Cortical Preparatory Activity Research Articles

Cortical preparatory activity indexes learned motor memories.

The brain's remarkable ability to learn and execute various motor behaviours harnesses the capacity of neural populations to generate a variety of activity patterns. Here we explore systematic changes in preparatory activity in motor cortex that accompany motor learning. We trained rhesus monkeys to learn an arm-reaching task1 in a curl force field that elicited new muscle forces for some, but not all, movement directions2,3. We found that in a neural subspace predictive of hand forces, changes in preparatory activity tracked the learned behavioural modifications and reassociated4 existing activity patterns with updated movements. Along a neural population dimension orthogonal to the force-predictive subspace, we discovered that preparatory activity shifted uniformly for all movement directions, including those unaltered by learning. During a washout period when the curl field was removed, preparatory activity gradually reverted in the force-predictive subspace, but the uniform shift persisted. These persistent preparatory activity patterns may retain a motor memory of the learned field5,6 and support accelerated relearning of the same curl field. When a set of distinct curl fields was learned in sequence, we observed a corresponding set of field-specific uniform shifts which separated the associated motor memories in the neural state space7-9. The precise geometry of these uniform shifts in preparatory activity could serve to index motor memories, facilitating the acquisition, retention and retrieval of a broad motor repertoire.

Cortical preparatory activity during motor learning reflects visuomotor retention deficits after punishment feedback.

Previous studies have shown that reinforcement-based motor learning requires the brain to process feedback-related information after movement execution. However, whether reinforcement feedback changes how the brain processes motor preparation before movement execution is unclear. By using electroencephalography (EEG), this study investigates whether reinforcement feedback changes cortical preparatory activity to modulate motor learning and memory. Human subjects were divided in three groups [reward, punishment, control] to perform a visuomotor rotation task under different conditions that assess adaptation (learning) and retention (memory) during the task. Reinforcement feedback was provided in the form of points after each trial that signaled monetary gains (reward) or losses (punishment). EEG was utilized to evaluate the amplitude of movement readiness potentials (MRPs) at the beginning of each trial for each group during the adaptation and retention conditions of the task. The results show that punishment feedback significantly decreased MRPs amplitude during both task conditions compared to Reward and Control groups. Moreover, the punishment-related decrease in MRPs amplitude paralleled decreases in motor performance during the retention but not the adaptation condition. No changes in MRPs or motor performance were observed in the Reward group. These results support the idea that reinforcement feedback modulates motor preparation and suggest that changes in cortical preparatory activity contribute to the visuomotor retention deficits observed after punishment feedback.

Fear of movement-related pain disturbs cortical preparatory activity after becoming aware of motor intention

Fear of movement-related pain is known to disturb the process of motor preparation in patients with chronic pain. In the present study, we aimed to clarify the neural mechanisms underlying the influence of fear movement-related pain on motor preparatory brain activity using Libet’s clock and electroencephalography (EEG). Healthy participants were asked to press a button while watching a rotating Libet’s clock-hand, and report the number on the clock (“W time”) when they made the “decision” to press the button with their right index finger. Immediately after pressing the button, a painful electrical stimulus was delivered to the dorsum of the left hand, causing participants to feel fear of movement (button press-related pain). We found that fear of movement-related pain caused the W time to be early, and that the amplitudes of readiness potentials (RPs) increased after awareness of motor intention emerged. In addition, fear of movement-related pain caused over-activation of the medial frontal cortex, supplementary motor area, cingulate motor area, and primary motor cortex after participants became aware of their motor intention. Such over-activation might result from conflict between the unrealized desire to escape from a painful experience and motivation to perform a required motor task.

Mechanisms that allow cortical preparatory activity without inappropriate movement.

We reveal a novel mechanism that explains how preparatory activity can evolve in motor-related cortical areas without prematurely inducing movement. The smooth eye movement region of the frontal eye fields (FEFSEM) is a critical node in the neural circuit controlling smooth pursuit eye movement. Preparatory activity evolves in the monkey FEFSEM during fixation in parallel with an objective measure of visual-motor gain. We propose that the use of FEFSEM output as a gain signal rather than a movement command allows for preparation to progress in pursuit without causing movement. We also show that preparatory modulation of firing rate in FEFSEM predicts movement, providing evidence against the 'movement-null' space hypothesis as an explanation of how preparatory activity can progress without movement. Finally, there is a partial reorganization of FEFSEM population activity between preparation and movement that would allow for a directionally non-specific component of preparatory visual-motor gain enhancement in pursuit.

Does hypnotic susceptibility influence information processing speed and motor cortical preparatory activity?

Responsiveness to suggestions while hypnotized is termed hypnotic susceptibility. An association between reaction time and hypnotic susceptibility has been demonstrated, but whether distinct changes in brain activity accompany this relationship remains unclear. We investigated the effect of hypnotic susceptibility on the speed of information processing and motor cortical preparatory activity. Twenty-one “low” (LowHS) and fifteen “high” (HighHS) hypnotically susceptible right-handed participants performed precued simple (SRT) and choice (CRT) reaction time key-press tasks under hypnotized and non-hypnotized conditions. Force and surface electromyography data were recorded from left and right index fingers. The contingent negative variation (CNV) was derived from electroencephalography data. Mean reaction time and premotor time was shorter in HighHS participants than LowHS participants for both simple and choice reaction time tasks. HighHS participants in the hypnotized state performed fewer errors than HighHS participants in the non-hypnotized state and LowHS participants in either state for the SRT task. HighHS participants made fewer errors overall than LowHS participants for the CRT task. Mean C3/C4 CNV amplitude was larger in HighHS than in LowHS participants. Furthermore, larger CNV amplitude was associated with shorter premotor time. Our findings indicate that shorter reaction time in the high hypnotically susceptible group is associated with a greater change in brain activity during motor preparation. One interpretation is that hypnotic susceptibility and neural mechanisms of arousal and selective attention are linked.

A cortico-cerebellar loop for motor planning.

Persistent and ramping neural activity in the frontal cortex anticipates specific movements1-6. Preparatory activity is distributed across several brain regions7,8, but it is unclear which brain areas are involved and how this activity is mediated by multi-regional interactions. The cerebellum is thought to be primarily involved in the short-timescale control of movement9-12; however, roles for this structure in cognitive processes have also been proposed13-16. In humans, cerebellar damage can cause defects in planning and working memory13. Here we show that persistent representation of information in the frontal cortex during motor planning is dependent on the cerebellum. Mice performed a sensory discrimination task in which they used short-term memory to plan a future directional movement. A transient perturbation in the medial deep cerebellar nucleus (fastigial nucleus) disrupted subsequent correct responses without hampering movement execution. Preparatory activity was observed in both the frontal cortex and the cerebellar nuclei, seconds before the onset of movement. The silencing of frontal cortex activity abolished preparatory activity in the cerebellar nuclei, and fastigial activity was necessary to maintain cortical preparatory activity. Fastigial output selectively targeted the behaviourally relevant part of the frontal cortex through the thalamus, thus closing a cortico-cerebellar loop. Our results support the view that persistent neural dynamics during motor planning is maintained by neural circuits that span multiple brain regions17, and that cerebellar computations extend beyond online motor control13-15,18.

Effects of amplitude cueing on postural responses and preparatory cortical activity of people with Parkinson disease.

Persons with Parkinson disease (PD) are unable to modify their postural responses, and show an associated increase in cortical preparatory activity for anticipated postural perturbations. In this study we asked whether participants with PD could modify their postural responses and cortical preparatory activity when cued to focus on increasing movement amplitude before a series of predictable postural perturbations. Twelve participants with PD performed postural responses to 30 identical backward surface translations. We cued participants to focus on increasing movement amplitude, and examined the effects of cueing by measuring postural responses (center-of-pressure initial rate of change, automatic postural response stability, peak trunk flexion, peak ankle extension) and preparatory cortical activity (electroencephalographic measures of contingent negative variation, alpha and beta event-related desynchronization). Participants with PD modified their postural responses during the amplitude trials by increasing trunk flexion, slowing center-of-pressure initial rate of change, and decreasing automatic postural response stability. However, no significant differences in contingent negative variation amplitude or alpha or beta event-related desynchronization were observed with versus without amplitude cueing. Persons with PD were able to modify their feet-in-place postural responses with amplitude cueing. These changes were not associated with changes in cortical preparation during amplitude cue trials, suggesting that other regions or measures of brain function were responsible for changes in postural responses. Future studies are needed to determine the effects of long-term amplitude-cueing practice on cortical preparation and postural stability.Video Abstract available. See Video (Supplemental Digital Content 1, http://links.lww.com/JNPT/A78) for more insights from the authors.

Cortical Preparatory Activity: Representation of Movement or First Cog in a Dynamical Machine?

The motor cortices are active during both movement and movement preparation. A common assumption is that preparatory activity constitutes a subthreshold form of movement activity: a neuron active during rightward movements becomes modestly active during preparation of a rightward movement. We asked whether this pattern of activity is, in fact, observed. We found that it was not: at the level of a single neuron, preparatory tuning was weakly correlated with movement-period tuning. Yet, somewhat paradoxically, preparatory tuning could be captured by a preferred direction in an abstract "space" that described the population-level pattern of movement activity. In fact, this relationship accounted for preparatory responses better than did traditional tuning models. These results are expected if preparatory activity provides the initial state of a dynamical system whose evolution produces movement activity. Our results thus suggest that preparatory activity may not represent specific factors, and may instead play a more mechanistic role.

Delay of Movement Caused by Disruption of Cortical Preparatory Activity

We tested the hypothesis that delay-period activity in premotor cortex is essential to movement preparation. During a delayed-reach task, we used subthreshold intracortical microstimulation to disrupt putative "preparatory" activity. Microstimulation led to a highly specific increase in reach reaction time. Effects were largest when activity was disrupted around the time of the go cue. Earlier disruptions, which presumably allowed movement preparation time to recover, had only a weak impact. Furthermore, saccadic reaction time showed little or no increase. Finally, microstimulation of nearby primary motor cortex, even when slightly suprathreshold, had little effect on reach reaction time. These findings provide the first evidence, of a causal and temporally specific nature, that activity in premotor cortex is fundamental to movement preparation. Furthermore, although reaction times were increased, the movements themselves were essentially unperturbed. This supports the suggestion that movement preparation is an active and actively monitored process and that movement can be delayed until inaccuracies are repaired. These results are readily interpreted in the context of the recently developed optimal-subspace hypothesis.

Movement-related cortical potentials associated with voluntary relaxation of foot muscles

Objective: In our previous study of movement-related cortical potential (MRCP) in association with the voluntary relaxation of the hand muscle, Bereitschaftspotential (BP) was maximal at the vertex and symmetrically distributed, and Negative Slope (NS′) was maximal over the contralateral central region. In order to clarify the generator sources of MRCP with voluntary muscle relaxation, we recorded MRCP in association with voluntary relaxation of the foot.Methods: MRCP in association with plantar flexion of the foot caused by voluntary relaxation of the tibialis anterior muscle was recorded in 10 normal subjects.Results: The BP started at about 1.7 s before the onset of the muscle relaxation, followed by NS′ starting at about 650 ms before it. Both were maximal at the vertex and symmetrically distributed. There was no additional EEG activity in the lateral frontal areas, which are presumably located over the primary negative motor areas (PNMA).Conclusions: It is concluded that the voluntary muscle relaxation, similarly to the voluntary muscle contraction, involves the cortical preparatory activity at least in the primary motor area (M1) and probably the supplementary motor areas (SMAs). There is no evidence to suggest that the PNMA is also active prior to the voluntary muscle relaxation.