Edited by: Lars Nyberg, Umeå University, Sweden
Reviewed by: Kirk I. Erickson, University of Illinois at Urbana-Champaign, USA; Anna Sundström, Umeå University, Sweden
*Correspondence: Louis Bherer, Département de psychologie, Université du Québec à Montréal, C.P. 8888 Succursale Centre-ville, Montréal, QC, Canada H3C 3P8.e-mail:
This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.
This study assessed the effects of an aerobic training program on reaction time tasks that manipulated preparatory intervals (PI) to produce temporal preparation effects using short (1, 3, 5 s) and long (5, 7, 9 s) PI. Older adults were assigned to either a 3-month aerobic training group or to a control group. Individuals in the training group participated in an aerobic training program of three 60-min sessions per week. The control group did not receive any training. Results indicated that 12 weeks of aerobic training induced a significant improvement in cardiorespiratory capacity (VO2max estimate). All participants who completed the aerobic program showed improvement after training in the choice RT task, along with enhanced preparation, such that they maintained preparation over time more efficiently after the training program. Moreover, enhanced ability to use the short PI was observed but only in lower fit individuals. Results of the present study suggest that improving aerobic fitness may enhance attentional control mechanisms in older adults.
Aging is accompanied by important changes in the central nervous system, which can lead to cognitive declines. In fact, substantial anatomical and physiological modifications have been observed in the frontal areas of the cerebral cortex in the aging brain (West,
Cross-sectional studies have suggested that physical activity can be an important moderator of age-related cognitive decline. For instance, Spirduso (
Further evidence for the moderating effect of physical activity on age-related cognitive declines stems from intervention studies. Dustman et al. (
Most of the studies reported previously suggest that in older adults, enhancing aerobic fitness leads to significant improvement in attentional control functions. However, some of them that used RT paradigms, reported equivalent improvement after training, in both simple and choice RT tasks. This observation is at odds with the assumption that fitness training has a larger impact on the controlled aspect of cognition, which should lead to larger training effects on choice compared to simple RT tasks (Hall et al.,
Preparatory processes are a voluntary or attention-demanding set of strategic behaviors that support an optimal processing state prior to the execution of movement (Stuss et al.,
The aim of the present study was to investigate whether sedentary older adults who participate in an aerobic fitness training program would demonstrate enhanced performances in a simple and a choice RT task. The temporal parameters of the RT tasks were varied to generate specific preparatory effects that have been shown to be affected in normal aging (Salthouse,
Prior to acceptance in the study, all the participants completed a telephone interview evaluating their physical health. Participants also completed the modified Questionnaire of aptitude to physical activity (QAA-P), a screening instrument used to detect individuals who may be at risk if they engage in intense physical activity, and the Modifiable Activity Questionnaire (MAQ; Vuillemin et al.,
Participants were excluded if they reported: a history of neurological disease or major surgery in the year preceding the study; auditory or visual impairments that have not been corrected; cardiovascular disease or vascular peripheral attacks, and/or moderate to severe hypertension. To exclude individuals with dementia or depression, participants completed the Mini-Mental State Examination (MMSE, Folstein et al.,
Seventy-seven older adults were recruited through advertizing announcements and posters in community centers in the Montreal area. Ten participants did not meet the inclusion criteria. Of the remaining 67, 32 participants were assigned to the experimental group and 35 were assigned to the control group that did not receive any intervention. Assignment was based on the order of recruitment in the study and on participants’ willingness to engage in a 3-month fitness training program. Seventeen individuals (7 assigned to the training group and 10 to the control) decided not to engage in the study for personal reasons after completing the pre-test session. In the training group, there was no difference in baseline characteristics between the seven individuals who discontinued and those who remained in the study (see Table
Control group | Training group | ||||
---|---|---|---|---|---|
Lower fit | Higher fit | Lower fit | Higher fit | ||
Age | 70.00 (6.09) | 64.82 (4.69) | 72.82 (5.56) | 63.86 (4.31) |
|
Education | 12.36 (2.31) | 13.64 (2.91) | 14.09 (5.28) | 14.57 (3.25) | |
MMSE | 29.43 (1.02) | 28.82 (1.25) | 28.64 (1.12) | 28.64 (1.08) | |
Similarities | 23.50 (3.98) | 22.45 (5.03) | 22.36 (5.99) | 23.21 (4.17) | |
GDS | 5.29 (3.41) | 5.55 (5.36) | 3.64 (1.43) | 5.33 (3.41) | |
MAQ | 3.04 (1.97) | 3.72 (3.34) | 5.57 (5.68) | 3.46 (2.96) |
*
In a first testing session, participants signed a consent form and completed all screening tests and questionnaires. In a second session all participants completed the simple and the choice RT tasks, followed by a test of cardiorespiratory fitness (Rockport one-mile test; Kline et al.,
Training group participants engaged in a 3-month physical exercise program with three, 1 h training sessions per week. During each training session, participants performed different physical activity routines that involved stretching and cardiorespiratory exercises (fast walking and aerobic dancing). Participants did not have a choice in the activities they were enroled in. Basic principles and guidelines for exercise programming (Nelson et al.,
The Rockport one-mile test (Kline et al.,
Response preparation was assessed with a RT paradigm that has shown age-related differences in response preparation (Bherer and Belleville,
The presentation order of the long and short duration conditions was counterbalanced across participants. Participants were asked to respond as quickly and accurately as possible to each trial. Dependent variables were initiation time (IT), which corresponds to the latency elapsed between the response signal and the release of the home key, and execution time (ET), measured by the time to move from the home key to the response key. Error rates were also recorded.
To assess the effect of baseline fitness level on training outcomes, all participants were categorized as higher or lower fit individuals based on a median split using the estimated VO2max score at baseline. The overall group median at baseline (18.95 ml kg−1 min−1) was used to ensure that the median was not affected by the assignment procedure. Twenty-five participants were part of the lower fit group with a mean VO2max estimate of 12.94 ml kg−1 min−1 (SD = 6.18). The higher fit group was also composed of 25 participants with a mean VO2max estimate of 25.67 ml kg−1 min−1 (SD = 6.54). In the training group 11 participants were qualified as lower fit, with a mean VO2max estimate of 10.20 ml kg−1 min−1 (SD = 7.82) and 14 participants as higher fit, with a mean VO2max estimate of 25.23 ml kg−1 min−1 (SD = 7.72). In the control group, 14 participants were qualified as lower fit with a mean VO2max estimate of 15.10 ml kg−1 min−1 (SD = 3.48), and 11 participants as higher fit, with a mean VO2max estimate of 26.23 ml kg−1 min−1 (SD = 4.94).
Participant's baseline characteristics as a function of baseline fitness level are presented in Table
Analyses performed on the VO2max estimate showed a main effect of baseline fitness level,
The two variables of interest in the RT tasks were IT and ET. IT corresponds to the latency elapsed between the moment where the response signal (the black circle) appears on the screen and the moment at which the participant releases the home key. ET was measured from the moment the participant raises the index from the home key and presses the response key. Only RTs for correct responses were included in the analyses and trials were excluded from the analyses if IT was shorter than 100 ms or global RT was longer than 3000 ms. Two types of errors can be produced in the RT tasks. Incorrect responses occur in the choice RT task and anticipation errors occur in both simple and choice RT tasks. In the choice RT task, participants produced virtually no incorrect responses. In fact, only two participants in the control group made one error at post-test. In general, participants made very few anticipation errors (leaving the home key before the response stimulus actually occurred). In the simple RT task, the mean number of anticipation errors at pre-test was 0.05 for the training group (lower fit: 0.06; higher fit: 0.04) and 0.04 for the control group (lower fit: 0.05; higher fit: 0.02). At post-test, the mean number of anticipation errors was 0.04 for the training group (lower fit: 0.06; higher fit: 0.02) and 0.09 for the control group (lower fit: 0.03; higher fit: 0.17). The mean number of anticipation errors in the choice RT task was 0.03 for the training group (lower fit: 0.04; higher fit: 0.05) and 0.03 for the control group (lower fit: 0.04; higher fit: 0.02) at pre-test, and at post-test, 0.02 for the training group (lower fit: 0.02; higher fit: 0.02) and 0.07 for the control group (lower fit: 0.03; higher fit: 0.11). Anticipation errors were submitted to non-parametric tests (Kruskal–Wallis), which revealed that experimental groups produced a comparable number of anticipation errors and obtained similar anticipation scores in the simple RT task at pre-test, χ2 (3,
Data were analyzed using an ANOVA with group (training and control) and baseline fitness level (lower fit and higher fit) as between-subjects factors, and time (pre- and post-test) and task (simple and choice) as within-subjects factors.
The IT analysis revealed main effects of baseline fitness level,
The ET analysis revealed no effect of time or interaction involving this factor. A significant main effect of task was observed,
Mean IT and standard deviation are presented in Table
Short duration window | Long duration window | |||||||
---|---|---|---|---|---|---|---|---|
Groups | 1st PI | 2nd PI | 3rd PI | 1st PI | 2nd PI | 3rd PI | ||
Lower fit | ||||||||
Pre-test | 529.97 (112.11) | 310.92 (55.24) | 300.23 (49.86) | 361.71 (68.25) | 330.59 (64.38) | 322.39 (60.50) | ||
Post-test | 452.87 (161.17) | 281.34 (37.82) | 287.28 (43.24) | 353.48 (87.88) | 302.78 (53.17) | 293.30 (47.01) | ||
Higher fit | ||||||||
Pre-test | 411.82 (91.71) | 293.57 (39.05) | 283.97 (33.82) | 340.18 (62.53) | 323.20 (62.12) | 317.31 (70.69) | ||
Post-test | 393.43 (58.96) | 275.50 (35.92) | 271.42 (29.55) | 349.12 (59.26) | 323.98 (80.24) | 304.55 (54.12) | ||
Lower fit | ||||||||
Pre-test | 460.92 (119.66) | 311.13 (60.37) | 301.61 (48.17) | 385.10 (51.98) | 348.62 (64.81) | 340.27 (48 83) | ||
Post-test | 417.10 (98.04) | 291.63 (47.59) | 298.79 (59.69) | 376.34 (61.36) | 335.18 (48.65) | 351.33 (57.90) | ||
Higher fit | ||||||||
Pre-test | 439.82 (75.63) | 282.23 (40.82) | 263.13 (31.68) | 360.31 (65.57) | 292.18 (47.63) | 298.13 (31.36) | ||
Post-test | 409.37 (80.92) | 288.67 (42.67) | 279.41 (38.01) | 374.04 (72.29) | 320.74 (41.60) | 317.56 (50.26) |
Short duration window | Long duration window | |||||||
---|---|---|---|---|---|---|---|---|
Groups | 1st PI | 2nd PI | 3rd PI | 1st PI | 2nd PI | 3rd PI | ||
Lower fit | ||||||||
Pre-test | 473.01 (86.66) | 390.23 (87.87) | 393.11 (93.01) | 463.84 (74.72) | 422.40 (73.44) | 418.55 (68 62) | ||
Post-test | 426.82 (63 14) | 334.65 (56.86) | 334.55 (67.31) | 405.51 (106.17) | 365.80 (72.00) | 366.29 (62.67) | ||
Higher fit | ||||||||
Pre-test | 403.76 (72.72) | 337.13 (49.15) | 333.01 (54.32) | 389.14 (48.48) | 364.86 (51.30) | 354.68 (48.30) | ||
Post-test | 384.06 (56.45) | 329.00 (40.53) | 318.64 (44.27) | 371.24 (64.66) | 354.28 (56.40) | 340.93 (52.41) | ||
Lower fit | ||||||||
Pre-test | 468.47 (76.89) | 381.48 (57.59) | 375.05 (59.72) | 440.88 (54.87) | 431.57 (52.30) | 404.74 (56.77) | ||
Post-test | 443.59 (55.75) | 384.71 (42.76) | 375.44 (47 050 | 436.82 (48 09) | 407.09 (45.10) | 425.36 (74.13) | ||
Higher fit | ||||||||
Pre-test | 399.69 (41.53) | 326.85 (51.21) | 322.88 (49.00) | 416.28 (90.71) | 384.71 (84.86) | 379.30 (80.85) | ||
Post-test | 448.28 (55 67) | 357.29 (54.69) | 348.98 (51.59) | 433.81 (52.07) | 402.17 (57.17) | 395.17 (51.90) |
In the short duration condition of the choice RT task, the IT analysis indicated a significant main effect of PI,
Positive effects of training were observed in the lower fit group only, which showed a group × time interaction at the 2nd PI,
In the long duration condition, the IT analysis revealed a main effect of PI,
The present study assessed the effect of a 3-month aerobic fitness training program on task complexity and response preparation in older adults, as a function of baseline fitness level, using simple and choice RT tasks designed to generate response preparation effects that have been associated to the integrity of the prefrontal cortex (see Vallesi et al.,
Our results support the notion that sedentary elderly persons can benefit from a structured aerobic exercise program after only 3 months. The cardiorespiratory fitness level assessed with the Rockport one-mile test (Kline et al.,
One goal of the present study was to assess the effect of aerobic fitness training in RT tasks while taking into account task complexity (simple vs. choice RT tasks). Past studies suggested that physical fitness should be associated to better performances in more complex tasks, because those tasks require controlled and effortful cognitive processing (Hall et al.,
Another important question addressed in the present study was the effect of an aerobic training program on response preparation processes. Salthouse (
The results observed in the present study suggest that an aerobic training intervention can lead to significant improvement in response preparation deficits in many ways, and that in some conditions, the improvement depends on the baseline fitness level of the participants. After controlling for age difference among higher and lower fit individuals, lower fit individuals that completed the aerobic training program showed better response preparation at the 2nd and the 3rd PI of the short temporal window of the choice RT task, suggesting enhanced ability to use stimulus probability. Moreover, all participants that completed the training program showed better performance in the long temporal window of the choice RT task, suggesting that they were better at maintaining a high level of preparation over time after the training program. The enhanced ability to maintain preparation over time was independent of the baseline fitness level.
These results bring further support to Hillman et al. (
One limitation of the present study is that the control group did not receive any form of intervention. One may argue that the effects of the intervention could be attributed to other factors than the aerobic intervention. For example, the training group was getting significantly more social interaction and this interaction could have contributed to improve cognition. However, other studies have controlled for this aspect and still found significant training effects. For instance, Kramer et al. (
This study provides further support to the notion that cardiorespiratory fitness may offer a protective buffer against age-related cognitive decline. Evidence from neuroimaging studies could help to explain why executive control functions tend to benefit more readily from fitness training. It has been shown that enhanced cardiovascular functions after aerobic training are associated with greater task-relevant activity in brain areas recruited in an attentional control task (Colcombe et al.,
Executive control functions are vital to the human autonomy, and although there is evidence for decline in these functions with advancing age, the results of the present study suggest that physical activity could be used as an intervention tool to attenuate this decline. The advantage of physical activity programs is that they can be relatively inexpensive, are accessible, and easy to begin at any age. Many everyday activities, such as driving, entail substantial executive controls demands. Indeed, the response preparation task using variable PIs design appears to reflect real-life demands as we often have to anticipate and prepare fast and accurate responses (e.g., at an intersection the yellow light warns the driver that a stop will soon be required). An important question for future research would be to see if the training benefits observed in experimental tasks as used in the present study transfer to everyday situations.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
This research was supported by a grant from the Institut universitaire de gériatrie de Montréal (CAREC program) and a scientist fellowship from the Fonds de Recherche en Santé du Québec to Louis Bherer. The authors wish to thank Guillaume Boussardon, Thierno Diallo, Laëtitia Haller, Delphine Middermacht, Martine Vézina, and Julie Brunet for their collaboration in the study as well as Charles H. Hillman for helpful comments on a previous version of this manuscript.
1Kline et al. (