Visual Reafference Research Articles

Paradoxical adaptation of successful movements: The crucial role of internal error signals.

Visuo-motor adaptation has been classically studied using movements aimed at visual targets with visual feedback. In this type of experimental design, the respective roles of the different error signals cannot be fully disentangled. Here, we show that visuo-motor adaptation occurs despite the terminal success of the action and the compensation of the external error by a jump of the visual target. By using three grasping task conditions we manipulated the retinal error signal between the seen hand and the target (external error) and the conflict between the hand's visual reafference and either the proprioceptive or the efference copy signal (internal error), in order to estimate their respective roles in prism adaptation. In all conditions, subjects were asked to rapidly grasp an object. In the classical 'Prism' condition the object was stationary, which provided both external and internal errors. In the 'Prism & Jump' condition, at movement onset the object was suddenly displaced (jump) toward its virtual image location (visually displaced by the prism) which also corresponded to the location where the movement was planned to and executed through prisms. This jump therefore cancelled the external error (between the seen target and the seen hand), whereas the internal error (between the seen hand and the expected visual reafference of the hand, or between the seen hand and the hand felt by proprioception) was unchanged (because it is independent of the presence of the goal). In the 'Jump' condition, the movement was planned and executed without prismatic goggles and consequently with no internal error (no difference between where the hand visual reafference is expected to be and where it actually is), but the object was suddenly displaced at movement onset by a displacement equivalent to a prism shift which provided an external error. The 'Prism' and 'Prism & Jump' conditions exhibited similar aftereffects, whereas no aftereffect was observed in the 'Jump' condition. These results suggest that successful actions can be subjected to adaptation and that internal error is the only signal necessary to elicit true visuomotor adaptation characterized by context-independent generalization.

Distinct fMRI Responses to Self-Induced versus Stimulus Motion during Free Viewing in the Macaque

Visual motion responses in the brain are shaped by two distinct sources: the physical movement of objects in the environment and motion resulting from one's own actions. The latter source, termed visual reafference, stems from movements of the head and body, and in primates from the frequent saccadic eye movements that mark natural vision. To study the relative contribution of reafferent and stimulus motion during natural vision, we measured fMRI activity in the brains of two macaques as they freely viewed >50 hours of naturalistic video footage depicting dynamic social interactions. We used eye movements obtained during scanning to estimate the level of reafferent retinal motion at each moment in time. We also estimated the net stimulus motion by analyzing the video content during the same time periods. Mapping the responses to these distinct sources of retinal motion, we found a striking dissociation in the distribution of visual responses throughout the brain. Reafferent motion drove fMRI activity in the early retinotopic areas V1, V2, V3, and V4, particularly in their central visual field representations, as well as lateral aspects of the caudal inferotemporal cortex (area TEO). However, stimulus motion dominated fMRI responses in the superior temporal sulcus, including areas MT, MST, and FST as well as more rostral areas. We discuss this pronounced separation of motion processing in the context of natural vision, saccadic suppression, and the brain's utilization of corollary discharge signals. Visual motion arises not only from events in the external world, but also from the movements of the observer. For example, even if objects are stationary in the world, the act of walking through a room or shifting one's eyes causes motion on the retina. This "reafferent" motion propagates into the brain as signals that must be interpreted in the context of real object motion. The delineation of whole-brain responses to stimulus versus self-generated retinal motion signals is critical for understanding visual perception and is of pragmatic importance given the increasing use of naturalistic viewing paradigms. The present study uses fMRI to demonstrate that the brain exhibits a fundamentally different pattern of responses to these two sources of retinal motion.

Neuronal responses in MST reflect the post-saccadic enhancement of short-latency ocular following responses

Movements of the visual scene evoke short latency ocular following responses (OFRs) in monkeys that are mediated at least in part by the medial superior temporal area of the cortex (MST). It is known that the sensitivity of the OFR to motion is transiently enhanced immediately after a saccade and this post-saccadic enhancement is largely secondary to visual reafference during the antecedent saccade. As part of an investigation of the neural basis of this post-saccadic enhancement, we examined the dependence of OFR-related neuronal activity in MST on the post-saccadic delay interval in alert monkeys (Macaca fuscata). Large-field motion stimuli were applied either 50 or 150 ms after a centering saccade and response measures were based on the initial (open-loop) changes in (a) eye position and (b) discharge rate. Of the 67% of MST neurons whose OFR-related activity showed significant dependence on the post-saccadic delay, 91% mirrored the OFR, showing higher sensitivity to motion at the shorter post-saccadic delay interval. However, the sensitivity of OFR-related neurons in MST to post-saccadic delay varied considerably from cell to cell and, on average, was 79.6% of that shown by the OFR. We suggest that this enhanced OFR-related activity in the wake of a saccade is causally linked to the visually based post-saccadic enhancement of the OFR.

P.2.20 Nicotine antagonizes caffeine-induced but not pentylenetetrazole-induced anxiogenic effect in mice

Investigation of eye movement-related activities and photic responsiveness using behaving cats demonstrated distinctive representations of eye movement signals in different areas of the lateral suprasylvian cortex: visual reafference in the medial bank of the middle suprasylvian sulcus and non-visual signals (proprioceptive reafference or efference copy) in the lateral bank.

Visual, saccade-related, and cognitive activation of single neurons in monkey extrastriate area V3A.

Area V3A is an extrastriate visual area that provides a major input to parietal cortex. To identify the sensory, saccade-related, and cognitive signals carried by V3A neurons, we recorded from single units in alert monkeys during performance of fixation and memory guided saccade tasks. We found that visual responses to stationary stimuli in area V3A were affected by the behavioral relevance of the stimulus. The amplitude of the visual response differed between the memory-guided saccade task, in which the monkey had to use the information provided by the stimulus to guide its behavior, and the fixation task. For 18% (29/163) of V3A neurons, the response was significantly enhanced in the memory-guided saccade task as compared with that in the fixation task. For 8% (13/163) of V3A neurons, the amplitude of response in the memory-guided saccade task was significantly suppressed. We also observed task-related modulation of activity prior to stimulus onset. Among the V3A neurons (37/163) that showed significant differences between tasks in prestimulus activity, the majority (89%; 33/37) showed greater prestimulus activity in the memory-guided saccade task. Task-related increases in prestimulus activity in the memory-guided saccade task were not always matched by increases in the sensory response, indicating that visual responses and prestimulus activity can be modulated independently. Activity in the memory period was suppressed compared with prestimulus activity for 83% (49/59) of the V3A neurons that showed a significant difference in activity (59/197) between these two epochs. For some neurons, memory-period activity dropped even below the baseline level in the fixation task, indicating that there may be an active suppression mechanism. Many V3A neurons (75%, 148/197) also had activity in the saccade epoch. This activity was most prominent immediately after the saccade. Postsaccadic activity was observed even when testing was carried out in total darkness, indicating that this activity reflects, at least in part, extraretinal signals and is not simply a response to visual reafference. These results indicate that several kinds of signals are carried by single neurons in extrastriate area V3A. Moreover, activity in V3A is subject to modulation by extraretinal factors, including attention, anticipation, memory, and saccadic eye movements.

Deafferentation and pointing with visual double-step perturbations.

The capability of reprogramming movement responses following changes in the visual goal has been studied through the double-step paradigm. These studies have shown that: (a) continuous internal feedback-loops correct unconsciously the dynamic errors throughout the movement; (b) proprioceptive information and/or the efference copy have a privileged status among central processes, insuring on-line regulation of the initial motor commands; and (c) generation of the motor program starts after target presentation, and is continuously updated in the direction of the current internal representation of the target, at least until the onset of hand movement. This main corrective process of the initial program appears to be basically independent of visual reafference from the moving hand. However, the agreement with the possibility of a visuomotor loop, based on the comparison of the new updated representation of the target position and on the information from the moving hand, has not determined whether the correcting process is proprioceptive feedback dependent, or whether internal feedback-loops (efferent copies) are responsible for quick corrections of unfolding motor responses. To answer this question, the present experiment investigated the pointing behavior of a deafferented subject, using a double-step paradigm under various conditions of visual feedback and movement initiation. Overall, the present study (a) clearly showed the capacity of the motor system to modify and correct erroneous trajectories on the mere basis of internal feedback-loops and (b) emphasized the crucial role played by the target jump/arm triggering delay and the importance of the eye efferent copy for providing information about the spatial goal of the movement.

Vectorial coding of movement: vision, proprioception, or both?

1. Subjects were asked to point toward visual targets without visual reafference from the moving hand in two conditions. In both conditions the pointing fingertip was viewed only before movement onset. 2. In one condition, the pointing fingertip was viewed through prisms that created a visual displacement without altering the view of the target. In another experimental condition, vision of the fingertip was not displaced. Comparison of these two conditions showed that virtually shifting finger position before movement through prisms induced a pointing bias in the direction opposite to the shift. The extent of this pointing bias was about one third of the prismatic shift applied to the fingertip. 3. Analysis of movement initial direction demonstrated that it was also less deviated than predicted from the prismatic shift. In addition, the reaction time and movement time of the reaching movement were increased. 4. This result is interpreted in the framework of the vectorial coding of reaching movement. Proprioception and vision provide two possible sources of information about initial hand position, i.e., the origin of the movement vector. The question remains as to how these two sources of information interact in specifying initial hand position when they are simultaneously available. 5. Our results are thus discussed with respect to a visual-to-visual movement vector hypothesis and a proprioceptive-to-visual vector hypothesis. It is argued that the origin of the putative movement vector is encoded by weighted fusion of the visual and the proprioceptive information about hand initial position.

Error processing in pointing at randomly feedback-induced double-step stimuli.

Two experiments were conducted to determine the spatial and temporal organization of the arm trajectory in human subjects as they pointed to single- and double-step target displacements. Subjects pointed either without (Experiment 1) or with (Experiment 2) vision of their moving hand throughout the trial. In both experiments, target perturbation occurring in double-step trials was clearly perceived by the subjects and was randomly introduced either at the onset or at peak velocity of hand movement. Regardless of whether or not visual reafference from the pointing hand was available, subjects corrected the trajectory of their moving hand to accommodate the double-step. Moreover, asymmetrical velocity profiles were observed for responses to both types of target, with or without vision of the moving hand. The acceleration phase was a fixed pattern independent of the type of step stimulation. However, a clear dissociation, both in the deceleration phase and accuracy of responses to double-step targets, emerged according to the timing of target perturbation. When targets were perturbed at the onset of hand movement, subjects modulated the deceleration phase of their response to compensate for 88 to 100% of the second target displacement. In contrast, when targets were perturbed at peak velocity of hand movement, subjects were unable to modulate the deceleration phase adequately and compensated for only 20 to 40% of the perturbation. These results suggest that motor error is dynamically evaluated during the acceleration phase of a movement toward a perturbed target, allowing amendments to the trajectory to be performed during the deceleration phase. This main corrective process appears to be basically independent of visual reafference from the moving hand.

Locust flight steering

Locusts, Locusta migratoria, flying under closed-loop conditions in a flight simulator, control the stability of their visual environment by means of correctional steering and so minimize retinal slip (the optomotor reaction). Correctional steering includes modulation of the wingbeat, ruddering with abdomen and legs and compensatory head movements. Pulsed ultrasounds that simulate bat echolocation signals elicit avoidance steering in flying locusts: ruddering and yaw torque are directed away from the sound source. In this article the two modes of steering are compared and their interaction is studied. 1. In both correctional and avoidance steering ruddering is directed to the side of the turn. However, during correctional manoeuvres, head movements are also directed to the side of the turn, while during avoidance steering the head moves in the direction opposite to that of the turn (Fig. 4). 2. The components and temporal organization of both sorts of steering are similar. Head movements occur some 30–40 ms after torque production begins (Fig. 5). Thus, neither correctional nor avoidance steering is initiated by head movements. 3. Under closed-loop conditions, avoidance steering generates pronounced rotation of the panorama (Figs. 6, 7) that is not counteracted by the compensatory optomotor reflex. 4. Acoustically elicited head turns are also performed in darkness (Fig. 4a), and irrespective of the sign of the visual reafference (Fig. 9), which indicates that they are temporarily independent of visual information. A mechanism is proposed in which optomotor interference is prevented by an inhibitory corollary discharge of acoustic origin. 5. Locusts prevented from moving their heads still perform avoidance turns (Fig. 8), but these are of shorter duration than when the head is free. 6. The role of head movements in steering is discussed. It is proposed that neck proprioception assists visual and acoustic information in adaptive flight steering. Head movements in closed-loop corrective steering reduce steering overshoot; during avoidance steering opposite head movements may in turn favor steering overshoot.

Eye movement-related activities in cells of the lateral suprasylvian cortex of the cat

Investigation of eye movement-related activities and photic responsiveness using behaving cats demonstrated distinctive representations of eye movement signals in different areas of the lateral suprasylvian cortex: visual reafference in the medial bank of the middle suprasylvian sulcus and non-visual signals (proprioceptive reafference or efference copy) in the lateral bank.

Role of structured visual field and visual reafference in accuracy of pointing movements.

In a visuo-motor pointing task, the accuracy of response was measured in situations which differ in the visual information available and the speed of execution of movement. Results confirm the role of visual cues received from self-produced movement in the control of the trajectory of a limb. Furthermore, it can be shown that a structured visual background is important in the treatment of sensory data concerned with the movement and in target localization. This effect is absent in rapidly executed pointing response.

Specialized adaptation to displaced vision.

Two conditions of exposure to prism rearrangement were used to explore specificity of visuo—motor adaptation. In one condition subjects viewed, in sequential alternation of one minute periods, the movements of one arm through base right prisms and those of the other arm through base left prisms for a total of 20 min. In the second condition subjects viewed the movements of only one arm for one minute periods followed by closing the eyes for the next, alternating between viewing arm movements and closing the eyes for a total of 20 min. The magnitude of postexposure sensorimotor changes following the alternating limb-exposure condition was equivalent and opposite in direction in each limb. Unilateral exposure generated commensurate sensorimotor changes in responses entailing the exposed arm. These results show that prism-mediated visual reafference from arm movements acts to recalibrate target-directed orientations of that arm only, and does not interact, or interfere with, recalibration of directed orientations of the other limbs.