RESUMEN
The subthalamic nucleus (STN) of the basal ganglia is key to the inhibitory control of movement. Consequently, it is a primary target for the neurosurgical treatment of movement disorders like Parkinson's Disease, where modulating the STN via deep-brain stimulation (DBS) can release excess inhibition of thalamo-cortical motor circuits. However, the STN is also anatomically connected to other thalamo-cortical circuits, including those underlying cognitive processes like attention. Notably, STN-DBS can also affect these processes. This suggests that the STN may also contribute to the inhibition of non-motor activity, and that STN-DBS may cause changes to this inhibition. We here tested this hypothesis in humans. We used a novel, wireless outpatient method to record intracranial local field potentials (LFP) from STN DBS implants during a visual attention task (Experiment 1, N=12). These outpatient measurements allowed the simultaneous recording of high-density EEG, which we used to derive the steady-state visual evoked potential (SSVEP), a well-established neural index of visual attentional engagement. By relating STN activity to this neural marker of attention (instead of overt behavior), we avoided possible confounds resulting from STN's motor role. We aimed to test whether the STN contributes to the momentary inhibition of the SSVEP caused by unexpected, distracting sounds. Furthermore, we causally tested this association in a second experiment, where we modulated STN via DBS across two sessions of the task, spaced at least one week apart (N=21, no sample overlap with Experiment 1). The LFP recordings in Experiment 1 showed that reductions of the SSVEP after distracting sounds were preceded by sound-related γ-frequency (>60Hz) activity in the STN. Trial-to-trial modeling further showed that this STN activity statistically mediated the sounds' suppressive effect on the SSVEP. In Experiment 2, modulating STN activity via DBS significantly reduced these sound-related SSVEP reductions. This provides causal evidence for the role of the STN in the surprise-related inhibition of attention. These findings suggest that the human STN contributes to the inhibition of attention, a non-motor process. This supports a domain-general view of the inhibitory role of the STN. Furthermore, these findings also suggest a potential mechanism underlying some of the known cognitive side-effects of STN-DBS treatment, especially on attentional processes. Finally, our newly-established outpatient LFP recording technique facilitates the testing of the role of subcortical nuclei in complex cognitive tasks, alongside recordings from the rest of the brain, and in much shorter time than perisurgical recordings.
RESUMEN
Most studies contributing to identify the brain network for inhibitory control have investigated the cancelation of prepared-discrete actions, thus focusing on an isolated and short-lived chunk of human behavior. Aborting ongoing-continuous actions is an equally crucial ability but remains little explored. Although discrete and ongoing-continuous rhythmic actions are associated with partially overlapping yet largely distinct brain activations, it is unknown whether the inhibitory network operates similarly in both situations. Thus, distinguishing between action types constitutes a powerful means to investigate whether inhibition is a generic function. We, therefore, used independent component analysis (ICA) of EEG data and show that canceling a discrete action and aborting a rhythmic action rely on independent brain components. The ICA showed that a delta/theta power increase generically indexed inhibitory activity, whereas N2 and P3 ERP waves did so in an action-specific fashion. The action-specific components were generated by partially distinct brain sources, which indicates that the inhibitory network is engaged differently when canceling a prepared-discrete action versus aborting an ongoing-continuous action. In particular, increased activity was estimated in precentral gyri and posterior parts of the cingulate cortex for action canceling, whereas an enhanced activity was found in more frontal gyri and anterior parts of the cingulate cortex for action aborting. Overall, the present findings support the idea that inhibitory control is differentially implemented according to the type of action to revise.
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Mapeo Encefálico , Corteza Motora , Encéfalo , Electroencefalografía , Humanos , Inhibición PsicológicaRESUMEN
Inhibitory control is a crucial cognitive-control ability for behavioral flexibility that has been extensively investigated through action-stopping tasks. Multiple neurophysiological features have been proposed to represent 'signatures' of inhibitory control during action-stopping, though the processes signified by these signatures are still controversially discussed. The present study aimed to disentangle these processes by comparing simple stopping situations with those in which additional action revisions were needed. Three experiments in female and male humans were performed to characterize the neurophysiological dynamics involved in action-stopping and - changing, with hypotheses derived from recently developed two-stage 'pause-then-cancel' models of inhibitory control. Both stopping and revising an action triggered an early broad 'pause'-process, marked by frontal EEG ß-bursts and non-selective suppression of corticospinal excitability. However, partial-EMG responses showed that motor activity was only partially inhibited by this 'pause', and that this activity can be further modulated during action-revision. In line with two-stage models of inhibitory control, subsequent frontocentral EEG activity after this initial 'pause' selectively scaled depending on the required action revisions, with more activity observed for more complex revisions. This demonstrates the presence of a selective, effector-specific 'retune' phase as the second process involved in action-stopping and -revision. Together, these findings show that inhibitory control is implemented over an extended period of time and in at least two phases. We are further able to align the most commonly proposed neurophysiological signatures to these phases and show that they are differentially modulated by the complexity of action-revision.
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Behavioral adaptation to changing contextual contingencies often requires the rapid inhibition of planned or ongoing actions. Inhibitory control has been mostly studied using the stop-signal paradigm, which conceptualizes action inhibition as the outcome of a race between independent GO and STOP processes. Inhibition is predominantly considered to be independent of action type, yet it is questionable whether this conceptualization can apply to stopping an ongoing action. To test the claimed generality of action inhibition, we investigated behavioral stop-signal reaction time (SSRT) and scalp electroencephalographic (EEG) activity in two inhibition contexts: Using variants of the stop-signal task, we asked participants to cancel a prepared-discrete action or to stop an ongoing-rhythmic action in reaction to a STOP signal. The behavioral analysis revealed that the discrete and rhythmic SSRTs were not correlated. The EEG analysis showed that the STOP signal evoked frontocentral activity in the time and frequency domains (Delta/Theta range) in a task-specific manner: The P3 onset latency was the best correlate of discrete SSRT whereas N2/P3 peak-to-peak amplitude was the best correlate of rhythmic SSRT. These findings do not support a conceptualization of inhibition as action-independent but rather suggest that the differential engagement of both components of the N2/P3-complex as a function of action type pertains to functionally independent inhibition subprocesses.
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Electroencefalografía , Inhibición Psicológica , Humanos , Tiempo de Reacción/fisiologíaRESUMEN
Multisensory facilitation is known to improve the perceptual performances and reaction times of participants in a wide range of tasks, from detection and discrimination to memorization. We asked whether a multimodal signal can similarly improve action inhibition using the stop-signal paradigm. Indeed, consistent with a crossmodal redundant signal effect that relies on multisensory neuronal integration, the threshold for initiating behavioral responses is known for being reached faster with multisensory stimuli. To evaluate whether this phenomenon also occurs for inhibition, we compared stop signals in unimodal (human faces or voices) versus audiovisual modalities in natural or degraded conditions. In contrast to the expected multisensory facilitation, we observed poorer inhibition efficiency in the audiovisual modality compared with the visual and auditory modalities. This result was corroborated by both response probabilities and stop-signal reaction times. The visual modality (faces) was the most effective. This is the first demonstration of an audiovisual impairment in the domain of perception and action. It suggests that when individuals are engaged in a high-level decisional conflict, bimodal stimulation is not processed as a simple multisensory object improving the performance but is perceived as concurrent visual and auditory information. This absence of unity increases task demand and thus impairs the ability to revise the response.
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Estimulación Acústica , Percepción Auditiva/fisiología , Estimulación Luminosa , Tiempo de Reacción/fisiología , Percepción Visual/fisiología , Adulto , Femenino , Humanos , MasculinoRESUMEN
Although the engagement of sensorimotor cortices in movement is well documented, the functional relevance of brain activity patterns remains ambiguous. Especially, the cortical engagement specific to the pre-, within-, and post-movement periods is poorly understood. The present study addressed this issue by examining sensorimotor EEG activity during the performance as well as STOP-signal cued suppression of movements pertaining to two distinct classes, namely, discrete vs. ongoing rhythmic movements. Our findings indicate that the lateralized readiness potential (LRP), which is classically used as a marker of pre-movement processing, indexes multiple pre- and in- movement-related brain dynamics in a movement-class dependent fashion. In- and post-movement event-related (de)synchronization (ERD/ERS) observed in the Mu (8-13 Hz) and Beta (15-30 Hz) frequency ranges were associated with estimated brain sources in both motor and somatosensory cortical areas. Notwithstanding, Beta ERS occurred earlier following cancelled than actually performed movements. In contrast, Mu power did not vary. Whereas Beta power may reflect the evaluation of the sensory predicted outcome, Mu power might engage in linking perception to action. Additionally, the rhythmic movement forced stop (only) showed a post-movement Mu/Beta rebound, which might reflect an active "clearing-out" of the motor plan and its feedback-based online control. Overall, the present study supports the notion that sensorimotor EEG modulations are key markers to investigate control or executive processes, here initiation and inhibition, which are exerted when performing distinct movement classes.
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Ritmo beta/fisiología , Movimiento/fisiología , Corteza Sensoriomotora/fisiología , Adulto , Femenino , Humanos , MasculinoRESUMEN
In order to gauge the executive processes underlying adaptive behavior, a central criterion in psychology is the extent to which experimental findings generalize across response types. The latency of two major acts of control, action initiation and inhibition, was evaluated using a stop-signal paradigm with two response types, involving either a finger key-pressing or a wrist pen-swiping response. In both conditions, 40 participants were instructed to respond quickly to a GO stimulus but to cancel their responses when a STOP signal was presented, which occurred randomly in 25% of the trials. Taken together, analyses of reaction times and of inhibition probability functions indicated that action initiation generalized across the two response types. In contrast, the finger key-pressing and the wrist pen-swiping responses involved independent inhibition processes. These results challenge a strictly top-down view for some acts of control by showing an interaction between the executive and motor levels in terms of response modality specificity.
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Inhibición Psicológica , Movimiento , Animales , Cognición , Dedos , Caballos , Humanos , Desempeño Psicomotor , Tiempo de ReacciónRESUMEN
This study evaluated the reliability, precision, and clinically important change of the Nine-Hole Peg Test (9-HPT) over a 1-week period. Sixty-nine patients with multiple sclerosis completed the 9-HPT on two occasions 1 week apart. Test-retest reliability was based on intraclass correlation coefficient, and precision was based on standard error of measurement and coefficient of variation. Clinically important change was based on the minimal detectable change. Intraclass correlation coefficients exceed 0.90 for all 9-HPT metrics. Standard error of measurements for dominant (DH) and nondominant (NDH) hand time were 1.58 and 2.69 s, and 0.03 peg/s for both DH and nondominant NDH speed, respectively. Coefficient of variations for DH and NDH time were 4.3 and 3.8%, and 4.5 and 4.6% for DH and NDH speed. Minimal detectable changes for DH and NDH time were 19.4 and 29.1%, and 18.6 and 20.5% for DH and NDH speed. These data provide evidence on reliability, precision, and clinically important change of the 9-HPT over a 1-week period in multiple sclerosis for clinicians and researchers.