Fnbeh 16 957677

Download as pdf or txt
Download as pdf or txt
You are on page 1of 14

TYPE Review

PUBLISHED 23 September 2022


DOI 10.3389/fnbeh.2022.957677

The effects of acute


OPEN ACCESS high-intensity aerobic exercise
EDITED BY
Chong Chen,
Yamaguchi University Graduate School
on cognitive performance: A
of Medicine, Japan

REVIEWED BY
structured narrative review
Tao Huang,
Shanghai Jiao Tong University, China
Zhaowei Kong, Mizuki Sudo1*, Joseph T. Costello2 , Terry McMorris2,3 and
University of Macau, Macao SAR, China Soichi Ando4*
Lei Cui,
Beijing Normal University, China 1
Physical Fitness Research Institute, Meiji Yasuda Life Foundation of Health and Welfare, Tokyo,
*CORRESPONDENCE Japan, 2 Extreme Environments Laboratory, School of Sport, Health and Exercise Science, University
Mizuki Sudo of Portsmouth, Portsmouth, United Kingdom, 3 Institute of Sport, University of Chichester,
[email protected] Chichester, United Kingdom, 4 Graduate School of Informatics and Engineering, The University
Soichi Ando of Electro-Communications, Chofu, Japan
[email protected]

SPECIALTY SECTION
This article was submitted to
Motivation and Reward, It is well established that acute moderate-intensity exercise improves
a section of the journal
Frontiers in Behavioral Neuroscience cognitive performance. However, the effects of acute high-intensity aerobic
RECEIVED 31May 2022
exercise on cognitive performance have not been well characterized. In
ACCEPTED 29 August 2022 this review, we summarize the literature investigating the exercise-cognition
PUBLISHED 23 September 2022
interaction, especially focusing on high-intensity aerobic exercise. We discuss
CITATION methodological and physiological factors that potentially mediate cognitive
Sudo M, Costello JT, McMorris T and
Ando S (2022) The effects of acute performance in response to high-intensity exercise. We propose that the
high-intensity aerobic exercise on effects of high-intensity exercise on cognitive performance are primarily
cognitive performance: A structured
narrative review. affected by the timing of cognitive task (during vs. after exercise, and
Front. Behav. Neurosci. 16:957677. the time delay after exercise). In particular, cognitive performance is more
doi: 10.3389/fnbeh.2022.957677
likely to be impaired during high-intensity exercise when both cognitive
COPYRIGHT
and physiological demands are high and completed simultaneously (i.e.,
© 2022 Sudo, Costello, McMorris and
Ando. This is an open-access article the dual-task paradigm). The effects may also be affected by the type of
distributed under the terms of the cognitive task, physical fitness, exercise mode/duration, and age. Second,
Creative Commons Attribution License
(CC BY). The use, distribution or we suggest that interactions between changes in regional cerebral blood
reproduction in other forums is flow (CBF), cerebral oxygenation, cerebral metabolism, neuromodulation by
permitted, provided the original
author(s) and the copyright owner(s)
neurotransmitters/neurotrophic factors, and a variety of psychological factors
are credited and that the original are promising candidates that determine cognitive performance in response
publication in this journal is cited, in
to acute high-intensity exercise. The present review has implications for
accordance with accepted academic
practice. No use, distribution or recreational, sporting, and occupational activities where high cognitive and
reproduction is permitted which does physiological demands are required to be completed concurrently.
not comply with these terms.

KEYWORDS

cognition, dual task, cerebral blood flow, cerebral oxygenation, cerebral metabolism,
neuromodulation

Frontiers in Behavioral Neuroscience 01 frontiersin.org


Sudo et al. 10.3389/fnbeh.2022.957677

Introduction effects of acute high-intensity exercise on cognitive performance


are poorly understood.
A growing body of evidence suggests that acute moderate- In this review, we first summarize the findings of studies
intensity exercise improves cognitive performance (Lambourne investigating the exercise-cognition interaction, especially
and Tomporowski, 2010; Chang et al., 2012; Ando et al., 2020; focusing on high-intensity aerobic exercise. Then, we explore
McMorris, 2021). It has been speculated that the relationship methodological and physiological factors which may alter
between exercise intensity and cognitive performance is cognitive performance in response to high-intensity exercise.
inverted-U shaped (Lambourne and Tomporowski, 2010; This review has implications for recreational, sporting, and
Chang et al., 2012; McMorris, 2021). In the inverted-U theory, occupational activities where high cognitive and physiological
acute exercise gradually increases arousal to an optimal level demands are simultaneously required.
from rest to moderate intensity and thus improves cognitive
performance. A recent review summarized that improvements
in cognitive performance following moderate-intensity exercise Methodology
are frequently accompanied by the changes in brain activation
assessed by electroencephalogram (EEG) (Kao et al., 2020), A literature search was undertaken using Pubmed to identify
which appears to support the theory that acute exercise studies that examined the effects of high-intensity aerobic
alters brain activity and that this is associated with cognitive exercise on cognitive performance, assessed during and/or
performance. Acute high-intensity aerobic exercise leads to after exercise. The reference lists of relevant articles were also
metabolic, circulatory, and neurohormonal changes at the level searched. The searches were undertaken in February 2022
of the brain (Ide and Secher, 2000; Meeusen et al., 2001; Nybo and relevant articles were obtained. This review focused on
and Secher, 2004; Ogoh and Ainslie, 2009; Seifert and Secher, healthy adults, and no restrictions were placed on publication
2011). In contrast to moderate-intensity exercise, theoretically, date, study design, methodology, or method of assessing
high-intensity exercise may, therefore, also lead to altered, cognitive performance. High-intensity aerobic exercise was
and potentially impaired cognitive performance. Indeed, the defined as exercise equating to ≥ 80% maximum power
inverted-U theory predicts that high-intensity exercise increases output (Browne et al., 2017), ≥ 80% maximal oxygen uptake
arousal levels beyond the optimal level and leads to a temporary (V̇O2 ) (McMorris, 2016b), or equivalent [e.g., ≥ 80% maximal
reduction in cognitive performance. However, the current heart rate (HR)]. Physiological demands are different between
literature base detailing the effects of high-intensity exercise on continuous and intermittent high-intensity exercise. Thus, we
cognitive performance is not fully supportive of this theory and included high-intensity aerobic exercise in this review, and
is somewhat ambiguous and contradictory (Browne et al., 2017; studies incorporating high-intensity interval exercise (HIIE)
Moreau and Chou, 2019; Cantelon and Giles, 2021; McMorris, were considered outside the scope of this review. If specifically
2021; Zheng et al., 2021). interested in this, readers are referred to a recent review
Dietrich and Audiffren (2011) proposed the hypofrontality that has already explored the effects of HIIE on executive
hypothesis to explain how acute high-intensity exercise affects function (Hsieh et al., 2021). In addition, we did not include
cognitive performance. The prefrontal cortex (PFC) orchestrates studies conducted in extreme environments, such as hypoxia
higher-order brain function including cognitive function and hot/cold environments. However, we referred to evidence
(Miller and Cohen, 2001; Cools and Arnsten, 2021) and from HIIE studies, or studies in extreme environments, for
is thought to play a central role in cognitive performance. discussion since physiological mechanisms underlying cognitive
Acute exercise activates brain regions including motor and improvement/impairment in response to HIIE exercise or
sensory cortices, insular cortex, and cerebellum (Williamson exercise in extreme environments are, at least partly, shared with
et al., 1997; Christensen et al., 2000; Hiura et al., 2014). those induced by high-intensity aerobic exercise.
Hence, the hypofrontality theory speculates that extensive
activation of motor and sensory systems during high-intensity
exercise likely attenuates higher-order functions of the PFC Results
as the brain has finite metabolic resources (Dietrich and
Audiffren, 2011). More recently, McMorris proposed an Details of the included studies are shown in Table 1,
interoceptive model to explain the effects of high-intensity comprising a total of 40 studies (assessed during exercise
exercise on cognitive performance (McMorris, 2021). This only, n = 20; assessed both during and after exercise, n = 3;
model offers a more holistic overview of the interaction as it assessed after exercise only, n = 17). In many studies,
incorporates motivation, perceived effort costs, and perceived cognitive performance was impaired during high-intensity
availability of resources, together with regional activations and exercise (Chmura et al., 1994; McMorris and Keen, 1994;
neurotransmitter releases in the brain. Nevertheless, to date, the Brisswalter et al., 1997; McMorris et al., 2009; Labelle et al.,
physiological and psychological mechanism(s) mediating the 2013; Wang et al., 2013; Dutke et al., 2014; Mekari et al., 2015;

Frontiers in Behavioral Neuroscience 02 frontiersin.org


Frontiers in Behavioral Neuroscience

Sudo et al.
TABLE 1 Summary of the findings.

References Participants Category of Cognitive task(s) (number Exercise Exercise duration Timing of Physiological Main findings
(F) cognitive task of trials, duration) modality/intensity (high intensity only) cognitive variables
or until exhaustion task

Chmura et al. N = 22 (0) Young Psychomotor task Choice RT (30 trials, 107 s) Cycling Near maximal (300 W) 6 min During Blood catecholamine, RT: impairment
(1994) lactate
McMorris and N = 12 (4) Young Psychomotor task Simple RT (15 trials) Cycling 100% maximum Not reported During - RT: impairment
Keen (1994) workload
McMorris and N = 12 (0) Young Attentional task Soccer specific visual search task (30 Cycling 100% maximum power Not reported During - Visual search: improvement
Graydon executive function slides) Soccer specific decision output Decision making: improvement
(1997) making task (15 trials)
McMorris et al.N = 24 (0) Young Executive function Flanker task (96 trials) Cycling 80% maximum aerobic 15 min or until exhaustion During Blood catecholamine, RT: impairment Accuracy:
(2009) power adrenocorticotropic impairment
hormone, cortisol
Ando et al. N = 12 (0) Young Executive function Flanker task (40 trials, 3 min 20 s) Cycling 80% V̇O2peak 6.5 min During Cerebral oxygenation EMG-RT≈ Accuracy≈
(2011)
Huertas et al. N = 18 (0) Young Executive function Attention network test (modified Cycling 95% LT 25 min During Blood lactate RT: improvement
(2011) flanker task, 480 trials, 25 min)
Shields et al. N = 30 (15) Young Attentional task Visual threat-detection task (256 Cycling 80% maximal HR Not reported During - RT: improvement Accuracy:
(2011) trials) improvement
03

Labelle et al. N = 37 (18) Young Executive function Stroop task (80 trials) Cycling 80% peak power output 6.5 min During - Accuracy: impairment RT
(2013) High fit = 16 Low variability: impairment in lower
fit = 21 fit
Wang et al. N = 80 (31) Young Executive function Wisconsin card sorting test (128 Cycling 80% HRR 30 min During - Performance: impairment
(2013) response cards)
Dutke et al. N = 60 (14) Young Memory task Word comparison (Primary task, 60 Cycling 120% AT > 27 min During - Number of correct response≈
(2014) attentional task trials, 27 min) Interval production Response time≈ Interval
(simultaneously) (Secondary task, press a button every production error: impairment
2 s, 27 min)
Davranche N = 14 (3) Young Executive function Simon task (200 trials, 4 min) Cycling 20% above VT 20 min During - RT: improvement Accuracy≈
et al. (2015)
Mekari et al. N = 19 (12) Young Executive function Stoop task (30 trials × 2 blocks) Cycling 85% peak power output 9 min During Cerebral oxygenation RT: impairment Accuracy:
(2015) impairment
Schmit et al. N = 15 (5) Young Executive function Flanker task (40 trials, as many blocksCycling 85% maximal aerobic Until exhaustion During Cerebral oxygenation RT≈ Accuracy: impairment

10.3389/fnbeh.2022.957677
(2015) as possible) power
Smith et al. N = 15 (9) Young Executive function Go/No-Go task (100 trials, 2 min) Running 90% HRR 10 min During - RT: impairment Accuracy:
(2016) impairment
Gonzalez- N = 24 (12) Young Psychomotor task Psychomotor vigilance task (mean Cycling 100% ventilatory 5 min During - RT: impairment
frontiersin.org

Fernandez 46.8 trials) anaerobic threshold


et al. (2017)

(Continued)
Frontiers in Behavioral Neuroscience

Sudo et al.
TABLE 1 (Continued)

References Participants Category of Cognitive task(s) (number Exercise Exercise duration Timing of Physiological Main findings
(F) cognitive task of trials, duration) modality/intensity (high intensity only) cognitive variables
or until exhaustion task

Tempest et al. N = 14 (5) Young Executive function Flanker task (2 min × 10 blocks) Cycling 10% above VT 60 min During Cerebral oxygenation RT (flanker task): improvement
(2017) 2-back task (60 trials × 10 blocks, Accuracy (n-back): impairment
20 min)
Ciria et al. N = 20 (0) Young Attentional task Oddball task (20 min) Cycling 80% V̇O2peak 20 min During EEG RT≈ Accuracy≈
(2019)
Tempest and N = 13 (7) Young Executive function N-back task (0-back, 60 trials; Cycling 115% first ventilatory 16 min During Cerebral oxygenation Response time≈ Accuracy≈
Reiss (2019) 2-back, 60 trials) threshold (VT1) (fNIRS)
Komiyama N = 17 (0) Young Executive function Spatial delayed response Go/No-Go Cycling 80% V̇O2peak 8 min During Middle cerebral artery RT≈ Accuracy: impairment
et al. (2020) tasks (24 trials, ∼5 min) blood velocity Cerebral
oxygenation
Stone et al. N = 13 (5) Young Executive function Cedar operator workload assessment Running 100% HRR Until exhaustion During Cerebral oxygenation Accuracy: impairment
(2020) tool
Travlos and N = 20 (0) Young Attentional task Random number generation test Cycling during 80% V̇O2max Until exhaustion During/ - Random number generation test
Marisi (1995) High fit = 10 Low psychomotor task Choice RT (15 trials × 4) and after volitional exhaustion (> 10 min) immediately (during)≈ RT (after)≈
fit = 10 after
Brisswalter N = 20 (0) Young Psychomotor task Simple detection RT (20 trials) Cycling during 80% maximal 10 min During/1 min - RT (during): impairment in only
et al. (1997) High fit = 10 Low aerobic power after low fit Accuracy≈ in both groups
04

fit = 10
Fery et al. N = 13 (0) Young Memory task Short-term memory task (20 trials) Cycling during 90% V̇O2max and Until exhaustion During/ - RT (during)≈ RT (after):
(1997) Volitional exhaustion immediately impairment
after
Kamijo et al. N = 12 (0) Young Executive function S1-S2 RT (Go/No-Go) task (60 trials, Cycling Volitional exhaustion Until exhaustion Immediately EEG (CNV, P300) EMG-RT≈
(2004a, 2004b) 10 min) after (< 3 min)
McMorris et al.N = 12 (0) Young Psychomotor task Whole body choice RT (9 trials) Cycling 100% maximal power Until exhaustion Immediately Blood lactate RT: impairment
(2005) output after (20 s later)
Winter et al. N = 27 (0) Young Memory task Vocabulary learning task (600 Running (two sprints, started at Until exhaustion 15 min after Blood catecholamine, Learning speed: improvement RT:
(2007) training trials + retention) 8 km/h, increased every 10 s by BDNF improvement (1 week later)
2 km/h) Volitional exhaustion
Coco et al. N = 17 (0) Young Psychomotor task RT task Attention and concentration Cycling Volitional exhaustion Until exhaustion 5 min after Blood lactate RT: impairment Accuracy:
(2009) Attentional task task Lactate infusion (N = 6) impairment
Luft et al. N = 30 (7) Young Psychomotor task Simple RT (35 correct trials, 90 s) Running Volitional exhaustion Until exhaustion 10–15 min after HR variability Working memory: improvement

10.3389/fnbeh.2022.957677
(2009) Executive function Choice RT (30 correct trials, 90 s) Others≈
Memory task Working memory task (one back task,
Attentional task 30 correct trials, 90 s) Short-term
memory task (42 trials, 2–3 min)
frontiersin.org

Continuous monitoring task (30


correct trials, 90 s)

(Continued)
Frontiers in Behavioral Neuroscience

Sudo et al.
TABLE 1 (Continued)

References Participants Category of Cognitive task(s) (number Exercise Exercise duration Timing of Physiological Main findings
(F) cognitive task of trials, duration) modality/intensity (high intensity only) cognitive variables
or until exhaustion task

Thomson et al. N = 163 (0) Young Psychomotor task Speed discrimination Running Volitional exhaustion Until exhaustion 1 min after - Time: improvement Accuracy:
(2009) (decision-making) impairment
Griffin et al. N = 47 (0) Young Memory task Face-name matching task Stroop task Running Volitional exhaustion Until exhaustion < 30 min After Blood BDNF, IGF-1 Face-name matching task:
(2011) Executive function improvement Stroop task≈
Etnier et al. N = 16 (7) Young Memory task Rey Auditory Verbal Learning Test Running Volitional exhaustion Until exhaustion Immediately Blood BDNF Memory performance:
(2016) (15 words × 2) after (after blood improvement (24 h later)
sampling)
Hwang et al. N = 58 (32) Young Executive function Stroop test (100 items × 3 conditions, Running Target HR 10 min 10 min after Blood BDNF Stroop test: improvement Trail
(2016) 4 min) Trail making test (< 2 min) corresponding to 85–90% making test: improvement
V̇O2max
Chang et al. N = 36 (36) Young Executive function Stroop test (neutral 60 s, incongruent Running 80% HRR 30 min 15 min after Cerebral oxygenation RT≈
(2017) 60 s)
Sudo et al. N = 32 (0) Young Executive function Spatial delayed response task (20 Cycling Volitional exhaustion Until exhaustion 2 min after Cerebral oxygenation, RT≈ Accuracy≈
(2017) trials) Go/No-Go task (20 trials) Blood catecholamine,
BDNF, IGF-1, lactate
Zimmer et al. N = 119 (41) Young Executive function Tower of London Cycling Volitional exhaustion Until exhaustion Immediately Blood lactate Thinking time: impairment
05

(2017) after (< 3 min)


Du Rietz et al. N = 29 (0) Young Executive function Cued continuous performance task Cycling 20% delta (difference 20 min 30 min after EEG RT≈ Accuracy≈
(2019) Psychomotor task (modified Go/No-Go task, 80 trials, between gas exchange threshold
11 min) Flanker task (400 trials, and V̇O2peak )
13 min) Choice RT task (72 trials,
10 min)
Hill et al. N = 13 (0) Young Executive function Flanker task (100 trials, < 3 min) Cycling and arm cranking Until exhaustion Immediately - Cycling: impairment Arm
(2019) Volitional exhaustion after cranking: improvement
Coco et al. N = 30 (?) Psychomotor task Simple RT Stroop color word test (50 Cycling Volitional exhaustion Until exhaustion Immediately Blood lactate Simple RT: impairment Stroop
(2020a) Young = 15 Old = 15Executive function names, 50 circles, and 50 words) Trail after Color Word Test: impairment
making test Trail Making Test: improvement
(Young)
Loprinzi et al. N = 120 (77) Young Memory task Word list memory task (15 words) Running 75% HRR 20 min 5 min after - Memory: improvement
(2021)
Marin Bosch N = 18 (0) Young Psychomotor task Psychomotor vigilance task (RT) Cycling 75% maximal cardiac 15 min 24 min after Neural activity (fMRI), RT≈ Accuracy≈

10.3389/fnbeh.2022.957677
et al. (2021) Memory task Associative memory task (8 series of 6frequency (Psychomotor Blood endocannabinoids,
successive pictures) task) and 69 BDNF
min after
(memory task)
frontiersin.org

F, females; N, number of participants; RT, reaction time; W, watts; V̇O2p eak , peak oxygen uptake; EMG, electromyogram; LT, lactate threshold; HR, heart rate; HRR, heart rate reserve; AT, anaerobic threshold; VT, ventilatory threshold; EEG,
electroencephalogram; fNIRS, functional near-infrared spectroscopy; CNV, contingent negative variation; P300, positive 300; V̇O2m ax , maximal oxygen uptake; BDNF, brain-derived neurotrophic factor; IGF-1, insulin-like growth hormone factor-1;
fMRI, functional magnetic resonance imaging. ≈, no effect.
Sudo et al. 10.3389/fnbeh.2022.957677

Schmit et al., 2015; Smith et al., 2016; Gonzalez-Fernandez et al., the timing of the cognitive tasks is typically less considered
2017; Tempest et al., 2017; Komiyama et al., 2020; Stone et al., within the literature.
2020). In these studies, impairments in both reaction time (RT) Table 1 indicates that the adverse effects are most prominent
and accuracy were frequently observed. Seven studies reported during high-intensity exercise. These findings are corroborated
no changes in cognitive performance (Travlos and Marisi, 1995; by a recent review and suggest that impairments in cognitive
Fery et al., 1997; Ando et al., 2011; Dutke et al., 2014; Ciria et al., performance are more likely to occur during high-intensity
2019; Tempest and Reiss, 2019; Komiyama et al., 2020). Five exercise (Zheng et al., 2021). Based on the assumption
studies reported improvement in RT and/or accuracy during that metabolic resources are limited in the brain, extensive
high-intensity exercise (McMorris and Graydon, 1997; Huertas activation in several brain regions (e.g., motor and sensory
et al., 2011; Shields et al., 2011; Davranche et al., 2015; Tempest cortices) may attenuate higher-order functions of the PFC and
et al., 2017). impair cognitive performance (Dietrich and Audiffren, 2011).
Conversely, cognitive performance after high-intensity Furthermore, in the majority of the included studies, cognitive
exercise is heterogeneous; with improvements (Winter et al., performance was assessed using manual responses where
2007; Luft et al., 2009; Thomson et al., 2009; Griffin et al., activations of the motor-related areas are required. Given a
2011; Etnier et al., 2016; Hwang et al., 2016; Hill et al., 2019; limited capacity of the brain to simultaneously activate multiple
Coco et al., 2020a; Loprinzi et al., 2021), impairments (Fery regions involved in cognitive performance and high-intensity
et al., 1997; McMorris et al., 2005; Coco et al., 2009, 2020a; exercise, it is plausible that cognitive performance is more likely
Thomson et al., 2009; Zimmer et al., 2017; Hill et al., 2019), to be impaired during high-intensity exercise, particularly when
and no changes (Travlos and Marisi, 1995; Brisswalter et al., both cognitive and physiological demands are high. Indeed,
1997; Kamijo et al., 2004a,b; Luft et al., 2009; Griffin et al., in four studies reporting cognitive improvement during high-
2011; Chang et al., 2017; Sudo et al., 2017; Du Rietz et al., 2019; intensity exercise (Huertas et al., 2011; Shields et al., 2011;
Marin Bosch et al., 2021) reported within the literature. These Davranche et al., 2015; Tempest et al., 2017), exercise intensities
findings suggest that cognitive performance after high-intensity were relatively less demanding (i.e., HR < 170 bpm). Relatively
exercise appears to be dependent on experimental design (see lower physiological demands may be responsible for cognitive
below). In the following sections, we discuss the methodological, improvements during high-intensity exercise in these studies.
physiological, and psychological factors that affect cognitive Furthermore, McMorris (2021) argued that performance would
performance “during” and “after” high-intensity exercise. depend to a large extent on the perception of task costs
(demands) and resources available. These two judgments may
be difficult to make in the dual-task situation, leading to over-
or under-confidence. This could alter motivation, which would
Methodological factors affect cognitive performance.
A recent meta-analysis demonstrated that acute high-
Here we discuss the potential methodological and intensity exercise had a small, significant facilitating effect on
experimental factors that contribute to the inconsistent findings.
cognitive performance after high-intensity exercise (Moreau
These include the following: timing of cognitive task, type of
and Chou, 2019). In the current review, we observed
cognitive task, physical fitness, exercise mode/duration, and age.
that cognitive performance after high-intensity exercise is
inconsistent: and improvements, impairments, and no changes
were reported. EEG studies reported reductions in P3
Timing of cognitive task amplitudes after high intensity (Kamijo et al., 2004b) or
HIIE (Kao et al., 2017). On the contrary, Du Rietz and
When participants perform cognitive tasks during exercise, colleagues reported improvements in P3 amplitude and delta
they perform the exercise and cognitive tasks simultaneously power reflecting executive and sustained attention after high-
(i.e., a dual-task paradigm). However, when cognitive tasks are intensity exercise (Du Rietz et al., 2019). These findings suggest
performed after exercise, participants only perform a single that brain activity after exercise may be dependent on the
task. A meta-analysis reported higher effect sizes in single- experimental design employed (e.g., exercise intensity, time
task conditions (after exercise) when compared with dual-task delay after exercise). Indeed, most physiological changes start
conditions (during exercise) (Lambourne and Tomporowski, to recover immediately after high-intensity exercise (Ide et al.,
2010), while another meta-analysis reported that effect sizes 2000; Gonzalez-Alonso et al., 2004; Curtelin et al., 2017; Sudo
were not different between single and dual-task conditions et al., 2017). Thus, rapid recovery of physiological variables
(Chang et al., 2012). Furthermore, McMorris and Hale (2012) to homeostatic resting levels may, at least in part, explain
undertook statistical analyses and found that there were no the contradictory findings related to cognitive performance
differences in effect sizes obtained during compared after after high-intensity exercise. To explore this possibility, we
exercise. Nevertheless, as recently highlighted (McMorris, 2021), summarized the impacts of the timeframe in which cognitive

Frontiers in Behavioral Neuroscience 06 frontiersin.org


Sudo et al. 10.3389/fnbeh.2022.957677

performance was assessed after exercise (Table 2). When included studies, we classified executive function into response
multiple cognitive tasks were examined in a single study, or inhibition (Go/No-Go task), interference control (Flanker task,
when both improvement and impairment were reported in a Simon task, and Stroop task), working memory (n-back task
cognitive task (e.g., improvement in RT and impairment in and spatial delayed response task), and others (soccer-specific
accuracy), all results are reported. We observed heterogeneous task, Wisconsin card sorting task, Cedar Operator Workload
findings when cognitive performance was assessed within 5 min Assessment Tool, Tower of London, and Trail making test).
of completing high-intensity exercise. Intriguingly, however, no During high-intensity exercise, impairments in cognitive
impairments were reported when the timing of cognitive tasks performance were prominent in executive function and
was > 6 min after exercise. These findings support the notion psychomotor tasks (Table 3), which is thought to be closely
that a rapid recovery to homeostatic resting levels is critical related to dual-task paradigm. Thus, in most cognitive tasks,
for cognitive performance after high-intensity exercise. Taken adverse effects are more likely to occur during high-intensity
collectively, we propose that the effects of high-intensity exercise exercise. Conversely, we found improvements in several studies.
on cognitive performance are closely related to, and impacted In three studies (Huertas et al., 2011; Davranche et al., 2015;
by, the timing of cognitive task (during vs. after exercise, and Tempest et al., 2017), cognitive improvements were observed
the time delay after exercise). in interference control (i.e., Flanker task and Simon task).
These findings imply that performances in these cognitive
tasks may benefit from high-intensity exercise relative to the
Type of cognitive task other subcomponents of executive function. Furthermore, in the
study reporting improvements in soccer-specific cognitive tasks
Different brain regions are thought to be activated (both soccer-specific and attentional tasks) in college soccer
during different cognitive tasks (Macintosh et al., 2014; players (McMorris and Graydon, 1997), the cognitive tasks
Chen A. G. et al., 2016; Won et al., 2019). Thus, we can were probably autonomous to the soccer players and therefore
assume that the type of cognitive task is one of the factors less demanding. Hence, cognitive improvements during high-
that determine how acute high-intensity exercise impacts intensity exercise appear to be related to cognitive demands.
cognitive performance. This may be particularly relevant A meta-analysis review reported that facilitating effects
when exercise and cognitive tasks are concurrently performed of performance were similarly observed in subcomponents of
since multiple brain regions are presumably activated. In this executive function (i.e., working memory, inhibitory control,
review, we classified the type of cognitive task into executive cognitive flexibility, and attention) after high-intensity exercise
function, psychomotor, memory, and attentional tasks (Table 3). (Moreau and Chou, 2019). In the present review, we failed
Executive function encompasses several subdomains and to find clear associations between the type of cognitive task
consists of basic components of inhibition, working memory, and cognitive performance after high-intensity exercise. It
and cognitive flexibility (Diamond, 2013). Thus, based on the should be noted, however, that improvements in memory

TABLE 2 Summary of impacts of time delay after exercise.

0–5 min 6–10 min 11–20 min >20 min

Improvement (↑) No change (↔) Impairment (↓) ↑ ↔ ↓ ↑ ↔ ↓ ↑ ↔ ↓

Number of black circles indicates the number of studies.

TABLE 3 Summary of impacts of the type of cognitive task.

Executive function Psychomotor task Memory task Attentional task

Improvement (↑) No change (↔) Impairment (↓) ↑ ↔ ↓ ↑ ↔ ↓ ↑ ↔ ↓

During *** †*# †**$$##

After *$# †††*$$# *$

Number of symbols indicates the number of studies.


† Response inhibition (Go/No-Go task).

*Interference control (Flanker task, Simon task).


$ Interference control (Stroop task).
# Working memory (n-back task, spatial delayed response task).

• Others (soccer-specific task, Wisconsin card sorting task, Cedar Operator Workload Assessment Tool, Tower of London, and Trail making test), psychomotor task, memory task,
attentional task.

Frontiers in Behavioral Neuroscience 07 frontiersin.org


Sudo et al. 10.3389/fnbeh.2022.957677

performance were often observed after high-intensity exercise Running is kinematically less stable compared to cycling, and
(Winter et al., 2007; Griffin et al., 2011; Etnier et al., thus it may be difficult to complete cognitive performance
2016; Loprinzi et al., 2021). In particular, high-intensity during high-intensity running. Indeed, only two studies
exercise may be beneficial for retention (Winter et al., 2007; examined cognitive performance during high-intensity running,
Etnier et al., 2016; Loprinzi et al., 2021). Additional studies and both reported impairments in cognitive performance
are necessary to further elucidate potential physiological (Smith et al., 2016; Stone et al., 2020). Given the nature of
mechanisms underlying the improvement. In this review, we the dual-task paradigm, running may be more detrimental
may not have been sufficiently powered to identify the effects of to cognitive performance relative to cycling during high-
different cognitive tasks/domains. Further research is required intensity exercise.
to establish the effects of high-intensity exercise on a variety of After high-intensity cycling, in most cases, we observed no
cognitive tasks and domains. changes or impairments in cognitive performance. Conversely,
after high-intensity running, improvements or no changes in
cognitive performance were predominant. Since participants
Physical fitness level of participants perform only a cognitive task after exercise (i.e., single
task) regardless of exercise mode, the findings are somewhat
It has been previously speculated that exercise-cognition unexpected. There are several physiological differences in
interaction is influenced by physical fitness (Lambourne and ventilatory and metabolic responses, HR, and motor unit
Tomporowski, 2010; Chang et al., 2012). For example, despite recruitment between cycling and running (Millet et al., 2009).
matched relative exercise intensity, individuals with lower Hence, the recovery of physiological variables to resting levels
physical fitness levels were more susceptible to cognitive could be different between high-intensity cycling and running.
impairments during high-intensity exercise, when compared Collectively, these findings suggest that the mode of exercise
with those who had higher aerobic capacities (Brisswalter et al., is one of the factors that affect cognitive performance, and
1997; Labelle et al., 2013). Furthermore, choice RT performance these effects are presumably influenced by the timing of
gradually improves during incremental exercise until at ∼75% cognitive task (during vs. after exercise, and the time delay
V̇O2max in young soccer players (Chmura et al., 1994). Aerobic after exercise). Future studies are required to understand how
capacity has been suggested to be one of the moderators exercise mode influences cognitive performance after high-
that affect cognitive performance in response to high-intensity intensity exercise.
exercise (Browne et al., 2017). McMorris (2021) claimed that
fitness levels would affect the individual’s perception of effort
costs and, hence, their motivation level. Further, well-powered Exercise duration
studies are also necessary to clarify the relationship between
cognitive performance and physical fitness before this theory Exercise duration also potentially affects cognitive
can be confirmed. performance in response to high-intensity exercise. We
summarized the relationship between exercise duration
and cognitive performance in Table 5. During exercise,
Exercise mode cognitive impairments were observed when exercise
duration was < 10 min. The findings were inconsistent
A previous meta-analysis suggested that exercise mode is when exercise duration was > 11 min or exhaustive
one of the factors that affect exercise-cognition interaction exercise. Thus, it is less likely that exercise duration per se
(Lambourne and Tomporowski, 2010). We summarized the affects cognitive performance. Rather, interactions between
impacts of high-intensity cycling and running in Table 4. exercise duration and intensity would be more important
The effects of high-intensity exercise on cognitive performance for cognitive performance during high-intensity exercise.
during cycling were inconsistent, but reductions in cognitive In most studies that assessed cognitive performance after
performance appeared to be more likely during cycling. high-intensity exercise, exercise was continued until exhaustion

TABLE 4 Summary of impacts of exercise mode.

Cycling (+ arm cranking) Running

Improvement (↑) No change (↔) Impairment (↓) ↑ ↔ ↓

During
After

Number of black circles indicates the number of studies.

Frontiers in Behavioral Neuroscience 08 frontiersin.org


Sudo et al. 10.3389/fnbeh.2022.957677

TABLE 5 Summary of impacts of exercise duration.

<10 min 11–20 min >20 min Until exhaustion

Improvement No change Impairment ↑ ↔ ↓ ↑ ↔ ↓ ↑ ↔ ↓


(↔) (↓)
(↑)

During
After

Number of black circles indicates the number of studies.

(Table 5). Nevertheless, the results were heterogeneous and Cerebral blood flow
suggest that exercise duration in isolation is not critical for
cognitive performance after exhaustive exercise. Assuming During exercise, CBF is regulated by complex interactions
that the duration of high-intensity exercise is likely limited, between neural activity and metabolism, partial pressure of
exercise duration alone is, therefore, not likely to determine oxygen, carbon dioxide (CO2 ), blood pressure, cardiac output,
cognitive performance. and sympathetic nervous system activity (Ogoh and Ainslie,
2009; Smith and Ainslie, 2017). CBF gradually increases
during mild- to moderate-intensity exercise in response to
Age neural activity and metabolism (Ogoh and Ainslie, 2009).
However, during high-intensity exercise, hyperventilation-
Coco and colleagues compared the effects of exhaustive induced hypocapnia constricts the cerebral vessels, thereby
exercise on the cognitive performance of young and older reducing CBF (Ogoh and Ainslie, 2009; Smith and Ainslie,
adults (Coco et al., 2020a). They reported impairments in the 2017). This suggests that brain metabolic demands might
performance of simple RT and the Stroop color-word test after be inadequate during high-intensity exercise. Ogoh et al.
exhaustive exercise in both groups. However, improvements (2014) reported that an increase in CBF, achieved using
in trail making test were observed only in the younger CO2 inhalation, did not affect cognitive performance during
group. These results suggest that the effects of high-intensity prolonged moderate-intensity exercise (Ogoh et al., 2014). More
exercise on cognitive performance may be different in young recently, Komiyama and colleagues tested the hypothesis that a
and older adults. Cerebral perfusion appears to be lower reduction in CBF is directly linked to impairment in cognitive
in older individuals during high-intensity exercise, although performance during high-intensity exercise (Komiyama et al.,
the cerebral extraction of glucose, lactate, and oxygen is 2020). By restoring CBF via CO2 inhalation, the authors
similar (Braz and Fisher, 2016). Thus, age may be one demonstrated that middle cerebral artery (MCA) velocity
factor that may influence cognitive performance and reduced (a surrogate for CBF) did not prevent impaired cognitive
cerebral perfusion could affect cognitive performance in older performance during high-intensity exercise. These results
individuals in particular. Given the brevity of studies in suggest that a reduction in CBF per se may not be responsible for
this area, definitive conclusion on the impact of age is impaired cognitive performance during high-intensity exercise.
not yet feasible. However, given that CBF supplies oxygen and nutrients,
the association between cognitive performance and regional
CBF (e.g., blood flow to the PFC) in response to high-
Physiological factors intensity exercise should be further investigated. In particular,
a recent study indicated physiological “uncoupling” between
As noted above, high-intensity exercise induces a the PFC oxygenation and MCA velocity during high-intensity
variety of physiological effects within the human brain. exercise with CO2 inhalation (Hansen et al., 2020). Follow-up
Here, we summarize and discuss the physiological factors studies are needed to fully understand the association between
that are linked to cognitive performance during and regional CBF and cognitive performance in response to high-
after high-intensity exercise and we identify some of the intensity exercise.
potential physiological factors that may contribute to
the inconsistent findings. These include the separate and
combined effects of cerebral blood flow (CBF), cerebral Cerebral oxygenation
oxygenation, cerebral metabolism, neuromodulation by
neurotransmitters and neurotrophic factors, and various Cerebral oxygenation reflects the balance between cerebral
psychological factors. oxygen availability and utilization (Boushel et al., 2001;

Frontiers in Behavioral Neuroscience 09 frontiersin.org


Sudo et al. 10.3389/fnbeh.2022.957677

Komiyama et al., 2017), which is generally measured from following maximal exercise may be associated with cognitive
the PFC. Cerebral oxygenation reduces during high-intensity performance (Sudo et al., 2017). This finding suggests that the
exercise close to maximal intensity (Rooks et al., 2010). Some recovery of cerebral oxygenation after high-intensity exercise
studies suggest that a reduction in cerebral oxygenation is not may, at least in part, account for the differential effects of high-
associated with impairments in cognitive performance during intensity exercise on cognitive performance between single (i.e.,
high-intensity exercise (Ando et al., 2011; Schmit et al., 2015; after) and dual (i.e., during) conditions.
Tempest et al., 2017). In contrast, others have indicated that
impairments in cognitive performance were accompanied by
reduction in cerebral oxygenation during high-intensity exercise Cerebral metabolism
(Mekari et al., 2015; Stone et al., 2020). The latter studies
suggest that impairments in cognitive performance may be It is generally accepted that blood glucose is the primary
associated with attenuated PFC oxygenation. However, several energy source for the brain at rest (Gold, 1995). Komiyama
studies have shown that cognitive performance improved et al. (2016) reported that cognitive performance improves
during acute moderate-intensity exercise in hypoxia despite during moderate-intensity exercise after skipping breakfast.
substantial reductions in cerebral oxygenation (Ando et al., This suggests that substrates other than glucose may compensate
2013; Komiyama et al., 2015, 2017). Hence, it is likely for the reduced availability of blood glucose during moderate-
that a reduction in cerebral oxygenation, in isolation, does intensity exercise. It is plausible that the same would be
not result in impaired cognitive performance. However, true for high-intensity exercise. Indeed, blood glucose uptake
reduction in cerebral oxygenation during high-intensity exercise is thought to be reduced in the brain during high-intensity
may impair cognitive performance in concert with other exercise (Kemppainen et al., 2005). In contrast, blood lactate
physiological factors. substantially increases during/after high-intensity exercise, and
Cerebral oxygenation starts to recover immediately after it is taken up by the brain (Ide et al., 2000; Gonzalez-
maximal exercise (Gonzalez-Alonso et al., 2004; Sudo et al., Alonso et al., 2004; Quistorff et al., 2008; Siebenmann
2017). Notably, the degree of recovery of cerebral oxygenation et al., 2021). Several studies suggested that blood lactate

FIGURE 1
(Upper) Summary of methodological factors that affect cognitive performance in response to high-intensity exercise. (Lower) Potential
physiological and psychological factors that mediate cognitive performance.

Frontiers in Behavioral Neuroscience 10 frontiersin.org


Sudo et al. 10.3389/fnbeh.2022.957677

would provide energy that contributes to improvements in and IGF-1 play a role in cognitive performance during/after
cognitive performance following HIIE (Tsukamoto et al., 2016; high-intensity exercise.
Hashimoto et al., 2018; Herold et al., 2022). In particular,
Hashimoto et al. (2018) directly measured lactate uptake in
the brain after HIIE and suggested that lactate production in Psychological factors
extra-cerebral tissues supports brain function. On the contrary,
Coco et al. (2020b) suggested that high levels of blood lactate In most studies, psychological factors are typically not well
have detrimental effects on cognitive performance. Interestingly, considered when attempting to elucidate the effects of high
Coco et al. (2009) indicated that intravenous lactate infusion intensity on cognitive performance. However, as suggested by
of a lactate solution impaired attentional performance. Hence, McMorris (2021), psychological factors such as the motivation
further studies are warranted to investigate how blood lactate and perception of effort may affect the acute exercise–
acts as a mediator of exercise-induced alterations in cognitive catecholamine–cognition interaction. Cantelon and Giles also
performance (Ando et al., 2022). suggested that psychological factors are moderating factors that
affect exercise–cognition interaction (Cantelon and Giles, 2021).
At present, and given the lack of empirical evidence, further
Neuromodulation by investigations are needed to investigate the association between
neurotransmitters and neurotrophic psychological factors and cognitive performance during and
factors after high-intensity exercise.

In humans, it is less clear how acute exercise alters central


neurotransmitter release due to technical and methodological Integration of physiological and
challenges. Nevertheless, given that rodent studies indicate that psychological factors
acute exercise releases neurotransmitters in the brain (Meeusen
et al., 2001; Hasegawa et al., 2011; Goekint et al., 2012; Chen It is likely that the effects of high-intensity exercise on
C. et al., 2016), acute exercise is likely to influence brain cognitive performance are multifactorial and determined by the
circuits involving a number of neurotransmitters including integration of several physiological and psychological factors
dopamine and noradrenaline (McMorris, 2016a; Ando et al., (Figure 1). We propose that interactions of these factors
2020). Dopamine and noradrenaline modulate the strength of influence neural activity associated with cognitive performance
the PFC network connections, and regulation of dopamine and and that this determines cognitive performance during and
noradrenaline is required for appropriate prefrontal cognitive after high-intensity exercise. This is consistent with McMorris
function (Arnsten, 2011). Furthermore, excess noradrenaline (2021) claiming that the perception of physiological stress
and dopamine appear to weaken the signal-to-noise ratio, which affects the motivation and perception of effort costs. However,
may result in impairments in the PFC function (Arnsten, the current literature base is insufficient to substantiate this
2011; Cools and Arnsten, 2021). Hence, the available literature speculation and this should be the focus of future research in
suggests that excess neuromodulators in the brain may have this area. A recent fNIRS study detected cognitive task-related
adverse effects on cognitive performance during/after high- hemodynamic changes from the left PFC during high-intensity
intensity exercise. High-intensity exercise also seems to increase exercise (Tempest and Reiss, 2019). Furthermore, an fMRI
brain-derived neurotrophic factors (BDNFs) (Ferris et al., 2007; study indicated that HIIE decreased brain activation associated
Winter et al., 2007; Fernandez-Rodriguez et al., 2021) and with cognitive performance (Mehren et al., 2019). Thus, future
insulin-like growth hormone factor-1 (IGF-1) (Sudo et al., studies using sophisticated neuroimaging methods (e.g., fNIRS,
2017). Several studies have implicated that changes in BDNF fMRI, and PET) are required to fully understand how a single
are associated with cognitive improvement induced by acute bout of high-intensity exercise affects cognitive performance.
exercise (Winter et al., 2007; Lee et al., 2014; Skriver et al.,
2014; Hwang et al., 2016). However, BDNF and IGF-1 are
known to play a crucial role in angiogenesis, synaptogenesis, Conclusion
and neurogenesis following long-term exercise (Cotman and
Berchtold, 2002; Voss et al., 2011; Nieto-Estevez et al., 2016). This narrative review summarized the literature examining
High concentrations of dopamine, noradrenaline, and BDNF the effects of acute high-intensity exercise on cognitive
are necessary for long-term potentiation, which is essential performance. We propose that the effects of high-intensity
for long-term memory (McMorris, 2021). A couple of studies exercise on cognitive performance are primarily affected by
have shown positive effects of high-intensity exercise on long- a variety of methodological, physiological, and psychological
term memory (Winter et al., 2007; Griffin et al., 2011). At factors. Specifically, these include the timing of cognitive task
present, it is premature to conclude that changes in BDNF (during vs. after exercise, and the time delay after exercise),

Frontiers in Behavioral Neuroscience 11 frontiersin.org


Sudo et al. 10.3389/fnbeh.2022.957677

cognitive task(s), fitness level, exercise mode/duration, Conflict of interest


and age. It is also likely that a complex interaction
between changes in regional CBF, cerebral oxygenation, The authors declare that the research was conducted in the
cerebral metabolism, neurotransmitters/neurotrophic factors, absence of any commercial or financial relationships that could
and a variety of psychological factors contributes to the be construed as a potential conflict of interest.
heterogeneous findings reported. The review is likely to
have implications for recreational, sporting, and occupational
activities where high cognitive and physiological demands are
Publisher’s note
required simultaneously.
All claims expressed in this article are solely those of the
authors and do not necessarily represent those of their affiliated
Author contributions organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
MS, JC, TM, and SA drafted the manuscript. All authors claim that may be made by its manufacturer, is not guaranteed
approved the final version of the manuscript. or endorsed by the publisher.

References
Ando, S., Hatamoto, Y., Sudo, M., Kiyonaga, A., Tanaka, H., and Higaki, Y. Chmura, J., Nazar, K., and Kaciuba-Uscilko, H. (1994). Choice reaction time
(2013). The effects of exercise under hypoxia on cognitive function. PLoS One during graded exercise in relation to blood lactate and plasma catecholamine
8:e63630. doi: 101371/journal.pone.0063630 thresholds. Int. J. Sports Med. 15, 172–176. doi: 101055/s-2007-1021042
Ando, S., Kokubu, M., Yamada, Y., and Kimura, M. (2011). Does cerebral Christensen, L. O. D., Johannsen, P., Sinkjaer, T., Petersen, N., Pyndt, H. S., and
oxygenation affect cognitive function during exercise? Eur. J. Appl. Physiol. 111, Nielsen, J. B. (2000). Cerebral activation during bicycle movements in man. Exp.
1973–1982. Brain Res. 135, 66–72.
Ando, S., Komiyama, T., Sudo, M., Higaki, Y., Ishida, K., Costello, J. T., Ciria, L. F., Luque-Casado, A., Sanabria, D., Holgado, D., Ivanov, P. C., and
et al. (2020). The interactive effects of acute exercise and hypoxia on cognitive Perakakis, P. (2019). Oscillatory brain activity during acute exercise: Tonic and
performance: a narrative review. Scand. J. Med. Sci. Sports 30, 384–398. doi: transient neural response to an oddball task. Psychophysiology 56:e13326. doi:
101111/sms.13573 101111/psyp.13326
Ando, S., Komiyama, T., Tanoue, Y., Sudo, M., Costello, J. T., Uehara, Y., Coco, M., Buscemi, A., Guerrera, C. S., Di Corrado, D., Cavallari, P., Zappala,
et al. (2022). Cognitive improvement after aerobic and resistance exercise is not A., et al. (2020a). Effects of a bout of intense exercise on some executive functions.
associated with peripheral biomarkers. Front. Behav. Neurosci. 16:853150. doi: Int. J. Environ. Res. Public Health 17:898. doi: 103390/ijerph17030898
103389/fnbeh.2022.853150
Coco, M., Buscemi, A., Ramaci, T., Tusak, M., Corrado, D. D., Perciavalle, V.,
Arnsten, A. F. (2011). Catecholamine influences on dorsolateral prefrontal et al. (2020b). Influences of blood lactate levels on cognitive domains and physical
cortical networks. Biol. Psychiatry 69, e89–e99. health during a sports stress. Brief review. Int. J. Environ. Res. Public Health
Boushel, R., Langberg, H., Olesen, J., Gonzales-Alonzo, J., Bulow, J., and Kjaer, 17:9043. doi: 103390/ijerph17239043
M. (2001). Monitoring tissue oxygen availability with near infrared spectroscopy Coco, M., Di Corrado, D., Calogero, R. A., Perciavalle, V., Maci, T., and
(NIRS) in health and disease. Scand. J. Med. Sci. Sports 11, 213–222. Perciavalle, V. (2009). Attentional processes and blood lactate levels. Brain Res.
Braz, I. D., and Fisher, J. P. (2016). The impact of age on cerebral perfusion, 1302, 205–211.
oxygenation and metabolism during exercise in humans. J. Physiol. 594, 4471– Cools, R., and Arnsten, A. F. T. (2021). Neuromodulation of prefrontal
4483. cortex cognitive function in primates: THE powerful roles of monoamines and
Brisswalter, J., Arcelin, R., Audiffren, M., and Delignieres, D. (1997). Influence acetylcholine. Neuropsychopharmacology 47, 309–328. doi: 101038/s41386-021-
of physical exercise on simple reaction time: Effect of physical fitness. Percept Mot. 01100-8
Skills 85, 1019–1027. Cotman, C. W., and Berchtold, N. C. (2002). Exercise: a behavioral intervention
Browne, S. E., Flynn, M. J., O’neill, B. V., Howatson, G., Bell, P. G., and to enhance brain health and plasticity. Trends Neurosci. 25, 295–301. doi: 101016/
Haskell-Ramsay, C. F. (2017). Effects of acute high-intensity exercise on cognitive s0166-2236(02)02143-4
performance in trained individuals: a systematic review. Prog. Brain Res. 234, Curtelin, D., Morales-Alamo, D., Torres-Peralta, R., Rasmussen, P., Martin-
161–187. Rincon, M., Perez-Valera, M., et al. (2017). Cerebral blood flow, frontal lobe
Cantelon, J. A., and Giles, G. E. (2021). A review of cognitive changes during oxygenation and intra-arterial blood pressure during sprint exercise in normoxia
acute aerobic exercise. Front. Psychol. 12:653158. doi: 103389/fpsyg.2021.653158 and severe acute hypoxia in humans. J. Cereb. Blood Flow Metab. 38, 136–150.
doi: 101177/0271678X17691986
Chang, H., Kim, K., Jung, Y. J., and Kato, M. (2017). Effects of acute high-
intensity resistance exercise on cognitive function and oxygenation in prefrontal Davranche, K., Brisswalter, J., and Radel, R. (2015). Where are the limits of the
cortex. J. Exerc. Nutr. Biochem. 21, 1–8. doi: 1020463/jenb.2017.0012 effects of exercise intensity on cognitive control? J. Sport Health Sci. 4, 56–63.
Chang, Y. K., Labban, J. D., Gapin, J. I., and Etnier, J. L. (2012). The effects of Diamond, A. (2013). Executive functions. Annu. Rev. Psychol. 64, 135–168.
acute exercise on cognitive performance: a meta-analysis. Brain Res 1453, 87–101. Dietrich, A., and Audiffren, M. (2011). The reticular-activating hypofrontality
Chen, A. G., Zhu, L. N., Yan, J., and Yin, H. C. (2016). Neural basis of working (RAH) model of acute exercise. Neurosci. Biobehav. Rev. 35, 1305–1325. doi:
memory enhancement after acute aerobic exercise: fMRI study of preadolescent 101016/j.neubiorev.2011.02.001
children. Front. Psychol. 7:1804. doi: 101016/j.ijpsycho.2020.09.018
Du Rietz, E., Barker, A. R., Michelini, G., Rommel, A. S., Vainieri,
Chen, C., Nakagawa, S., Kitaichi, Y., An, Y., Omiya, Y., Song, N., et al. (2016). I., Asherson, P., et al. (2019). Beneficial effects of acute high-intensity
The role of medial prefrontal corticosterone and dopamine in the antidepressant- exercise on electrophysiological indices of attention processes in young
like effect of exercise. Psychoneuroendocrinology 69, 1–9. doi: 101016/j.psyneuen. adult men. Behav. Brain Res. 359, 474–484. doi: 10.1016/j.bbr.2018.11.
2016.03.008 024

Frontiers in Behavioral Neuroscience 12 frontiersin.org


Sudo et al. 10.3389/fnbeh.2022.957677

Dutke, S., Jaitner, T., Berse, T., and Barenberg, J. (2014). Acute physical Kamijo, K., Nishihira, Y., Hatta, A., Kaneda, T., Kida, T., Higashiura, T.,
exercise affected processing efficiency in an auditory attention task more than et al. (2004a). Changes in arousal level by differential exercise intensity. Clin.
processing effectiveness. J. Sport Exerc. Psychol. 36, 69–79. doi: 10.1123/jsep.2013- Neurophysiol. 115, 2693–2698.
0044
Kamijo, K., Nishihira, Y., Hatta, A., Kaneda, T., Wasaka, T., Kida, T., et al.
Etnier, J. L., Wideman, L., Labban, J. D., Piepmeier, A. T., Pendleton, D. M., (2004b). Differential influences of exercise intensity on information processing in
Dvorak, K. K., et al. (2016). The effects of acute exercise on memory and brain- the central nervous system. Eur .J. Appl. Physiol. 92, 305–311. doi: 101007/s00421-
derived neurotrophic factor (BDNF). J. Sport Exerc. Psychol. 38, 331–340. 004-1097-2
Fernandez-Rodriguez, R., Alvarez-Bueno, C., Martinez-Ortega, I. A., Martinez- Kao, S. C., Cadenas-Sanchez, C., Shigeta, T. T., Walk, A. M., Chang, Y. K.,
Vizcaino, V., Mesas, A. E., and Notario-Pacheco, B. (2021). Immediate effect of Pontifex, M. B., et al. (2020). A systematic review of physical activity and
high-intensity exercise on brain-derived neurotrophic factor in healthy young cardiorespiratory fitness on P3b. Psychophysiology 57:e13425. doi: 101111/psyp.
adults: a systematic review and meta-analysis. J. Sport Health Sci. 11, 367–375. 13425
doi: 101016/j.jshs.2021.08.004
Kao, S. C., Westfall, D. R., Soneson, J., Gurd, B., and Hillman, C. H. (2017).
Ferris, L. T., Williams, J. S., and Shen, C. L. (2007). The effect of acute exercise Comparison of the acute effects of high-intensity interval training and continuous
on serum brain-derived neurotrophic factor levels and cognitive function. Med. aerobic walking on inhibitory control. Psychophysiology 54, 1335–1345. doi:
Sci. Sports Exerc. 39, 728–734. 101111/psyp.12889
Fery, Y. A., Ferry, A., Vom Hofe, A., and Rieu, M. (1997). Effect of physical Kemppainen, J., Aalto, S., Fujimoto, T., Kalliokoski, K. K., Langsjo, J., Oikonen,
exhaustion on cognitive functioning. Percept Mot. Skills 84, 291–298. V., et al. (2005). High intensity exercise decreases global brain glucose uptake in
humans. J. Physiol. 568, 323–332. doi: 101113/jphysiol.2005.091355
Goekint, M., Bos, I., Heyman, E., Meeusen, R., Michotte, Y., and Sarre, S. (2012).
Acute running stimulates hippocampal dopaminergic neurotransmission in rats, Komiyama, T., Katayama, K., Sudo, M., Ishida, K., Higaki, Y., and Ando, S.
but has no influence on brain-derived neurotrophic factor. J. Appl. Physiol (1985) (2017). Cognitive function during exercise under severe hypoxia. Sci. Rep. 7:10000.
112, 535–541. doi: 101152/japplphysiol.00306.2011 Komiyama, T., Sudo, M., Higaki, Y., Kiyonaga, A., Tanaka, H., and Ando, S.
Gold, P. E. (1995). Role of glucose in regulating the brain and cognition. Am. J. (2015). Does moderate hypoxia alter working memory and executive function
Clin. Nutr. 61, 987S–995S. during prolonged exercise? Physiol. Behav. 139, 290–296. doi: 101016/j.physbeh.
2014.11.057
Gonzalez-Alonso, J., Dalsgaard, M. K., Osada, T., Volianitis, S., Dawson, E. A.,
Yoshiga, C. C., et al. (2004). Brain and central haemodynamics and oxygenation Komiyama, T., Sudo, M., Okuda, N., Yasuno, T., Kiyonaga, A., Tanaka, H.,
during maximal exercise in humans. J. Physiol. 557, 331–342. et al. (2016). Cognitive function at rest and during exercise following breakfast
omission. Physiol. Behav. 157, 178–184. doi: 101016/j.physbeh.2016.02.013
Gonzalez-Fernandez, F., Etnier, J. L., Zabala, M., and Sanabria, D. (2017).
Vigilance performance during acute exercise. Inter. J. Sport Psychol. 48, 435–447. Komiyama, T., Tanoue, Y., Sudo, M., Costello, J. T., Uehara, Y., Higaki, Y.,
et al. (2020). Cognitive impairment during high-intensity exercise: Influence
Griffin, E. W., Mullally, S., Foley, C., Warmington, S. A., O’mara, S. M., of cerebral blood flow. Med. Sci. Sports Exerc. 52, 561–568. doi: 101249/MSS.
and Kelly, A. M. (2011). Aerobic exercise improves hippocampal function and 0000000000002183
increases BDNF in the serum of young adult males. Physiol. Behav. 104, 934–
941. Labelle, V., Bosquet, L., Mekary, S., and Bherer, L. (2013). Decline in executive
control during acute bouts of exercise as a function of exercise intensity and fitness
Hansen, R. K., Nielsen, P. S., Schelske, M. W., Secher, N. H., and Volianitis, level. Brain Cogn. 81, 10–17. doi: 101016/j.bandc.2012.10.001
S. (2020). CO2 supplementation dissociates cerebral oxygenation and middle
cerebral artery blood velocity during maximal cycling. Scand. J. Med. Sci. Sports Lambourne, K., and Tomporowski, P. (2010). The effect of exercise-induced
30, 399–407. doi: 101111/sms.13582 arousal on cognitive task performance: a meta-regression analysis. Brain Res. 1341,
12–24. doi: 101016/j.brainres.2010.03.091
Hasegawa, H., Takatsu, S., Ishiwata, T., Tanaka, H., Sarre, S., and Meeusen,
R. (2011). Continuous monitoring of hypothalamic neurotransmitters and Lee, J. K., Koh, A. C., Koh, S. X., Liu, G. J., Nio, A. Q., and Fan, P. W.
thermoregulatory responses in exercising rats. J. Neurosci. Methods 202, 119–123. (2014). Neck cooling and cognitive performance following exercise-induced
doi: 101016/j.jneumeth.2011.05.024 hyperthermia. Eur. J. Appl. Physiol. 114, 375–384. doi: 101007/s00421-013-2774-9

Hashimoto, T., Tsukamoto, H., Takenaka, S., Olesen, N. D., Petersen, L. G., Loprinzi, P. D., Day, S., Hendry, R., Hoffman, S., Love, A., Marable, S.,
Sorensen, H., et al. (2018). Maintained exercise-enhanced brain executive function et al. (2021). The effects of acute exercise on short- and long-term memory:
related to cerebral lactate metabolism in men. FASEB J. 32, 1417–1427. doi: considerations for the timing of exercise and phases of memory. Eur. J. Psychol.
101096/fj.201700381RR 17, 85–103. doi: 105964/ejop.2955

Herold, F., Behrendt, T., Meißner, C., Müller, N., and Schega, L. (2022). Luft, C. D., Takase, E., and Darby, D. (2009). Heart rate variability and cognitive
The influence of acute sprint interval training on cognitive performance of function: effects of physical effort. Biol. Psychol. 82, 164–168.
healthy younger adults. Int. J. Environ. Res. Public Health19:613. doi: 103390/ Macintosh, B. J., Crane, D. E., Sage, M. D., Rajab, A. S., Donahue, M. J., Mcilroy,
ijerph19010613 W. E., et al. (2014). Impact of a single bout of aerobic exercise on regional brain
Hill, M., Walsh, S., Talbot, C., Price, M., and Duncan, M. (2019). Exercise perfusion and activation responses in healthy young adults. PLoS One 9:e85163.
intensity-dependent effects of arm and leg-cycling on cognitive performance. PLoS doi: 101371/journal.pone.0085163
One 14:e0224092. doi: 101371/journal.pone.0224092 Marin Bosch, B., Bringard, A., Logrieco, M. G., Lauer, E., Imobersteg, N.,
Hiura, M., Nariai, T., Ishii, K., Sakata, M., Oda, K., Toyohara, J., et al. (2014). Thomas, A., et al. (2021). A single session of moderate intensity exercise influences
Changes in cerebral blood flow during steady-state cycling exercise: a study using memory, endocannabinoids and brain derived neurotrophic factor levels in men.
oxygen-15-labeled water with PET. J. Cereb. Blood Flow Metab. 34, 389–396. Sci. Rep. 11:14371. doi: 101038/s41598-021-93813-5
doi: 101038/jcbfm.2013.220 McMorris, T. (2016b). “History of research into the acute exercise–cognition
Hsieh, S. S., Chueh, T. Y., Huang, C. J., Kao, S. C., Hillman, C. H., Chang, Y. K., interaction,” in Exercise-Cognition Interaction: Neuroscience Perspective, ed. T.
et al. (2021). Systematic review of the acute and chronic effects of high-intensity Mcmorris (Amsterdam: Elsevier).
interval training on executive function across the lifespan. J. Sports Sci. 39, 10–22. McMorris, T. (2016a). Developing the catecholamines hypothesis for the acute
doi: 101080/02640414.2020.1803630 exercise-cognition interaction in humans: Lessons from animal studies. Physiol.
Huertas, F., Zahonero, J., Sanabria, D., and Lupianez, J. (2011). Functioning of Behav. 165, 291–299. doi: 101016/j.physbeh.2016.08.011
the attentional networks at rest vs. During acute bouts of aerobic exercise. J. Sport McMorris, T. (2021). The acute exercise-cognition interaction: From the
Exerc. Psychol. 33, 649–665. doi: 101123/jsep.33.5.649 catecholamines hypothesis to an interoception model. Int. J. Psychophysiol. 170,
75–88. doi: 101016/j.ijpsycho.2021.10.005
Hwang, J., Brothers, R. M., Castelli, D. M., Glowacki, E. M., Chen, Y. T., Salinas,
M. M., et al. (2016). Acute high-intensity exercise-induced cognitive enhancement McMorris, T., and Graydon, J. (1997). The effect of exercise on cognitive
and brain-derived neurotrophic factor in young, healthy adults. Neurosci. Lett. performance in soccer-specific tests. J. Sports Sci. 15, 459–468.
630, 247–253.
McMorris, T., and Hale, B. J. (2012). Differential effects of differing
Ide, K., and Secher, N. H. (2000). Cerebral blood flow and metabolism during intensities of acute exercise on speed and accuracy of cognition: a meta-
exercise. Prog. Neurobiol. 61, 397–414. analytical investigation. Brain Cogn. 80, 338–351. doi: 101016/j.bandc.2012.09.
001
Ide, K., Schmalbruch, I. K., Quistorff, B., Horn, A., and Secher, N. H. (2000).
Lactate, glucose and O2 uptake in human brain during recovery from maximal McMorris, T., and Keen, P. (1994). Effect of exercise on simple reaction times of
exercise. J. Physiol. 522(Pt 1), 159–164. recreational athletes. Percept Mot. Skills 78, 123–130.

Frontiers in Behavioral Neuroscience 13 frontiersin.org


Sudo et al. 10.3389/fnbeh.2022.957677

McMorris, T., Davranche, K., Jones, G., Hall, B., Corbett, J., and Minter, C. Skriver, K., Roig, M., Lundbye-Jensen, J., Pingel, J., Helge, J. W., Kiens, B., et al.
(2009). Acute incremental exercise, performance of a central executive task, and (2014). Acute exercise improves motor memory: exploring potential biomarkers.
sympathoadrenal system and hypothalamic-pituitary-adrenal axis activity. Int. J. Neurobiol. Learn Mem. 116, 46–58. doi: 101016/j.nlm.2014.08.004
Psychophysiol. 73, 334–340. doi: 101016/j.ijpsycho.2009.05.004
Smith, K. J., and Ainslie, P. N. (2017). Regulation of cerebral blood flow and
McMorris, T., Delves, S., Sproule, J., Lauder, M., and Hale, B. (2005). Effect of metabolism during exercise. Exp. Physiol. 102, 1356–1371.
incremental exercise on initiation and movement times in a choice response, whole
body psychomotor task. Br. J. Sports Med. 39, 537–541. doi: 101136/bjsm.2004. Smith, M., Tallis, J., Miller, A., Clarke, N. D., Guimaraes-Ferreira, L., and
014456 Duncan, M. J. (2016). The effect of exercise intensity on cognitive performance
during short duration treadmill running. J. Hum. Kinet. 51, 27–35. doi: 101515/
Meeusen, R., Piacentini, M. F., and De Meirleir, K. (2001). Brain microdialysis hukin-2015-0167
in exercise research. Sports Med. 31, 965–983.
Stone, B. L., Beneda-Bender, M., Mccollum, D. L., Sun, J., Shelley, J. H., Ashley,
Mehren, A., Diaz Luque, C., Brandes, M., Lam, A. P., Thiel, C. M., Philipsen, A., J. D., et al. (2020). Understanding cognitive performance during exercise in reserve
et al. (2019). Intensity-dependent effects of acute exercise on executive function. officers’. training corps: Establishing the executive function-exercise intensity
Neural Plast. 2019:8608317. relationship. J. Appl. Physiol. 129, 846–854. doi: 101152/japplphysiol.00483.2020
Mekari, S., Fraser, S., Bosquet, L., Bonnery, C., Labelle, V., Pouliot, P., et al. Sudo, M., Komiyama, T., Aoyagi, R., Nagamatsu, T., Higaki, Y., and Ando, S.
(2015). The relationship between exercise intensity, cerebral oxygenation and (2017). Executive function after exhaustive exercise. Eur. J. Appl. Physiol. 117,
cognitive performance in young adults. Eur. J. Appl. Physiol. 115, 2189–2197. 2029–2038.
Miller, E. K., and Cohen, J. D. (2001). An integrative theory of prefrontal cortex Tempest, G. D., and Reiss, A. L. (2019). The utility of functional near-infrared
function. Annu. Rev. Neurosci. 24, 167–202. spectroscopy for measuring cortical activity during cycling exercise. Med. Sci.
Millet, G. P., Vleck, V. E., and Bentley, D. J. (2009). Physiological differences Sports Exerc. 51, 979–987.
between cycling and running: lessons from triathletes. Sports Med. 39, 179–206. Tempest, G. D., Davranche, K., Brisswalter, J., Perrey, S., and Radel, R. (2017).
doi: 102165/00007256-200939030-00002 The differential effects of prolonged exercise upon executive function and cerebral
Moreau, D., and Chou, E. (2019). The acute effect of high-intensity exercise on oxygenation. Brain Cogn. 113, 133–141. doi: 101016/j.bandc.2017.02.001
executive function: a meta-analysis. Perspect Psychol. Sci. 14, 734–764. Thomson, K., Watt, A. P., and Liukkonen, J. (2009). Differences in ball sports
Nieto-Estevez, V., Defterali, C., and Vicario-Abejon, C. (2016). IGF-I: A key athletes speed discrimination skills before and after exercise induced fatigue.
growth factor that regulates neurogenesis and synaptogenesis from embryonic to J. Sports Sci. Med. 8, 259–264.
adult stages of the brain. Front. Neurosci. 10:52. doi: 103389/fnins.2016.00052 Travlos, A. K., and Marisi, D. Q. (1995). Information processing and
Nybo, L., and Secher, N. H. (2004). Cerebral perturbations provoked by concentration as a function of fitness level and exercise-induced activation to
prolonged exercise. Prog. Neurobiol. 72, 223–261. exhaustion. Percept Mot. Skills 80, 15–26. doi: 102466/pms.1995.80.1.15

Ogoh, S., and Ainslie, P. N. (2009). Cerebral blood flow during exercise: Tsukamoto, H., Suga, T., Takenaka, S., Tanaka, D., Takeuchi, T., Hamaoka,
Mechanisms of regulation. J. Appl. Physiol. 107, 1370–1380. T., et al. (2016). Repeated high-intensity interval exercise shortens the positive
effect on executive function during post-exercise recovery in healthy young males.
Ogoh, S., Tsukamoto, H., Hirasawa, A., Hasegawa, H., Hirose, N., and Physiol. Behav. 160, 26–34. doi: 101016/j.physbeh.2016.03.029
Hashimoto, T. (2014). The effect of changes in cerebral blood flow on cognitive
function during exercise. Physiol. Rep. 2:e12163. Voss, M. W., Nagamatsu, L. S., Liu-Ambrose, T., and Kramer, A. F. (2011).
Exercise, brain, and cognition across the life span. J. Appl. Physiol. 111, 1505–1513.
Quistorff, B., Secher, N. H., and Van Lieshout, J. J. (2008). Lactate fuels the
human brain during exercise. FASEB J. 22, 3443–3449. Wang, C. C., Chu, C. H., Chu, I. H., Chan, K. H., and Chang, Y. K. (2013).
Executive function during acute exercise: the role of exercise intensity. J. Sport
Rooks, C. R., Thom, N. J., Mccully, K. K., and Dishman, R. K. (2010). Exerc. Psychol. 35, 358–367.
Effects of incremental exercise on cerebral oxygenation measured by near-infrared
spectroscopy: a systematic review. Prog. Neurobiol. 92, 134–150. doi: 101016/j. Williamson, J. W., Nobrega, A. C., Mccoll, R., Mathews, D., Winchester, P.,
pneurobio.2010.06.002 Friberg, L., et al. (1997). Activation of the insular cortex during dynamic exercise
in humans. J. Physiol. 503(Pt 2), 277–283. doi: 10.1111/j.1469-7793.1997.277bh.x
Schmit, C., Davranche, K., Easthope, C. S., Colson, S. S., Brisswalter, J., and
Radel, R. (2015). Pushing to the limits: The dynamics of cognitive control during Winter, B., Breitenstein, C., Mooren, F. C., Voelker, K., Fobker, M.,
exhausting exercise. Neuropsychologia 68, 71–81. doi: 101016/j.neuropsychologia. Lechtermann, A., et al. (2007). High impact running improves learning. Neurobiol.
2015.01.006 Learn Mem. 87, 597–609. doi: 10.1016/j.nlm.2006.11.003
Seifert, T., and Secher, N. H. (2011). Sympathetic influence on cerebral blood Won, J., Alfini, A. J., Weiss, L. R., Callow, D. D., and Smith, J. C. (2019).
flow and metabolism during exercise in humans. Prog. Neurobiol. 95, 406–426. Brain activation during executive control after acute exercise in older adults. Int. J.
Psychophysiol. 146, 240–248. doi: 10.1016/j.ijpsycho.2019.10.002
Shields, M. R., Larson, C. L., Swartz, A. M., and Smith, J. C. (2011). Visual threat
detection during moderate- and high-intensity exercise. Emotion 11, 572–581. Zheng, K., Zou, L., Wei, G., and Huang, T. (2021). Concurrent performance of
doi: 101037/a0021251 executive function during acute bouts of exercise in adults: a systematic review.
Brain Sci. 11:1364. doi: 103390/brainsci11101364
Siebenmann, C., Sorensen, H., Bonne, T. C., Zaar, M., Aachmann-Andersen,
N. J., Nordsborg, N. B., et al. (2021). Cerebral lactate uptake during exercise Zimmer, P., Binnebossel, S., Bloch, W., Hubner, S. T., Schenk, A., Predel, H. G.,
is driven by the increased arterial lactate concentration. J. Appl. Physiol. 131, et al. (2017). Exhaustive exercise alters thinking times in a tower of London task in
1824–1830. doi: 101152/japplphysiol.00505.2021 a time-dependent manner. Front. Physiol. 7:694. doi: 103389/fphys.2016.00694

Frontiers in Behavioral Neuroscience 14 frontiersin.org

You might also like