Response selection versus feedback analysis in conditional visuo-motor learning (original) (raw)

Understanding the Neural Computations of Arbitrary Visuomotor Learning through fMRI and Associative Learning Theory

Cerebral Cortex, 2007

Associative theory postulates that learning the consequences of our actions in a given context is represented in the brain as stimulus-response--outcome associations that evolve according to predictionerror signals (the discrepancy between the observed and predicted outcome). We tested the theory on brain functional magnetic resonance imaging data acquired from human participants learning arbitrary visuomotor associations. We developed a novel task that systematically manipulated learning and induced highly reproducible performances. This granted the validation of the model-based results and an in-depth analysis of the brain signals in representative single trials. Consistent with the Rescorla--Wagner model, prediction-error signals are computed in the human brain and selectively engage the ventral striatum. In addition, we found evidence of computations not formally predicted by the Rescorla--Wagner model. The dorsal fronto-parietal network, the dorsal striatum, and the ventrolateral prefrontal cortex are activated both on the incorrect and first correct trials and may reflect the processing of relevant visuomotor mappings during the early phases of learning. The left dorsolateral prefrontal cortex is selectively activated on the first correct outcome. The results provide quantitative evidence of the neural computations mediating arbitrary visuomotor learning and suggest new directions for future computational models.

Neural activity in the primate prefrontal cortex during associative learning

Neuron, 1998

CITATIONS 353 READS 43 3 authors: Some of the authors of this publication are also working on these related projects: Synchrony of beta oscillations in the frontoparietal network View project Category representations in parietal and prefrontal cortex on different levels of category abstractness

Neurodynamics of the prefrontal cortex during conditional visuomotor associations

2008

Abstract The prefrontal cortex is believed to be important for cognitive control, working memory, and learning. It is known to play an important role in the learning and execution of conditional visuomotor associations, a cognitive task in which stimuli have to be associated with actions by trial-and-error learning. In our modeling study, we sought to integrate several hypotheses on the function of the prefrontal cortex using a computational model, and compare the results to experimental data.

Experience-dependent activation patterns in human brain during visual-motor associative learning

2003

Multiple brain regions, including parietal and frontal cortical areas, seem to participate in learning and rehearsing associations between spatially defined visual cues and appropriate motor responses. However, because most previous studies have related learning to changes in brain activation according to elapsed time or number of trials but not categories based on performance, it remains unclear how and when areas implicated in learning sensory-motor associations actually participate in the process. The current experiment used functional magnetic resonance imaging to examine changes in brain activation when participants learned to associate an arbitrarily located visual cue with a finger movement. Associative trials were categorized as incorrect, first correct, or subsequent correct. Participants also performed a spatially compatible visual-motor control task. A group analysis revealed four major findings addressing the behavioral processes occurring during forming and rehearsing visual-motor rules. First, brain networks related to processing associative information, through initial learning to rehearsal, yielded more activation in a myriad of neocortical structures than did a simple motor task. Second, we revealed frontal and parietal areas that differentially processed errors and correct responses. Third, we found frontal-parietal networks that seemed to mediate the transition of learning to rehearsing arbitrary visual-motor associations and that this activation exhibited dynamic characteristics. Last, we found a frontal-parietal network that appeared to have a key role in expressing the learned sensory-motor association. The current results provide a foundation for understanding how neocortical structures participate in the various behavioral processes that combine to form and consolidate novel and arbitrary sensory-motor associations.

Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning

Experimental Brain Research, 2000

This paper provides evidence that the ventral prefrontal cortex plays a role in the learning of tasks in which subjects must learn to associate visual cues and responses. Imaging with both positron-emission tomography (PET) and functional magnetic-resonance imaging (fMRI) reveals learning-related increases in activity when normal subjects learn visual associative tasks. Evidence is also presented from an event-related fMRI study that activity in this area is time-locked both to the presentation of the visual stimuli and also to the time of the motor response. Finally, it is shown in a study of monkeys that removal of the ventral prefrontal area 12 (including 45 A) impairs the ability of monkeys to relearn a visual associative task (visual matching), even though there were no demands on working memory. It is, therefore, proposed that the ventral prefrontal cortex constitutes part of the circuitry via which associations are formed between visual cues and the actions or choices that they specify. On the basis of the existing anatomical and electrophysiological data, it is argued that the prefrontal cortex is the only area that can represent cues, responses and outcomes.

Frontal and parietal networks for conditional motor learning: a positron emission tomography study

Journal of neurophysiology, 1997

Studies on nonhuman primates show that the premotor (PM) and prefrontal (PF) areas are necessary for the arbitrary mapping of a set of stimuli onto a set of responses. However, positron emission tomography (PET) measurements of regional cerebral blood flow (rCBF) in human subjects have failed to reveal the predicted rCBF changes during such behavior. We therefore studied rCBF while subjects learned two arbitrary mapping tasks. In the conditional motor task, visual stimuli instructed which of four directions to move a joystick (with the right, dominant hand). In the evaluation task, subjects moved the joystick in a predetermined direction to report whether an arrow pointed in the direction associated with a given stimulus. For both tasks there were three rules: for the nonspatial rule, the pattern within each stimulus determined the correct direction; for the spatial rule, the location of the stimulus did so; and for the fixed-response rule, movement direction was constant regardless...

Presupplementary motor area activation during sequence learning reflects visuo-motor association

The Journal of neuroscience : the official journal of the Society for Neuroscience, 1999

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 paradig...

Medial prefrontal and subcortical mechanisms underlying the acquisition of motor and cognitive action sequences in humans

2002

that in humans and animals supports behaviors based on reward and reinforcement (Apicella et al., 1991; Delgado et al., 2000; Schultz et al., 1992) and that mediates the acquisition of motor action plans (Doyon et al.; Shidara et al., 1998). In addition, both VS and 75005 Paris AMPC are important projection sites of dopaminergic France neurons that are known to implement motivational and 2 Cognitive Neuroscience Section reinforcement mechanisms (Lewis et al., 1988; Robbins NINDS and Everitt, 1996; Schultz, 1997). Bethesda, Maryland 20892

Striatal Indirect Pathway Contributes to Selection Accuracy of Learned Motor Actions

Journal of Neuroscience, 2012

The dorsal striatum, which contains the dorsolateral striatum (DLS) and dorsomedial striatum (DMS), integrates the acquisition and implementation of instrumental learning in cooperation with the nucleus accumbens (NAc). The dorsal striatum regulates the basal ganglia circuitry through direct and indirect pathways. The mechanism by which these pathways mediate the learning processes of instrumental actions remains unclear. We investigated how the striatal indirect (striatopallidal) pathway arising from the DLS contributes to the performance of conditional discrimination. Immunotoxin targeting of the striatal neuronal type containing dopamine D 2 receptor in the DLS of transgenic rats resulted in selective, efficient elimination of the striatopallidal pathway. This elimination impaired the accuracy of response selection in a two-choice reaction time task dependent on different auditory stimuli. The impaired response selection was elicited early in the test sessions and was gradually restored as the sessions continued. The restoration from the deficits in auditory discrimination was prevented by excitotoxic lesion of the NAc but not by that of the DMS. In addition, lesion of the DLS mimicked the behavioral consequence of the striatopallidal removal at the early stage of test sessions of discriminative performance. Our results demonstrate that the DLS-derived striatopallidal pathway plays an essential role in the execution of conditional discrimination, showing its contribution to the control of selection accuracy of learned motor responses. The results also suggest the presence of a mechanism that compensates for the learning deficits during the repetitive sessions, at least partly, demanding accumbal function.

Functional coupling underlying motor and cognitive functions of the dorsal premotor cortex

Behavioural Brain Research, 2009

This review article discusses mechanisms of how distinct behavioral operations are organized by different modules distributed in the frontal cortex. Cognitive manipulation often requires a flow of multiple elementary sub-operations processed in specialized brain regions. The dorsolateral prefrontal cortex (dlPFC) is likely responsible for attentional selection, which orients organisms' mental resources to behaviorally relevant information. The dorsal premotor cortex (PMd) is implicated to possess a functional gradient along the rostral-caudal axis. The rostral sector of the PMd (pre-PMd) is involved in various cognitive/premovement processes while its caudal sector (PMd proper) primarily controls actual movement. Neurophysiology studies in monkeys have shown that the pre-PMd, when functionally coupled with the dlPFC, may transform independent working memory items into a single sequence (sequence generation). A neuroimaging study has shown that the pre-PMd is indeed involved in sequence generation under the influence of the dlPFC in humans. It has been also indicated that the dlPFC and the pre-PMd are functionally coupled when attentional selection and sequence generation are to be unified for serial information processing. Functional interplay through the prefrontal-premotor connections may mediate the integration of specific sub-operations for multi-step cognitive manipulation. Furthermore, evidence from a metaanalysis of the imaging literature is argued for an idea that the coupling pattern with other frontal cortical areas may characterize of the function of the pre-PMd and PMd proper in various motor and cognitive tasks.