Women’s performance on math and verbal tests is best at higher temperatures, while men perform best on the same tests at lower temperatures, according to a study published May 22, 2019 in the open-access journal PLOS ONE by Tom Chang and Agne Kajackaite from the USC Marshall School of Business, Los Angeles, USA, and the WZB Berlin Social Science Center, Berlin, Germany.
Although many surveys have shown that women tend to prefer higher indoor temperatures than men, no experimental research examining temperature’s effect on cognitive performance has taken possible gender differences into account.
To address this gap, between September-December 2017, 24 groups of 23-25 students (542 participants total) took logic, math, and verbal tests in a room cooled or heated to one of a range of temperatures between 16.19 C/61.14 F and 32.57 C/90.63 F, receiving cash rewards based on the number of questions correctly answered. 41% of the participating students identified as female.
The authors found that female students generally performed better on math and verbal tests when the room temperature was at the warmer end of the distribution, submitting more correct responses as well as more responses overall.
Conversely, male students generally performed better on these tests at lower temperatures – at the warmer end of the temperature distribution, they submitted fewer responses, as well as fewer correct responses.
The improved performance of women in response to higher temperature was larger and more precisely estimated than the corresponding decrease in male performance.
Temperature did not appear to impact performance on the logic test for either gender.
The authors found that female students generally performed better on math and verbal tests when the room temperature was at the warmer end of the distribution, submitting more correct responses as well as more responses overall. The image is in the public domain.
The study participants were a relatively homogenous group of German university students, so the effects of temperature might vary for other demographic groups.
Nonetheless, the authors suggest that ambient temperature might impact more than just comfort, noting that it’s possible that “ordinary variations in room temperature can affect cognitive performance significantly and differently for men and women.”
Kajackaite and Chang summarize:
“In a large laboratory experiment, over 500 individuals performed a set of cognitive tasks at randomly manipulated indoor temperatures.
Consistent with their preferences for temperature, for both math and verbal tasks, women perform better at higher temperatures while men perform better at lower temperatures.”
Cognitive function defines performance in objective tasks that require conscious mental effort. Extreme environments, namely heat, hypoxia, and cold can all alter human cognitive function due to a variety of psychological and/or biological processes.
The aims of this Focused Review were to discuss; (1) the current state of knowledge on the effects of heat, hypoxic and cold stress on cognitive function, (2) the potential mechanisms underpinning these alterations, and (3) plausible interventions that may maintain cognitive function upon exposure to each of these environmental stressors.
The available evidence suggests that the effects of heat, hypoxia, and cold stress on cognitive function are both task and severity dependent.
Complex tasks are particularly vulnerable to extreme heat stress, whereas both simple and complex task performance appear to be vulnerable at even at moderate altitudes.
Cold stress also appears to negatively impact both simple and complex task performance, however, the research in this area is sparse in comparison to heat and hypoxia.
In summary, this focused review provides updated knowledge regarding the effects of extreme environmental stressors on cognitive function and their biological underpinnings.
Tyrosine supplementation may help individuals maintain cognitive function in very hot, hypoxic, and/or cold conditions. However, more research is needed to clarify these and other postulated interventions.
For example, when 17,000 safety observations were made over a 14 month period in factory workers, the relationship between the ambient temperature and unsafe behaviors formed a U-shaped curve.
Specifically, minimum unsafe behaviors occurred when the ambient temperature was between 17 and 23°C, whereas temperatures outside of this range saw increasing unsafe behaviors displayed (Ramsey et al., 1983).
Utilizing logistic regression (heat stress and occupational injury), it was demonstrated that ~20% of Taiwanese workers (n = 58.495) experienced occupational heat stress, which was strongly and significantly associated with workplace accident rates (Tawatsupa et al., 2013).
The notion that indoor workers are generally sufficiently protected via air conditioning, fans, or other cooling systems does not apply to most industrial workplaces in low and middle income countries, that are located in hot regions of the world (Balakrishnan et al., 2010).
Occupations at risk of extreme heat exposure may include mining, shearing, farming, factory work, firefighting, and other emergency/military services (Arbury et al., 2014).
Performing occupational tasks in close proximity to heat-generating equipment can also generate exceptionally hot environments.
Additionally, several occupations (e.g., firefighting, chemical waste, and bomb disposal) require workers to wear impermeable protective clothing, which interferes with evaporative heat loss mechanisms and may overwhelm the ability of this primary heat loss effector system to maintain core temperature (Tc) at ~37°C (Cheung et al., 2000; Armstrong et al., 2010).
Examining the relationship between heat stress and cognitive function is a challenging task as there are many confounding factors that may have influenced results from previous investigations.
Examples of these methodological inconsistencies include severity of heat exposure (duration and temperature), the complexity of the cognitive task(s) completed, previous experience of participants, hydration status, the definition of heat stress (high ambient or Tc), and the design employed to attain an increase in Tc (passive or exercise induced).
Discussing each of these confounding issues in detail is beyond the scope of this focused review, however, the reader is directed to reviews which have addressed each of these issues at length (Hancock and Vasmatzidis, 2003; Hancock et al., 2007; Gaoua, 2010).
When discussing both the mechanistic and observational evidence regarding heat stress induced cognitive alterations, the authors’ have drawn upon data from studies using human passive heat stress models (to eliminate any confounding effect of exercise).
Relevant recent literature in this area is collated within Table Table2,2, and is drawn upon when making conclusions regarding the true effects of passive heat stress on cognitive function.
The effects of passive heat stress on cognitive function.
|Author and date||Environment (temperature)||Duration||Cognitive assessment tool||Physiological response||Cognitive alterations|
|Gaoua et al., 2012||50°C, 30% r.h.||15 min||Reaction time and task planning||Tc not elevated. Tsk elevated by ~3°C.||Decreased accuracy in task planning. Subjects took more time (41% increase) to find correct response.|
|Liu et al., 2013||50°C, 40% r.h.||45 min||Attention Network Test||Tc elevated to 38.5°C. Tsk not reported.||Impaired executive function.|
|Lenzuni et al., 2014||53.3–66.9°C||15–20 min||Driving in a straight line, and identifying a cue and reacting correctly||Tc elevated by ~0.3°C. Tsk not reported.||Impaired cognitive function in both simple and complex tasks ~50%|
|Berg et al., 2015||26°C||30 min||Peg transfer and intracoporeal knot tying||None reported||None despite reduced thermal comfort|
|Watkins et al., 2014||30°C, 50% r.h.||90 min with 15 min normothermic exposure at half-way||Dual task (tracking + simple reaction) and numerical vigilance||Tc elevated by ~0.2°C. Tsk elevated by ~4°C.||None|
|Gaoua et al., 2011||50°C, 50% r.h.||45 min||Attention and memory tests||Tc elevated to 38.6°C. Tsk elevated to 39.6°C.||Attention not impaired but memory impaired|
|Racinais et al., 2008||50°C, 50% r.h.||15 min walk at 3–5 km/h. Followed by 45 min passive exposure.||Attention, working and visual memory||Tc elevated to 38.8°C. Tsk elevated to 39°C.||Attention not impaired but working and visual memory impaired|
|Sun et al., 2012||50°C, 40% r.h.||60 min||Attention Network Test||Tc elevated to 38.4°C||Impaired executive function|
|Wijayanto et al., 2013||42°C||45 min||Short term memory||Delta Tc elevated by 0.31°C||None|
|Simmons et al., 2008||45°C, 50% r.h.||Until Tc increased by 1°C. (Time unknown)||Reaction time and numerical vigilance||Tc elevated by 1°C. Tsk elevated by 6°C.||Faster reaction time but reduced accuracy|
It is generally accepted that simple task performance is less vulnerable to heat stress than complex task performance, a viewpoint that has been supported by recent literature reviews (Hancock, 1986; Pilcher et al., 2002; Hancock and Vasmatzidis, 2003; Gaoua, 2010).
Complex tasks such as working memory (spatial span test, pattern recognition) were significantly impaired through heat stress [45 min at 50°C, 50% relative humidity (r.h.)], whereas simple attentional tasks (match to sample, choice reaction time, rapid visual information processing) were not affected (Gaoua et al., 2011).
Moreover, Watkins et al. (2014) recently demonstrated that soccer goal line officials’ ability to complete simple tasks (tracking, simple reaction time, and numerical vigilance) does not deteriorate during a 90 min passive exposure to 30°C, 40% r.h.
However, the authors neglected to assess complex cognitive task performance and the severity of heat stress was unlikely to impose significant stress, especially using a passive model.
Previous reviews also suggest that cognitive function is generally unaffected unless the external stimulus is sufficient in intensity and duration to increase Tc away from a homeostatic range approximate to 37°C (Hancock and Vasmatzidis, 2003).
An early study led to this theory (Wilkinson et al., 1964), whereby as Tc increased to 38.5°C (through passive heating), simple task performance (vigilance) improved but complex task performance (mental addition) was compromised. However, in a later study, it was shown that passively heating individuals up to 39.05°C did not affect short or long term memory, verbal logic problems, and numerical subtraction performance (Holland et al., 1985).
Therefore, it seems that in a hot environment Tc alone may not be a reliable predictor of cognitive performance decline. In support, recent research suggests that an increased skin temperature (Tsk), independent of any rise in Tc, may be responsible for any heat induced cognitive deteriorations (Gaoua et al., 2012).
Participants in the aforementioned study were passively exposed to 50°C, 30% r.h. for ~15 min, and were required to complete simple (reaction time) and complex (working memory) tasks during the exposure.
The results demonstrated that simple task performance was not affected, however complex task performance was significantly impaired.
Thus, it appears that Tsk (which was significantly increased in the heat by ~3°C) and a reduced thermal comfort (~8 points on a 20 point scale) in the heat, whereby subjects reported more negative feelings (i.e., they felt hotter and less comfortable), were responsible for the reductions in complex task performance, which again were independent of any change in Tc (Gaoua et al., 2012).
It may therefore be suggested that the subjective state of the individual could be a key factor affecting cognitive function in the heat, as these responses led to alterations in complex task performance independent of variations in Tc. Indeed, selective head skin cooling (induced by three cooling packs) has been shown to preserve some complex cognitive functions (Gaoua et al., 2011).
Therefore, it seems that increasing thermal comfort (rather than mitigating Tc increases) may be effective in maintaining complex cognitive function (and consequently safety) in passively experienced thermally stressful environments.
Recent investigations have utilized the attention network test (ANT) and functional magnetic resonance imaging (fMRI) to provide an insight into brain blood flow alterations upon exposure to heat stress, and how these changes affect aspects of the attention network (Jiang et al., 2013; Liu et al., 2013; Sun et al., 2013).
The ANT (Macleod et al., 2010) is a tool used to measure the efficiency of three major attention networks; alerting (simple task; related to maintaining readiness), orienting (simple task; responsible for selecting the region of space or channel to be attended), and executive control (complex task; involved in resolving conflict among possible actions).
These three aspects of attention differ from one another in brain activation locations (Petersen and Posner, 2012), hence, the application of fMRI has allowed researchers to accurately and simultaneously quantify how blood flow/activation in these areas vary upon exposure to environmental heat stress and relative to differential (simple or complex) cognitive tasks. In support of previous findings (see Table Table2),2), passive heat exposure (1 h at 50°C, 40% r.h.) did not alter simple task (alerting and orienting) performance for reaction time or accuracy (Liu et al., 2013).
The lack of heat induced cognitive alteration in these tasks appear to be due to increased activation in alternative brain regions i.e., a compensatory effect (see Table Table3).3).
Conversely, passive hyperthermia had a significant adverse effect on complex cognitive processes involving executive function, with reaction time increasing by ~22 ms.
During the executive function task, there was no difference in activation at the anterior cingulate cortex (brain region involved in executive functioning) between the normothermic and hyperthermic groups, but again there appeared to be compensatory activation (Table (Table3).3).
It is currently unclear why this type of complex task performance is consistently impaired by heat stress (Table (Table2)2) given the apparent compensatory activation. Similar results have been found elsewhere (Sun et al., 2012, 2013), however it is currently unknown if these changes were mediated by an increased Tsk (not reported) or Tc (peak ~38.5°C).
A plausible explanation for these behavioral changes is that the increase in plasma serotonin (5-hydroxytryptamine; 5-HT) witnessed during passive heat stress (McMorris et al., 2006) inhibits the production of dopamine (DA), a neurotransmitter that appears to play a major role in complex task performance [executive function; (Rektor et al., 2003)].
As stated previously, the precise relationship between Tsk and 5-HT is currently unknown, therefore future work should examine if; (1) 5-HT plays a major role in these heat stress induced cognitive alterations, and (2) if plasma (human) and/or brain (animal models) 5-HT increases in response to an elevated Tsk and/or Tc differentially. To our knowledge, this relationship is yet to be examined.
Summary of activated and depressed brain regions during passive heat stress (Liu et al., 2013).
|Alerting network||Orienting network||Executive network|
|Increased activity||Right superior frontal gyrus||Temporal lobe||Frontal lobe|
Superior temporal gyrus
|Depressed activity||Right middle occipital gyrus||Frontal Parietal lobe||Post-central gyrus|
|Left inferior parietal lobe||Occipital lobe|
KEY CONCEPT 1
Neuroscientific studies suggest that specific attentional functions are carried out by several interconnected brain networks. The attentional functions and related networks go under different names, but a classification into the three networks of alerting, orienting, and executive control is common. It is now understood that under many circumstances these networks interact and influence each other.
KEY CONCEPT 2
Functional Magnetic Resonance Imaging
This method highlights differences in brain activity by measuring related blood oxygenation levels. It yields information regarding relative differences in brain activity when comparing two or more experimental conditions and thus offers useful insight as to which brain areas are selectively active during certain mental processes.
The available evidence demonstrates that heat stress related cognitive decline is primarily mediated by a reduction in thermal comfort (Gaoua et al., 2012) and/or changes in regional brain blood flow (Liu et al., 2013; Qian et al., 2013).
Although the involvement of 5-HT is not yet well established, evidence has shown that augmenting the bioavailability of the amino acid tyrosine (a precursor for DA synthesis) may preserve cognitive function during thermal stress (Wurtman et al., 1980).
In support, it has recently been shown that tyrosine (6.5 g) ingested 90 min prior to passive heat stress (90 min at 45°C, 30% r.h.) significantly decreased event related potential (P300) latency and contingent negative variation latency compared with a placebo (Kishore et al., 2013).
Moreover, there was a significant increase in plasma DA concentrations when participants ingested tyrosine (Kishore et al., 2013), an effect which may be responsible for the improved cognitive function.
Conversely, it has been shown that 150 mg·kg−1 tyrosine ingestion prior to exhaustive exercise did not affect cognitive function in a warm environment compared to a placebo (Watson et al., 2012). However, the environmental conditions (i.e., thermal stress) may not have been sufficient in magnitude to increase plasma 5-HT, as to our knowledge, this has not been shown to increase in such a mild environment.
Thus, as plasma DA levels were not assessed in the aforementioned study, and tyrosine works by increasing DA concentrations, it is impossible to draw conclusions about the true effects of tyrosine in this work.
Although there are very few well controlled studies in this area, the evidence available (Kishore et al., 2013) suggests that ingestion of tyrosine may be an effective strategy to maintain cognitive function during passive heat stress.
Finally, as sensory displeasure (decreased thermal comfort elicited through an increased Tsk) may be the primary factor mediating heat stress induced cognitive disturbances (Gaoua et al., 2012), it is reasonable to suggest that improving thermal comfort (through an acute reduction in Tsk) may also combat the negative side effects of heat stress on complex cognitive functioning.
However, results to date have not wholly supported this notion. For example, a recent study has shown that ingestion of menthol lozenges had no such effect (Zhang et al., 2014) during simulated firefighting in the heat. However, when applied directly to the skin, menthol has a stimulating action on the peripheral cold receptor TRPM8 (Eccles, 2000), thus, the ingestion of menthol lozenges is likely to be an inferior intervention compared to direct menthol application to the skin.
It is important to note that the effect of menthol on thermal comfort is dose dependent, whereby concentrations of <2% elicit a cool sensation (Cliff and Green, 1994), but concentrations >2% may cause irritation and burning sensations (Yosipovitch et al., 1996). Research is needed to determine if topically applied menthol (at concentrations <2%) is effective at improving thermal comfort and consequently maintaining complex cognitive function during heat stress.
KEY CONCEPT 3
Tyrosine, a non-essential amino acid synthesized in the liver from phenylalanine, is a precursor for the synthesis of catecholamines. Nutritional supplementation of tyrosine increases its ratio to other large chain amino acids, and can result in a greater cerebral uptake of dopamine and noradrenaline. Evidence suggests that this response helps maintain cognitive function in extreme environmental conditions.
Cold stress is experienced in occupational (military, fishing trawlers, emergency disaster workers) and athletic (winter sports) settings (Muller et al., 2012).
It appears that both moderate and extreme reductions in ambient temperature may have a negative effect on cognitive function (Banderet et al., 1986; Palinkas, 2001). Specifically, cold exposure (−20 to 10°C) has led to decrements in memory [complex task (Thomas et al., 1989; Patil et al., 1995)], vigilance [complex task (Flouris et al., 2007)], reaction time [simple task (Teichner, 1958; Ellis, 1982)], and decision making [complex task; see Table Table4;4; (Watkins et al., 2014)]. Such consistent findings across such diverse ambient temperatures may be explained by traditional theories of cold induced cognitive decrement (Teichner, 1958; Enander, 1987; Muller et al., 2012).
The distraction theory (Teichner, 1958) explains that exposure to cold conditions provides alternative stimuli to interrupt focus which would otherwise be fixed on the cognitive task at hand (i.e., attention is focused on feeling cold rather than completing the cognitive task provided).
This theory is supported by recent findings where temperatures as mild as 10°C (Muller et al., 2012) may have provided enough of a sensory challenge to distract participants from a set cognitive task. Regression analysis from a recent study (Watkins et al., 2014) reported a significant relationship between alterations in thermal comfort and cognitive function in the cold.
The effects of passive cold exposure on cognitive function.
|Author and date||Environment (temperature)||Duration||Cognitive assessment tool||Physiological response||Cognitive alterations|
|Shurtleff et al., 1994||4°C||30 min||Match to Sample||Increased systolic blood pressure following cold exposure||Cold exposure reduced matching accuracy|
|Patil et al., 1995||2–3°C (Cold Water Immersion)||3 min||Variety of simple and complex tasks||Increased systolic and diastolic blood pressure following cold water immersion||Cold exposure increased alertness, but worsened short-term memory|
|Banderet et al., 1986||Night: −4 to −10°C; Day: −23 to −25°C||5 days||Pattern and number comparison, grammatical reasoning, coding||None reported||All cognitive tasks impaired aside from grammatical reasoning|
|Marrao et al., 2005||9 day range: −24 to 4.4°C||9 days||Logical planning, reasoning, vigilance||No significant thermoregulatory changes||None|
|Mäkinen et al., 2006||10°C||10 days||Cognitive Battery (ANAM-ICE)||Significant reductions in Tc, Tsk and finger temperature across exposure||Cold exposure increased response time, decreased accuracy, and efficiency of tasks|
|O’Brien et al., 2007||10 or 15°C (Cold Water Immersion). Subsequent cold air exposure until Tcore reached 35.5°C.||N/A||Match to Sample, complex reaction time, logical reasoning, visual vigilance, addition and subtraction, repeated acquisition||Cold water immersion reduced Tc by 0.3 to 1°C. Tsk reduced to ~26°C. Finger temperature reduced to ~15°C.||Cognitive function was not affected by cold water immersion|
Exposure to cold conditions alters the concentration of central catecholamines [DA, epinephrine and norepinephrine (Avakian et al., 1984)]. Alterations in levels of central catecholamines (Rauch and Lieberman, 1990) may have a detrimental effect on cognition as brain regions such as the prefrontal cortex are reliant on these neurotransmitters for normal function (Rektor et al., 2003; Friston et al., 2014). There is a plethora of evidence which demonstrates that tyrosine supplementation improves cognitive function during acute cold stress (Shurtleff et al., 1993, 1994; Yeghiayan et al., 2001; Palinkas et al., 2005; Mahoney et al., 2007; O’Brien et al., 2007). Given that tyrosine is a precursor for the synthesis of norepinephrine and DA, these studies support the notion that alterations in catecholamine concentrations may play a role for cold stress induced cognitive impairment. However, further support is needed to clarify if this is the case in humans.
Tyrosine supplementation is likely to improve cognitive function during exposure to cold environmental conditions (as previously described). Similar augmentation of cognitive function was observed following the use of caffeine, although this was during exposure to multiple stressors [cold, intense physical and psychological stress (Lieberman et al., 2002)]. The implementation of multiple stressors makes it difficult to attribute any improvements in cognitive function to caffeine supplementation. However, as caffeine may increase metabolic rate (and potentially increase in Tc; Poehlman et al., 1985) this may provide a favorable physiological effect when exposed to cold conditions. Adequate clothing for cold, dry environments should aim to block airflow but enable water vapor to dissipate if sweating occurs, i.e., to maintain body heat balance (Holmér, 1988). Cold acclimation or acclimatization is suggested to result in reduced vasoconstriction, increased skin temperature, delayed onset of shivering, dampened release of stress hormones, and reduced thermal discomfort (Mäkinen et al., 2006). Specifically, a reduction in cold stress from acclimation or acclimatization should in theory limit shivering and thermal discomfort and thus potentially limit the level of distraction and thus may positively influence cognitive function. Despite this, it was demonstrated that 10 days repeated exposure to 10°C did not significantly alter cognitive function, including accuracy, efficiency and response time, when compared to control (Mäkinen et al., 2006).
Given the equivocal nature of acclimation/acclimatization and tyrosine supplementation on cold induced cognitive function disturbances, appropriate clothing to maintain thermal comfort is the only robust intervention presently available. Evidently, further interventional work is required to positively influence the cold environment cognition nexus.
Agne Kajackaite – PLOS
The image is in the public domain.
Original Research: Open access
“Battle for the thermostat: Gender and the effect of temperature on cognitive performance”. Tom Y. Chang, Agne Kajackaite .
PLOS ONE. doi:10.1371/journal.pone.0216362