Visuomotor Associations Research Articles

Old age impairs the use of arbitrary visual cues for predictive control of fingertip forces during grasp.

Old age impairs the ability to form new associations for declarative memory, but the ability to acquire and retain procedural memories remains relatively intact. Thus, it is unclear whether old age affects the ability to learn the visuomotor associations needed to set efficient fingertip forces for handling familiar objects. We studied the ability for human subjects to use visual cues (color) about the mechanical properties (texture or weight) of a grasped object to control fingertip forces during prehension. Old and young adults (mean age 77 years and 22 years, respectively) grasped and lifted an object that varied in texture at the gripped surfaces (experiment 1: sandpaper versus acetate surface materials) or weight (experiment 2: 200 g versus 400 g). The object was color-coded according to the mechanical property in the "visual cue" condition, and the mechanical property varied unpredictably across lifts in the "no visual cue" condition. In experiment 1 (texture), the young adults' grip force (force normal to the gripped surface) when the object lifted from the support surface was 24% smaller when the surfaces were color-coded. The old adults' grip force did not vary between the visual conditions despite their accurate reports of the grip surface colors prior to each lift. Comparable findings were obtained in experiment 2, when object weight was varied and peak grip force rate prior to object lift-off was measured. Furthermore old and young subjects alike used about 2 N of grip force when lifting the 200 g object in experiment 2. Therefore, the old adults' failure to adjust grip force when the color cue was present cannot be attributed to a general inability or unwillingness to use low grip force when handling objects. We conclude that old age affects the associative learning that links visual identification of an object with the fingertip forces for efficiently handling the object. In contrast, old and young subjects' grip force was influenced by the preceding lift, regardless of visual cues, which supports existing theories that multiple internal representations govern predictive control of fingertip forces during prehension.

Interaction of ventral and orbital prefrontal cortex with inferotemporal cortex in conditional visuomotor learning.

Five rhesus monkeys (Macaca mulatta) were trained to learn novel conditional visuomotor associations, to perform this task with familiar stimuli, and to perform a visual matching-to-sample task with the same familiar stimuli. Removal of the orbital and ventral prefrontal cortex (PFv+o) in 1 hemisphere and inferotemporal cortex (IT) in the other, thus completing a surgical disconnection of these 2 regions, yielded an impairment on all 3 tasks. Addition of a premotor cortex lesion to the hemisphere containing the PFv+o lesion did not worsen the impairments. The results indicate that PFv+o interacts with IT in both the learning and retention of conditional visuomotor associations. In addition to those associations, which might be considered lower order rules for choosing a response, frontotemporal interaction also appears to be important for higher order rules, such as those involved in the matching task.

Fornix transection impairs conditional visuomotor learning in tasks involving nonspatially differentiated responses.

Rhesus monkeys learned a series of conditional visuomotor associations involving two-dimensional "objects" that instructed one of three responses: tapping a touch screen, steady contact with the screen for a brief period, or steady contact for a longer period. Relative to controls, fornix-transected monkeys were impaired in the acquisition of new associations and in the retention of preoperatively learned ones. These findings challenge the view that the hippocampal system participates in associative learning only when spatial information is relevant to either the stimulus or the response.

Neural correlates of visuomotor associations. Spatial rules compared with arbitrary rules.

A green button may be the target of a movement, or it may instruct the opening of an adjacent door. In the first case, its spatial configuration serves to guide the hand, whereas in the second case its colour allows a decision between alternative courses of action. This study contrasts these two categories of visuomotor transformation. Our goal was to test the hypothesis that visual information can influence the motor system through different, task-dependent pathways. We used positron emission tomography (PET) to measure human brain activity during the performance of two tasks requiring the transformation of visual stimuli to motor responses. The stimuli instructed either a spatially congruent grasping movement or an arbitrarily associated hand movement. The experimental design emphasised preparatory- over movement-related activity. We expected ventral parieto-precentral regions to contribute to the visuomotor transformations underlying grasping movements, and fronto-striatal circuitry to contribute to the selection of actions on the basis of associative rules. We found that selecting between alternative courses of action on the basis of associative rules specifically involved ventral prefrontal, striatal and dorsal precentral areas. Conversely, spatially congruent grasping movements evoked specific differential responses in ventral precentral and parietal regions. The results suggest that visual information can flow through the dorsal system to determine how actions are performed, but that fronto-striatal loops are involved in specifying which action should be performed in the current context.

Learning Arbitrary Visuomotor Associations: Temporal Dynamic of Brain Activity

Primates can give behavioral responses on the basis of arbitrary, context-dependent rules. When sensory instructions and behavioral responses are associated by arbitrary rules, these rules need to be learned. This study investigates the temporal dynamics of functional segregation at the basis of visuomotor associative learning in humans, isolating specific learning-related changes in neurovascular activity across the whole brain. We have used fMRI to measure human brain activity during performance of two tasks requiring the association of visual patterns with motor responses. Both tasks were learned by trial and error, either before (visuomotor control) or during (visuomotor learning) the scanning session. Epochs of tasks performance (∼30 s) were alternated with a baseline period over the whole scanning session (∼50 min). We have assessed both linear and nonlinear modulations in the differential signal between tasks, independently from overall task differences. The performance indices of the visuomotor learning task smoothly converged onto the values of a steady-state control condition, according to nonlinear timecourses. Specific visuomotor learning-related activity has been found over a distributed cortical network, centred on a temporo-prefrontal circuit. These cortical time-modulated activities were supported early in learning by the hippocampal/parahippocampal complex, and late in learning by the basal ganglia system. These findings suggest the inferior temporal and the ventral prefrontal cortex are critical neural nodes for integrating perceptual information with executive processes.

Pallidal activity is involved in visuomotor association learning in monkeys.

In order to examine whether the basal ganglia are involved in arbitrary visuomotor association, we recorded neuronal activity in the internal segment of the globus pallidus (GPi) of monkeys during a conditional visuomotor learning task. Two monkeys were presented a cueing visual stimulus, and following a delay period required to push, pull or turn a manipulator according to the cue. GPi neurons showed changes in activity during the delay period when the animals performed the task on the basis of a familiar stimulus-response association. Those changes in delay activity were enhanced as the monkeys were learning a new visuomotor association. The enhancement of the changes was selective to a following response. These results suggest that the basal ganglia are involved in arbitrary visuomotor association, especially during the learning of new associations.

Movement Preparation and Motor Intention

This paper addresses the functional anatomy of movement representation. We have used associative visuomotor tasks with instructed delays to elicit motor preparatory activity. We regard such activity, when independent from transient stimulus-locked responses, as a likely candidate for the neural basis of movement representation (M. Jeannerod, The Cognitive Neuroscience of Action. Blackwell, Oxford, 1997). In a first event-related fMRI experiment, we found that preparing to move according to arbitrary visuomotor associations relies not only on parietofrontal circuitry, but also on portions of the posterior superior temporal sulcus. In a separate behavioral experiment, we discarded the hypothesis that such activities were confounded by working memory processes. In a second imaging experiment, we have further defined the relative contributions of these parietal, premotor, and temporal areas to the preparatory process and their involvement in motor representations. We conclude that posterior parietal cortex is interested in evaluating the potential motor significance of sensory stimuli, irrespectively of the likelihood of providing a response (“motor intention”). Conversely, preparatory activity in frontal premotor regions appears to be a function of the probability of a subsequent movement. Finally, on the basis of the present and published data, we suggest that posterior temporal cortex might be involved in the extraction of contextual and intentional cues during goal-oriented behavior.

Stimulus–Response Incompatibility Activates Cortex Proximate to Three Eye Fields

We used functional magnetic resonance imaging (fMRI) to investigate cortical activation during the performance of three oculomotor tasks that impose increasing levels of cognitive demand. (1) In a visually guided saccade (VGS) task, subjects made saccades to flashed targets. (2) In a compatible task, subjects made leftward and rightward saccades in response to foveal presentation of the uppercase words “LEFT” or “RIGHT.” (3) In a mixed task, subjects made rightward saccades in response to the lowercase word “left” and leftward saccades in response to the lowercase word “right” on incompatible trials (60%). The remaining 40% of trials required compatible responses to uppercase words. The VGS and compatible tasks, when compared to fixation, activated the three cortical eye fields: the supplementary eye field (SEF), the frontal eye field (FEF), and the parietal eye field (PEF). The mixed task, when compared to the compatible task, activated three additional cortical regions proximate to the three eye fields: (1) rostral to the SEF in medial frontal cortex; (2) rostral to the FEF in dorsolateral prefrontal cortex (DLPFC); (3) rostral and lateral to the PEF in posterior parietal cortex. These areas may contribute to the suppression of prepotent responses and in holding novel visuomotor associations in working memory.

The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatta).

Four rhesus monkeys (Macaca mulatta) were trained to learn novel sets of visuomotor associations in 50 trials or less, within single test sessions. After bilateral ablation of the orbital and ventral prefrontal cortex, the monkeys lost the ability to learn these associations within a session, although they could learn them when given several daily sessions. Thus, relatively slow, across-session visuomotor learning depends on neither the ventral nor orbital prefrontal cortex, but rapid, within-session learning does. The ablations also eliminated at least 2 response strategies, repeat-stay and lose-shift, which might account, in part, for the deficit in rapid learning. The deficit is unlikely to result from a failure of visual discriminative ability or working memory: The monkeys could discriminate similar stimulus material within a session, and reducing the working memory load did not improve within-session learning.

Deficit in conditional visuomotor learning by local infusion of bicuculline into the ventral prefrontal cortex in monkeys.

To explore the role of the ventral prefrontal cortex (PFv) in conditional visuomotor learning, we infused locally bicuculline, a GABAergic antagonist, into the PFv of two monkeys, well trained on a two-problem visuomotor task. The task required the monkeys to execute one of two motor actions (moving a handle to the left or to the right) in response to one of two familiar visual patterns (circle or triangle). The two patterns mapped 1:1 onto the two motor actions: for each pattern one and only one motor action was scored, correct and reinforced. In contrast to these sessions with familiar patterns, in the learning sessions the monkeys were presented with one or two novel patterns and required to learn the arbitrarily determined associations between these patterns and the two motor actions. We found that bilateral infusion of bicuculline into PFv dramatically impaired the monkeys' ability to learn novel pattern-response associations: the trials and errors to criterion (90% correct) increased significantly. The errors were mainly an inability to apply 'Win-Stay', 'Lose-Shift' and 'Change-Shift' strategies. There was no effect on the monkeys' performance in responding to familiar patterns. Similar infusion of bicuculline into the dorsal prefrontal cortex was without effect on either novel-pattern learning or familiar-pattern performance. We conclude that the ventral prefrontal cortex is necessary for learning new visuomotor associations, but has less importance, if any, for performing pre-established ones.

Contextual modulation of visuomotor associations in bumble‐bees ( Bombus terrestris )

We performed the following experiment to investigate whether contextual cues can prevent interference during the acquisition of potentially competing visuomotor associations. In the bumble‐bee ( Bombus terrestris ). Bees discriminated between horizontally and vertically orientated gratings of black and white stripes in order to reach a feeder and between different diagonally orientated gratings to gain access to their nest. Once bees were well trained on these two tasks, the discrimination task at the nest was changed so that bees had to distinguish between horizontal and vertical gratings at both sites. Whereas they still approached the horizontal grating to reach food, they now had to approach a vertical grating in order to return to their nest. The new task was learnt rapidly. Errors at the feeder did not increase during or after the acquisition of this potentially competing behaviour at the nest entrance. For a brief period during acquisition, bees showed some hesitation at the feeder and hovered for slightly longer before choosing between horizontals and verticals. After acquisition was complete, bees showed a slight increase in their preference for verticals over a more ambiguous stimulus of an array of dots. These findings are consistent with the hypothesis that different contextual signals are associated with approaching the nest or approaching the feeder, and that these contextual signals facilitate learnt associations between orientation detectors and motor commands.

Presupplementary Motor Area Activation during Sequence Learning Reflects Visuo-Motor Association

In preceding studies (Hikosaka et al., 1996; Sakai et al., 1998) we have shown that the presupplementary motor area (pre-SMA), an anterior part of the medial premotor cortex, is active during visuo-motor sequence learning. However, the paradigm required the subjects first to acquire correct visuo-motor association and then to acquire correct sequence, and it was still unknown which of the two processes the pre-SMA is involved in. To further characterize the role of pre-SMA, we have conducted another series of functional magnetic resonance imaging experiments using three learning paradigms. The three were the same in that they involved a visuo-motor association component, but they differed in terms of the involvement of sequential components; one involved no sequence learning, whereas the other two involved learning of motor sequence or perceptual sequence. Comparison of the learning conditions with the any-order button press condition revealed pre-SMA activation in all three paradigms. The pre-SMA activation remained unchanged during learning of visuo-motor associations but decreased during learning of sequences, suggesting that the pre-SMA is related to visuo-motor association rather than sequence. The decrease of pre-SMA activation in the sequential paradigms may reflect the process by which individual visuo-motor associations were replaced by the formation of sequential procedural memory, which occurs outside the pre-SMA. Thus activation of the pre-SMA was related to the extent to which the task performance depended on conscious visuo-motor associations.

Inhibitory control of competing motor memories.

The ability to inhibit previously learned visuomotor associations is essential for efficient learning of novel behaviors. While the neural basis of the system that might control interactions between competing motor memories is not known, it has been demonstrated that animals with ventral and orbital prefrontal cortex (PFC) deficits have particular difficulties in learning to withhold responses to previously conditioned sensory stimuli. Here we measured regional cerebral blood flow (rCBF), using positron emission tomography, during learning of a novel motor task that required inhibition of a previously learned motor memory. Subjects (n=24) learned reaching movements in a force field (field A). After a variable time interval, some subjects (n=15) learned to reach in a field with a reversed pattern of forces (field B). When the time interval was short (10 min), learning in field B was coincident with a reactivation of regions that had become initially activated during learning in field A: the left putamen and bilaterally in the dorsolateral PFC. Behaviorally, this was accompanied with perseveration that lasted for hundreds of movements, suggesting an instantiation of the internal model for field A during learning in field B. Neither the reactivation nor the perseveration were observed in a different group of subjects that learned field B at 5.5 h. We found that the regions which significantly differentiated the two groups during learning of B were in the ventrolateral PFC (bilaterally): there were sharp decreases in rCBF here in the 5.5 group but not in the 10-min group. At 5.5 h motor learning again involved the striatum, but this time in the left caudate. Neither the caudate nor the ventral PFC had exhibited learning-related activity in field A. Instead, they showed changes in rCBF during the reversal of the learning problem when the previously acquired motor memory was successfully gated. The results demonstrate that: (1) perseveration of a competing motor memory may be linked to reactivation of the neural circuit that participated in acquiring that memory, and (2) the ventral PFC may play an important role in the inhibitory control of the competing motor memory.

Role of the hippocampus plus subjacent cortex but not amygdala in visuomotor conditional learning in rhesus monkeys.

Rhesus monkeys were trained to learn a large series of visuomotor conditional associations, each involving the arbitrary coupling of a visual stimulus with 1 of 3 potentially correct forelimb movements. The monkeys then received bilateral aspiration lesions of either the amygdala plus subjacent cortex or the hippocampus plus subjacent cortex. Hippocampal but not amygdala removals significantly retarded the learning of new visuomotor associations. Neither lesion affected retention. The findings argue against a general role for the amygdala in associating information across modalities, construed broadly to include motor information. By contrast, the finding that the hippocampal formation and its subjacent cortex play a role in learning new sensorimotor associations supports the view that this region participates in the long-term storage of associative information or in the recall of recently acquired information.

Neuronal activity in the supplementary eye field during acquisition of conditional oculomotor associations.

1. The supplementary eye field (SEF) has been viewed as a premotor cortical field for the selection and control of saccadic eye movements. Drawing on studies of the neighboring premotor cortex, we hypothesized that if the SEF participates in the selection of action based on arbitrary stimulus-response associations, then task-related activity in the SEF should change during the learning of such associations. 2. Rhesus monkeys were operantly conditioned to make a saccadic eye movement to one of four targets (7 deg up, down, left, and right from center) in response to a foveal instruction stimulus (IS). One and only one of those four possible responses was arbitrarily designated "correct" for each IS. The monkeys responded to familiar ISs, four stimuli that remained unchanged throughout training and recording, as well as to novel ISs, which the monkeys had not previously seen. The monkeys initially chose responses to novel stimuli by trial and error, with near chance levels of performance, but quickly learned to select the correct saccade. 3. We studied 186 SEF cells as monkeys learned new visuomotor associations. Neuronal activity was quantified in four task periods: during the presentation of the IS, during an instructed delay period (i.e., after the removal of the IS but before a trigger or "go" stimulus), just before the saccade, and after the saccade during fixation of the target location. The discharge rate in each task period was considered a separate case for analysis, compared with that in a reference period preceding the IS, and eliminated from further analysis if not significantly different. 4. We observed two main categories of activity change during learning, which we termed learning selective and learning dependent. Learning-selective cases showed a significant evolution in activity as the monkeys learned which saccade was instructed by a novel IS, but had no significant modulation during trials with familiar ISs. Many of these cells were virtually inactive on trials with familiar ISs. However, they initially showed dramatic modulation when tested with a novel IS. As the monkey chose the correct saccade (or target) with increasing reliability, the modulation often decremented until the cell was again relatively unmodulated, as observed during familiar-IS trials. These cells usually remained relatively inactive until the monkeys were challenged to start learning another new stimulus-response association. Learning-selective activity was observed in all task periods, and 33 (18%) of the 186 adequately tested SEF cells showed learning-selective activity in one or more task periods.(ABSTRACT TRUNCATED AT 400 WORDS)

Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations

It has been proposed that the premotor cortex plays a role in the selection of motor programs based on environmental context. To test this hypothesis, we recorded the activity of single neurons as monkeys learned visuomotor associations. The hypothesis predicts that task-related premotor cortical activity before learning should differ from that afterward. We found that a substantial population of premotor cortex neurons, over half of those adequately tested, showed the predicted learning-dependent changes in activity. The present findings support a role for premotor cortex in motor preparation, generally, and suggest a specific role in the selection of movements on the basis of arbitrary associations.

Visuo‐Motor Reaction Times of Normal Subjects and Schizophrenics Using Inverting Prisms

The visuo-motor reaction times of normal subjects and schizophrenics were measured to investigate adaptation of eye-hand coordination in schizophrenics under modified vision. Reaction time was measured in 32 normal subjects and 32 schizophrenics by using a rectangular board with 24 illuminated buttons. Subjects' task was to press an illuminated button as quickly as possible under normal and modified vision. Time elapsed from when the light was switched on to when the button was pressed was measured as the visuo-motor reaction time in msec. Three conditions were set up: control in normal vision; inverted using an inverting goggle; reversed using a reversing goggle. In general the visuo-motor reaction times of schizophrenics were slower than those of normal subjects. But in the reversed condition, there was no significant difference between normal subjects and schizophrenics. The visuo-motor reaction times of schizophrenics in the reversed condition showed a large dispersion with the fastest being faster than that of any normal subjects. It is suggested that there may be a group among schizophrenics whose basic paradigm of visuo-motor association is different from that of normal subjects.