Richard B. Ivry

Functional mapping of sequence learning in normal humans

The brain localization of motor sequence learning was studied in normal subjects with positron emission tomography. Subjects performed a serial reaction time (SRT) task by responding to a series of stimuli that occurred at four different spatial positions. The stimulus locations were either determined randomly or according to a 6-element sequence that cycled continuously. The SRT task was performed under two conditions. With attentional interference from a secondary counting task there was no development of awareness of the sequence. Learning-related increases of cerebral blood flow were located in contralateral motor effector areas including motor cortex, supplementary motor area, and putamen, consistent with the hypothesis that nondeclarative motor learning occurs in cerebral areas that control limb movements. Additional cortical sites included the rostral prefrontal cortex and parietal cortex. The SRT learning task was then repeated with a new sequence and no attentional interference. In this condition, 7 of 12 subjects developed awareness of the sequence. Learning-related blood flow increases were present in right dorsolateral prefrontal cortex, right premotor cortex, right ventral putamen, and biparieto-occipital cortex. The right dorsolateral prefrontal and parietal areas have been previously implicated in spatial working memory and right prefrontal cortex is also implicated in retrieval tasks of verbal episodic memory. Awareness of the sequence at the end of learning was associated with greater activity in bilateral parietal, superior temporal, and right premotor cortex. Motor learning can take place in different cerebral areas, contingent on the attentional demands of the task.

Dissociation of the lateral and medial cerebellum in movement timing and movement execution

SummaryIn a previous study (Ivry and Keele, in press), cerebellar patients were found to be impaired on both a motor and a perceptual task which required accurate timing. This report presents case study analyses of seven patients with focal lesions in the cerebellum. The lesions were predominantly in the lateral, hemispheric regions for four of the patients. For the remaining three patients, the lesions were centered near the medial zone of the cerebellum. The clinical evaluation of the patients also was in agreement with the different lesion foci: lateral lesions primarily impaired fine motor coordination, especially apparent in movements with the distal extremities and medial lesions primarily disturbed balance and gait. All of the patients were found to have increased variability in performing rhythmic tapping when tapping with an effector (finger or foot) ipsilateral to the lesion in comparison to their performance with a contralateral effector. Separable estimates of a central timekeeper component and an implementation component were derived from the total variability scores following a model developed by Wing and Kristofferson (1973). This analysis indicated that the poor performance of patients with lateral lesions can be attributed to a deficit in the central timing process. In contrast, patients with medial lesions are able to accurately determine when to make a response, but are unable to implement the response at the desired time. A similar dissociation between the lateral and medial regions has been observed on a time perception task in patients with cerebellar atrophy. It is concluded that the lateral regions of the cerebellum are critical for the accurate functioning of an internal timing system.

The neural representation of time

This review summarizes recent investigations of temporal processing. We focus on motor and perceptual tasks in which crucial events span hundreds of milliseconds. One key question concerns whether the representation of temporal information is dependent on a specialized system, distributed across a network of neural regions, or computed in a local task-dependent manner. Consistent with the specialized system framework, the cerebellum is associated with various tasks that require precise timing. Computational models of timing mechanisms within the cerebellar cortex are beginning to motivate physiological studies. Emphasis has also been placed on the basal ganglia as a specialized timing system, particularly for longer intervals. We outline an alternative hypothesis in which this structure is associated with decision processes.

The representation of temporal information in perception and motor control.

The representation of temporal information can be examined from both a neurological and a computational perspective. Recent evidence suggests that two subcortical structures, the cerebellum and basal ganglia, play a critical role in the timing of both movement and perception. At a computational level, models of an internal clock have been developed in which timing is based on either endogenous oscillatory processes or distributed interval-based representations derived from relatively slow physiological processes.

The cerebellum and event timing

Abstract: Damage to the cerebellum disrupts performance on a range of tasks that require precise timing including the production of skilled movements, eyeblink conditioning, and perceptual tasks such as duration discrimination. We hypothesize that such tasks involve event timing, a form of representation in which the temporal goals are explicitly represented. For example, during finger tapping, the goal to produce evenly paced intervals invokes an explicit temporal representation of the time between successive contact points with the tapping surface. In contrast, timing can be an emergent property in other actions, reflecting temporal consistencies that arise through the control of other movement parameters. One example is continuous circle drawing, a task in which temporal consistency can be achieved by maintaining a constant angular velocity or minimizing higher‐order derivatives (e.g., jerk). Temporal consistency on event and emergent timing tasks is not correlated and patients with cerebellar damage show no increase in temporal variability during continuous circle drawing. While the cerebellum likely contributes to performance of a wide range of skilled behaviors, it appears to be especially important when the tasks entail event timing.

The Cognitive and Neural Architecture of Sequence Representation

The authors theorize that 2 neurocognitive sequence-learning systems can be distinguished in serial reaction time experiments, one dorsal (parietal and supplementary motor cortex) and the other ventral (temporal and lateral prefrontal cortex). Dorsal system learning is implicit and associates noncategorized stimuli within dimensional modules. Ventral system learning can be implicit or explicit It also allows associating events across dimensions and therefore is the basis of cross-task integration or interference, depending on degree of cross-task correlation of signals. Accordingly, lack of correlation rather than limited capacity is responsible for dual-task effects on learning. The theory is relevant to issues of attentional effects on learning; the representational basis of complex, sequential skills; hippocampal-versus basal ganglia-based learning; procedural versus declarative memory; and implicit versus explicit memory.

Dedicated and intrinsic models of time perception

Two general frameworks have been articulated to describe how the passage of time is perceived. One emphasizes that the judgment of the duration of a stimulus depends on the operation of dedicated neural mechanisms specialized for representing the temporal relationships between events. Alternatively, the representation of duration could be ubiquitous, arising from the intrinsic dynamics of nondedicated neural mechanisms. In such models, duration might be encoded directly through the amount of activation of sensory processes or as spatial patterns of activity in a network of neurons. Although intrinsic models are neurally plausible, we highlight several issues that must be addressed before we dispense with models of duration perception that are based on dedicated processes.

Perception and production of temporal intervals across a range of durations: evidence for a common timing mechanism

Study participants performed time perception and production tasks over a set of 4 intervals ranging from 325 to 550 ms. In 3 experiments, variability on both the production and perception tasks was found to be linearly related to the square of the target intervals. If the perception and production of short temporal intervals use a common timing mechanism, the slopes of the functions for the 2 tasks should be identical. The results of Experiment 1 failed to support this prediction. However, when the 2 tasks were made more similar by providing a single (Experiment 2) or multiple (Experiment 3) presentations of the target interval per judgment or production, the perception and production functions were nearly identical. The results suggest that temporal judgments and productions are based on an integrated internal representation of the target interval rather than reference to an internal oscillatory process.

Does the Cerebellum Provide a Common Computation for Diverse Tasks? A Timing Hypothesisa

The cerebellum provides a temporal computation for a number of tasks. We have found that the accuracy in timing motor responses is correlated across different motor effectors. Moreover, perceptual acuity in judging durations of auditory intervals is correlated with motoric measures of timing. These results suggest a common process underlying timing of different sorts, and that this process may depend on a specific neural system. Our data indicate that damage to the cerebellum impairs motor and perceptual timing. Patients with cerebellar lesions are also impaired at judging the velocity of a moving visual stimulus, a process that would appear to require precise timing. Furthermore, the lateral cerebellum has been implicated in classical “eyeblink” conditioning of the rabbit’s nictitating membrane response. Because classical conditioning of discrete, adaptive responses is precisely timed, we argue that the cerebellum is the conditioning site for this response because of the need for temporal computation. Classical conditioning of responses such as of heart rate, which is not so precisely timed, does not depend on the cerebellum. The cerebellar influence on locomotion may also be one of providing temporal information. Clumsy children appear as a group to have poor timing, not only on motor production but on perception as well, as would be expected if a general computation is impaired. Because of the importance of the discovery of a cerebellar role in classical conditioning, we begin our argument with respect to classical conditioning.

Dynamics of hemispheric specialization and integration in the context of motor control

Behavioural and neurophysiological evidence convincingly establish that the left hemisphere is dominant for motor skills that are carried out with either hand or those that require bimanual coordination. As well as this prioritization, we argue that specialized functions of the right hemisphere are also indispensable for the realization of goal-directed behaviour. As such, lateralization of motor function is a dynamic and multifaceted process that emerges across different timescales and is contingent on task- and performer-related determinants.