Deficits and recovery in visuospatial memory during head motion after bilateral labyrinthine lesion.
ABSTRACT To keep a stable internal representation of the environment as we move, extraretinal sensory or motor cues are critical for updating neural maps of visual space. Using a memory-saccade task, we studied whether visuospatial updating uses vestibular information. Specifically, we tested whether trained rhesus monkeys maintain the ability to update the conjugate and vergence components of memory-guided eye movements in response to passive translational or rotational head and body movements after bilateral labyrinthine lesion. We found that lesioned animals were acutely compromised in generating the appropriate horizontal versional responses necessary to update the directional goal of memory-guided eye movements after leftward or rightward rotation/translation. This compromised function recovered in the long term, likely using extravestibular (e.g., somatosensory) signals, such that nearly normal performance was observed 4 mo after the lesion. Animals also lost their ability to adjust memory vergence to account for relative distance changes after motion in depth. Not only were these depth deficits larger than the respective effects on version, but they also showed little recovery. We conclude that intact labyrinthine signals are functionally useful for proper visuospatial memory updating during passive head and body movements.
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ABSTRACT: To maintain perception of the world around us during body motion, the brain must update the spatial presentation of visual stimuli, known as space updating. Previous studies have demonstrated that vestibular signals contribute to space updating. Nonetheless, when being passively rotated in the dark, the ability to keep track of a memorized earth-fixed target involves learning mechanism(s). We tested whether such learning generalizes across different earth-fixed target eccentricities. Furthermore, we ascertained whether learning transfers to similar target eccentricities but in the opposite direction. Participants were trained to predict the position of an earth-fixed target (located at 45° to their left) while being rotated counterclockwise (i.e., they press a push button when they perceived that their body midline have cross the position of the target). Overall, the results indicated that learning transferred to other target eccentricity (30° and 60°) for identical body rotation direction. In contrast, vestibular learning partly transferred to target locations matching body rotation but in the opposite rotation direction. Generalization of learning implies that participants do not adopt cognitive strategies to improve their performance during training. We argue that the brain learned to use vestibular signals for space updating. Generalization of learning while being rotated in the opposite direction implies that some parts of the neural networks involved in space updating is shared between trained and untrained direction.Neuroscience 12/2013; · 3.33 Impact Factor
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ABSTRACT: To contribute appropriately to voluntary reaching during body motion, vestibular signals must be transformed from a head- to a body-centered reference frame. We quantitatively investigated the evidence for this transformation during online reach execution by using galvanic vestibular stimulation (GVS) to simulate rotation about a head-fixed, roughly naso-occipital axis as human subjects made planar reaching movements to a remembered location with their head in different orientations. If vestibular signals that contribute to reach execution have been transformed from a head- to a body-centered reference frame, the same stimulation should be interpreted as body tilt with the head upright but as vertical-axis rotation with the head inclined forward. Consequently, GVS should perturb reach trajectories in a head-orientation-dependent way. Consistent with this prediction, GVS applied during reach execution induced trajectory deviations that were significantly larger with the head forward as compared to upright. Only with the head forward were trajectories consistently deviated in opposite directions for rightward versus leftward simulated rotation, as appropriate to compensate for body vertical-axis rotation. These results demonstrate that vestibular signals contributing to online reach execution have indeed been transformed from a head- to a body-centered reference frame. Reach deviation amplitudes were comparable to those predicted for ideal compensation for body rotation using a biomechanical limb model. Finally, by comparing the effects of applying GVS during reach execution versus prior to reach onset we also provide evidence that spatially transformed vestibular signals contribute to at least partially distinct compensation mechanisms for body motion during reach planning versus execution.Journal of Neurophysiology 02/2014; · 3.04 Impact Factor
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ABSTRACT: How does the visuomotor system decide whether a target is moving or stationary in space or whether it moves relative to the eyes or head? A visual flash during a rapid eye-head gaze shift produces a brief visual streak on the retina that could provide information about target motion, when appropriately combined with eye and head self-motion signals. Indeed, double-step experiments have demonstrated that the visuomotor system incorporates actively generated intervening gaze shifts in the final localization response. Also saccades to brief head-fixed flashes during passive whole-body rotation compensate for vestibular-induced ocular nystagmus. However, both the amount of retinal motion to invoke spatial updating and the default strategy in the absence of detectable retinal motion remain unclear. To study these questions, we determined the contribution of retinal motion and the vestibular canals to spatial updating of visual flashes during passive whole-body rotation. Head- and body-restrained humans made saccades toward very brief (0.5 and 4 ms) and long (100 ms) visual flashes during sinusoidal rotation around the vertical body axis in total darkness. Stimuli were either attached to the chair (head-fixed) or stationary in space and were always well localizable. Surprisingly, spatial updating only occurred when retinal stimulus motion provided sufficient information: long-duration stimuli were always appropriately localized, thus adequately compensating for vestibular nystagmus and the passive head movement during the saccade reaction time. For the shortest stimuli, however, the target was kept in retinocentric coordinates, thus ignoring intervening nystagmus and passive head displacement, regardless of whether the target was moving with the head or not.Journal of Neuroscience 07/2011; 31(29):10558-68. · 6.75 Impact Factor