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The neural correlates of memory formation in humans have long been investigated by exposing subjects to diverse material and comparing responses to items later remembered to those forgotten. Tasks requiring memorization of sensory sequences afford unique possibilities for linking neural memorization processes to behavior, because, rather than comparing across different items of varying content, each individual item can be examined across the successive learning states of being initially unknown, newly learned, and eventually, fully known. Sequence learning paradigms have not yet been exploited in this way, however. Here, we analyze the event-related potentials of subjects attempting to memorize sequences of visual locations over several blocks of repeated observation, with respect to pre- and post-block recall tests. Over centro-parietal regions, we observed a rapid P300 component superimposed on a broader positivity, which exhibited distinct modulations across learning states that were replicated in two separate experiments. Consistent with its well-known encoding of surprise, the P300 deflection monotonically decreased over blocks as locations became better learned and hence more expected. In contrast, the broader positivity was especially elevated at the point when a given item was newly learned, i.e., started being successfully recalled. These results implicate the Broad Positivity in endogenously-driven, intentional memory formation, whereas the P300, in processing the current stimulus to the degree that it was previously uncertain, indexes the cumulative knowledge thereby gained. The decreasing surprise/P300 effect significantly predicted learning success both across blocks and across subjects. This presents a new, neural-based means to evaluate learning capabilities independent of verbal reports, which could have considerable value in distinguishing genuine learning disabilities from difficulties to communicate the outcomes of learning, or perceptual impairments, in a range of clinical brain disorders.

Adapting movements to a visual rotation involves the activation of right posterior parietal areas. Further performance improvement requires an increase of slow wave activity in subsequent sleep in the same areas. Here we ascertained whether a post-learning trace is present in wake EEG and whether such a trace is influenced by sleep slow waves.In two separate sessions, we recorded high-density EEG in 17 healthy subjects before and after a visuomotor rotation task, which was performed both before and after sleep. High-density EEG was recorded also during sleep. One session aimed to suppress sleep slow waves, while the other session served as a control.After learning, we found a trace in the eyes-open wake EEG as a local, parietal decrease in alpha power. After the control night, this trace returned to baseline levels, but it failed to do so after slow wave deprivation. The overnight change of the trace correlated with the dissipation of low frequency (8 Hz) NREM sleep activity only in the control session.Visuomotor learning leaves a trace in the wake EEG alpha power that appears to be renormalized by sleep slow waves.These findings link visuomotor learning to regional changes in wake EEG and sleep homeostasis.

We investigated whether dopamine influences the rate of adaptation to a visuomotor distortion and the transfer of this learning from the right to the left limb in human subjects. We thus studied patients with Parkinson disease as a putativein vivomodel of dopaminergic denervation. Despite normal adaptation rates, patients showed a reduced transfer compared with age-matched healthy controls. The magnitude of the transfer, but not of the adaptation rate, was positively predicted by the values of dopamine-transporter binding of the right caudate and putamen. We conclude that striatal dopaminergic activity plays an important role in the transfer of visuomotor skills.

Motor sequence learning is not a unitary phenomenon, but involves optimizing different components that include declarative and procedural aspects. In this work we designed an experimental approach that allows monitoring all the aspects of sequence learning using a finger opposition task and a movement-by-movement analysis. Subjects performed a visuomotor sequence learning paradigm with (Explicit) or without (Implicit) instructions and we measured response time (RT) and touch duration (TD) for each finger opposition movement of the sequence. Our results indicated that sequence learning induced a double-faced effect on motor performance: a decrease of RT and an increase of TD. However, the above changes manifested differently among subjects: all subjects that, by the end of session, had complete recall of the sequence order, reached an equal level of performance by the last sequence block while in those who had on average only a poor recall of the sequence order, learning was evident only as a slight decrease of RT across sequence blocks, while no kinematic changes (i.e., changes in TD) occurred. Our results indicate that, in the absence of specific instructions, learning evolves from an early stage in which only small decreases of RT are observed to a phase in which progressive knowledge of the sequential structure allows for dramatic changes of RT, together with a progressive change of motor performance (i.e., changes in TD).

Observation of people performing movements facilitates motor planning, execution and memory formation. Tempo, a crucial aspect involved in the execution of rhythmic movements, is normally perceived and learned through auditory channels. In this work, we ascertained whether: first, the frequency of self-paced finger movements (SPMs), which in normal subjects is around 2 Hz, is modified by prior observation of movements performed at either 1 or 3 Hz; second, such changes are lasting; third, there is an effect of time interval between observation and performance. We finally determined the effect of providing explicit information about the upcoming motor task. Seventy-two normal subjects (12 groups) performed a simple finger sequence at different intervals after observation of videos of either landscapes or finger opposition movements. Both with and without information about the upcoming task, observation influenced the tempo of SPMs and led to memory formation. With knowledge of the upcoming task, such changes occurred at all observation-execution intervals, while without instructions, changes took place only when SPMs were performed immediately after observation. Compared to explicit instructions, the absence of instructions produced tempo's changes that more closely resembled the observed rhythms. We conclude that learning requires a prompt comparison between visual and sensorimotor representations of movements; moreover, learning with explicit instructions is more efficient, as activity in both the dorsal and ventral streams might be potentiated by the chatecholaminergic attentional systems that promote long-term potentiation. These results provide the bases for novel neurorehabilitation strategies in terms of temporal re-organization of movement.

The ability to perform accurate sequential movements is essential to normal motor function. Learning a sequential motor behavior is comprised of two basic components: explicit identification of the order in which the sequence elements should be performed and implicit acquisition of spatial accuracy for each element. Here we investigated the time course of learning of these components for a first sequence (SEQA) and their susceptibility to interference from learning a second sequence (SEQB). We assessed explicit learning with a discrete index, the number of correct anticipatory movements, and implicit learning with a continuous variable, spatial error, which decreased during learning without subject awareness. Spatial accuracy to individual sequence elements reached asymptotic levels only when the whole sequence order was known. Interference with recall of the order of SEQA persisted even when SEQB was learned 24 h after SEQA. However, there was resistance to interference by SEQB with increased initial training with SEQA. For implicit learning of spatial accuracy, SEQB interfered at 5 min but not 24 h after SEQA. As in the case of sequence order, prolonged initial training with SEQA induced resistance to interference by SEQB. We conclude that explicit sequence learning is more susceptible to anterograde interference and implicit sequence learning is more susceptible to retrograde interference. However, both become resistant to interference with saturation training. We propose that an essential feature of motor skill learning is the process by which discrete explicit task elements are combined with continuous implicit features of movement to form flawless sequential actions.

The authors' aim was to determine the cortical mechanisms that underlie the transition from effective performance to its disruption. They thus used transcranial magnetic stimulation (TMS) to study changes of corticospinal excitability after a motor exercise that did not produce overt or perceived neuromuscular fatigue. Forty-four subjects performed either 5 or 10 min of repetitive finger movements paced by tones at 2 Hz, a frequency below the spontaneous movement rate. Changes of corticospinal excitability were assessed with TMS at rest and during motor response preparation (premovement facilitation paradigm). Over time, variability of movement rate increased, while the average movement rate shifted toward self-paced rhythms, without significant changes in other kinematic parameters. Amplitudes of motor evoked potentials at rest decreased depending on task duration and TMS intensity. Moreover, 5-min exercise induced fully compensatory increases in premovement facilitation, while 10-min exercise produced partially compensatory increases with loss of temporal modulation. Our findings suggest that protracted exercise induces significant decrements in corticospinal excitability with initial impairment of the phasic motor neurons that are recruited at higher stimulus intensities. Changes in premovement facilitation likely represent compensation of premotor areas for decreased efficiency of the primary motor cortex induced by exercise.

Recent EEG studies have shown that implicit learning involving specific cortical circuits results in an enduring local trace manifested as local changes in spectral power. Here we used a well characterized visual sequence learning task and high density-(hd-)EEG recording to determine whether also declarative learning leaves a post-task, local change in the resting state oscillatory activity in the areas involved in the learning process. Thus, we recorded hd-EEG in normal subjects before, during and after the acquisition of the order of a fixed spatial target sequence (VSEQ) and during the presentation of targets in random order (VRAN). We first determined the temporal evolution of spectral changes during VSEQ and compared it to VRAN. We found significant differences in the alpha and theta bands in three main scalp regions, a right occipito-parietal (ROP), an anterior-frontal (AFr), and a right frontal (RFr) area. The changes in frontal theta power during VSEQ were positively correlated with the learning rate. Further, post-learning EEG recordings during resting state revealed a significant increase in alpha power in ROP relative to a pre-learning baseline. We conclude that declarative learning is associated with alpha and theta changes in frontal and posterior regions that occur during the task, and with an increase of alpha power in the occipito-parietal region after the task. These post-task changes may represent a trace of learning and a hallmark of use-dependent plasticity.

With a series of novel arm-reaching tasks, we have shown that visuomotor sequence learning encompasses the acquisition of the order of sequence elements, and the ability to combine them in a single, skilled behavior. The first component, which is mostly declarative, is reflected by changes in movement onset time (OT); the second, which occurs without subject’s awareness, is measured by changes in kinematic variables, including movement time (MT). Key-press-based serial reaction time tasks (SRTT) have been used to investigate sequence learning and results interpreted as indicative of the implicit acquisition of the sequence order. One limitation to SRT studies, however, is that only one measure is used, the response time, the sum of OT and MT: this makes interpretation of which component is learnt difficult and disambiguation of implicit and explicit processes problematic. Here, we used an arm-reaching version of SRTT to propose a novel interpretation of such results. The pattern of response time changes we obtained was similar to the key-press-based tasks. However, there were significant differences between OT and MT, suggesting that both partial learning of the sequence order and skill improvement took place. Further analyses indicated that the learning of the sequence order might not occur without subjects’ awareness.

Learning deficits may be part of the early symptoms of Huntington's disease (HD). Here we characterized implicit and explicit aspects of sequence learning in eleven pre-symptomatic HD gene carriers (pHD) and eleven normal controls. Subjects moved a cursor on a digitizing tablet and performed the following tasks: SEQ: learning to anticipate the appearance of a target sequence in two blocks; VSEQ: learning a sequence by attending to the display without moving for one block, and by moving to the sequence in a successive block (VSEQtest). Explicit learning was measured with declarative scores and number of anticipatory movements. Implicit learning was measured as a strategy change reflected in movement time. By the end of SEQ, pHD had a significantly lower number of correct anticipatory movements and lower declarative scores than controls, while in VSEQ and VSEQtest these indices improved. During all three tasks, movement time changed in controls, but not in pHD. These results suggest that both explicit and implicit aspects of sequence learning may be impaired before the onset of motor symptoms. However, when attentional demands decrease, explicit, but not implicit, learning may improve.

C. Ghez, J. Gordon, and M. F. Ghilardi (1995; J. Gordon, M. F. Ghilardi, & C. Ghez, 1995; R. L. Sainburg, M. F. Ghilardi, H. Poizner, & C. Ghez, 1995) have found that proprioceptive deafferentation impairs feedforward and feedback mechanisms that control reaching movements. In the present study, the authors found immobilization-induced changes in limb kinematics, including joint motion, in 32 healthy participants who performed out-and-back movements before and after 0, 6, or 12 hr of immobilization of the left arm. Control participants did not undergo the arm immobilization procedure. Immobilization for 12 hr, but not 6 hr, caused trajectories with increased hand-path areas and altered interjoint coordination. The abnormalities were smaller in amplitude but similar in quality to those reported in deafferented patients (R. L. Sainburg et al.). In addition, movement onset point significantly drifted after immobilization. Thus, short-term limb disuse can affect interjoint coordination by acting on feedforward mechanisms. These behavioral alterations are potentially related to cortical plastic changes.