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Asian Journal of Psychiatry 51 (2020) 102046

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Asian Journal of Psychiatry


journal homepage: www.elsevier.com/locate/ajp

Baduanjin mind-body exercise improves logical memory in long-term T


hospitalized patients with schizophrenia: A randomized controlled trial
Mingli Lia,b,*, Jing Fangb, Yang Gaob, Yali Wub, Lili Shenb, Yiming Yusubujiangb, Jin Luob,**
a
Mental Health Center and Psychiatric Laboratory, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, China
b
The Mental Rehabilitation Centers, Karamay Municipal People’s Hospital, Karamay, Xinjiang 830054, China

A R T I C LE I N FO A B S T R A C T

Keywords: Neurocognitive impairment is one of the core symptoms in schizophrenia and poses a great challenge to effective
Baduanjin exercise treatment. Sixty-one long-term hospitalized patients with schizophrenia were recruited and randomly assigned
Mind-body intervention to two groups: Baduanjin exercise and brisk walking. Patients in the Baduanjin group received 24 weeks of
Neurocognitive function Baduanjin training (5 days/week, 40 min/day), while patients in the brisk walking group received 24 weeks of
Schizophrenia
brisk walking (5 days/week, 40 min/day). Scores on the Wechsler Memory Scale, Digit Symbol Substitution Test
Memory
(DSST), and the positive and negative syndrome scale were used to evaluate the logical memory (LM), processing
speed, and clinical symptoms of all participants, while the score of Trail Making Test-A (TMT-A) was applied to
assess the visual attention and graphomotor speed, at baseline and the 16th week and 24th week of intervention.
The one-way repeated measures analysis of variance (ANOVA) was used to test the differences in neurocognitive
changes between the two groups. Repeated measures ANOVA showed significant differences between the two
groups in the LM immediate (F = 6.21, p = 0.003) and LM delayed (F=5.60, p = 0.005) scores, but not in the
completion times of TMT-A (F=.22, p = 0.806) or DSST scores (F=0.97, p = 0.328). A significant effect of time
was also detected in the LM immediate (F=10.24, p = 0.000) and LM delayed (F=4.93, p = 0.009) scores and
in the completion time of the TMT-A (F=33.10, p = 0.000), but not in the DSST scores (F=2.12, p = 0.122).
Baduanjin exercise could improve logical memory in the long-term hospitalized patients with schizophrenia.

1. Introduction Rass et al., 2012; Sartory et al., 2005; Wang et al., 2019). However,
besides the inconsistent results and the small effect sizes of these stu-
Neurocognitive impairment is one of the core symptoms in schizo- dies, these therapeutic methods would impose additional financial
phrenia. Almost all the domains of neurocognitive function, such as burdens on patients with schizophrenia, and are unavailable in poor
memory, attention, processing speed, verbal learning, reasoning and rural areas and primary hospitals. Therefore, there is a need to develop
executive functions, are affected by the disease (Ma et al., 2007; Melle, an efficient and cost-effective therapeutic method for cognitive deficits
2019). Neurocognitive impairment usually appears at the onset of in schizophrenia.
schizophrenia, but may appear even prior to the onset, and persists Some empirical data suggest that physical activities and mental
throughout the course of the disease (Mollon and Reichenberg, 2018; training practices have positive impacts on cognitive function in pa-
Shmukler et al., 2015). It is also highly related to the disability and tients with mild cognitive impairment (MCI) or age-related cognitive
social function outcomes of patients with schizophrenia (Addington and impairment (Vakhrusheva et al., 2016). In particular, traditional Chi-
Addington, 2000; Sheffield et al., 2018). Unlike positive symptoms that nese mind-body exercises such as Tai Chi and Baduanjin exercise–which
could be significantly improved by treatment with antipsychotics, the combine physical exercise postures with breathing and deep relaxation
treatment of cognitive deficits still poses significant challenges. techniques–could enhance neurocognition in patients with MCI
Pharmacology, cognitive remediation, and repetitive transcranial (Sungkarat et al., 2017, 2018; Tao et al., 2019). For example, Baduanjin
magnetic stimulation are currently the three main trial therapies for exercise could improve executive functions of the young and healthy
cognitive deficits in schizophrenia(Choi et al., 2017; Jiang et al., 2019; people after 8-week exercise (90 min/day, 5 days/week) (Chen et al.,


Corresponding author at: The Mental Health Center and psychiatric Laboratory, West China Hospital, Sichuan University, No 28 Dian Xin Nan Road, Chengdu,
Sichuan 610041, China.
⁎⁎
Corresponding author at: The Mental Rehabilitation Centers, Karamay Municipal People’s Hospital, No 5 Fenghua Road, Karamay, Xinjiang 830054, China.
E-mail addresses: limingli0517@qq.com (M. Li), 577827619@qq.com (J. Luo).

https://doi.org/10.1016/j.ajp.2020.102046
Received 7 September 2019; Received in revised form 20 March 2020; Accepted 25 March 2020
1876-2018/ © 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/BY-NC-ND/4.0/).
M. Li, et al. Asian Journal of Psychiatry 51 (2020) 102046

2016), and attention ability (Schulte Grid test) of college students after 2.2. Design
12-week exercise (Li et al., 2015). These findings endorse the potential
ability of Baduanjin exercise in improving neurocognition and well- The sample size for the study was calculated by the G*Power soft-
being. ware (Faul et al., 2007). With 95 % power (β = 0.050), a type I error
To date, no randomized controlled clinical study has been con- rate of 5 % (α = 0.05), and effect size of 20 %, the estimated total
ducted to test if Baduanjin exercise can improve cognitive deficits in sample size was 56 participants. With an estimated dropout rate of 10
schizophrenia. In the present study, comparing with the effects of brisk %, a final sample size of 61 was required. Patients were randomly as-
walking, we explored the intervention effects of 24 weeks of Baduanjin signed to the Baduanjin exercise (treatment) or the brisk walking
exercise on memory, visual attention, graphomotor speed, and proces- (control) groups using a random permuted block design. The types of
sing speed in patients with long-term hospitalized schizophrenia. intervention were written on a piece of paper and put in a sealed black
box, and we picked one for each patient who agreed to be in the study.
30 patients were randomly allocated to the Baduanjin group, and the
2. Methods other 31 patients were assigned to the brisk walking control group.

2.1. Participants 2.3. Intervention

A longitudinal randomized controlled trial design was employed. 2.3.1. The Baduanjin exercise group
Participants were recruited from the mental rehabilitation center in Patients in the Baduanjin group received 24 weeks of Baduanjin
Karamay Municipal People’s Hospital. All the patients were diagnosed training (based on the Health Qigong Baduanjin Standard published by
with schizophrenia based on the structured clinical interview for DSM- the General Administration of Sport of China, 2003) with a frequency of
IV (First et al., 1997). All the patients had been inpatient for at least 1 2 Baduanjin sessions 5 days/week, totally 40 min/day. The sessions
year, and had been on a stable dose for at least 3 months. The patients included a 5 min warm up, 30 min of Baduanjin training, and a 5 min
received antipsychotic medications, mood stabilizers, and anti- cool down. During the warm-up stage, the participants relieved their
depressants according to the preferences of the treating clinician and tension and warmed up their joints, while during the cool-down stage,
the patient. The dosage of antipsychotic medication taken by each pa- they regulated their breathing patterns. Nurse Fang and Nurse Wu
tient was recorded and converted to equivalent dosages of chlorpro- guided the patients to conscientiously take part in the Baduanjin ex-
mazine using the conversion tables provided by Atkins (Maria Atkins, ercise.
1997) and Woods (Woods, 2003) (Table 1). The exclusion criteria were
as follows: (1) having serious physical diseases, such as severe cardio- 2.3.2. Brisk walking group
vascular, pulmonary and musculoskeletal system diseases; (2) having Patients in the brisk walking group received 24 weeks of brisk
uncorrected vision and/or hearing problems and inability to complete walking (5 days/week, 40 min/day). Nurse Shen guided the patients to
the neurocognitive test; (3) having acute or chronic conditions that complete the walking sessions.
would preclude exercise; (4) exercising regularly within 6 months of the
study (or > 6 months with a frequency of 3–4 times per week and at 2.4. Clinical and neurocognitive assessment
least 30 min per session).
All participants were give a complete description of the study before The memory, visual attention, graphomotor speed, and processing
they provided written informed consent. The trial was approved by the speed were assessed for all participants at 3 time points: before the
Ethics Committee of Karamay Municipal People’s Hospital. intervention, at the 16th week of intervention, and at the 24th week of
intervention.
The positive and negative syndrome scale (PANSS) was used to
evaluate the clinical symptoms of the patients; Dr. Yusubujiang con-
Table 1 ducted these assessments.
Demographics and clinical symptom scales characteristics of participants. Memory was assessed by Logical Memory (LM) subtest in the
Wechsler Memory Scale. Participants were instructed to listen to, and
group Baduanjin Walking group T/χ2 df P value
remember, the contents of a short story that was verbally presented to
group (n = 30) (n = 31)
them, then repeated it immediately. After a delay of 30 min, they were
Age (year) 51.00(6.86) 50.97(8.54) 0.016 59 0.987 asked to repeat each story as accurately as possible again. Three dif-
Education (year) 10.77(2.61) 10.77(3.31) −0.010 59 0.992 ferent stories were presented at the 3 time points, so as to avoid
Duration of illness 21.63(10.13) 19.84(10.47) 0.680 59 0.499
learning effects. visual attention and graphomotor speed were assessed
(year)
Gender(male/ 24/6 23/8 0.055 1 0.814 using the Trail Making Test (TMT)-A, in which patients were instructed
female) to draw a line and connect consecutive numbers in numerical order as
Ethnicity (Han/ 26/4 23/8 0.815 1 0.367 quickly and correctly as possible (Kortte et al., 2002). Processing speed
other) was evaluated by the Digit Symbol Substitution Test (DSST). The coding
Medication
AP typical /atypical 0/30 1/30
task involved translating 9 different symbols into the digits 1–9 ac-
Mood stabilizer 5 7 cording to a key of digital-symbol pairs, which was presented on top of
Antidepressants 4 1 the task sheet. The participants were asked to decode the list of symbols
Total CPZ (5 rows, each with 25 symbols) one by one as fast as possible, within a
equivalent
preset limit of 90 min (Cornelis et al., 2014).
dosages (g)
16weeks 40.41(22.81) 36.97(15.79) 0.687 59 0.495 The neurocognitive tests of all patients were administered by Dr.
24weeks 61.74(34.42) 55.40(23.90) 0.838 59 0.405 Luo, who was blinded to the participants’ group assignment. All pa-
The score of PANSS tients were inpatients, and completed all assessments during the trial.
Baseline 61.67(11.38) 62.58(14.42) −0.274 59 0.785
16weeks 60.47(12.55) 61.77(14.14) −0.381 59 0.704
24weeks 59.47(13.84) 59.16(16.87) 0.304 59 0.939
2.5. Statistical analysis

Note: CPZ, chlorpromazine; AP, Antipsychotic; PANSS, Positive and Negative All statistical analyses were performed using SPSS software (IBM
Syndrome Scale. Corp. Released 2012. IBM SPSS Statistics for Windows, Version 21.0.

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M. Li, et al. Asian Journal of Psychiatry 51 (2020) 102046

Armonk, NY: IBM Corp). hospitalized patients with schizophrenia.


Demographic variables were analyzed using independent Student’s Contrary to our expectations, we found that only Baduanjin exercise
t-tests (for continuous variables) and χ2 tests (for nominal variables). caused significant improvements in the memory function of patients
The one-way repeated measures analysis of variance (ANOVA) was with schizophrenia. A moderate effect size (partial eta squared = 0.09)
applied to test the differences in neurocognitive changes between the 2 was observed for this intervention (Cohen, 2013). Possible explanations
groups. The within-subject factor between time points was denoted by for this might include the following factors: firstly, although a number
“Time”, and the between-subject factor, i.e. Baduanjin exercise vs. brisk of studies have found that exercise has some effect on memory (Loprinzi
walking was denoted by “Group”. A significant “Time × Group inter- et al., 2018), most of the results are from treatments with acute exercise
action” thus indicated a difference in response between the two inter- (Roig et al., 2013; Yanes and Loprinzi, 2018), and secondly, the ex-
vention groups. Partial Eta Squared (ɳ2) was used to assess effect size in ercise-memory interaction is intensity- and time-dependent (Loprinzi,
ANOVA model. The significance level was set at p < 0.05 (2-sided). 2018; Loprinzi et al., 2019). Only acute exercise with moderate-to-
vigorous intensity (Erickson et al., 2019; Loprinzi et al., 2019), and
3. Result acute exercise prior to memory encoding, is reported to be optimal in
enhancing memory function (Haynes Iv et al., 2019; Loprinzi, 2018;
3.1. Clinical and demographic characteristics Loprinzi et al., 2019). In our study, patients in the brisk walking group
only received mild-to-moderate intensity exercise, and no acute ex-
The flow chart of patient participation is shown in Supplementary ercise overall. Moreover, Baduanjin exercise involves not only physical
Fig. No patients dropped out during this study. exercise, but also mindfulness training. Previous studies have shown
There were no significant differences between the participants in that meditation can improve memory of adults with subjective cogni-
the Baduanjin exercise and brisk walking groups at baseline in terms of tive decline (Farhang et al., 2019; Innes et al., 2017; Wong et al., 2017),
demographic characteristics such as age (51.00 ± 6.86 and and that mind-body interventions such as Yoga, Tai Chi, and Qigong
50.97 ± 8.54 years, respectively), gender (male/female: 24/6 and 23/ could also improve memory of older adults with MCI (Brenes et al.,
8, respectively), years of education (10.77 ± 2.61 and 10.77 ± 3.31 2019; Farhang et al., 2019).
years, respectively), ethnicity (Han/others: 24/6 and 23/8, respec- Several studies have suggested that both the hippocampus and the
tively), and duration of illness (21.63 ± 10.13 and 19.84 ± 10.47 prefrontal cortex play important roles in memory (Barker et al., 2017;
years, respectively), or in the type of antipsychotic medicine and the Eichenbaum, 2017; Geib et al., 2017), and neuroimaging studies have
equivalent dosages of chlorpromazine. We also found no significant found that memory deficits in patients with schizophrenia might be
differences in PANSS scores between the two groups at the 3 time points related with structural impairment and dysfunction of the hippocampus
(Table 1). and prefrontal cortex (Avery et al., 2018; Hutcheson et al., 2015;
Ragland et al., 2017). Exercise may affect memory by modulating the
3.2. Neurocognitive assessment function of the hippocampus (Loprinzi et al., 2017). In alignment with
these studies, Tao et al. (2017b) reported that participants had higher
There were no significant differences in the LM immediate (t59 = volumes of gray matter in the left hippocampus, left amygdala, bilateral
0.28, p = 0.778), LM delayed (t=−0.64, p = 0.949) scores, comple- putamen, and left insula after 12 weeks of Baduanjin exercise. Fur-
tion time of TMT-A (t=0.23, p = 0.816), or DSST scores (t=0.43, p = thermore, the volumes of the left hippocampus and putamen were as-
0.672) between the 2 groups at baseline. sociated with changes in the memory quotient (Tao et al., 2017b). The
For repeated measures ANOVA, a significant effect of “Time” was Baduanjin exercise group also had a higher fractional amplitude of low-
detected in the LM immediate (F = 10.24, p < 0.001, ɳ2 = 0.148), LM frequency fluctuations (fALFF) in the medial prefrontal cortex in the
delayed (F = 4.93, p = 0.009, ɳ2 = 0.077) scores, and in the com- slow-5 and low-frequency bands, and this increase was positively as-
pletion time of the TMT-A (F = 33.10, p < 0.001, ɳ2 = 0.359), but not sociated with memory function improvement (Tao et al., 2017a). These
in the DSST (F = 2.14, p = 0.122, ɳ2 = 0.035) scores. findings might reveal the likely neurobiological mechanisms of Ba-
A significant effect of “Group” was detected in the LM scores (LM duanjin exercise in improving memory of patients.
immediate: F = 4.91, p = 0.031, ɳ2 = 0.077; LM delayed: F = 4.07, p Patients with schizophrenia show deficits in visual attention and
= 0.048, ɳ2 = 0.064), but not in the completion time of the TMT-A (F graphomotor speed even in their first-episode untreated stage, and take
= .004, p = 0.949, ɳ2 < 0.001), or the DSST (F = 0.97, p = 0.328, ɳ2 longer to complete the TMT-A (He et al., 2012; Ma et al., 2007). Con-
= 0.016) scores. sistent with previous studies, physical exercise is reported to be bene-
A significant “Time × Group interaction” effect was found in the ficial to executive functions in healthy peoples (Smith et al., 2010), as
LM immediate (F = 6.21, p = 0.003, ɳ2 = 0.095) and LM delayed (F = well as patients with schizophrenia (Firth et al., 2017). In this study, we
5.60, p = 0.005, ɳ2 = 0.087) scores, but not on the TMT-A timing (F = found that after 24 weeks of exercise, long-term hospitalized patients in
0.22, p = 0.806, ɳ2 = 0.004), or DSST (F = 2.12, p = 0.125, ɳ2 = both groups showed improved ability in completing TMT-A. Our find-
0.035) scores (Table 2, Fig. 1). ings suggest that psychiatrists should encourage their patients to ex-
ercise regularly, although the mechanism through which aerobic ex-
4. Discussion ercises could improve visual attention and graphomotor speed have not
been fully understood yet. Our previous study found that decreased
In the present study, we have 3 primary findings. Firstly, compared fALFF in the left superior gyrus was negatively correlated with the
with brisk walking, Baduanjin exercise improved the logical memory mean executive time of TMT-A (He et al., 2012), suggesting that that
functions of long-term hospitalized patients with schizophrenia. prefrontal cortex might be the neural substrate of deficits in processing
Patients experienced 48 % and 52 % improvements in immediate and speed of patients with schizophrenia.
30-min delayed logical memory, respectively. Secondly, both Baduanjin In this study, we found that the DSST score did not change sig-
exercise and brisk walking reduced the completion time of TMT-A, nificantly after 24 weeks of exercise intervention. DSST primarily re-
indicating that regular exercise could improve the visual attention and flects the processing speed of subjects. Our finding is in line with the
graphomotor speed of patients with schizophrenia. Thirdly, the scores results of a recent systematic review and meta-analysis study, which
of DSST were unchanged in both groups, indicating that the two ex- showed that processing speed does not respond to aerobic exercise in
ercises have little effect on processing speed in these patients. These patients with schizophrenia (Firth et al., 2017). While another meta-
findings suggested that Baduanjin exercise might be an effective alter- analysis including 2021 participants suggested that aerobic exercise
native method to improve logical memory of the chronic, long-term could significantly improve processing speed (Smith et al., 2010), the

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M. Li, et al. Asian Journal of Psychiatry 51 (2020) 102046

Table 2
Memory, Executive function and Processing speed outcomes after 16 weeks and 24 weeks intervention in schizophrenia.
group Baduanjin Walking Time Group Time * group
(n = 30) (n = 31) (F, p value, ɳ2)

LM immediately
Baseline 7.67 (4.19) 7.35(4.42)
16 weeks 9.93(5.23) 6.90(3.83)
24weeks 11.37(5.03) 7.97(4.22) 10.24, 0.000, 0.148 4.91, 0.031, 0.077 6.21, 0.003, 0.095
LM delayed
Baseline 6.57(4.25) 6.65(5.33)
16 weeks 8.77(5.66) 5.42(4.37)
24weeks 10.03(5.68) 6.74(4.45) 4.93, 0.009, 0.077 4.07, 0.048, 0.064 5.60, 0.005, 0.087
Time of TMT
Baseline 123.92(96.41) 118.77(74.88)
16 weeks 84.02(72.59) 86.58(43.05)
24weeks 76.11(70.82) 75.57(38.43) 33.10, 0.000, 0.359 .004, 0.949, 0.000 0.22, 0.806, 0.004
Score of DSST
Baseline 29.43(17.45) 27.61(15.97)
16 weeks 29.67(14.12) 26.81(14.29)
24weeks 33.03(12.11) 27.26(12.50) 2.14, 0.122, 0.016 0.97, 0.328, 0.016 2.12, 0.125, 0.035

Note: LM, logical memory; TMT, Trail Making Test; DSST, Digital-Symbol Substitution Test. ɳ2, Partial Eta Squared was used to assess the effect size.

participants in that study were highly heterogeneous, including elderly outpatients with schizophrenia to test if Baduanjin exercise could also
adults with MCI, healthy young adults, healthy elderly adults, seden- be effective for other types of schizophrenia. It should be noted that this
tary adults, and so on. Physical exercise might not affect the processing study employed very few neurocognitive tests, and further studies that
speed of patients with schizophrenia. In our study, the DSST score of include and assess many more neurocognitive domains need to be
patients with schizophrenia increased by 12 % after 24 weeks in the conducted. Moreover, there was no non-active comparator or placebo
Baduanjin exercise group, but not in the brisk walking group. This group in this trial. The significant effect of variable “Time” detected in
suggests that Baduanjin exercise might have a negligible effect on this study could not entirely reliably exclude confounding by learning
processing speed even after a prolonged duration of intervention. effects. Finally, this study lacked a follow-up assessment after the post-
However, physical activity as a part of healthy lifestyle behavior was assessment.
beneficial to prevent premature mortality and positive symptoms of
patients with schizophrenia (Abdul Rashid et al., 2019; Gandhi et al., 5. Conclusion
2019a, b), we still recommend patients to engaged in it.
Several limitations of this study should be noted. Since we only In summary, this study found that 24-week Baduanjin exercise could
recruited 61 patients from a single hospital, further multi-center studies improve the memory function of the long-term hospitalized patients
with larger sample sizes are needed to validate our results. The patients with schizophrenia. We recommend the application of this free, simple,
in this study were inpatients who had chronic schizophrenia, and were and safe technique to patients with schizophrenia, as an intervention to
long-term hospitalized; however, studies also need be conducted for help deal with their memory deficits.

Fig. 1. Scores of four neurocognitive test at baseline and following 16 and 24 weeks.
LM, logical memory, DSST, digital-symbol substitution test.

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M. Li, et al. Asian Journal of Psychiatry 51 (2020) 102046

Funding He, Z., Deng, W., Li, M., Chen, Z., Jiang, L., Wang, Q., Huang, C., Collier, D., Gong, Q.,
Ma, X., 2012. Aberrant intrinsic brain activity and cognitive deficit in first-episode
treatment-naive patients with schizophrenia. Psychol. Med. 1, 1–12.
Funding for this study was provided by 1.3.5 project for disciplines Hutcheson, N.L., Sreenivasan, K.R., Deshpande, G., Reid, M.A., Hadley, J., White, D.M.,
of excellence, West China Hospital, Sichuan University (Grant Nos. Ver Hoef, L., Lahti, A.C., 2015. Effective connectivity during episodic memory re-
ZY2016203 & ZY2016103). trieval in schizophrenia participants before and after antipsychotic medication. Hum.
Brain Mapp. 36, 1442–1457.
Innes, K.E., Selfe, T.K., Khalsa, D.S., Kandati, S., 2017. Meditation and music improve
Declaration of Competing Interest memory and cognitive function in adults with subjective cognitive decline: a pilot
randomized controlled trial. J. Alzheimer’s Dis. 56, 899–916.
Jiang, Y., Guo, Z., Xing, G., He, L., Peng, H., Du, F., McClure, M.A., Mu, Q., 2019. Effects
All the authors declare no conflict of interest. of high-frequency transcranial magnetic stimulation for cognitive deficit in schizo-
phrenia: a meta-analysis. Front. Psychiatry 10, 135.
Kortte, K.B., Horner, M.D., Windham, W.K., 2002. The trail making test, part B: cognitive
Acknowledgement
flexibility or ability to maintain set? Appl. Neuropsychol. 9, 106–109.
Li, M., Fang, Q., Li, J., Zheng, X., Tao, J., Yan, X., Lin, Q., Lan, X., Chen, B., Zheng, G.,
We thank all individuals who have participated in this study. Chen, L., 2015. The effect of Chinese traditional exercise-baduanjin on physical and
psychological well-being of college students: a randomized controlled trial. PLoS One
10, e0130544.
Appendix A. Supplementary data Loprinzi, P.D., 2018. Intensity-specific effects of acute exercise on human memory
function: considerations for the timing of exercise and the type of memory. Health
Supplementary data associated with this article can be found, in the Promot. Perspect. 8, 255–262.
Loprinzi, P.D., Edwards, M.K., Frith, E., 2017. Potential avenues for exercise to activate
online version, at https://doi.org/10.1016/j.ajp.2020.102046. episodic memory-related pathways: a narrative review. Eur. J. Neurosci. 46,
2067–2077.
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