Cognitive effects of hyperthermia

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Studies of occupational settings generally report greater subjective fatigue and discomfort when working in hot environments (Chen et al., 2003) and also increased frequency of unsafe behaviors (Ramsey et al., 1983), with increasing decrements with duration of exposure. Much of the research into the effects of human exposure to heat stress has focused on the core temperature responses or the underlying physiological (e.g., cardiovascular, neuromuscular, immunological) mechanisms (Cheung et al., 2000). As a result, the development of health and occupational exposure limits are heavily weighted toward physiological determinants (Parsons, 1993, 1995). In contrast, the effects of thermal stress on cognitive function and complex task performance are less intensively explored. Yet, it is critical to understand how elevations in body temperature impact on cognitive function because: (1) cognitive performance may be much more sensitive to environmental stress than physiological markers (Hancock and Vasmatzidis, 1998; Pilcher et al., 2002), and (2) errors in judgment and decision making can have severe consequences for the health and safety of the individual. Given the complexity of modern work environments and the dangers from even minor errors, this leads to concerns that occupational safety limits should be supplemented or indeed driven by psychological rather than physiological parameters (Hancock and Vasmatzidis, 1998).

In altered thermal environments, performance impairments in complex tasks could reflect impairments in one or more stages of information processing, from signal detection through to central integration and motor response. However, one major problem in defining the nature of this relationship is in establishing cognitive measures that are both scientifically and extrinsically valid. These sometimes-competing validity requirements has led to a wide variety of cognitive measures and tests being employed, along with differing magnitudes and durations of heat stress and subsequent heat strain, making it difficult to compare results across different studies and to establish clear patterns. Indeed, different cognitive processes (e.g., perception, decision making, motor planning and execution) might have different thresholds for impairment under thermal stress, and the reader is referred to excellent recent reviews comprehensively surveying the available literature on the effects of both hot and cold stress on information processing (Pilcher et al., 2002; Hancock and Vasmatzidis, 2003), and physical fitness and exercise on cognitive functioning (Etnier et al., 1997). This review will focus on some of the major implications of heat stress and cognitive functioning relating to exercise performance.

Brain activity and hyperthermia

Brain activity, specifically the ratio of low frequency (a = 8-13 Hz) and high frequency (b = 13-30 Hz) brain waves as an indicator of arousal, during hyperthermia and exercise has been explored in humans cycling at 60% aerobic power in both a hot (~40°C) and a cool (M9°C) environment (Nielsen et al., 2001). A progressive reduction in b waves in the hot exercise condition was evident, such that the ratio of a/b waves was increased. This is similar to what happens during sleep, so it may reflect a reduced state of arousal in hyperthermic subjects. Furthermore, the magnitude of increase in the a/b ratio was strongly correlated to elevated core temperature (r2 = 0.94-0.98) (Nielsen et al., 2001). Similarly, with passive hype-rthermia a reduction in electroencephalographic (EEG) frequency has been reported in primates, but not until a brain (epidural) temperature of -41.5°C (Eshel and Safar, 2002). The functional significance of altered EEG activity remains to be determined but it is worth noting that the altered brain activity was associated with changes in ratings of perceived exertion (Nielsen et al., 2001) during exercise in humans. Subjects continually rated their effort higher during hyperthermic trials, with the best predictor of the rate of perceived exertion being a reduction in EEG frequency in the frontal cortex of the brain (Nielsen et al., 2001) (Fig. 1).

Problems in the literature

One fundamental problem in defining the role of thermal stress on cognitive impairment and task performance is that few studies have systematically and completely tracked thermal stress with changes in physiological and/or perceptual thermal strain through to cognitive and ultimately task performance impairments. For example, Neave et al. (2004) reported impaired attention and vigilance along with slower reaction times, but no changes in either physiological or perceptual responses, in young cricket batsmen. While it is intuitive that these cognitive abilities are critical determinants of batting performance, the lack of batting data preclude

Fig. 1. a Power spectrum areas (A), ß power spectrum areas (B), and exercise a/ß index (C), all as a percentage of the first measurement made 2 min of exercise in the hot and control conditions. Mean + SE for seven subjects. *Significantly different from 2-min value (P<0.05). y Significantly different from control (P<0.05). (Adapted with permission from Nielsen et al., 2001.)

Fig. 1. a Power spectrum areas (A), ß power spectrum areas (B), and exercise a/ß index (C), all as a percentage of the first measurement made 2 min of exercise in the hot and control conditions. Mean + SE for seven subjects. *Significantly different from 2-min value (P<0.05). y Significantly different from control (P<0.05). (Adapted with permission from Nielsen et al., 2001.)

conclusive determination of this connection. Other studies expose subjects to heat for a set and often short period of time and assume that subjects experience similar levels of heat strain without any physiological quantification (Chase et al., 2003). Cognitive impairment, while sensitive to thermal stress, may also be negated or minimized by other compensatory mechanisms, such that performance outcomes may be much less susceptible to thermal impairment than presumed from cognitive changes alone (Hancock and Vasmatzidis, 2003). For example, mild and stable levels of whole body heating or cooling, the latter including significant cooling of hand temperatures, produced subjective thermal discomfort but actually improved some aspects of both precision and accuracy amongst trained marksmen in a shooting simulator (Tikuisis et al., 2002a), but unfortunately the lack of cognitive-based test measures in this study precludes an exploration of the underlying mechanisms.

Hocking et al. (2001) used steady-state probe topography to demonstrate an increase in amplitude and a decrease in latency of visually evoked potentials with increased core temperature, suggesting that hyperthermia systematically altered electrical responses of the brain. Hocking's research (2001) highlights the ability of neural potential recording and analysis to quantify cognitive output. Similarly, event-related potential (ERP) recording allows comparison of potentials to a timed sequence of events, offering specific details on a given temporal or spatial aspect of neural functioning. Paired with appropriate neuropsy-chological tests, ERP analysis has proven to be both a valuable assessment tool of cognitive performance in psychological research (Picton, 1992) and also more recently as a clinical diagnostic tool (Polich, 1998; Connolly and D'Arcy, 2000; Marchand et al., 2002). While potentially promising, research applications for ERP analysis in thermal physiology are yet to be explored in detail. The use of ERP assessment may allow for accurate determination of cognitive performance regardless of physiological deficits such as loss of manual dexterity from shivering, as measurable ERP events can occur before, after, or in the absence of behavioral responses, and do not require behavioral observations to fully correlate the relative timing of processing to a specific event (Connolly and D'Arcy, 2000).

Perception of heat stress

The perception of the magnitude and the all-esthesial quality of thermal stress plays a major role in human behavioral thermoregulation and possibly exercise capacity. Preferred self-adjusted ambient temperature for a group of European males and females averaged 26.6 + 2.6°C, though substantial inter-individual and diurnal variability were observed (Grivel and Candas, 1991). Exercise in the heat at a constant workload resulted in higher cardiovascular and thermal strain while eliciting a greater thermal discomfort and perception of effort (Maw et al., 1993). The perception of thermal stimuli and its subsequent influence on exercise performance and tolerance in the heat remains a complex issue. While the dominant center for overall thermal stimuli integration and response resides within the hypothalamus, a hierarchic system of less complex thermal integration sites also exist elsewhere within the central nervous system (Satinoff, 1983). This is informed in part by cold and warm receptors under human skin existing at an average depth of 0.15-0.17 mm and 0.3-0.6mm, respectively (Hensel, 1981). The overall integration of these signals, and the role of individual factors, play a significant role in modulating the perception of thermal stress, and potentially the behavioral response to heat stress and also possibly the capacity for exercise.

Peripheral and regional sensitivity

The relative role of central versus peripheral afferents in perceptual responses to thermal stimuli is made difficult by methodological problems in manipulating one variable without altering the other. For example, Frank et al. (1999) used a combination of a thermally controlled mattress (at 14, 34, or 42°C) to passively alter and maintain mean skin temperature to cool, neutral, and hot, followed by 4°C intravenous saline infusion at 70mLmin_1 to achieve rapid core cooling. A clear separation of thermal perception and physiological response was observed, with multiple linear regression analyses demonstrating that core and skin temperature contributed about equally to perceptions of perceived temperature, but that core temperature dominated in driving vasomotor tone, metabolic heat production with core cooling, and epinephr-ine and norepinephrine response (Frank et al.,

1999). While such research is important in understanding the relative weighting of thermal afferents, care must be taken to avoid assuming a philosophical construct of central and peripheral afferents as two distinct entities with minimal interaction. Rather, to develop models of mean body temperature inputs into thermal stimuli integration, it would be interesting to extend such work to different levels and rates of core temperature alterations along with exploring regional skin temperature manipulations during exercise in the heat.

In addition to the interactions between central and peripheral thermoreceptors, thermal sensation may be determined in part by regional variability in thermosensitivity of different skin surface regions with local heating or cooling. Local thermal stimulation of different skin surface regions plays a major role in thermal perception of heat stress independent of core temperature, and thermal comfort may be strongly tied to the alliesthesial effects of sweating rate and skin wettedness (Mower, 1976). The existence of thermosensitivity variability across different skin regions, notably the face, has been both supported (Crawshaw et al., 1975) and rejected (Libert et al., 1984). However, one systematic limitation of these studies is the closed-loop approach to thermal manipulation, such that one region is thermally stimulated without thermal clamping of the other skin regions or core temperature, thus altering the overall thermal afferent input apart from the stimulated site. Recently, Cotter and Taylor (2005) employed a water-perfused suit enabling an open-loop approach, whereby skin regions could be stimulated while thermal clamping of non-stimulated regions could be maintained. Using this design, cooling of the face was demonstrated to be two to five times more effective in suppressing sweating response and thermal discomfort than an equivalent skin surface area elsewhere (Cotter and Taylor, 2005). The neurological origins of this increased sensitivity in humans is unclear but, based on animal models, it may be due to a higher facial thermo-receptor density (Dickenson et al., 1979) or minimal thermoafferent convergence (Dawson and Hellon, 1979). Overall, though the existence and importance of selective brain cooling in humans remain contentious (see Chapter by Nybo), both the behavioral and autonomic (e.g., sudomotor) sensitivity of the face suggests an effective potential site for targeted local cooling to lower perceived heat stress and possibly prolonged exercise capacity during hyperthermia (see Heat Stress Countermeasures) (Fig. 2).

Individual variability in thermal perception

Along with differing physiological thermoregula-tory strategies and abilities, thermal perception appears to differ throughout the human lifespan. Prepubertal children have been proposed to lose heat faster due to a higher surface area to volume ratio, but both the onset threshold and sensitivity of their sweating response (Falk et al., 1991, 1992; Anderson and Mekjavic, 1996), along with thirst sensation (Meyer and Bar-Or, 1994; Bar-Or and Wilk, 1996), appear to be diminished compared to young adults. This is accompanied and possibly compensated by a heightened subjective sensitivity to increases in core temperature (Anderson and Mekjavic, 1996). With aging, there also appears to be a gradual decrement in heat dissipation and conservation capacities (Natsume et al., 1992), with greater core temperature changes required to initiate sweating and shivering (Ogawa et al., 1993; Anderson et al., 1996). This is accompanied by decreased perception to changes in thermal stimuli or thirst (Miescher and Fortney, 1989; Natsume et al., 1992; Ogawa et al., 1993), thus requiring a greater thermal stimulus to elicit behavioral responses (Taylor et al., 1995). In contrast, others argue that aging minimally influences thermoreg-ulatory ability, and that functional capacity (e.g., aerobic fitness, body composition) and health status are the primary determinants of physiological thermoregulatory capacity with aging (Kenney and Havenith, 1993; Pandolf, 1997).

Concomitant with maturational issues, aerobic fitness and training history are other interindividual variables that may also alter individual perception of thermal stress. During exercise in an uncompensable heat stress environment, Tikuisis et al. (2002b) compared the linkage between subjective ratings of perceived exertion and thermal discomfort as behavioral analogs for the respective

Fig. 2. Local cutaneous thermosensitivities for sudomotor control and whole-body thermal discomfort (alliesthesia). (A) Data are site-specific; mean sudomotor (shaded bars) and alliesthesial thermosensitivities ( + S.E.M.) derived across three localized thermal treatments (N = 12): mild warming (4°C), mild cooling (—4°C), and moderate cooling (— 11°C). Significant differences (P<0.05) between local sites were only apparent with respect to the face (y), abdomen (J), and back (§). The inset (B) displays the relation between changes in whole-body thermal discomfort and local skin temperature (Tskl), and represents the alliesthesial thermosensitivity for these treatments at the face. (Adapted with permission from Cotter and Taylor, 2005.)

Fig. 2. Local cutaneous thermosensitivities for sudomotor control and whole-body thermal discomfort (alliesthesia). (A) Data are site-specific; mean sudomotor (shaded bars) and alliesthesial thermosensitivities ( + S.E.M.) derived across three localized thermal treatments (N = 12): mild warming (4°C), mild cooling (—4°C), and moderate cooling (— 11°C). Significant differences (P<0.05) between local sites were only apparent with respect to the face (y), abdomen (J), and back (§). The inset (B) displays the relation between changes in whole-body thermal discomfort and local skin temperature (Tskl), and represents the alliesthesial thermosensitivity for these treatments at the face. (Adapted with permission from Cotter and Taylor, 2005.)

physiological parameters of heart rate and rectal temperature. While aerobically untrained subjects were generally very close in matching the modeled perceptual strain with its physiological counterpart, aerobically trained subjects consistently underestimated their modeled physiological strain during exercise in the heat while wearing semipermeable chemical protective clothing (Tikuisis et al., 2002b). This difference between perceived and physiological strain during exercise in the heat could contribute to the significantly greater endpoint core temperatures consistently attained by aerobically fit individuals (Cheung and McLellan, 1998; Selkirk and McLellan, 2001), and also the ability of highly fit runners to sustain highly elevated core temperatures throughout prolonged competition (Noakes et al., 1991). Overall, this suggests the somewhat counterintuitive notion that highly fit individuals, due to their higher metabolic rate — and therefore heat production — along with their perceptual attenuation, may be at a greater risk for developing heat exhaustion

(Noakes et al., 1991). Epidemiological evidence argues against this though, with low running ability and high body mass index (kgm—2) being strong predictors of heat illness in Marine Corp recruits (Gardner et al., 1996). Regardless, occupational monitoring and the awareness of heat illness risks and symptoms appear critical in all worker and athletic populations exposed to heat stress.

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