Enhanced Neuronal Synchrony During Skilled Reaching at High Altitude

Motor skills are a critical aspect of human behavior (Ellens et al., 2016), yet become compromised at altitudes greater than 2500 m (Milledge et al., 2007). How the central motor system changes in response to these extreme and hypoxic environments remains an open question. Previous studies have investigated the effect of hypoxic conditions on brain activity during simple tasks and in simulated environments (Guger et al., 2008), but fail to recapitulate real challenges and stresses faced by humans acutely exposed to high altitude (Coppel, 2015). We, therefore, established a method of measuring and characterizing task-related neuronal activity during high-altitude exposure. We implemented cortical electroencephalography (EEG) on two healthy, right-handed subjects during a self-paced skilled reaching task for a 7-day ascent to more than 4100 m in the north-central region of Nepal. We correlated task-centered sensorimotor oscillatory activity of five physiologically relevant EEG bands (delta, 0.5–3.5 Hz; theta, 4–8 Hz; alpha, 7.5–12.5 Hz; beta, 13–30 Hz; gamma, 30–100 Hz) with daily measures of altitude, ascent, and blood oxygen saturation (SpO₂). Our data reveal a significant positive correlation between altitude and sensorimotor delta amplitude and phase synchrony (Fig. 1). These findings have the potential to inform future work concerning neuronal homeostasis, motor task execution, and high-altitude safety.

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FIG. 1.

Task-centered delta band EEG activity of 7-day ascent to high altitude. Each plot is centered on the lift-off event of a small rubber ball from a freestanding platform. Small black circles down the y-axis mark all trial start and end times, displaying consistent task timing for each day and between subjects. The z-amplitude was calculated using the session-wide mean and standard deviation of the delta-filtered EEG signal. Wrist-based accelerometer data are shown in volts for the primary direction of arm movement. Significance was evaluated for all 7 days using a linear fit of ±1 second mean z-amplitude (subject 1: R² = 0.854, p = 0.003; subject 2: R² = 0.689, p = 0.020) and mean phase locking value (subject 1: R² = 0.882, p = 0.002; subject 2: R² = 0.516, p = 0.068).

The prevalence of delta synchrony in lower vertebrates, children, and decorticated or pathological brain states (i.e., sleep, injury, disease, and fatigue) suggests that delta oscillations are a correlate of basic homeostatic processes (Knyazev, 2012). Significant evidence supports a role for spontaneous delta power increases during cerebral hypoxic and ischemic hypoxia (Kraaier et al., 1988), with one study identifying enhanced spontaneous delta oscillations as an early biomarker for the development of altitude mountain sickness (Feddersen et al., 2007). Delta oscillations are a strong indicator of adenosine release responsible for adenosine triphosphate production (Dworak et al., 2011) and coincide with the resynthesis of brain glycogen (Benington and Heller, 1995). Together, these findings suggest that delta oscillations play a fundamental role in cerebral energy homeostasis during stress/resource scarcity.

Central pattern generators for the delta rhythm exist independently in the brain stem, thalamus, and cortical pyramidal neurons, the latter suggesting a high-level role for delta oscillations beyond sympathetic homeostasis (Güntekin and Başar, 2016). The temporal resolution and low energy demands of slow-wave oscillations in the delta band make them ideally suited for coordinating activity between distant brain structures (Buzsáki and Draguhn, 2004). By modulating neuronal excitability, delta oscillations may enable “communication through coherence” and allocate neuronal resources at the right time (Lachaux et al., 1999; Fries, 2005). Therefore, the delta rhythm may serve as a general oscillatory framework for optimal sensorimotor processing (Stefanics et al., 2010; Khanna and Carmena, 2015).

The presence of task-related delta oscillations has been correlated with task accuracy (Arnal et al., 2015) and is positively associated with neuronal resources available for a task (Emek-sava et al., 2016). Furthermore, sensorimotor delta oscillations have been shown to encode task-related neural representations of reaching kinematics while coordinating with distant central motor structures through phase synchronization (Jerbi et al., 2007). In impaired subjects, cognitive and motor task-related delta oscillations are attenuated rather than enhanced (Güntekin and Başar, 2016). Başar (1980) suggests that this paradox is because of spontaneous delta activity that acts to keep the network “busy,” thereby disrupting the crucial role of delta oscillations in task utilization. It is important here to highlight that dual tasks (e.g., walking while talking) may not conform to the same framework. Dual tasks are severely compromised by neurological (Fritz et al., 2015) and physical stressors (Taylor et al., 2015) and may require that the brain flexibly implements spared resources and/or multiple oscillatory regimes at once.

Although we experienced significant changes in SpO₂ at altitude, our task performance remained unchanged. The characteristics of our EEG activity at high altitude indicate the recruitment of additional sensorimotor resources. We hypothesize that homeostatic delta oscillations represent a separate oscillatory system that is driving cortical-level compensation to maintain task coordination. Although healthy individuals in normal environments may have relatively robust compensation machinery, it may break down in subjects with disease, under abnormal stress, or generally in situations in which basic brain functions serving survival are paramount.

The future of high-altitude exploration relies on our ability to implement therapies designed to increase survival and enhance performance. Although many solutions address the former by minimizing fatigue or addressing homeostatic imbalances (Luks et al., 2014), only recently have technologies such as transcranial electric stimulation explored positively augmenting sensorimotor capabilities (Bellesi et al., 2014). Altogether, potential countermeasures for high-altitude mountaineers may benefit from a dual approach: one that regulates homeostatic processes and another that modulates task-related cortical networks.