As I pushed my oxygen-starved body up an interminable slope somewhere above 8000 m while heading for our 8300 m high camp on the north ridge of Mount Everest, I found myself repeatedly pondering one particular morbid truth. My preoccupation seemed to focus on the fact that if the unacclimatized sea level dweller were suddenly exposed to this sort of altitude, survival would exceed that of the unprotected person in outer space by only a few short minutes. All who have attempted to climb the world's highest mountains realize that they are pushing their personal physiological envelope to near—but hopefully not over—its limit. Life tends to become rather challenging in multifaceted ways at altitudes approaching and exceeding 8000 m, and it is difficult not to focus on the near maximal work of the heart and lungs during ascent to such heights. However, less obvious—but just as, if not more, important—is the effect of extreme altitudes on the function of the brain. A quote from a well-respected high altitude physiology and medicine textbook puts this issue in perspective: Most obvious is the breathlessness we experience [at high altitude] … . More sinister, though, because it is usually not apparent to us, is the decline in some of our most sophisticated cognitive skills due to the effect of altitude on the function of our brain. In many instances safety in these spectacular yet hazardous environments is dependent upon proper and timely decisions about what courses of action to take and what to avoid. Such decisions depend upon a functioning brain.1(p377)
The authors of the textbook chapter from which the above quote is taken go on to say that loss of judgment due to brain hypoxia at the more extreme altitudes may have contributed to numerous tragedies on the world's highest mountains. To be sure, any such neuropsychological performance deficits suffered while climbing at extreme altitude is almost surely to be confounded by other influences such as fatigue and anxiety. It is nonetheless well understood that a number of research studies have shown impairment in arithmetic, memory, and metamemory, language, perception, learning, cognitive flexibility, and psychomotor skills upon ascent to high altitude,
2
–6 all of which are indicative of a fundamental slowing of neuronal processing. Eric Shipton, well known to mountaineering historians for his many Himalayan expeditions to extreme altitude in the 1930s, possessed a very clear and practical understanding of the mental consequences of operating in this environment during an era when research evidence had only just begun to recognize the effect of severe hypoxia on cognitive function. He wrote: Altitude has the same effect upon the mind as upon the body; one's intellect becomes dull and unresponsive … mental processes are so sluggish and inefficient that it is most difficult to retain a clear memory of what has actually occurred.7(pp387-390)
Important Early Studies
The 1935 International High Altitude Expedition to Chile was a sophisticated field-based medical research undertaking that had as its scientific leader Dr David Bruce Dill of the Harvard Fatigue Laboratory. Ross McFarland, a scientific investigator who participated in this field study, did much to contribute to the early appreciation of neurological-related phenomena associated with high altitude exposure. McFarland described sensory, motor, emotional, and psychosomatic reactions during the 1935 expedition's gradual 3-month-long ascent to altitudes up to 20 140 ft (6139 m).8,9 He noted that even with such a slow ascent and presumably ideal acclimatization, concentration diminished and impairments were generally most obvious in the time taken to perform a task than in the actual quality of performance. In other words, McFarland found that, at altitude, one could have speed or one could have accuracy but not necessarily both.
A decade earlier, the team physician for the 1924 British Mount Everest expedition, R.W.G. Hingston, had described his observations of the performance of simple arithmetical tests by expedition members at altitudes exceeding those experienced on the 1935 International High Altitude Expedition. That was probably the first neuropsychological testing carried out on a Himalayan mountaineering expedition. By increased effort, the problems could be solved quite easily with no loss of accuracy. Nearly everyone experienced mental lassitude, however, and although the mind was clear, there was a disinclination toward effort, especially if the task required thought. 10
Hingston noted that members of the 1924 Everest team displayed behavioral changes at high altitude such as amplified criticism of the behavior of others, increased irritability, sluggish thought, compulsive repetition, and short-term memory deficit. 10 Hingston was also afforded the opportunity to provide an appendix regarding Everest for a landmark high altitude physiology text, The Respiratory Function of the Blood: Part 1, Lessons From High Altitudes, published in 1925 by the eminent Cambridge physiology professor Sir Joseph Barcroft (1872–1947). 11 Barcroft is well known today for, among other things, being a key figure in elucidating the oxygen dissociation curve. The aforementioned book is a Barcroft “classic,” and appeared shortly after his 1921–1922 International High Altitude Expedition to Cerro de Pasco, Peru (4330 m). During this scientific venture, Barcroft had made measurements of mental ability in his scientific colleagues who had accompanied him to the highlands of Peru. In The Respiratory Function of the Blood: Part 1, Lessons From High Altitudes, he observed: “Chronic oxygen want, like mental fatigue, breeds a mental apathy which may amount merely to carelessness, but which, on the other hand, may go so far as to produce complete distortion of the values of things. Matters of vital importance appear trivial and are neglected.11(p163)
Reflecting on Hingston's observations of behavioral changes at high altitude on the 1924 British Everest expedition (increased irritability, amplified criticism of the behavior of others, and so forth), it may be relevant to recall the words of another physician, Raymond Greene. Greene not only had extensive clinical experience treating patients with disease-related chronic hypoxia, but he also accumulated a significant amount of medical experience on some the world's highest mountains during several well-known Himalayan expeditions in the 1930s. In the article “Mental performance in chronic anoxia” written for a 1957 issue of the British Medical Journal, Greene reflected back on his experiences treating patients with heart failure and advanced pulmonary disease. He noted that One feels that one of the effects of the [chronic hypoxic] illness is to strip the veneer off a man and expose the quality of his mind naked to the world. I think that the same thing happens in alcoholic intoxication and in the chronic anoxia of great altitudes.
12
Barcroft was also discerning about other altitude-related physiological observations—particularly about sleep, or as he put it, “the sleeplessness factor.11(p166) In a simulated altitude acclimatization experiment at his Cambridge laboratory, Barcroft lived in a normobaric hypoxia chamber (ie, the air within was enriched with nitrogen to lower the inspired partial pressure of oxygen [Pi The two opinions [his vs that of the student observers] can only be reconciled on the hypothesis that whilst I spent most of the night in sleep, the slumber was very light and fitful with incessant dreams. Even some low degree of consciousness which fell short of absolute wakefulness. At Cerro [de Pasco] it was the same: measured in hours we slept well, but the quality of the sleep in most cases was of an inferior order. The night seemed long and we woke unrefreshed.11(p166)
Modern sleep research has shown that Barcroft was quite right in noting that sleep, or lack thereof, is a very real performance-related concern at high altitude. Sleep-disorder–related (or sleep-restriction–related) performance deficits will be briefly introduced and discussed in a forthcoming paragraph.
Later Evidence
Subsequent decades have seen explicit testing of task performance during acclimatization not only on mountaineering expeditions, but also during simulated ascents to high altitude in hypobaric pressure chambers. For instance, cognitive performance was evaluated during a simulated 40-day ascent to the pressure equivalent of the summit of Mount Everest during Operation Everest II in 1985. 13 Kennedy et al 14 found that tests of cognition (such as grammatical reasoning) performed during the study—compared to tests of pure motor function—were more consistently and intensely affected at a barometric pressure of 282 mm Hg (approximately 7620 m) than at a pressure of 429 mm Hg (approximately 4572 m). More recently, another simulated, decompression-chamber “ascent” of Everest 15 noted that psychomotor performance and mental efficiency deteriorated progressively above 5500 m to 6500 m, but the changes did not become statistically significant in the 8 subjects until a pressure equivalent of approximately 8000 m was reached. The work of Lieberman et al 16 also supports the suggestion that complex cognitive functions in well-acclimatized persons are likely to be impaired at very high altitudes. These investigators observed speech, motor performance, and cognition in members of a 1993 Everest expedition. They found that, for example, the time required to comprehend a sentence and formulate a response increased as altitude increased from 5300 m to 7150 m.
That there is ample evidence for decline in cognitive function that is related to the hypobaric hypoxic environment found on the world's highest mountains will come as no surprise to those who are familiar with the neuropsychological effects suffered by patients with chronic hypoxic diseases. 17 Several studies have established that chronic obstructive pulmonary disease (COPD) is accompanied by striking neuropsychological deficits. 18 –20 Patients with moderate-severe COPD display impairment in a number of cognitive functions, such as memory, intelligence, and motor coordination. The levels of escalating cognitive decline in COPD patients is directly associated with the progressively increasing degree of hypoxemia that is seen as the disease worsens. 17
The “Sleeplessness Factor”
When unacclimatized lowlanders arrive at high altitude, they commonly experience poor quality (as well as a reduced quantity of) sleep. There may be difficulty in trying to initiate sleep, increased fragmentation of sleep by frequent brief arousals, and a feeling of tiredness the following day. This is typically due to cycles of nocturnal periodic breathing that happens because of the hypoxia and hypocapnia experienced at high altitude, as well as increased chemosensitivity known to occur during unconsciousness. Furthermore, at high altitude, the architecture of sleep tends to move toward lighter sleep stages, with marked deterioration of slow-wave sleep and erratic decreases in rapid eye movement (REM) sleep. Thus, the decline in daytime cognitive function at high altitude is undoubtedly caused in part directly by hypoxemia—perhaps compounded by the effects of cerebral vasoconstriction caused by hypocapnia. But often overlooked when identifying factors responsible for the decrement in intellectual function at very high altitudes is the likely contribution of sleep fragmentation and overall decline in sleep quality. 21
The results of recent work on the neuropsychological effects of sleep loss, however, do suggest much that is clearly of relevance to operating at extreme altitude. There seems to be little contention today that sleep loss can result in significant neurocognitive decline, particularly in the domains of executive control, working memory, and attention. 22 In a recent review of the neuropsychological effects of sleep loss, Waters and Bucks 23 presented a comprehensive summary of findings regarding the impact of sleep loss on cognition in healthy people. The following abbreviated synopsis characterizes the main points they discovered in their review of the evidence. 23 1) Sleep loss has a marked impact on performance through decreases in cognitive functions and specific effects on brain regions that support cognitive performance. 2) Decreased speed of processing is the most reliable finding after sleep loss. 3) Sleep loss impacts on multiple aspects of cognition, with the largest effect size on processing speed and attention/vigilance; however, a notable feature of cognitive performance after sleep loss is distinct intraindividual variability. 4) Functional neuroimaging findings are consistent in showing that sleep loss produces abnormal activation in the prefrontal cortex, parietal lobes, thalamus, and temporal lobes. 5) A quantitative link exists between sleep loss and cognition, with performance worsening with increasing time awake. 6) Task performance decreases as sleep debt accumulates in a manner that is “dose dependent.”
Conclusions
These findings from the sleep restriction/deprivation literature suggest that the decline in intellectual function at very high altitudes is (very likely) not merely a matter of the brain being starved of oxygen, but also a matter of the brain being denied the quantity and quality of restorative sleep it requires for first-rate functioning. It would, of course, require a suitable experimental scheme to sort out the actual respective pathological contributions that hypoxemia and sleep deprivation might have on daytime cognitive functioning. Nonetheless, it is reasonable to suggest that, in many instances, their combined effect may lead to a significant decline in performance at extreme altitude. The practical implications of this collective assault on one's intellect at altitude are numerous, and many of the potential cognitive deficits are mentioned in the preceding discussion. But the loss of self-awareness may, in many instances, make the other deficits pale in comparison. Wilfrid Noyce, a British mountaineer and writer, comments on his experiences at extreme altitude in his book South Col. He notes that during the first ascent of Mount Everest in 1953, “Life was a routine existence of meals and arrangements and gossip, with the top layer of the mind comfortably skimmed away, as I now realize. At the time I thought I was as alert as at sea level.”24(p182)
Similar to inebriated persons insisting that they are not so impaired that they can't safely drive a car, the climber ascending to extreme altitude is in danger of not being able to properly grasp the seriousness of any given situation at hand. Of course, the use of supplemental oxygen while climbing can alleviate this risk to some degree, provided the flow (and quantity) of gas is sufficient for the task at hand. Typically rationing the oxygen at a low flow to conserve the meager supply, the mountaineer can thus only hope to keep heart and lungs from having to work at their absolute limit throughout the course of ascent.
Decisions having life and death implications can, in this extreme environment, at times be broached in a fashion so cavalier that a person would likely be shocked at such actions at altitudes closer to sea level. Many of the accidents and deaths that occur in this high realm—a realm so very unforgiving of errors—are nonetheless precipitated by a simple and seemingly innocuous miscalculation that slowly but surely places one's head further into the noose. Moreover, since the beginning of human sojourns to the world's highest terrestrial altitudes, perceptive mountaineers have not necessarily been ignorant or unaware of this lurking menace. The well-known British climber George Leigh Mallory (whose name will be forever associated with the pioneering Everest expeditions of the 1920s) summed up the essence of the problem almost 90 years ago in a rather blunt, but accurate, fashion: “Mountaineers have often observed a lack of clarity in their mental state at high altitudes; it is difficult for the stupid mind to observe how stupid it is.”25(p129)
Footnotes
Acknowledgment
The author wishes to thank Dr Harvey Lankford for bringing the historical quotes included in this article to his attention.
