Using mobile EEG to assess the Bereitschaftspotential before 192-meter extreme bungee jumping

Surjo R. Soekadar (left) and Marius Nann (right)

Surjo R. Soekadar (left) and Marius Nann (right)

by Surjo R. Soekadar1 and Marius Nann1

1Applied Neurotechnology Laboratory
Department of Psychiatry and Psychotherapy
University Hospital of Tübingen
Calwerstr. 14, 72076 Tübingen, Germany

Acknowledgement

This user research article summarizes our publication “To jump or not to jump: The Bereitschaftspotential required to jump into 192-meter abyss”, Marius Nann, Leonardo G. Cohen, Lüder Deecke, Surjo R. Soekadar, bioRxiv 255083; doi: https://doi.org/10.1101/255083.

Short Abstract

Self-initiated voluntary acts, such as moving the finger, are preceded by a negative electrical brain potential, the Bereitschaftspotential (BP), occurring up to two seconds before the actual movement. Up to now, the BP has only been recorded under well-controlled laboratory conditions, but never in extreme real-life situations, e.g. before self-initiated extreme bungee jumping. Here we report, for the first-time successful recording of the BP before self-initiated 192-meter extreme bungee jumping across two semi-professional cliff divers. Our results pave the way to further investigate the neural substrates and mechanisms underlying real-world decision making and behaviour.

Introduction

Self-initiated acts, such as jumping from a rock in cliff diving, require integration and synchronization of internal and external sensory information. When acting requires overcoming fundamental (genetically programmed) fears such as the fear of heights, willpower and specific cognitions (i.e. beliefs, attitudes and motivations) that are typically attributed to frontal brain regions have to overrule a fear-induced avoidance response (e.g. freezing or stepping back from the cliff edge).

While neurophysiological experimentations up to the 1960s were mainly influenced by behaviourism focusing on stimulus-response paradigms, the neurophysiological basis of self-initiated voluntary acts, i.e. acts that are not triggered by external stimuli, remained uncharted. In 1965, EMG-triggered “reverse computation” of EEG signals revealed that self-initiated finger movements are preceded by a negative electric brain potential building up approximately 1.5 seconds before any muscle contraction is detectable (Fig. 1A). In this first study, participants had to sit still in a Faraday cage with their head reclined into a headrest to avoid EEG artefacts (Fig. 1B). The recorded brain potential, termed Bereitschaftspotential (BP) (engl. readiness potential), was most evident at the vertex electrode and reached amplitudes of up to 10 – 15 μV (Kornhuber & Deecke, 1965).

Fig. 1A: The discovery of the „Bereitschaftspotential“ (BP) (in engl. also readiness potential) by Kornhuber & Deecke (1965) provided the first important insights to the neural origins of self-initiated acts (Kornhuber & Deecke, 1965) (adapted from Deecke et al. 1976). 1B: Subjects had to sit still in a Faraday cage with the head reclined into a headrest to avoid EEG artifacts (photograph provided by Lüder Deecke, Germany).

Fig. 1A: The discovery of the „Bereitschaftspotential“ (BP) (in engl. also readiness potential) by Kornhuber & Deecke (1965) provided the first important insights to the neural origins of self-initiated acts (Kornhuber & Deecke, 1965) (adapted from Deecke et al. 1976).
Fig. 1B: Subjects had to sit still in a Faraday cage with the head reclined into a headrest to avoid EEG artifacts (photograph provided by Lüder Deecke, Germany).

Despite a growing body of literature, the neural origins of self-initiated acts are still not well understood and their interpretation is controversial (Murakami, Vicente, Costa, & Mainen, 2014). While it was shown that the magnitude and waveform of the BP depend on various factors, such as the force exerted, the speed, precision or pace of movement as well as its complexity (Benecke, Dick, Rothwell, Day, & Marsden, 1985), the impact of willpower on the BP’s waveform has not been investigated yet. The main reason for this gap in knowledge is that the BP was never recorded in a real-life situation outside the laboratory where such impact could be assessed. It was, thus, unknown whether recordings obtained in a laboratory under well-controlled conditions could be generalized into real-life situations, and whether other factors than force exerted or complexity of movement, such as the magnitude of willpower required for self-initiating a bungee jump, can impact the BP’s magnitude and waveform.

In our study To jump or not to jump: The Bereitschaftspotential required to jump into 192-meter abyss, we report for the first time successful recording of the BP across two semi-professional cliff divers who performed several bungee jumps from a 192-meter bungee platform (the second highest bungee platform in Europe) (Fig. 2A&B). To evaluate the influence of necessary willpower on the BP’s onset and waveform, BPs recorded before bungee jumping were compared to BPs recorded before jumping from a 1-meter block.

Fig. 2A: Preparation of the active EEG electrode cap (actiCAP, Brain Products GmbH, Gilching, Germany). 2B: One of the bungee jumpers in free fall.

Fig. 2A: Preparation of the active EEG electrode cap (actiCAP, Brain Products GmbH, Gilching, Germany).
Fig. 2B: One of the bungee jumpers in free fall.

Methods

Experimental setup
Two semi-professional cliff divers (both males and 19 years) performed up to 15 self-initiated voluntary jumps, once outside the laboratory from a 192-meter bungee jumping platform ( Europa Bridge in Innsbruck, Austria), and once under well-controlled laboratory conditions from a 1-meter block.

Mobile electroencephalography (EEG) and signal processing
For EEG recordings, a mobile 8-channel EEG system (LiveAmp, Brain Products GmbH, Gilching, Germany) in combination with an easy-to-mount active electrode system (actiCAP, Brain Products GmbH) was used (Fig. 2A). EEG was recorded from eight conventional recording sites (Fz, FC1, FC2, C3, Cz, C4, CP1, CP2 according to international 10/10 system). Ground and reference electrodes were placed at Fpz and the mastoid, respectively. Before every jump impedance of all electrodes indicated by the coloured LED of the actiCAP electrodes was checked to ensure high EEG signal quality. For precise detection of movement onset, an acceleration sensor was used. The EEG amplifier and acceleration sensor were fixed to the jumper’s occiput using adhesive tape and an elastic net dressing (Fig. 3C). Besides allowing for EEG recordings for up to 3 hours, the system transmitted the recorded signals wirelessly via Bluetooth to a tablet computer. EEG and accelerometer data were sampled at 250 Hz and band-pass-filtered at 0.1 to 3 and 5 Hz, respectively. EEG signals recorded from the vertex electrode (Cz) before each jump (defined as trial) were time locked to the onset of an accelerometer signal exceeding the 95% confidence interval recorded during movement preparation at rest (defined as detected movement onset, Fig. 3B) and then epoched into 3-second windows. Epochs ranged from -2.5 s to +0.5 s with a baseline correction relative to the first 0.5 s (reference window) (Fig. 3A). Epochs with non-physiological signal amplitudes exceeding ±100 µV or large drifts before detected movement onset were excluded from further analysis.

Fig. 3A: EEG recordings before 192-meter bungee jumping evidenced a negative potential shift over the vertex electrode (Cz) with the characteristic features of the Bereitschaftspotential (BP) (orange: jumper 1, blue: jumper 2; average over all trials). Orange and blue shaded areas indicate the 95 % confidence intervals. 3B: Movement onset before bungee jumping was detected by an accelerometer integrated into the EEG system (LiveAmp, Brain Products GmbH, Gilching, Germany). The solid line shows the averaged accelerometer signal across all trials of both jumpers. Grey shaded are indicate the 95 % confidence interval. 3C: One of the semi-professional cliff divers in pre-bungee jumping posture.

Fig. 3A: EEG recordings before 192-meter bungee jumping evidenced a negative potential shift over the vertex electrode (Cz) with the characteristic features of the Bereitschaftspotential (BP) (orange: jumper 1, blue: jumper 2; average over all trials). Orange and blue shaded areas indicate the 95 % confidence intervals. 3B: Movement onset before bungee jumping was detected by an accelerometer integrated into the EEG system (LiveAmp, Brain Products GmbH, Gilching, Germany). The solid line shows the averaged accelerometer signal across all trials of both jumpers. Grey shaded are indicate the 95 % confidence interval. 3C: One of the semi-professional cliff divers in pre-bungee jumping posture.

Outcome measures and statistics
Successful detection of a BP was defined as negative deflection of the EEG signal 400 ms before movement onset across all trials (Shibasaki & Hallett, 2006). The BP onset was defined as the time point whereby the averaged EEG signal evidenced a continuous negative deflection for more than 500 ms. Statistical differences between BP onsets of both jumping heights were assessed using the Mann-Whitney-U test. Similarity of waveform was defined as a Spearman’s rank correlation coefficient of higher than 0.6 (i.e. strong correlation) when comparing BPs recorded before bungee jumping and 1-meter box jumping. Significance level was set to p = .05 for all analyses.

Results

Analysis of EEG recordings showed a clear negative deflection beginning approximately 1.5 seconds before movement onset (Fig. 3A). The maximum EEG deflection across all bungee jumps ranged at 17.62±1.09 µV.

Further analysis evidenced successful detection of a BP before jumping from a 1-meter box (jumper 1: M = -19.23 µV, SD = 9.21 µV, t(9) = -2.087, p = .033; jumper 2: M = -10.49 µV, SD = 4.12 µV, t(11) = -2.548, p = .014) and before bungee jumping (jumper 1: M = -11.63 µV, SD = 2.71 µV,  t(14) = -4.293, p < .001; jumper 2: M = -8.37 µV, SD = 3.86 µV, t(11) = -2.167, p = .027).

We found no difference in BP onset comparing BPs recorded before jumping from a 1-meter box (jumper 1: Mdn = -1.81 s; jumper 2: Mdn = -1.29 s) and BPs recorded before bungee jumping (jumper 1: Mdn = -1.80 s; jumper 2: Mdn = -1.06 s) (jumper 1: U = 75, p = .978, jumper 2: U = 72, p = .684).

Moreover, comparison between BP waveforms recorded before bungee jumping and BP waveforms recorded before 1-meter box jumping showed a strong correlation across both jumpers (jumper 1: rs = .639, p < .001; jumper 2: rs = .80, p < .001).

Discussion

The aim of our study was to investigate the characteristics of the BP in an extreme real-life situation, such as self-initiating a 192-meter bungee jump. Successful implementation of such recordings was documented by averaging mobile EEG data from less than 15 trials. Direct comparison between BPs recorded before self-initiated 192-meter bungee jumps with BPs recorded before 1-meter block jumps indicated that neither the BP’s onset nor its waveform is influenced by the magnitude of willpower required for self-initiating a voluntary act.

Our results pave the way for further studies elucidating the neural substrates and mechanisms underlying self-initiated acts in real-world environments. It could be argued that in most lab-based investigations decision-making, i.e. the decision to obey the instruction to self-initiate a particular movement, e.g. to press a button, was already concluded before the beginning of the actual experiment. If so, participants only have to decide when to press and not whether to press. Under such conditions, the ability to choose between different courses of actions is rather unimpeded. In bungee jumping or other extreme activities that require extraordinary willpower, this decision-making process cannot be assumed to be concluded at any point in time before the actual jump. Many bungee jumping novices interrupt their first attempt and need an external trigger to overrule their inner (fear-related) resistance. Even bungee jumpers with year-long experience and dozens of jumps report that each jump requires them to overcome this inner resistance suggesting a decisive role of the frontal brain areas coordinating neuronal circuits related to executive functions and fear responses. While our data indicate that this coordination process does not influence the onset or waveform of the pre-bungee jumping BP, the limited number of electrodes and trials did not allow for in-depth analyses of fronto-parietal cortico-cortical interactions. Further studies are needed to elucidate these possible network interactions and their relationship to the generation of the BP. In this context, use of virtual reality may be particularly helpful as a complementary approach to investigate the neural origins of self-initiated acts also in laboratory environments.

Besides gaining a better understanding of the neurophysiological basis of self-initiated acts in real-world scenarios, the feasibility to assess the BP in everyday life environments may be also instrumental for improving the reliability and versatility of brain-machine interfaces (BMI), e.g. in the context of driving an EEG-controlled brain/neural hand-exoskeleton (B/NHE) after quadriplegia or stroke (Soekadar et al., 2016).

References
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Increase of the Bereitschaftspotential in simultaneous and sequential movements
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[2] Kornhuber, H. H., & Deecke, L. (1965)
Changes in the Brain Potential in Voluntary Movements and Passive Movements in Man: Readiness Potential and Reafferent Potentials. Pflugers Arch Gesamte Physiol Menschen Tiere, 284, 1-17.
[3] Murakami, M., Vicente, M. I., Costa, G. M., & Mainen, Z. F. (2014)
Neural antecedents of self-initiated actions in secondary motor cortex.
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What is the Bereitschaftspotential?
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