampus, whereas the highly parallel task, delay conditioning, does not. First, we determined when gene expression was most regulated during trace conditioning. Rats were exposed to 200 trials per day of paired and unpaired stimuli each day for 4 days. Changes in gene expression were most apparent 24 h after exposure to 200 trials. Therefore, we profiled gene expression in the hippocampus 24 h after 200 trials of trace eyeblink conditioning, on multiple arrays using additional animals. Of 1,186 genes on the filter array, seven genes met the statistical criteria and were also validated by real-time polymerase chain reaction. These genes were growth hormone (GH), c-kit receptor tyrosine kinase (c-kit), glutamate receptor, metabotropic 5 (mGluR5), nerve growth factor-beta (NGF-beta), Jun oncogene (c-Jun), transmembrane receptor Unc5H1 (UNC5H1), and transmembrane receptor Unc5H2 (UNC5H2). All these genes, except for GH, were downregulated in response to trace conditioning. GH was upregulated; therefore, we also validated the downregulation of the GH inhibitor, somatostatin (SST), even though it just failed to meet criteria on the arrays. By during situ hybridization, GH was expressed throughout the cell layers of the hippocampus in response to trace conditioning. None of the genes regulated in trace eyeblink conditioning were similarly affected by delay conditioning, a task that does not require the hippocampus. These findings demonstrate that transcriptional profiling can exhibit a repertoire of genes sensitive to the formation of hippocampal-dependent associative memories.

Non-NASA Center

Spatial learning and memory is preserved in rats after early development in a microgravity environment

This study evaluated the cognitive mapping abilities of rats that spent part of their early development in a microgravity environment. Litters of male and female Sprague-Dawley rat pups were launched into space aboard the National Aeronautics and Space Administration space shuttle Columbia on postnatal day 8 or 14 and remained in space for 16 days. These animals were designated as FLT groups. Two age-matched control groups remained on Earth: those in standard vivarium housing (VIV) and those in housing identical to that aboard the shuttle (AGC). On return to Earth, animals were tested in three different tasks that measure spatial learning ability, the Morris water maze (MWM), and a modified version of the radial arm maze (RAM). Animals were also tested in an open field apparatus to measure general activity and exploratory activity. Performance and search strategies were evaluated in each of these tasks using an automated tracking system. Despite the dramatic differences in early experience, there were remarkably few differences between the FLT groups and their Earth-bound controls in these tasks. FLT animals learned the MWM and RAM as quickly as did controls. Evaluation of search patterns suggested subtle differences in patterns of exploration and in the strategies used to solve the tasks during the first few days of testing, but these differences normalized rapidly. Together, these data suggest that development in an environment without gravity has minimal long-term impact on spatial learning and memory abilities. Any differences due to development in microgravity are quickly reversed after return to earth normal gravity.

NASA Discipline Neuroscience

Relationship between alertness, performance, and body temperature in humans

Body temperature has been reported to influence human performance. Performance is reported to be better when body temperature is high/near its circadian peak and worse when body temperature is low/near its circadian minimum. We assessed whether this relationship between performance and body temperature reflects the regulation of both the internal biological timekeeping system and/or the influence of body temperature on performance independent of circadian phase. Fourteen subjects participated in a forced desynchrony protocol allowing assessment of the relationship between body temperature and performance while controlling for circadian phase and hours awake. Most neurobehavioral measures varied as a function of internal biological time and duration of wakefulness. A number of performance measures were better when body temperature was elevated, including working memory, subjective alertness, visual attention, and the slowest 10% of reaction times. These findings demonstrate that an increased body temperature, associated with and independent of internal biological time, is correlated with improved performance and alertness. These results support the hypothesis that body temperature modulates neurobehavioral function in humans.

Non-NASA Center

Prospective memory in dynamic environments: effects of load, delay, and phonological rehearsal

A new paradigm was developed to examine prospective memory performance in a visual-spatial task that resembles some aspects of the work of air traffic controllers. Two experiments examined the role of workload (number of aeroplanes that participants directed), delay (between receipt of prospective instructions and execution), and phonological rehearsal. High workload increased prospective memory errors but increasing delay from 1-3 or 5 minutes had no effect. Shadowing aurally presented text reduced prospective memory performance, presumably because it prevented verbal rehearsal of the prospective instructions. However, performance on the foreground task of directing aeroplanes to routine destinations was affected only by workload and not by opportunity for rehearsal. Our results suggest that ability to maintain performance on a routine foreground task while performing a secondary task--perhaps analogous to conversation--does not predict ability to retrieve a prospective intention to deviate from the routine.

Aerospace Medicine

Deblurring

In most instances, traditional EEG methodology provides insufficient spatial detail to identify relationships between brain electrical events and structures and functions visualized by magnetic resonance imaging or positron emission tomography. This article describes a method called Deblurring for increasing the spatial detail of the EEG and for fusing neurophysiologic and neuroanatomic data. Deblurring estimates potentials near the outer convexity of the cortex using a realistic finite element model of the structure of a subject's head determined from their magnetic resonance images. Deblurring is not a source localization technique and thus makes no assumptions about the number or type of generator sources. The validity of Deblurring has been initially tested by comparing deblurred data with potentials measured with subdural grid recordings. Results suggest that deblurred topographic maps, registered with a subject's magnetic resonance imaging and rendered in three dimensions, provide better spatial detail than has heretofore been obtained with scalp EEG recordings. Example results are presented from research studies of somatosensory stimulation, movement, language, attention and working memory. Deblurred ictal EEG data are also presented, indicating that this technique may have future clinical application as an aid to seizure localization and surgical planning.

Non-NASA Center

The effect of visual context on manual localization of remembered targets

This paper examines the contribution of egocentric cues and visual context to manual localization of remembered targets. Subjects pointed in the dark to the remembered position of a target previously viewed without or within a structured visual scene. Without a remembered visual context, subjects pointed to within 2 degrees of the target. The presence of a visual context with cues of straight ahead enhanced pointing performance to the remembered location of central but not off-center targets. Thus, visual context provides strong visual cues of target position and the relationship of body position to target location. Without a visual context, egocentric cues provide sufficient input for accurate pointing to remembered targets.

NASA Center JSC

Saccades to remembered targets: the effects of smooth pursuit and illusory stimulus motion

1. Measurements were made in four normal human subjects of the accuracy of saccades to remembered locations of targets that were flashed on a 20 x 30 deg random dot display that was either stationary or moving horizontally and sinusoidally at +/-9 deg at 0.3 Hz. During the interval between the target flash and the memory-guided saccade, the "memory period" (1.4 s), subjects either fixated a stationary spot or pursued a spot moving vertically sinusoidally at +/-9 deg at 0.3 Hz. 2. When saccades were made toward the location of targets previously flashed on a stationary background as subjects fixated the stationary spot, median saccadic error was 0.93 deg horizontally and 1.1 deg vertically. These errors were greater than for saccades to visible targets, which had median values of 0.59 deg horizontally and 0.60 deg vertically. 3. When targets were flashed as subjects smoothly pursued a spot that moved vertically across the stationary background, median saccadic error was 1.1 deg horizontally and 1.2 deg vertically, thus being of similar accuracy to when targets were flashed during fixation. In addition, the vertical component of the memory-guided saccade was much more closely correlated with the "spatial error" than with the "retinal error"; this indicated that, when programming the saccade, the brain had taken into account eye movements that occurred during the memory period. 4. When saccades were made to targets flashed during attempted fixation of a stationary spot on a horizontally moving background, a condition that produces a weak Duncker-type illusion of horizontal movement of the primary target, median saccadic error increased horizontally to 3.2 deg but was 1.1 deg vertically. 5. When targets were flashed as subjects smoothly pursued a spot that moved vertically on the horizontally moving background, a condition that induces a strong illusion of diagonal target motion, median saccadic error was 4.0 deg horizontally and 1.5 deg vertically; thus the horizontal error was greater than under any other experimental condition. 6. In most trials, the initial saccade to the remembered target was followed by additional saccades while the subject was still in darkness. These secondary saccades, which were executed in the absence of visual feedback, brought the eye closer to the target location. During paradigms involving horizontal background movement, these corrections were more prominent horizontally than vertically. 7. Further measurements were made in two subjects to determine whether inaccuracy of memory-guided saccades, in the horizontal plane, was due to mislocalization at the time that the target flashed, misrepresentation of the trajectory of the pursuit eye movement during the memory period, or both. 8. The magnitude of the saccadic error, both with and without corrections made in darkness, was mislocalized by approximately 30% of the displacement of the background at the time that the target flashed. The magnitude of the saccadic error also was influenced by net movement of the background during the memory period, corresponding to approximately 25% of net background movement for the initial saccade and approximately 13% for the final eye position achieved in darkness. 9. We formulated simple linear models to test specific hypotheses about which combinations of signals best describe the observed saccadic amplitudes. We tested the possibilities that the brain made an accurate memory of target location and a reliable representation of the eye movement during the memory period, or that one or both of these was corrupted by the illusory visual stimulus. Our data were best accounted for by a model in which both the working memory of target location and the internal representation of the horizontal eye movements were corrupted by the illusory visual stimulus. We conclude that extraretinal signals played only a minor role, in comparison with visual estimates of the direction of gaze, in planning eye movements to remembered targ.

Clinical Trial