Sample characteristics
The number of participants, mean age, and gender distribution for each intervention group in the 19 included studies are summarized in Table 1. Five studies had small sample sizes (N < 15) in one or more groups [83]: 2 groups, N ≤ 7 per group; [85]: 2 groups, N ≤ 13 per group; [86]: 2 groups, N ≤ 11 per group; [87]: control group, N = 13; [96]: physical-cognitive training group, N = 12). In most of the included studies sample sizes per group were larger than 15, and in three studies sample sizes per group were equal to or larger than 50 [92, 97, 99]. In all studies the number of females was larger than that of males, however information about gender distribution within each intervention group was not always available. In one study [98], all of the included participants were female. Subject ages ranged from 55 to 97 years old and mean group ages ranged from 65.5 ± 6.3 [89] to 81.9 ± 6.3 years old [97].
Interventions
Studies included in this review reported multiple outcome measures, and an extensive range and diverse types of intervention protocols. The most frequent intervention protocol (11 of the 19 included studies) was combined exercise training (e.g. aerobic training followed by resistance training) [82,83,84, 88, 90, 91, 97,98,99,100]. The second most frequent intervention protocol (9 of 19 included studies) was combined physical-cognitive training. Here physical exercise training was either conducted simultaneously with a cognitive task in a dual-task manner [84, 91, 93, 94, 96, 100], or was followed by separate cognitive interventions [83, 92, 97]. The remaining intervention protocols consisted of single-exercise training paradigms, involving aerobic training [89, 95], resistance training [85, 89], balance training [86, 89] or dance [87, 88]. Nine studies included a passive control group [85, 86, 89,90,91, 93, 94, 96, 98]. Alternatively, participants in control groups underwent health education classes [87, 92, 99] or were subjected to lesser physical (or cognitive) training, for example training of gross motor activities [82] or training of a single cognitive task [96].
Types and durations of the interventions varied considerably between studies. The durations of the intervention period varied, ranging from 6 weeks [85, 86] to 12 months [99]. In most studies the intervention lasted 8 to 12 weeks and consisted of 24 training sessions (or classes) in total. Exercise protocols also varied greatly between studies. For example, the intensity of the aerobic exercise varied from light (e.g. [94]) to moderate-high (e.g. [89]). Durations of the training sessions (for all types of interventions) were inconsistent as well, ranging from 15 to 20 min [89] for balance training to 60–70 min [87, 88] for dance. Similar to the differences in exercise intensity and duration, the type and combinations of exercises varied greatly between studies. For example, three studies that included a combined-exercise training consisted of aerobic-strength training [82, 88, 91], and three studies consisted of strength-balance training [83, 97, 100], whereas in five studies all three exercise paradigms were used in a single training session [85, 88, 90, 98, 99]. Finally, six studies that combined physical-cognitive intervention protocols consisted of physical exercise training with a dual task [84, 91, 93, 94, 96, 100], whereas the interventions in the remaining studies were made up of separate blocks of physical exercise and cognitive training [83, 97] or involved social interactions [92]. Exercises in the physical-cognitive intervention consisted of aerobic training [92,93,94, 96, 100] or combined aerobic/strength/balance training [83, 84, 91, 97].
Main outcome measures
Due to the large heterogeneity in exercise protocols and testing methods, it was difficult to arrive at a synthesis of the search findings. Therefore, we performed a descriptive analysis where performance gains (or negative effects) were sorted and summed according to four motor outcome measures and five cognitive outcome measures. The four motor outcome measures were: functional lower limb mobility and gait characteristics [82,83,84, 86,87,88,89,90, 92,93,94, 96,97,98,99,100], static and/or dynamic balance [86, 87, 89, 94, 97,98,99], muscle strength [82, 85, 89, 90, 92, 99], and psychomotor (RT) tasks [83, 85, 91, 93,94,95, 97, 98]. The five cognitive outcome measures were: processing speed [85,86,87,88,89,90,91,92,93,94,95,96,97,98,99], working memory [82, 84, 88, 90, 92, 95, 96, 98, 99], inhibition [82, 84, 89, 93,94,95,96, 98, 99], attention [85, 87,88,89,90,91,92,93,94,95,96,97,98,99], and dual-task cost [82,83,84, 86, 88, 92,93,94, 96, 97, 100]. Other outcome measures were aerobic fitness [82, 95], depression scores [87, 90, 92], quality-of-life and life-satisfaction scores [87, 90, 92], and markers of brain plasticity (brain-derived neurotrophic factor – BDNF) [85, 98]. Battery of tests used for the assessments of the aforementioned motor/cognitive outcome measures in each of the included studies are specified in Table 1.
The outcome effects of each intervention on specific cognitive and motor functions are presented in Table 1. Data are summarized in Fig. 2 for the overall motor/cognitive gains in each intervention category, and in Figs. 3 and 4 for the specific motor (Fig.3) and cognitive (Fig. 4) gains in each intervention category. As can be seen in Fig. 2, the highest number of reported performance gains and negative findings were reported for the combined exercise training and cognitive-motor training. However, the abovementioned interventions were also the most frequent (Table 1). In line with the first main objective of the current systematic review, the specific effects of the different intervention categories on motor and cognitive gains are described in detail next.
Motor performance gains as a function of intervention
Motor performance gains (from a number of studies) are illustrated in Fig. 3 for each of the six interventions. The majority of test batteries (or protocols) examined gains in functional tasks (i.e. mobility and strength) [82, 84, 86,87,88,89,90, 92, 94, 97,98,99,100], gross motor skills (i.e. balance) [84, 86,87,88,89, 94, 96,97,98,99], or RT [83, 91, 93,94,95, 97, 98]. None of the included studies examined fine motor skills or motor learning. Four studies used aerobic [89, 95], strength [85, 89],or balance [86, 89] training as a single intervention. In one study [89], the three interventions and a passive control group were included in a single study design (see Table 1; [89]). Significant gains induced by aerobic training were found only for a mobility pre/post-test (gait speed, One Mile Walk Test), significant gains induced by resistance training were found for the strength pre/post-tests (One Repetition Maximum test in all trained muscles), and significant positive gains induced by balance training have been shown only for a balance pre/post-test (Stork Balance Stand Test). No gains on all elements of the test battery were observed in the passive control group. For the remaining studies, aerobic training [95], resistance training [85], or balance training [86] were applied as single interventions. Likely beneficial gains in performance of the visuomotor RT task (i.e. shorter responses times at likelihood of 80.2%) were reported in [85] and significant gains in gait stability were reported in [86]. Taken together, observations from the four studies suggest that using aerobic [89, 95], strength [85, 89], or balance [86, 89] training as a single intervention may have only limited effects on motor performance gains. However, findings cannot be generalized due to limitations caused by the small number of studies or the diversity in testing protocols – specifically, no inclusion of psychomotor tests [86, 89] and no inclusion of mobility, balance, and strength tests [85, 95].
Two studies focused on dance as a single exercise [87, 88]. Observations from these studies are summarized in Fig. 3D. Irrespective of differences in the intervention and testing protocols, both studies showed a significant increase in gait speed. One of these studies also reported a significant increase in backward gait speed as well as faster performance time on the Four-Square Step Test [87].
Eleven studies used combined-exercise training protocols: (i) aerobic and strength [82, 88, 91], (ii) aerobic and flexibility [90], (iii) strength and balance [83, 95, 97], or (iv) aerobic, strength, and balance exercises combined [84, 88, 98,99,100]. Observations from these studies are summarized in Fig. 3E. In all studies but two [91, 95], mobility tests were applied pre- and post-intervention, and in seven of nine studies significant gains were observed in one or more mobility performance tests: Time Up & Go (TUG) [82, 98], Walking Speed [82, 97,98,99,100], Stride Length Variability [88], and Chair Stand [82, 97, 99]. Improvements in mobility characteristics were observed for all training protocols in which strength exercises were included [82, 88, 97,98,99,100], albeit pre-to-post gains in strength were reported only by one study [82] in which two intervention groups and one control group were tested. Three studies reported significant pre-to-post improvements in balance [97,98,99] and three of four studies reported significant pre-to-post improvements in the performance of one or more psychomotor tests [83, 91, 97]. However, all three studies that reported pre-to-post improvements in balance also included balance training in their intervention. Finally, pre-to-post gains on RT were found in five studies [83, 91, 95, 97, 98]. In two of the studies the training protocol consisted of combined strength and balance exercises [83, 97]. The three remaining studies consisted of aerobic-strength training [91] or aerobic-strength-balance training [98].
Nine intervention studies used one or more paradigms of combined physical-cognitive training. Observations from these studies are summarized in Fig. 3F. In six of the nine studies [84, 91, 93, 94, 96, 100], physical and cognitive training were conducted in a dual-task manner. In the remaining studies [83, 92, 97], participants received the cognitive intervention [83, 97] or social intervention [92] at the end of the physical training. Intervention protocols consisted of: (i) aerobic exercise combined with: a battery of cognitive-psychomotor training [93], memory training [96], a video game [94]; (ii) strength-balance exercise [83, 97] combined with computerized cognitive training for attention; and (iii) aerobic-strength-balance exercise combined with dual-task interference and/or a battery of psychomotor and memory tasks [84, 91, 100]. Most of the pre-to-post performance gains were reported for mobility outcome measures, specifically TUG [92], walking speed [97, 100], stride length/gait speed variability [84, 96], and chair stand [97]. Significant pre-to-post gains were also observed for balance [94, 97]. However, observed gains in the above-mentioned studies were not specific to the intervention, nor to the type of physical exercises or the cognitive training protocols involved. Finally, pre-to-post gains in RT were examined in five studies, in which attention training and/or dual task training exercises were applied [83, 91, 93, 94, 97]. In all five studies a significant improvement in simple RT and/or movement time was observed post-intervention, but significant group differences were evident only when a passive control group was included [91, 93]. Thus, the existence of an evident link between these two types of cognitive training and respective pre-to-post gains in Stepping Reaction Time (SRT) cannot be generalized. To conclude, intervention protocols using single-exercise training tended to result in focal performance gains [86, 89], whereas multiple exercise training [82, 83, 97,98,99] or physical-cognitive training [83, 94, 97] typically resulted in gains of multiple motor outcome measures.
Cognitive performance gains as function of intervention
Cognitive performance gains (from the number of studies) are illustrated in Fig. 4 for each of the six interventions. Again, pre-to-post performance gains on cognitive outcome measures were more visible in groups that underwent combined physical exercise training [82,83,84, 88, 90, 91, 97,98,99,100] or combined physical-cognitive training [82, 84, 91,92,93,94, 96, 97, 100] than in groups that underwent aerobic training [89, 95], strength training [85, 89] or balance training [86, 89] as a single exercise. Pre-to-post improvements on processing and attention were found in both studies in which aerobic training was applied as a single intervention [89, 95], whereas significant improvements on memory [89] or inhibition [95] were evident only in one of the two studies. Finally, the beneficial effects of strength training [89, 95] or balance training [86, 95] on cognition were marginal, with evidence pointing to possible gains in processing speed [85], attention [89] or motor interference task [86], but not on inhibition [85, 89] or cognitive interference task [86] (see, Figs. 4A-C).
The effects of dance as a single intervention on cognitive functions in older adults were reported in two studies [87, 88]. In one study [87], no pre-to-post gains in cognition were reported. In contrast, the other study [88], which used a cognitive-motor interference task (a serial three subtractions test while walking), found a significant decrease in the average time required to recite the successive subtractions and a marginal increase in the percentage of correct answers, suggesting pre-to-post improvements in processing speed, working memory, attention, and dual-task cost (see, Fig. 4D). Of note, the durations of the single training sessions in both studies were largely similar (90 min including warm-up and cool-down). However, the duration of the intervention was twice as long in one study [88] (26 weeks) than in the other study [87] (12 weeks). This could partially explain the absence of significant post-intervention effects in the latter study.
Findings from the eleven studies in which combined-exercise training protocols were used (see, Fig. 4E) and the nine studies in which combined physical-cognitive training protocols were used (see, Fig. 4F) are discussed next. Due to the large variety among the applied cognitive test batteries, pre-to-post intervention effects are presented for each of the five outcome measures separately, as a function of the different training protocols. Statistically significant pre-to-post-intervention differences on one or more outcome measures of processing were reported for aerobic-flexibility training [90], for strength-balance training [97], and for aerobic-strength-balance [98]. Improvements were found on: (i) Digit Symbol Substitution Test (DSST) and Analogy test scores [90], (ii) TMT parts A and B time scores [97], and (iii) California Older Adult Stroop Test (COAST) and TMT (parts A and B) time scores [98]. Significant pre-to-post-intervention differences on one or more outcome measures of processing were also reported in four studies in which combined physical-cognitive training protocols were used [91,92,93, 97]. In three of those studies [92, 93, 97], significant pre-to-post improvements on one or more outcome measures of attention or dual-task cost were also found. Significant pre-to-post differences were found: (i) in TMT parts A and B time scores following strength-balance training and computerized attention training [97]; (ii) on the Categorical Word Fluency element of the 5-Cog test, the digit symbol substitution test (DSST), and the Yamaguchi Kanji symbol substitution tests following aerobic training combined with social interaction [92]; (iii) in a visual processing (Useful Field of View Test (UFOV)) [93], and (iv) in the Simple/Choice RT elements of the Vienna Test System [91].
Statistically significant pre-to-post-intervention differences on one or more outcome measures of memory were reported for aerobic-strength training [82] and aerobic-flexibility training [90]. In [82], improvements in two elements of the Random Generator Number test (RNG, R scores, and mean repetition gap (MRG)) were observed only during a dual task (i.e., performing the RNG test during walking), and were more prominent for the intervention group that underwent aerobic training combined with strength exercise of the upper body muscles (UBS-A group) than in the intervention group that underwent strength exercise of the lower body muscles (LBS-A group). Pre-to-post gains on MRG scores of the RNG test were found only for the UBS-A and control groups, but not for the LBS-A. For [90], a significant gain was reported on the Cued Recall Test of the Five-Cog task. However, a comparable improvement was also found in the control group. Pre-to-post-intervention improvements in memory were observed in only one [92] of the three studies [84, 92, 96] where memory tests were conducted after the implementation of combined physical-cognitive training.
Statistically significant pre-to-post-intervention differences on one or more outcome measures of inhibition were reported for aerobic-strength training [82] and aerobic-strength-balance training [98]. In one study [82], significant gains were found for the Turning Point Index (TPI, changes between ascending and descending phases) and the adjacency score (numbers presented in pairs; i.e. 3–4) of the RNG test that were visible in both the single-and dual-task test conditions. However, improvements were not statistically different as a function of the group, and were not consistent across test conditions. With respect to the studies in which combined physical-cognitive training protocols were used, pre-to-post-intervention improvements in the performance of the inhibition component in the RNG test was reported only in one study following an intervention with dual-task walking [84].
Statistically significant pre-to-post-intervention differences on one or more outcome measures of attention were reported for aerobic-flexibility training [90], strength-balance training [97], and aerobic-strength-balance training [98]. Testing protocols were not identical across the three abovementioned studies. For [97], significant pre-to-post improvements were reported in the performance of the divided attention task of the Vienna Test System. For [90], a significant gain was reported on the Character Position Referencing task of the Five-Cog task, but a comparable improvement was also found for participants in the passive control group. Finally, [98] reported significant pre-to-post improvement on performance of the TMT parts A and B tests (see also improvement in processing), but not on the Letter-Number Sequencing task. No significant gains were reported by [95] for strength-balance training and for [88, 99] for aerobic-strength-balance training.
With respect to the studies in which combined physical-cognitive training protocols were used, significant pre-to-post-intervention improvements on one or more outcome measures of attention were reported in four studies [91,92,93, 97]. With respect to one study [97], significant pre-to-post improvements were also reported on all divided attention elements of the Vienna Test System. Finally, another study [93] reported significant pre-to-post improvement in the divided attention element of the UFOV evaluation tool.
Significant pre-to-post-intervention differences on Dual-Task Cost (DTC) were reported by [82] for aerobic-strength training and [83] for strength-balance training (however, statistical power in the latter study was poor due to the small sample size). In [82], improvements in DTC were associated with improvement in working memory and inhibition, as reported above. Interestingly, for three of the six studies mentioned above [91, 97, 100], significant pre-to-post improvements on DTC were reported when the same physical intervention protocols were repeated whilst cognitive training was added. With respect to the studies in which combined physical-cognitive training protocols were used, pre-to-post-intervention improvements in DTC were reported in seven of the eight studies where this outcome measure was tested [83, 92,93,94, 96, 97, 100]. Gains were not specific to the intervention program (either to the type of physical exercises or to the cognitive training protocols involved) or to the evaluation protocol.
Association between motor and cognitive gains
In line with the second major aim of the current review– looking into the dual effect of various training protocols on motor and cognition, we provided a qualitative overview of the extent by which pre-to-post gains in motor functions parallel improvements in the performance of cognitive functions. Specifically, a detailed inspection of the data in Table 1 indicates that parallel improvements in motor and cognitive performances were observed, mainly for interventions consisting of combined physical training or combined physical-cognitive training. The occurrences of parallel improvements in motor and cognitive outcome measures are illustrated in Fig. 5 for the two combined training interventions. It can be seen that parallel improvements were mainly found for: (i) mobility and dual-task cost (DTC) [82, 83, 92, 96, 97, 99, 100], (ii) mobility, balance, processing speed, and attention [97, 98], or (iii) psychomotor speed, processing speed, attention, and/or DCT [83, 91, 93, 94, 97]. To a lesser extent, we also found associations between: (i) mobility (TUG/gait speed/gait variability), balance and inhibition for physical-cognitive training [84, 98], or (ii) between gait speed, strength, and inhibition for combined exercise training [82].
For the remaining interventions (aerobic, strength, balance, and/or dance), parallel improvements in physical/motor outcome measures and cognitive outcome measures were found between: (i) mobility (gait speed) and processing speed, attention, memory, and DTC in dance [88]; (ii) mobility, attention, and processing speed in aerobic training [89]; (iii) psychomotor speed, attention, and processing speed for strength training [85]; and (iv) balance, processing speed, and DTC in balance training [86]. Overall, these qualitative analyses suggest that pre-post gains in gait, mobility, and balance were associated with cognitive improvements. However, most of the included studies did not examine correlations between the pre-post difference values of cognitive and motor outcome measures.
Direct assessment of the associations between pre-to-post difference values of cognitive and motor outcome measures were available in only two of the nineteen reviewed studies [84, 99]. One study [84] reported that increased inhibition efficiency was associated with decreased gait variability (r = −.65, p = .006) in the group that underwent physical-cognitive dual-task training. However, this effect was found only during dual-task walking with simple gait demands. The same authors reported a marginally significant association between the same outcome measures also for the group that underwent the physical training alone (aerobic-strength-balance combined). Here, a significant correlation between increase inhibition efficiency and decreased gait variability (r = −.47, p = .049) was reported for dual-task walking with complex gait demands (i.e., walking while negotiating hurdles). The second study [99] reported that pre-to-post gains in processing and attention (as measured with DSST) following aerobic-strength-balance training were positively correlated with improvements in the Short Physical Performance Battery (SPPB) scores (r = .38, p = .002), chair stand scores (r = .26, p = .012), and to some extent balance scores (r = .21, p = 047). The same authors also reported significant positive correlations between gains on short-term memory scores (Rey Auditory Verbal Learning Test, (RAVLT)) and gait velocity (r = 0.25, p = .019) or chair stand (r = .22, p = .039). Otherwise, correlations between pre-to-post changes in the performance of RAVLT or the inhibition test (Stroop), and pre-to-post changes in all other elements of the SPPB, did not reach the level of significance (r ≤ .20, p > .05).