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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

Sensorimotor aspects of high-speed artificial gravity: I. Sensory conflict in vestibular adaptation

Short-radius centrifugation offers a promising and affordable countermeasure to the adverse effects of prolonged weightlessness. However, head movements made in a fast rotating environment elicit Coriolis effects, which seriously compromise sensory and motor processes. We found that participants can adapt to these Coriolis effects when exposed intermittently to high rotation rates and, at the same time, can maintain their perceptual-motor coordination in stationary environments. In this paper, we explore the role of inter-sensory conflict in this adaptation process. Different measures (vertical nystagmus, illusory body tilt, motion sickness) react differently to visual-vestibular conflict and adapt differently. In particular, proprioceptive-vestibular conflict sufficed to adapt subjective parameters and the time constant of nystagmus decay, while retinal slip was required for VOR gain adaptation. A simple correlation between the strength of intersensory conflict and the efficacy of adaptation fails to explain the data. Implications of these findings, which differ from existing data for low rotation rates, are discussed.

Non-NASA Center

Multiple subclasses of Purkinje cells in the primate floccular complex provide similar signals to guide learning in the vestibulo-ocular reflex

The neural "learning rules" governing the induction of plasticity in the cerebellum were analyzed by recording the patterns of neural activity in awake, behaving animals during stimuli that induce a form of cerebellum-dependent learning. We recorded the simple- and complex-spike responses of a broad sample of Purkinje cells in the floccular complex during a number of stimulus conditions that induce motor learning in the vestibulo-ocular reflex (VOR). Each subclass of Purkinje cells carried essentially the same information about required changes in the gain of the VOR. The correlation of simple-spike activity in Purkinje cells with activity in vestibular pathways could guide learning during low-frequency but not high-frequency stimuli. Climbing fiber activity could guide learning during all stimuli tested but only if compared with the activity present approximately 100 msec earlier in either vestibular pathways or Purkinje cells.

Non-NASA Center

Dynamics of the human linear vestibulo-ocular reflex at medium frequency and modification by short-term training

We study here the effect of a short-term training paradigm on the gain and phase of the human translational VOR (the linear VOR: LVOR). Subjects were exposed to lateral sinusoidal translations on a sled, at 0.5 Hz, 0.3 g peak acceleration. With subjects tracking a remembered target at 1.2 m, the LVOR (slow-phase) under these conditions typically has a phase lead or lag, and a gain that falls short of compensatory. To induce short-term adaptation (training), we presented an earth-fixed visual scene at 1.2 m during sinusoidal translation (x 1 viewing) for 20 minutes, so as to drive the LVOR toward compensatory phase and gain. We examined both the slow-phase and the saccadic responses to these stimuli. Testing after training showed changes in slow-component gain and phase which were mostly but not always in the compensatory direction. These changes were more consistent in naive subjects than in subjects who had previous LVOR experience. Changes in gain were seen with step as well as sinusoidal test stimuli; gain changes were not correlated with vergence changes. There was a strong correlation between gain changes and phase changes across subjects. Fast phases (catch-up saccades) formed a large component of the LVOR under our testing conditions (approximately 30% of the changes in gain but not in phase due to training.

Non-NASA Center

Detection in fixed and random noise in foveal and parafoveal vision explained by template learning

Foveal and parafoveal contrast detection thresholds for Gabor and checkerboard targets were measured in white noise by means of a two-interval forced-choice paradigm. Two white-noise conditions were used: fixed and twin. In the fixed noise condition a single noise sample was presented in both intervals of all the trials. In the twin noise condition the same noise sample was used in the two intervals of a trial, but a new sample was generated for each trial. Fixed noise conditions usually resulted in lower thresholds than twin noise. Template learning models are presented that attribute this advantage of fixed over twin noise either to fixed memory templates' reducing uncertainty by incorporation of the noise or to the introduction, by the learning process itself, of more variability in the twin noise condition. Quantitative predictions of the template learning process show that it contributes to the accelerating nonlinear increase in performance with signal amplitude at low signal-to-noise ratios.

NASA Center ARC

Neural learning rules for the vestibulo-ocular reflex

Mechanisms for the induction of motor learning in the vestibulo-ocular reflex (VOR) were evaluated by recording the patterns of neural activity elicited in the cerebellum by a range of stimuli that induce learning. Patterns of climbing-fiber, vestibular, and Purkinje cell simple-spike signals were examined during sinusoidal head movement paired with visual image movement at stimulus frequencies from 0.5 to 10 Hz. A comparison of simple-spike and vestibular signals contained the information required to guide learning only at low stimulus frequencies, and a comparison of climbing-fiber and simple-spike signals contained the information required to guide learning only at high stimulus frequencies. Learning could be guided by comparison of climbing-fiber and vestibular signals at all stimulus frequencies tested, but only if climbing fiber responses were compared with the vestibular signals present 100 msec earlier. Computational analysis demonstrated that this conclusion is valid even if there is a broad range of vestibular signals at the site of plasticity. Simulations also indicated that the comparison of vestibular and climbing-fiber signals across the 100 msec delay must be implemented by a subcellular "eligibility" trace rather than by neural circuits that delay the vestibular inputs to the site of plasticity. The results suggest two alternative accounts of learning in the VOR. Either there are multiple mechanisms of learning that use different combinations of neural signals to drive plasticity, or there is a single mechanism tuned to climbing-fiber activity that follows activity in vestibular pathways by approximately 100 msec.

NASA Discipline Neuroscience

Working and strategic memory deficits in schizophrenia

Working memory and its contribution to performance on strategic memory tests in schizophrenia were studied. Patients (n = 18) and control participants (n = 15), all men, received tests of immediate memory (forward digit span), working memory (listening, computation, and backward digit span), and long-term strategic (free recall, temporal order, and self-ordered pointing) and nonstrategic (recognition) memory. Schizophrenia patients performed worse on all tests. Education, verbal intelligence, and immediate memory capacity did not account for deficits in working memory in schizophrenia patients. Reduced working memory capacity accounted for group differences in strategic memory but not in recognition memory. Working memory impairment may be central to the profile of impaired cognitive performance in schizophrenia and is consistent with hypothesized frontal lobe dysfunction associated with this disease. Additional medial-temporal dysfunction may account for the recognition memory deficit.

Memory Disorders/etiology/physiopathology

Behavioral analysis of signals that guide learned changes in the amplitude and dynamics of the vestibulo-ocular reflex

We characterized the dependence of motor learning in the monkey vestibulo-ocular reflex (VOR) on the duration, frequency, and relative timing of the visual and vestibular stimuli used to induce learning. The amplitude of the VOR was decreased or increased through training with paired head and visual stimulus motion in the same or opposite directions, respectively. For training stimuli that consisted of simultaneous pulses of head and target velocity 80-1000 msec in duration, brief stimuli caused small changes in the amplitude of the VOR, whereas long stimuli caused larger changes in amplitude as well as changes in the dynamics of the reflex. When the relative timing of the visual and vestibular stimuli was varied, brief image motion paired with the beginning of a longer vestibular stimulus caused changes in the amplitude of the reflex alone, but the same image motion paired with a later time in the vestibular stimulus caused changes in the dynamics as well as the amplitude of the VOR. For training stimuli that consisted of sinusoidal head and visual stimulus motion, low-frequency training stimuli induced frequency-selective changes in the VOR, as reported previously, whereas high-frequency training stimuli induced changes in the amplitude of the VOR that were more similar across test frequency. The results suggest that there are at least two distinguishable components of motor learning in the VOR. One component is induced by short-duration or high-frequency stimuli and involves changes in only the amplitude of the reflex. A second component is induced by long-duration or low-frequency stimuli and involves changes in the amplitude and dynamics of the VOR.

NASA Discipline Neuroscience

The cerebellum: a neuronal learning machine?

Comparison of two seemingly quite different behaviors yields a surprisingly consistent picture of the role of the cerebellum in motor learning. Behavioral and physiological data about classical conditioning of the eyelid response and motor learning in the vestibulo-ocular reflex suggests that (i) plasticity is distributed between the cerebellar cortex and the deep cerebellar nuclei; (ii) the cerebellar cortex plays a special role in learning the timing of movement; and (iii) the cerebellar cortex guides learning in the deep nuclei, which may allow learning to be transferred from the cortex to the deep nuclei. Because many of the similarities in the data from the two systems typify general features of cerebellar organization, the cerebellar mechanisms of learning in these two systems may represent principles that apply to many motor systems.

Non-NASA Center

Effects of restricted feeding schedules on circadian organization in squirrel monkeys

Free running circadian rhythms of motor activity, food-motivated lever-pressing, and either drinking (N = 7) or body temperature (N = 3) were recorded from 10 squirrel monkeys maintained in constant illumination with unlimited access to food. Food availability was then restricted to a single unsignaled 3-hour interval each day. The feeding schedule failed to entrain the activity rhythms of 8 monkeys, which continued to free-run. Drinking was almost completely synchronized by the schedule, while body temperature showed a feeding-induced rise superimposed on a free-running rhythm. Nonreinforced lever-pressing showed both a free-running component and a 24-hour component that anticipated the time of feeding. At the termination of the schedule, all recorded variables showed free-running rhythms, but in 3 animals the initial phase of the postschedule rhythms was advanced by several hours, suggesting relative coordination. Of the remaining 2 animals, one exhibited stable entrainment of all 3 recorded rhythms, while the other appeared to entrain temporarily to the feeding schedule. These results indicate that restricted feeding schedules are only a weak zeitgeber for the circadian pacemaker generating free-running rhythms in the squirrel monkey. Such schedules, however, may entrain a separate circadian system responsible for the timing of food-anticipatory changes in behavior and physiology.

Non-NASA Center

Perceptual learning through optimization of attentional weighting: human versus optimal Bayesian learner

Human performance in visual detection, discrimination, identification, and search tasks typically improves with practice. Psychophysical studies suggest that perceptual learning is mediated by an enhancement in the coding of the signal, and physiological studies suggest that it might be related to the plasticity in the weighting or selection of sensory units coding task relevant information (learning through attention optimization). We propose an experimental paradigm (optimal perceptual learning paradigm) to systematically study the dynamics of perceptual learning in humans by allowing comparisons to that of an optimal Bayesian algorithm and a number of suboptimal learning models. We measured improvement in human localization (eight-alternative forced-choice with feedback) performance of a target randomly sampled from four elongated Gaussian targets with different orientations and polarities and kept as a target for a block of four trials. The results suggest that the human perceptual learning can occur within a lapse of four trials (<1 min) but that human learning is slower and incomplete with respect to the optimal algorithm (23.3% reduction in human efficiency from the 1st-to-4th learning trials). The greatest improvement in human performance, occurring from the 1st-to-2nd learning trial, was also present in the optimal observer, and, thus reflects a property inherent to the visual task and not a property particular to the human perceptual learning mechanism. One notable source of human inefficiency is that, unlike the ideal observer, human learning relies more heavily on previous decisions than on the provided feedback, resulting in no human learning on trials following a previous incorrect localization decision. Finally, the proposed theory and paradigm provide a flexible framework for future studies to evaluate the optimality of human learning of other visual cues and/or sensory modalities.

Non-NASA Center