Biomedical subjects
A Berthoz
Publications and source records attributed to A Berthoz.
Functional MRI of galvanic vestibular stimulation.
The cortical processing of vestibular information is not hierarchically organized as the processing of signals in the visual and auditory modalities. Anatomic and electrophysiological studies in the monkey revealed the existence of multiple interconnected areas in which vestibular signals converge with visual and/or somatosensory inputs. Although recent functional imaging studies using caloric vestibular stimulation (CVS) suggest that vestibular signals in the human cerebral cortex may be similarly distributed, some areas that apparently form essential constituents of the monkey cortical vestibular system have not yet been identified in humans. Galvanic vestibular stimulation (GVS) has been used for almost 200 years for the exploration of the vestibular system. By contrast with CVS, which mediates its effects mainly via the semicircular canals (SCC), GVS has been shown to act equally on SCC and otolith afferents. Because galvanic stimuli can be controlled precisely, GVS is suited ideally for the investigation of the vestibular cortex by means of functional imaging techniques. We studied the brain areas activated by sinusoidal GVS using functional magnetic resonance imaging (fMRI). An adapted set-up including LC filters tuned for resonance at the Larmor frequency protected the volunteers against burns through radio-frequency pickup by the stimulation electrodes. Control experiments ensured that potentially harmful effects or degradation of the functional images did not occur. Six male, right-handed volunteers participated in the study. In all of them, GVS induced clear perceptions of body movement and moderate cutaneous sensations at the electrode sites. Comparison with anatomic data on the primate cortical vestibular system and with imaging studies using somatosensory stimulation indicated that most activation foci could be related to the vestibular component of the stimulus. Activation appeared in the region of the temporo-parietal junction, the central sulcus, and the intraparietal sulcus. These areas may be analogous to areas PIVC, 3aV, and 2v, respectively, which form in the monkey brain, the "inner vestibular circle". Activation also occurred in premotor regions of the frontal lobe. Although undetected in previous imaging-studies using CVS, involvement of these areas could be predicted from anatomic data showing projections from the anterior ventral part of area 6 to the inner vestibular circle and the vestibular nuclei. Using a simple paradigm, we showed that GVS can be implemented safely in the fMRI environment. Manipulating stimulus waveforms and thus the GVS-induced subjective vestibular sensations in future imaging studies may yield further insights into the cortical processing of vestibular signals.
Parietal and hippocampal contribution to topokinetic and topographic memory.
This paper reviews the involvement of the parietal cortex and the hippocampus in three kinds of spatial memory tasks which all require a memory of a previously experienced movement in space. The first task compared, by means of positron emission tomography (PET) scan techniques, the production, in darkness, of self-paced saccades (SAC) with the reproduction, in darkness, of a previously learned sequence of saccades to visual targets (SEQ). The results show that a bilateral increase of activity was seen in the depth of the intraparietal sulcus and the medial superior parietal cortex (superior parietal gyrus and precuneus) together with the frontal sulcus but only in the SEQ task, which involved memory of the previously seen targets and possibly also motor memory. The second task is the vestibular memory contingent task, which requires that the subject makes, in darkness, a saccade to the remembered position of a visual target after a passively imposed whole-body rotation. Deficits in this task, which involves vestibular memory, were found predominantly in patients with focal vascular lesions in the parieto-insular (vestibular) cortex, the supplementary motor area-supplementary eye field area, and the prefrontal cortex. The third task requires mental navigation from the memory of a previously learned route in a real environment (the city of Orsay in France). A PET scan study has revealed that when subjects were asked to remember visual landmarks there was a bilateral activation of the middle hippocampal regions, left inferior temporal gyrus, left hippocampal regions, precentral gyrus and posterior cingulate gyrus. If the subjects were asked to remember the route, and their movements along this route, bilateral activation of the dorsolateral cortex, posterior hippocampal areas, posterior cingulate gyrus, supplementary motor areas, right middle hippocampal areas, left precuneus, middle occipital gyrus, fusiform gyrus and lateral premotor area was found. Subtraction between the two conditions reduced the activated areas to the left hippocampus, precuneus and insula. These data suggest that the hippocampus and parietal cortex are both involved in the dynamic aspects of spatial memory, for which the name 'topokinetic memory' is proposed. These dynamic aspects could both overlap and be different from those involved in the cartographic and static aspects of 'topographic' memory.
The contribution of otoliths and semicircular canals to the perception of two-dimensional passive whole-body motion in humans.
1. Perception of two-dimensional (2-D) whole-body passive motion in the horizontal plane was studied in twelve blindfolded healthy volunteers: pure rotation in place (180 deg), linear motion (4.5 m) and a semicircular trajectory (radius, 1.5 m; angular acceleration, 0.2 rad s-2) were applied in random sequence by means of a remote-controlled robot equipped with a racing-car seat. The seat orientation in the horizontal plane was controlled by the experimenter, independent of the robot trajectory. Thus different degrees of otolith-canal interaction were obtained. The maximal linear acceleration during the semicircular trajectory was 0.1 g; however, the linear acceleration vector was complex as it rotated relative to the subject's head. 2. In the first of two sessions, subjects were instructed to maintain an angular pointer oriented towards a remote (15 m) previously seen target during the passive movements. In the second session they had to make a drawing of the path of the perceived trajectory, after the movement was finished. 3. The results showed that, on average, the movement of the pointer matched the dynamics of the rotatory component of the 2-D motion well. This suggests that, in the range of linear accelerations used in this study, no appreciable influence of otolith input on canal-mediated perception of angular motion occurred. 4. The curvature of the drawn paths was mostly explained by the input to the semicircular canals. Subjects' reconstruction of motion did not account for the directional dynamics of the input to the otoliths occurring during passive motion. 5. This finding proves that reconstructing trajectory in space does not imply a mathematically perfect transformation of the linear and angular motion-related inputs into a Cartesian or polar 2-D representation. Physiological constraints on the interaction between motion direction and change of heading play an important role in motion perception.
Mental navigation along memorized routes activates the hippocampus, precuneus, and insula.
Positron emission tomography was used to investigate the functional anatomy of mental simulation of routes (MSR) in five normal volunteers. Normalized regional cerebral blood flow was measured while subjects mentally navigated between landmarks of a route which had been previously learned by actual navigation. This task was contrasted with both static visual imagery of landmarks (VIL) and silent Rest. MSR appears to be subserved by two distinct networks: a non-specific memory network including the posterior and middle parts of the hippocampal regions, the dorsolateral prefrontal cortex and the posterior cingulum, and a specific mental navigation network, comprising the left precuneus, insula and medial part of the hippocampal regions.
Circular trajectory formation during blind locomotion: a test for path integration and motor memory.
Eight healthy subjects were asked to walk blindfolded along circular paths of different radii after several practice trials with vision. Their task was to stop after completing two full revolutions. They always walked counter-clockwise (CCW) in (a) a control condition (CONTROL), including the instructions mentioned above, (b) with the further instruction to count backwards in twos (MENTAL), (c) with the instruction to count loudly (LOUD). The movement of two markers lying along the head naso-occipital axis was recorded by means of an ELITE system. Total walked distance (DISTANCE), total head turning angle (ANGLE) and average radius (RADIUS) of the trajectories performed were measured. All subjects were able to perform approximately circular trajectories. They consistently overshot the ideal radius independently of the condition and circle size, undershot the total angle and overshot total distance. The LOUD condition induced greater errors in the performance but only on total distance (P<0.05). A strong correlation was found between the errors in radius and total distance but not between distance and total angle. Principal components analysis suggested that radius and distance share a common source of errors while total angle produced independent errors. The results indicate that (a) circular trajectories can be generated starting from spatial and/or motor memory, without the aid of visual information; (b) the task needs some attentional control and does not involve simple automatic processing of afferent information; (c) different sensory information or different processing modes are probably involved in the estimation of the curvature and length of the walked path on the one hand, and of the total rotation angle on the other.
Spatial orientation in humans: perception of angular whole-body displacements in two-dimensional trajectories.
Vestibular perception of whole-body passive rotation in the horizontal plane was studied by applying two-dimensional (2D) motion to eight blindfolded healthy volunteers: pure rotations in place, corner-like trajectories and arcs of a circular trajectory were randomly applied by means of a remotely controlled robot. Angles embedded in the 2D trajectories were 45 degrees, 90 degrees, 135 degrees and 180 degrees. Stimulation of semicircular canals was the same for all trajectories but was accompanied by concurrent otolith stimulation during circular motion. Subjects participated in two successive experimental sessions. In the first session they were instructed to use a pointer to reproduce the total angular displacement after the motion (REPRODUCTION); in the second session they had to keep pointing towards a remote (15 m) memorised target during the motion (TRACKING). In REPRODUCTION subjects tended to overestimate their rotation angle by 28 +/- 11% (mean +/- SD). There was no systematic effect of the trajectory. Overestimation also occurred when subjects were required to rotate in darkness by 180 degrees (by controlling a joystick). In TRACKING there was virtually no overestimation (6 +/- 17%) and the movement of the pointer matched the dynamics of angular motion. We conclude that (a) the brain can separate and memorise the angular component of complex 2D motion; however, a large inter-individual variability in estimating its amplitude exists; (b) in the range of linear accelerations used in the study, no appreciable effect of otolith-canal perceptual interaction was shown; (c) angular displacements can be dynamically transformed into matched pointing movements; (d) overestimation seems to be typical of delayed judgements of angular displacement and of self-controlled rotations in place. This could be due to the characteristics of the physiological calibration of the vestibular input.
Does the brain use sliding variables for the control of movements?
Delays in the transmission of sensory and motor information prevent errors from being instantaneously available to the central nervous system (CNS) and can reduce the stability of a closed-loop control strategy. On the other hand, the use of a pure feedforward control (inverse dynamics) requires a perfect knowledge of the dynamic behavior of the body and of manipulated objects. Sensory feedback is essential both to accommodate unexpected errors and events and to compensate for uncertainties about the dynamics of the body. Experimental observations concerning the control of posture, gaze and limbs have shown that the CNS certainly uses a combination of closed-loop and open-loop control. Feedforward components of movement, such as eye saccades, occur intermittently and present a stereotyped kinematic profile. In visuo-manual tracking tasks, hand movements exhibit velocity peaks that occur intermittently. When a delay or a slow dynamics are inserted in the visuo-manual control loop, intermittent step-and-hold movements appear clearly in the hand trajectory. In this study, we investigated strategies used by human subjects involved in the control of a particular dynamic system. We found strong evidence for substantial nonlinearities in the commands produced. The presence of step-and-hold movements seemed to be the major source of nonlinearities in the control loop. Furthermore, the stereotyped ballistic-like kinematics of these rapid and corrective movements suggests that they were produced in an open-loop way by the CNS. We analyzed the generation of ballistic movements in the light of sliding control theory assuming that they occurred when a sliding variable exceeded a constant threshold. In this framework, a sliding variable is defined as a composite variable (a combination of the instantaneous tracking error and its temporal derivatives) that fulfills a specific stability criterion. Based on this hypothesis and on the assumption of a constant reaction time, the tracking error and its derivatives should be correlated at a particular time lag before movement onset. A peak of correlation was found for a physiologically plausible reaction time, corresponding to a stable composite variable. The direction and amplitude of the ongoing stereotyped movements seemed also be adjusted in order to minimize this variable. These findings suggest that, during visually guided movements, human subjects attempt to minimize such a composite variable and not the instantaneous error. This minimization seems to be obtained by the execution of stereotyped corrective movements.
Biologically based artificial navigation systems: review and prospects.
Diverse theories of animal navigation aim at explaining how to determine and maintain a course from one place to another in the environment, although each presents a particular perspective with its own terminologies. These vocabularies sometimes overlap, but unfortunately with different meanings. This paper attempts to define precisely the existing concepts and terminologies, so as to describe comprehensively the different theories and models within the same unifying framework. We present navigation strategies within a four-level hierarchical framework based upon levels of complexity of required processing (Guidance, Place recognition-triggered Response, Topological navigation, Metric navigation). This classification is based upon what information is perceived, represented and processed. It contrasts with common distinctions based upon the availability of certain sensors or cues and rather stresses the information structure and content of central processors. We then review computational models of animal navigation, i.e. of animats. These are introduced along with the underlying conceptual basis in biological data drawn from behavioral and physiological experiments, with emphasis on theories of "spatial cognitive maps". The goal is to aid in deriving algorithms based upon insights into these processes, algorithms that can be useful both for psychobiologists and roboticists. The main observation is, however, that despite the fact that all reviewed models claim to have biological inspiration and that some of them explicitly use "Cognitive Map"-like mechanisms, they correspond to different levels of our proposed hierarchy and that none of them exhibits the main capabilities of real "Cognitive Maps"--in Tolman's sense--that is, a robust capacity for detour and shortcut behaviors.
Spatial memory and path integration studied by self-driven passive linear displacement. I. Basic properties.
According to path integration, the brain is able to compute the distance of a traveled path. In this research we applied our previously reported method for studying memory of linear distance, a crucial mechanism in path integration; our method is based on the overt reconstruction of a passive transport. Passive transport is a special case of navigation in which no active control is performed. Blindfolded subjects were first asked to travel 2 m forward, in darkness, by driving with a joystick the robot on which they were seated. The results show that all subjects but two undershot this distance, i.e., overestimated their own displacement. Then, subjects were submitted to a passive linear forward displacement along 2, 4, 6, 8, or 10 m, and had to reproduce the same distance, still blindfolded. The results show that the distance of the stimulus was accurately reproduced, as well as stimulus duration, peak velocity, and velocity profile. In this first condition, the imposed velocity profile was triangular and therefore stimulus distance and duration were correlated. In a second condition, it was shown that distance was correctly reproduced also when the information about stimulus duration was kept constant. Here, different velocity profiles were used as stimuli, and most subjects also reproduced the velocity profile. Statistical analyses indicated that distance was not reproduced as a consequence of duration, peak velocity, or velocity profile reproduction, but was uniquely correlated to stimulus distance. The previous hypothesis of a double integration of the otolith signal to provide a distance estimate can explain our results. There was a large discrepancy between the accuracy with which the subjects matched the velocity profiles and that of distance reproduction. It follows that, whereas the dynamics of passive motion are stored and available to further use, distance is independently estimated. It is concluded that vestibular and somatosensory signals excited by passive transport can be used to build a dynamic as well as a static representation of the traveled path. We found a close quantitative similarity between the present findings on distance reproduction and those obtained from active locomotion experiments in which the same paradigm was used. This resemblance suggests that the two types of navigation tasks draw on common physiological processes and extends the relevance of our results to naturally occurring path integration.
Updating an object's orientation and location during nonvisual navigation: a comparison between two processing modes.
In the present study, we compared the effects of two processing modes on the updating of the location and orientation of a previously viewed object in space during a guided walk without vision. In Experiment 1, in order to measure the error for initial perception of object's orientation, 12 subjects rotated a miniature model until it matched the memorized orientation of its counterpart object in space. In Experiment 2, they attempted either to keep track of the object continuously (in the object-centered [OC] task) or to estimate the object's perspective only at the terminal vantage point given the trajectory they walked (in the trajectory-centered [TC] task). Subjects indicated the location of the object by facing it, and then rotated the model in order to indicate its orientation from the new vantage point. Results showed that, with respect to the TC mode, the OC mode induced a slow-down of the subjects' self-paced locomotion velocity for both linear and angular movements, and a decrease of the latencies as well as smaller absolute errors for the orientation-of-the-object response. Mean signed errors on object's orientation were equivalent for both processing modes, suggesting that the latter induced different allocations of processing resources on a common representation of space updated by "path integration."
Whole-body rotations enhance hippocampal theta rhythmic slow activity in awake rats passively transported on a mobile robot.
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Functional anatomy of a prelearned sequence of horizontal saccades in humans.
We have used positron emission tomography (PET) to study the functional anatomy of the repetition of a prelearned sequence of horizontal saccadic eye movements. Five subjects had to memorize a sequence of six successive horizontal saccades. The subjects were scanned in total darkness under three different conditions: at rest, during the execution of self-paced horizontal saccades, and while repeating a prelearned saccades sequence. The repetition of the prelearned saccades sequence led to specific normalized regional cerebral blood flow (NrCBF) increases at the depth of the superior frontal sulcus as well as at the rostral part of the supplementary motor area, whereas at the parietal level an important activation was observed in the intraparietal sulcus extending up to the precuneus. In addition, it was noticed that compared with the resting control condition, both oculomotor tasks activated a common set of cortical and subcortical areas. At the cortical level, this network was composed of the frontal eye fields, the supplementary eye fields, the median part of the cingulate gyrus, and the insula. At the subcortical level, the lenticular nucleus and the thalamus as well as the cerebellar vermis were activated consistently. A direct comparison of our results with those of other PET studies on spatial vision suggest that the dorsal visuospatial pathway could be extended toward the frontal premotor region. In such a scheme, visuospatial information computed in the intraparietal sulcus would be transmitted to the frontal premotor cortex to optimize a spatial-oriented behavior. This is consistent with the early proposal that perceptual and intentional components of spatial information are mediated through superior parietal and frontal areas, respectively.
The predictive brain: anticipatory control of head direction for the steering of locomotion.
The control of head direction in humans walking along planned circular trajectories was investigated in this study. Five healthy volunteers were asked to walk at a constant speed along circular trajectories in the light and while blindfolded. Head and walking directions were analysed on a real-time basis. Head direction systematically anticipated changes in the direction of locomotion (by about 200 ms). The anticipation interval depended on the curvature of the circle. In the light, head orientation was deviated with respect to the walking direction, toward the inner concavity of the performed trajectory. The results suggest that head direction is controlled on a step-by-step basis in a predictive fashion. A 'go where you look' strategy seems to underlie steering along circular trajectories.
Activation of the hippocampal formation by vestibular stimulation: a functional magnetic resonance imaging study.
Functional MRI (f-MRI) is a non-invasive technique developed to permit functional mapping of the brain with a better temporal and spatial resolution than that offered by PET techniques. In our study, f-MRI was performed using blood oxygenation level dependent (BOLD) contrast imaging based on the magnetic properties of hemoglobin. This method relies on changes in the blood supply to the brain that accompany sensory stimulation or changes in cognitive state. All the images were obtained at 1.5 T on a Signa GEMS without ultrafast imaging. The vestibular stimulation was cold irrigation of the external auditory meatus (caloric stimulation). A population of normal healthy volunteers without a history of vestibular dysfunction was studied. The hippocampal formation as well as the retrosplenial cortex and the subiculum were activated by vestibular stimulation, suggesting that this activation may be related to spatial disorientation and a sensation of self-rotation experienced by the subjects during vestibular stimulation. The other results are similar to those obtained using PET.
Place- and behavior-independent sensory triggered discharges in rat hippocampal CA1 complex spike cells.
To test for access of spatial cues to the hippocampus of unrestrained animals, single unit recordings of CA1 complex spike cells were made in thirsty rats as they made alternating visits between the center and corners of an enclosed 60 x 60 cm square arena. At intervals, all lights were turned off in the arena and it was rotated. Although no neuronal discharge activity was found that encoded the rotation angle, 11 of 97 neurons were selectively activated after lights were turned off or on. This activity began at delays of up to several seconds and persisted for tens of seconds. These discharges had no location selectivity or behavioral correlates and continued even as the rat performed several behaviors in different parts of the arena. This confirms similar results in restrained rabbits while showing for the first time that this neuronal activity can be independent of place and behavior. In addition this shows that sensory stimuli can trigger hippocampal discharges even when the rat is not required to make any behavioral responses to them.
Quantitative analysis of human walking trajectory on a circular path in darkness.
Thirteen normal (eight young and five older) subjects and a patient who was removed left sided acoustic neurinoma were tested to walk blindfolded along circular paths. They were asked to walk completing two revolutions and to stop when they judged they had returned to the initial position with their head faced to the initial directions. Movements of two markers on the subjects head were recorded by three dimensional motion analyzing system (ELITE system) at 50 Hz which allowed us to measure (a) total walked distance, (b) average radius of the trajectory, and (c) cumulative angle of rotation. Eight young subjects were tested on three circles with radii 0.5, 0.9, and 1.15 m, in two conditions (control, and with mental arythmetic), only to clockwise direction. Five older subjects and a patient were tested on a circle of 0.9 m radius in two conditions, but to both directions, counterclockwise and clockwise. Walked trajectories of young subjects were smooth, whereas those of older subjects tended to be polygonal. Young subjects overshot the ideal distance (6.6%) and ideal radius (9.5%), whereas they undershot the ideal angle (5.1%). There was no effect of circle size or condition on these variables. On the other hand, there was a significant effect of condition on average radius in the older group. The performance of older subjects seemed to be affected by the concurrent mental task. Comparing the counterclockwise walk, the older subjects undershot the turning angle much more than the young subjects which suggest deficits in the vestibular function with aging. The patient showed larger radius and smaller angle while she turned to the healthy side (clockwise) than to the affected side (counterclockwise). Lack of unilateral vestibular information seemed to have affected the circular walking trajectory.
The role of inhibition in the hierarchical gating of executed and imagined movements.
A theory is presented concerning the neuronal mechanisms which may underlie the organisation of imagined versus executed movements. A review is first presented of previous theoretical and experimental evidence suggesting that the brain can use the same mechanisms for the imagination and the execution of movement. In particular the fact that adaptation of the vestibulo-ocular reflex can be obtained by pure mental effort and not solely by conflicting visual and vestibular cues has been suggestive of the fact that the brain could internally simulate conflicts and use the same adaptive mechanisms used when actual sensory cues were in conflict. The saccadic system is taken as a good model for the study of this question because the mechanisms which underlie saccade generation are now partially understood at different levels from the brain stem to the cortex. The central idea of the theory is based upon the fact that, in parallel with the excitatory mechanisms underlying saccade generation, several inhibitory mechanisms in cascade allow the selective modulation and blockage of saccades. Synaptic inhibition is therefore supposed to play a major role in a hierarchical selective gating of saccade execution not at one but at several levels allowing a variety of different types of "imagined movements' some involving only the higher levels some in which the execution is only blocked at the very immediate premotor level. But in all cases the theory proposes that imagination and execution have many mechanisms in common. PET data showing that indeed the same structures are activated in both types of movements support this idea although the final answer will have to be brought by neuronal data.