The effect of salient stimuli on neural oscillations, isometric force, and their coupling.

Survival in a suddenly-changing environment requires animals not only to detect salient stimuli, but also to promptly respond to them by initiating or revising ongoing motor processes. We recently discovered that the large vertex brain potentials elicited by sudden supramodal stimuli are strongly coupled with a multiphasic modulation of isometric force, a phenomenon that we named cortico-muscular resonance (CMR). Here, we extend our investigation of the CMR to the time-frequency domain. We show that (i) both somatosensory and auditory stimuli evoke a number of phase-locked and non-phase-locked modulations of EEG spectral power. Remarkably, (ii) some of these phase-locked and non-phase-locked modulations are also present in the Force spectral power. Finally, (iii) EEG and Force time-frequency responses are correlated in two distinct regions of the power spectrum. An early, low-frequency region (∼4 Hz) reflects the previously-described coupling between the phase-locked EEG vertex potential and force modulations. A late, higher-frequency region (beta-band, ∼20 Hz) reflects a second coupling between the non-phase-locked increase of power observed in both EEG and Force. In both time-frequency regions, coupling was maximal over the sensorimotor cortex contralateral to the hand exerting the force, suggesting an effect of the stimuli on the tonic corticospinal drive. Thus, stimulus-induced CMR occurs across at least two different types of cortical activities, whose functional significance in relation to the motor system should be investigated further. We propose that these different types of corticomuscular coupling are important to alter motor behaviour in response to salient environmental events

The effect of salient stimuli on neural oscillations, isometric force, and their coupling

Survival in a suddenly-changing environment requires animals not only to detect salient stimuli, but also to promptly respond to them by initiating or revising ongoing motor processes. We recently discovered that the large vertex brain potentials elicited by sudden supramodal stimuli are strongly coupled with a multiphasic modulation of isometric force, a phenomenon that we named cortico-muscular resonance (CMR). Here, we extend our investigation of the CMR to the time-frequency domain. We show that (i) both somatosensory and auditory stimuli evoke a number of phase-locked and non-phase-locked modulations of EEG spectral power. Remarkably, (ii) some of these phase-locked and non-phase-locked modulations are also present in the Force spectral power. Finally, (iii) EEG and Force time-frequency responses are correlated in two distinct regions of the power spectrum. An early, low-frequency (∼4 Hz) region reflects the previously-described coupling between the phase-locked EEG vertex potential and force modulations. A late, higher-frequency (beta-band, ∼20 Hz) region reflects a second coupling between the non-phase-locked increase of power observed in both EEG and Force. In both time-frequency regions, coupling was maximal over the sensorimotor cortex contralateral to the hand exerting the force, suggesting an effect of the stimuli on the tonic corticospinal drive. Thus, stimulus-induced CMR occurs across at least two different types of cortical activities, whose functional significance in relation to the motor system should be investigated further. We propose that these different types of corticomuscular coupling are important to alter motor behavior in response to salient environmental events

Towards a unified neural mechanism for reactive adaptive behaviour

Surviving in natural environments requires animals to sense sudden events and swiftly adapt behaviour accordingly. The study of such Reactive Adaptive Behaviour (RAB) has been central to a number of research streams, all orbiting around movement science but progressing in parallel, with little cross-field fertilization. We first provide a concise review of these research streams, independently describing four types of RAB: (1) cortico-muscular resonance, (2) stimulus locked response, (3) online motor correction and (4) action stopping. We then highlight remarkable similarities across these four RABs, suggesting that they might be subserved by the same neural mechanism, and propose directions for future research on this topic

Saliency Detection as a Reactive Process: Unexpected Sensory Events Evoke Corticomuscular Coupling.

Survival in a fast-changing environment requires animals not only to detect unexpected sensory events, but also to react. In humans, these salient sensory events generate large electrocortical responses, which have been traditionally interpreted within the sensory domain. Here we describe a basic physiological mechanism coupling saliency-related cortical responses with motor output. In four experiments conducted on 70 healthy participants, we show that salient substartle sensory stimuli modulate isometric force exertion by human participants, and that this modulation is tightly coupled with electrocortical activity elicited by the same stimuli. We obtained four main results. First, the force modulation follows a complex triphasic pattern consisting of alternating decreases and increases of force, time-locked to stimulus onset. Second, this modulation occurs regardless of the sensory modality of the eliciting stimulus. Third, the magnitude of the force modulation is predicted by the amplitude of the electrocortical activity elicited by the same stimuli. Fourth, both neural and motor effects are not reflexive but depend on contextual factors. Together, these results indicate that sudden environmental stimuli have an immediate effect on motor processing, through a tight corticomuscular coupling. These observations suggest that saliency detection is not merely perceptive but reactive, preparing the animal for subsequent appropriate actions.SIGNIFICANCE STATEMENT Salient events occurring in the environment, regardless of their modalities, elicit large electrical brain responses, dominated by a widespread "vertex" negative-positive potential. This response is the largest synchronization of neural activity that can be recorded from a healthy human being. Current interpretations assume that this vertex potential reflects sensory processes. Contrary to this general assumption, we show that the vertex potential is strongly coupled with a modulation of muscular activity that follows the same pattern. Both the vertex potential and its motor effects are not reflexive but strongly depend on contextual factors. These results reconceptualize the significance of these evoked electrocortical responses, suggesting that saliency detection is not merely perceptive but reactive, preparing the animal for subsequent appropriate actions

A cortical mechanism linking saliency detection and motor reactivity in rhesus monkeys

: Sudden and surprising sensory events trigger neural processes that swiftly adjust behavior. To study the phylogenesis and the mechanism of this phenomenon, we trained two male rhesus monkeys to keep a cursor inside a visual target by exerting force on an isometric joystick. We examined the effect of surprising auditory stimuli on exerted force, scalp electroencephalographic (EEG) activity, and local field potentials (LFP) recorded from the dorso-lateral prefrontal cortex. Auditory stimuli elicited (1) a biphasic modulation of isometric force: a transient decrease followed by a corrective tonic increase, and (2) EEG and LFP deflections dominated by two large negative-positive waves (N70 and P130). The EEG potential was maximal at the scalp vertex, highly reminiscent of the human 'vertex potential'. Electrocortical potentials and force were tightly coupled: the P130 amplitude predicted the magnitude of the corrective force increase, particularly in the LFPs recorded from deep rather than superficial cortical layers. These results disclose a phylogenetically-preserved cortico-motor mechanism supporting adaptive behavior in response to salient sensory events.Significance Statement Survival in the natural world depends on an animal's capacity to adapt ongoing behavior to unexpected events. To study the neural mechanisms underlying this capacity, we trained monkeys to apply constant force on a joystick while we recorded their brain activity from the scalp and, invasively, from the prefrontal cortex contralateral to the hand holding the joystick. Unexpected auditory stimuli elicited a biphasic force modulation: a transient reduction followed by a corrective adjustment. The same stimuli also elicited EEG and LFP responses, dominated by a biphasic wave that predicted the magnitude of the behavioral adjustment. These results disclose a phylogenetically-preserved cortico-motor mechanism supporting adaptive behavior in response to unexpected events

Lateralised dynamic modulations of corticomuscular coherence associated with bimanual learning of rhythmic patterns

Supplementary Information: The online version contains supplementary material available at https://doi.org/ 10.1038/s41598-022-10342-5Human movements are spontaneously attracted to auditory rhythms, triggering an automatic activation of the motor system, a central phenomenon to music perception and production. Cortico- muscular coherence (CMC) in the theta, alpha, beta and gamma frequencies has been used as an index of the synchronisation between cortical motor regions and the muscles. Here we investigated how learning to produce a bimanual rhythmic pattern composed of low- and high-pitch sounds affects CMC in the beta frequency band. Electroencephalography (EEG) and electromyography (EMG) from the left and right First Dorsal Interosseus and Flexor Digitorum Superficialis muscles were concurrently recorded during constant pressure on a force sensor held between the thumb and index finger while listening to the rhythmic pattern before and after a bimanual training session. During the training, participants learnt to produce the rhythmic pattern guided by visual cues by pressing the force sensors with their left or right hand to produce the low- and high-pitch sounds, respectively. Results revealed no changes after training in overall beta CMC or beta oscillation amplitude, nor in the correlation between the left and right sides for EEG and EMG separately. However, correlation analyses indicated that left- and right-hand beta EEG–EMG coherence were positively correlated over time before training but became uncorrelated after training. This suggests that learning to bimanually produce a rhythmic musical pattern reinforces lateralised and segregated cortico-muscular communication.This work was supported by a grant from the Australian Research Council (DP170104322)

Cortico-muscular coherence in sensorimotor synchronisation

This thesis sets out to investigate the neuro-muscular control mechanisms underlying the ubiquitous phenomenon of sensorimotor synchronisation (SMS). SMS is the coordination of movement to external rhythms, and is commonly observed in everyday life. A large body of research addresses the processes underlying SMS at the levels of behaviour and brain. Comparatively, little is known about the coupling between neural and behavioural processes, i.e. neuro-muscular processes. Here, the neuro-muscular processes underlying SMS were investigated in the form of cortico-muscular coherence measured based on Electroencephalography (EEG) and Electromyography (EMG) recorded in human healthy participants. These neuro-muscular processes were investigated at three levels of engagement: passive listening and observation of rhythms in the environment, imagined SMS, and executed SMS, which resulted in the testing of three hypotheses: (i) Rhythms in the environment, such as music, spontaneously modulate cortico-muscular coupling, (ii) Movement intention modulates cortico-muscular coupling, and (iii) Cortico-muscular coupling is dynamically modulated during SMS time-locked to the stimulus rhythm. These three hypotheses were tested through two studies that used Electroencephalography (EEG) and Electromyography (EMG) recordings to measure Cortico-muscular coherence (CMC). First, CMC was tested during passive music listening, to test whether temporal and spectral properties of music stimuli known to induce groove, i.e., the subjective experience of wanting to move, can spontaneously modulate the overall strength of the communication between the brain and the muscles. Second, imagined and executed movement synchronisation was used to investigate the role of movement intention and dynamics on CMC. The two studies indicate that both top-down, and somatosensory and/or proprioceptive processes modulate CMC during SMS tasks. Although CMC dynamics might be linked to movement dynamics, no direct correlation between movement performance and CMC was found. Furthermore, purely passive auditory or visual rhythmic stimulation did not affect CMC. Together, these findings thus indicate that movement intention and active engagement with rhythms in the environment might be critical in modulating CMC. Further investigations of the mechanisms and function of CMC are necessary, as they could have important implications for clinical and elderly populations, as well as athletes, where optimisation of motor control is necessary to compensate for impaired movement or to achieve elite performance

High-precision voluntary movements are largely independent of preceding vertex potentials elicited by sudden sensory events.

KEY POINTS: Salient and sudden sensory events generate a remarkably large response in the human brain, the vertex wave (VW). The VW is coupled with a modulation of a voluntarily-applied isometric force. In the present study, we tested whether the VW is also related to executing high-precision movements. The execution of a voluntary high-precision movement remains relatively independent of the brain activity reflected by the preceding VW. The apparent relationship between the positive VW and movement onset time is explained by goal-related but stimulus-independent neural activities. These results highlight the need to consider such goal-related but stimulus-independent neural activities when attempting to relate event-related potential amplitude with perceptual and behavioural performance. ABSTRACT: Salient and fast-rising sensory events generate a large biphasic vertex wave (VW) in the human electroencephalogram (EEG). We recently reported that the VW is coupled with a modulation of concomitantly-applied isometric force. In the present study, in five experiments, we tested whether the VW is also related to high-precision visuomotor control. We obtained three results. First, the saliency-induced increase in VW amplitude was paralleled by a modulation in two of the five extracted movement parameters: a reduction in the onset time of the voluntary movement (P < 0.005) and an increase in movement accuracy (P < 0.005). Second, spontaneous trial-by-trial variability in vertex wave amplitude, for a given level of stimulus saliency, was positively correlated with movement onset time (P < 0.001 in four out of five experiments). Third, this latter trial-by-trial correlation was explained by a widespread EEG negativity independent of the occurrence of the positive VW, although overlapping in time with it. These results indicate that (i) the execution of a voluntary high-precision movement remains relatively independent of the neural processing reflected by the preceding VW, with (ii) the exception of movement onset time, for which saliency-based contextual effects are dissociated from trial-by-trial effects. These results also indicate that (iii) attentional effects can produce spurious correlations between event-related potentials (ERPs) and behavioural measures. Although sudden salient stimuli trigger characteristic EEG responses coupled with distinct reactive components within an ongoing isometric task, the results of the present study indicate that the execution of a subsequent voluntary movement appears largely protected from such saliency-based modulation, with the exception of movement onset time

Brain Responses to Surprising Stimulus Offsets: Phenomenology and Functional Significance

Abrupt increases of sensory input (onsets) likely reflect the occurrence of novel events or objects in the environment, potentially requiring immediate behavioral responses. Accordingly, onsets elicit a transient and widespread modulation of ongoing electrocortical activity: the Vertex Potential (VP), which is likely related to the optimisation of rapid behavioral responses. In contrast, the functional significance of the brain response elicited by abrupt decreases of sensory input (offsets) is more elusive, and a detailed comparison of onset and offset VPs is lacking. In four experiments conducted on 44 humans, we observed that onset and offset VPs share several phenomenological and functional properties: they (1) have highly similar scalp topographies across time, (2) are both largely comprised of supramodal neural activity, (3) are both highly sensitive to surprise and (4) co-occur with similar modulations of ongoing motor output. These results demonstrate that the onset and offset VPs largely reflect the activity of a common supramodal brain network, likely consequent to the activation of the extralemniscal sensory system which runs in parallel with core sensory pathways. The transient activation of this system has clear implications in optimizing the behavioral responses to surprising environmental changes

IFCN-endorsed practical guidelines for clinical magnetoencephalography (MEG)

Magnetoencephalography (MEG) records weak magnetic fields outside the human head and thereby provides millisecond-accurate information about neuronal currents supporting human brain function. MEG and electroencephalography (EEG) are closely related complementary methods and should be interpreted together whenever possible. This manuscript covers the basic physical and physiological principles of MEG and discusses the main aspects of state-of-the-art MEG data analysis. We provide guidelines for best practices of patient preparation, stimulus presentation, MEG data collection and analysis, as well as for MEG interpretation in routine clinical examinations. In 2017, about 200 whole-scalp MEG devices were in operation worldwide, many of them located in clinical environments. Yet, the established clinical indications for MEG examinations remain few, mainly restricted to the diagnostics of epilepsy and to preoperative functional evaluation of neurosurgical patients. We are confident that the extensive ongoing basic MEG research indicates potential for the evaluation of neurological and psychiatric syndromes, developmental disorders, and the integrity of cortical brain networks after stroke. Basic and clinical research is, thus, paving way for new clinical applications to be identified by an increasing number of practitioners of MEG. (C) 2018 International Federation of Clinical Neurophysiology. Published by Elsevier B.V.Peer reviewe