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Front. Psychol. | doi: 10.3389/fpsyg.2019.01930

Understanding Neural Oscillations in the Human Brain: From movement to consciousness and vice & versa

  • 1Free University of Brussels, Belgium

Recent theories about consciousness (Edelman, 2003; Edelman et al., 2011; Seth et al., 2006) have paved the way for new experimental paradigms. Namely, thirteen features have been proposed (Seth et al., 2006) in order to better characterize the theoretical reference frame of consciousness. Among these items the three first established that: (1) fast, irregular and low-amplitude oscillations (around 12 to 70 Hz) convoyed consciousness; (2) these oscillatory neuronal activities are organized by the thalamocortical system acting as a “dynamic core” modulated by subcortical influences; (3) consciousness is dispatched in different cortical areas depending of the conscious content. The ten other items highlight that the conscious events are unitary and that only one conscious experience emerges at a time. Accordingly, the theory of neuronal group selection (TNGS) (Edelman G.M., 1987) is advanced as a biological foundation of consciousness. Following the TNGS, a Darwinism selection has ontogenetically shaped neuronal circuits based on positive or negative outcomes on the environment and related feedbacks. In this context, the reentry process linking numerous brainstem nuclei with the thalamocortical system (Edelman and Gally, 2013) and the recurrent circuit in the cortex assuming the function of working memory (McCormick, 2001) are crucial for consciousness (Edelman et al., 2011). This implies that consciousness is a dynamic embodied process (Seth et al., 2006) and that is closely related to voluntary movement production.
The basic control of the default mode
A first trivial observation is that experiences related to consciousness involve a basic awareness state during which the human participant can verbally report self-consciousness. This implies that any kind of experimental tentative to detect the emergence of consciousness related to a sensory item or to the production of a free will action depend on the quality of the reference state commonly considered as the resting or default mode network (DMN) (Raichle, 2015; Raichle et al., 2001) which presumes a non-relevant task state. The relative permanency of the self-referential and the time to time modulation of the mind wandering (Kucyi, 2018; Smallwood and Schooler, 2015) should be taken into account as a basic experimental control for the measurement of the conscious events (Northoff et al., 2010). Until now, such type of control remains difficult for generalizing. It was recently demonstrated (Davey et al., 2016) that body-self-referential processes are assumed by the posterior cingulate cortex and regulated by the medial prefrontal cortex which are two areas of the DMN. Also, the slow fluctuations of the eyes position during visual fixation influence the intrinsic DMN activity (Fransson et al., 2014). This indicates that both gaze position and also body posture probably influence the DMM activity as illustrated by ‘zazen’ meditation practice (Brandmeyer et al., 2019) during which the postural control is required.
The oscillatory dialogue between bottom-up and top-down
The bottom-up process is recognized as a stimulus-driven processing able to produce movement without volition and being out of the consciousness scope. In contrast, top-down is considered as an expectation-driven processing (Engel et al., 2001) which implies voluntary action realized in full consciousness. Three stages of the voluntary movement have been differentiated: the first one is preconceptual and involves an inner impulse constituting the bottom up component of the action, the second one where the intention is conceptual, specific and more conscious and the third one where it is decided whether to perform or to withhold the action constituting to the top-down component (Schmidt et l. 2016). Oscillations underly bottom-up and top-down processes (Engel et al., 2001; Varela et al., 2001) by linking separated and distant brain areas for being together involved at different levels of the network and ensuring complex and integrative functions. The functional integration role of oscillations make them an attractive candidate mechanism for approaching a so high level of complexity process as consciousness is (Crick, 1984; Tononi and Edelman, 1998). Dynamics of oscillations could thus underly the mechanisms of unity of consciousness (Cleeremans, 2003). In the same way that the 40 Hz oscillation in the visual cortex (Eckhorn et al., 1988; Gray et al., 1989) has been pointed as the neural correlate of the visual perceptive consciousness, the thalamocortical 40 Hz oscillation might play a major role synchronizing firing of separated and differentiated cortical neural populations underlying motion consciousness (Llinás RR, 2001). In this line it has recently been shown that self-consciousness involves the existence of gamma oscillation (~ 40 Hz) carried by dopamine-dependent recurrent GABAergic neurons located through a cortical network connecting the medial frontal pre-area. anterior cingulate area, medial parietal area, and posterior cingulate area (Lou et al., 2017).
From the early scientific and clinical interest of (Charcot JM, 1889) and Ramon y Cajal (Ramón y Cajal, S., 1889) (Sala et al., 2008) for hypnosis, its related underlying mechanisms remain unresolved. Recent attempts have been made to dissociate bottom-up and top-down processing during hypnosis which would modulate consciousness and would allow the discrimination of the report of actual movement from the intention to move (Terhune et al., 2017). Hypnosis has been used as a maneuver to enhance bottom-up processing in responders by reducing the top down control exerted by the prefrontal cortex as suggested by (Gruzelier and Warren, 1993). It should be noted that the motor paralysis induced by hypnosis would not be due to direct motor inhibition but to a complex self-monitoring processes generated by the suggestion guiding feigned behaviour (Cojan et al., 2009, 2013). Interestingly, individual differences in hypnotic susceptibility have been supported by different levels of EEG phase synchronization on the frontal lobe (Baghdadi and Nasrabadi, 2012; Egner et al., 2005) suggesting that hypnotic susceptibility is linked with the efficiency of the frontal attention system.
Motor and visual perceptive consciousness
The visual perceptive consciousness is strongly dependent of eye movements (Costela et al., 2017). An interesting easily feasible experiment is that of the Rubin’s picture which demonstrates the oscillating nature of the perceptive consciousness. The perception of the image can be either a vase or that of two human opposed face profiles. The two perceptions continually and rhythmically alternate up to the point one becomes dominant. The mechanism might be assimilated to that of competitive and recurrent oscillations around a dynamic attractor which basic models include an excitatory and an inhibitory neurons reciprocally interconnected forming competitive structures and acting as dynamic attractors. This is in agreement with the theory of neuronal groups of (Changeux, 1983; Edelman G.M., 1987) staying that the synchronization of the oscillating activity determines the establishment of neuronal sets acting coherently and leading to conscious perception of the world. However not only the oscillatory nature of brain function but also the fundamental role of the ocular movements should be considered to gain further understanding in such perceptive consciousness. It is indeed the gaze placement at certain points over the Rubin’s picture that determines the emergence of the perceptive alternation. An unresolved question is whether such movement results from a voluntary conscious command or not. In the same vein, body movement is ontogenetically driven by reaching reward linked to an object or to a living being situated somewhere in the space. For this, gaze movement is precisely oriented to the target by means of head-eye saccade commanded by the superior colliculus which receives specific basal ganglia inputs depending whether voluntary consciously or automatic subconsciously selected (Kim and Hikosaka, 2015).
Intentional actions in social context
The way we process the intentional actions of others in a social context can offer new experimental perspectives (Decety and Cacioppo, 2012). According to the Social Relevance Hypothesis (SRH) (Neufeld et al., 2016), various capacities in social cognition crucially depend on social stimuli to which a high degree of attentional relevance has been automatically assigned. Numerous social stimuli generate powerful bottom-up processes which produce automatic gesture. It is difficult to disregard, escape or suppress such inputs in the social environment. In this context, the mu rhythm has been considered as an oscillatory index of the intentional action processing (Perry et al., 2011). Concretely, it is suggested that mu rhythm plays a crucial function in the sensorimotor transformation (Pineda, 2005) and in the consciousness of motor action. For example, (Simon and Mukamel, 2016) studied consciousness perception of hand movements displayed on videos with different degrees of visibility. Conscious perception was characterized with event related desynchronization (ERD) of beta (15-25 Hz) oscillation at about 500 ms after the video onset and it was followed by mu (8-10 Hz) ERD oscillation at about 800 ms. These ERDs were stronger in the contralateral sensorimotor cortex. During unconscious perception, only beta ERD occurred. These results play in favor of a progressive recruitment of the neuronal activities of the mirror neuron system (MNS) from unconscious to conscious perception. The timing of the reported ERD (~ 500 ms) is compatible to the reentrant dynamic core concept (Edelman, 2003) which implies time for the activation of numerous loops integrating signals coming from the world, the body and the self. The ability to be conscious of the actions and the intentions of others has been suggested and supported by clinical studies, to be linked to the NMS (Avanzini et al., 2012)(Neufeld et al., 2016). Patients with anosognosia induced by right frontal and parietal cortices lesions are not only unconscious of their own paralyzed limb but also unconscious of the same side same limb of another person (Ramachandran and Rogers-Ramachandran, 1996). Mu ERD has been linked to the MNS as it is reduced in the affected sensorimotor hemisphere in stroke patients observing a grasping hand movement (Frenkel-Toledo et al., 2014). However, its role as index of the MNS seems to be compromised and it would be more related to the sensory processing Coll et al., (2017).
The individual self and body identity
From the integrated information theory (Tononi et al., 2016), the complexity of the interconnected brain tissue quantifies the level of consciousness and movement consciousness originates from movement experience together with the related and concomitant multi-sensory entries. The cause and effect relationships encoded during movement experience by the highly interconnected brain complex mechanisms will produce movement consciousness of which will be intrinsic and unified (Koch, 2018). The preservation of the individual self and the body identity can be considered as premise for experiencing the consciousness of movement execution. Phase locking in the beta oscillation has been shown in the superior temporal gyrus (BA39) in an experiment where participants observed another person's hand movement which triggered the electrical somatosensory stimulus that they received (Cebolla et al., 2014). Self-aspects of experienced spatial unity would explain such involvement of the right angular gyrus (BA39) (Blanke et al., 2005). In the same experiment, alpha, beta and gamma power spectrum increases were located in BA40 as part of the parietal operculum which was explained as an additional somatosensory information of the observer's body schema through reafferent signals associated with the observed action, that could be related to the preservation of his/ her individual “self” and “body identity” with respect to the person performing the movement seated next to him (Iacoboni et al., 1999).
The classical event related potential
The averaged signal of the slow cortical potential fluctuations preceding the action and known as the readiness potential has been classically associated to preconscious motor preparation. The late part of the readiness potential has been pointed to be the neural correlate of the decision of when to move. Such decision would be mainly determined by spontaneous subthreshold fluctuations of task-unrelated neuronal activity (Schurger et al., 2012). Importantly, it has been recently suggested that the early part of the readiness potential does neither have a preparatory nor a decision related origin (Schmidt et l. 2016). It would reflect the negative deflections from task-unrelated slow cortical potentials during which the excitability of the neural system related to action is raised. It is at this moment that an inner feeling of an urge to move would happen constituting the preconceptual bottom up component of the action.
The oscillations-movement-conscience triad
The understanding of the complex interrelationships in the oscillations-movement-conscience triad may be also approached from the sleep research and by using the lucid dreaming as paradigm as recently proposed (LaBerge et al., 2018). Lucid dreaming happens only during paradoxical sleep which is characterized by suppression of electromyography and H-reflex amplitude, by a reduced EEG alpha oscillation and by rapid eyes movements (Jouvet, 1994). Intriguingly, it has been shown that experienced lucid dreamers can exercise volitional control over their dreamed action while dreaming. Concretely, the tracking of visual imaged traced signs with the dreamers’ eyes pursuing the dreamed bodily images of the dreamers’ thumbs resulted in the corresponding shapes in the electrooculogram recordings (LaBerge et al., 2018).

Keywords: oscillation, Movement, Conscioussness, Brain, Intention

Received: 08 Apr 2019; Accepted: 06 Aug 2019.

Edited by:

Maurizio Bertollo, Università degli Studi G. d'Annunzio Chieti e Pescara, Italy

Reviewed by:

Stephane Perrey, Université de Montpellier, France
Tsung-Min Hung, National Taiwan Normal University, Taiwan
Penny C. Werthner, University of Calgary, Canada  

Copyright: © 2019 Cebolla and Cheron. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Guy Cheron, Free University of Brussels, Brussels, Belgium,