ORIGINAL RESEARCH

published: 14 March 2017
doi: 10.3389/fnagi.2017.00056

Evolution of Neuroplasticity in
Response to Physical Activity in
Old Age: The Case for Dancing
Patrick Müller 1 *, Kathrin Rehfeld 2 , Marlen Schmicker 1 , Anita Hökelmann 2 ,
Milos Dordevic 1 , Volkmar Lessmann 3,4 , Tanja Brigadski 3,4,5 , Jörn Kaufmann 6
and Notger G. Müller 1,4,6
1
Neuroprotection Laboratory, German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany, 2 Institute of
Sport Science, Otto-von-Guericke-University, Magdeburg, Germany, 3 Medical Faculty, Institute of Physiology,
Otto-von-Guericke University, Magdeburg, Germany, 4 Center for Behavioral Brain Sciences (CBBS), Magdeburg, Germany,
5
Informatics and Microsystem Technology, University of Applied Science Kaiserslautern, Kaiserslautern, Germany, 6 Medical
Faculty, Clinic for Neurology, Otto-von-Guericke University, Magdeburg, Germany

From animal research, it is known that combining physical activity with sensory
enrichment has stronger and longer-lasting effects on the brain than either treatment
alone. For humans dancing has been suggested to be analogous to such combined
training. Here we assessed whether a newly designed dance training program that
stresses the constant learning of new movement patterns is superior in terms of
neuroplasticity to conventional fitness activities with repetitive exercises and whether
extending the training duration has additional benefits. Twenty-two healthy seniors
(63–80 years) who had been randomly assigned to either a dance or a sport group
completed the entire 18-month study. MRI, BDNF and neuropsychological tests were
Edited by: performed at baseline and after 6 and 18 months of intervention. After 6 months, we
Aurel Popa-Wagner,
University of Rostock, Germany found a significant increase in gray matter volume in the left precentral gyrus in the
Reviewed by: dancers compared to controls. This neuroplasticity effect may have been mediated
Daniel Ortuño-Sahagún, by the increased BDNF plasma levels observed in the dancers. Regarding cognitive
Centro Universitario de Ciencias de la
Salud, Mexico measures, both groups showed significant improvements in attention after 6 months and
Raluca Sandu Vintilescu, in verbal memory after 18 months. In addition, volume increases in the parahippocampal
University of Medicine and Pharmacy
of Craiova, Romania
region were observed in the dancers after 18 months. The results of our study suggest
*Correspondence:
that participating in a long-term dance program that requires constant cognitive and
Patrick Müller motor learning is superior to engaging in repetitive physical exercises in inducing
patrick.mueller@dzne.de
neuroplasticity in the brains of seniors. Therefore, dance is highly promising in its potential
Received: 23 December 2016
to counteract age-related gray matter decline.
Accepted: 27 February 2017
Keywords: neuroplasticity, VBM, exercise, dancing, neurodegeneration, BDNF
Published: 14 March 2017

Citation:
Müller P, Rehfeld K, Schmicker M, INTRODUCTION
Hökelmann A, Dordevic M,
Lessmann V, Brigadski T, Kaufmann J The current demographic change in Western societies, involving both a relative and an absolute
and Müller NG (2017) Evolution of increase in the number of older people, has sparked increasing scientific interest in geriatric issues.
Neuroplasticity in Response to In this context, concepts of successful aging are becoming increasingly important. Several studies
Physical Activity in Old Age:
have indicated that physical exercise may play a key role in healthy aging and in the prevention
The Case for Dancing.
Front. Aging Neurosci. 9:56. of cognitive decline and neurodegenerative diseases (Colcombe et al., 2006; Erickson et al., 2011).
doi: 10.3389/fnagi.2017.00056 Recent reviews summarizing epidemiological, cross-sectional and interventional studies support

Frontiers in Aging Neuroscience | www.frontiersin.org 1 March 2017 | Volume 9 | Article 56

(2013) have 52 participants were then randomly assigned to either the dance suggested that ‘‘dancing activities should be regarded as an or the sport group by using the website www. for the study. Lessmann and Brigadski. Park and Poo. therefore.. BDNF. 2014) have been shown to induce gray matter plasticity and recruited via announcements in local newspapers were screened enhance cognitive functions in older adults.com equivalent of enriched environmental conditions for humans and controlling for age.. 2014). we measured the BDNF levels in the peripheral blood. However. we sought to assess whether it is beneficial to extend interventions. 2012. Erickson et al.. In doing so. 2001. Hüfner et al. BDI-II > 13). (2011) have reported reduced volumes in several brain regions including the anterior hippocampal formation and parts of the parieto-insular vestibular cortex in professional dancers and slackliners compared with non- professionals. 10 subjects were excluded. Kattenstroth et al. diabetes mellitus. This finding may indicate that intensive and repetitive training of the same motor skills leads in context of specialization to reduced volumes of some brain regions. 2013. has been proposed to be a mediator of adult neuroplasticity (Flöel FIGURE 1 | Flow chart of participants’ recruitment. Voelcker-Rehage and Niemann. neurological hippocampus—and that only this combination ensures the diseases and regular exercising (≥1 h/week). von-Guericke University. of these criteria. (2012) Participants and Experimental Design have concluded that higher cardiorespiratory fitness and aerobic The study was designed as an 18-month controlled intervention. Finally.Müller et al. Magdeburg. In the first of 5. which took part in a conventional health sport fitness program in which participants typically performed repetitive physical exercises such as bicycling on an ergometer. 18 months of training (Figure 1).. Table 1 structure or function are scarce. the subjects trained twice per week in 90-min sessions for markedly reduced risk of dementia (Verghese et al. 2010). and all subjects signed a However.randomization. cognitive deficits effect on the genesis of new neurons—predominantly in the (Mini-Mental State Examination.. depression physical exercise with sensory enrichment has the strongest (Beck-Depressions Inventory. we compared our newly designed dance program to an active rather than a passive control group. Sixty-two healthy elderly individuals (63–80 years) et al. 2009. or whether there is a limit after which more training becomes detrimental. since they provide an individual with increased sensory. The remaining 1997.. 2016). 2014).org 2 March 2017 | Volume 9 | Article 56 . Bamadis et al. after 6 and after and cognitive demands. we therefore design a special dance training program that constantly required the participants to learn new movement patterns (Müller et al.. Animal research has suggested that a combination of tinnitus. To assess the specific benefits of this intervention. MMSE status and physical fitness. Dance Induced Brain Plasticity physical activity as a propitious method to induce neuroplasticity MATERIALS AND METHODS in late adulthood (Gregory et al. 2013.. because we were interested in the temporal dynamics of the interventions. van Praag et al. The results of a prospective study of Interventions 469 subjects older than 75 years over a median follow-up period The interventions were separated into two periods. motor Assessments were performed at baseline. Kattenstroth et al. MMSE < 27). Frontiers in Aging Neuroscience | www.’’ Despite this encouraging statement. tactile and motor performance in participating seniors... 2014) and cognitive training (Bamadis participation. not only cardiovascular fitness but also coordinative written informed and they did not receive payment for their exercise (Niemann et al. 2003). On the basis enduring survival of the newborn cells (Kempermann et al. Edelmann et al. Furthermore. The exclusion criteria were claustrophobia. tattoos.1 years have indicated that dancing is associated with a period. (2010) have reported significant group differences regarding the demographic data were found.frontiersin. in search of a potential mechanism underlying neuroplasticity. 2005). Twenty-two participants studies examining the effects of dance training on brain completed the entire intervention and all measurements. we assessed the effects on brain structure and function after 6 and 18 months of training. In this study. Several studies have suggested that BDNF promotes the differentiation of new neurons and synapses (Huang and Reichardt. because some brain regions may require more training than others. After a 6-month dancing provides detailed demographic data for these participants. metal implants. improvements in cognitive. et al. physical activity levels are associated with larger gray matter The study was approved by the ethics committee of Otto- volumes in the prefrontal regions and the hippocampus. No intervention.

only Education 15. London. (measured in watts) that a subject is able to achieve on a cycle relative physical capacity) did not differ between groups at Frontiers in Aging Neuroscience | www.40 (1. Over the course creation via DARTEL. Mini-Mental State Examination. Both intervention Fasting blood samples were taken in the mornings of the programs were performed in a group context with music to neuropsychological assessments. spatial normalization to standardized of the intervention.frontiersin. control for psychosocial interactions. 2016). 1990) and an Beck-Depressions Inventory. High-resolution T1-weighted MPRAGE sequences were Dance Group acquired using a 3D magnetization-prepared rapid gradient Participants in the dance group attended a newly designed echo imaging protocol (224 sagittal slices. post hoc t-tests strength-endurance training program with mainly repetitive between consecutive pairs of time points (0 vs. duration and frequency. sport) and time (0. UK).87) 27. Cardiovascular Fitness Cardiovascular fitness was assessed by the Physical Working Cardiovascular Fitness Capacity 130 Test (PWC 130). TI: 1100 ms.57) ‘‘VLMT’’ (an adapted German version of the ‘‘Rey Auditory BMI.org 3 March 2017 | Volume 9 | Article 56 . R&D Systems. situation and time pressure).35) the results of a verbal short.00 (3. 18 months) were calculated separately for each group. Preprocessing involved gray-matter segmentation. 6. the two training programs were MRI comparable in terms of intensity. Germany) sessions and by calculating the individual training heart rate as previously described (Schega et al..11) 16. but complex whole body movements The presentation of the results is structured as follows. threshold of p < 0. strength-endurance and flexibility training. VBM is a precision. the second 12-month intervention period comprised a BDNF reduced training frequency of once per week. 6 and 18 months) was applied. rock ‘‘n’’ roll and square dance). For calculations. a full-factorial design with the factors group Sport Group (dance. finally. A and memory. the MMSE 28. for differential effects of the two interventions (interaction group × time). PWC 130 is the power output Cardiovascular fitness as measured by the PWC 130 (Table 2. RESULTS sit-ups) were performed.8 × 0. From the blood samples.94) An extensive battery of neuropsychological tests were performed BDI-II 5. Verbal Learning Test’’.. trunk) morphometry (VBM) implemented in SPM 12 (Welcome in space under different strain conditions (physical strain.91) 68. ergometer under a heart rate of 130 bpm. new movement sequences. we used resting heart rate [min−1 ] and relative physical capacity Measure Dancing group Sport group [watt/kg]. squats. jazz dance. The flexibility looked for a general intervention effect (factor time). according to Karvonen et al. For the purpose of the current study. Hence. Dance Induced Brain Plasticity TABLE 1 | Demographic information on the participants at baseline. coordinative demands and time pressure Montreal Neurological Institute (MNI) space and smoothing were increased by introducing more complex dance moves and with an Gaussian kernel of 8 mm full width at half maximum choreographies and by increasing the beats per minute in the (FWHM). a more detailed analysis of the temporal Outcome Measures dynamics was performed via post hoc pairwise comparisons. Each session comprised 20-min units of endurance.6 for extensive endurance training. TE: 3. The MR images were analyzed using voxel-based coordination of different body parts (i. (1957) with a factor 0.and long-term memory test. In Participants in the sport group completed a conventional the case of significant group × time interactions. on memory as well. The subjects had to whole-brain unbiased technique for analysis of regional gray learn the choreographies by heart. alternating movements (e.47 ms. exercises and low demands in terms of whole-body coordination 6 vs. Both MR images were acquired on a 3 Tesla Siemens MAGNETOM were supervised by experienced instructors. The endurance training was performed on cycle ergometers. For practical reasons (availability of participants and trainers). Conditional load was plasma concentrations of BDNF were determined by sandwich examined by recording the pulse values during the training ELISAs (BDNF DuoSets.50 (2. biceps curls.77) on the subjects. Verio (Syngo MR B17) using a 32-channel head coil. TR: 2500 ms. music.50 (2. arms.94) 3.07) 29. N 12 10 Age (years) 68. 18. The program comprised five different 2000). Department of Cognitive Neurology. We first were avoided to keep coordinative demands low.8 × 0. template which were switched after every fourth session. To analyze the difference in gray matter volume changes between groups. Helmstaedter and Durwen.10 (0. body mass index. In the strength- endurance unit. 0 vs. thus imposing high demands matter volume and tissue changes (Ashburner and Friston. attention test battery (Test of Attentional Performance (TAP).60 (2.g. MMSE.51 (3.24 (2.8 mm3 .79) Gender (% female) 50% 40% Neuropsychological Testing BMI 27. Wiesbaden. BDI-II.001 (uncorrected) was applied for all analyses.33 (1.. then looked unit mainly consisted of stretching exercises. 6 months. 2002) are reported.25 (3. Zimmermann and Fimm. These choreographies required the flip angle: 7◦ ).Müller et al. genres (line dance.e. voxel size: training program in which they were constantly asked to learn 0. legs.

96) 75.83 (7.03 (33.63) 792.23) 11.86) 69.76 (1285.42 (6.19) = 19.36 (0. before the onset of training.80 (848. No further changes in BDNF occurred after 18 months in any group (Figure 2).29) 52.66) 611. the intraindividual BDNF level remained constant after 6 months of training in the sport group. The relative increase in BDNF levels was quantified. an additional volume was also the only significant change in the interval from increase was observed in the right parahippocampal gyrus of 6 to 18 months. p = 0. The a significant increase in gray matter volume in the left conventional sport program focused mainly on repetitive motor precentral gyrus of only the dancers.frontiersin.19) VLMT late recall (points) 10.21 (0.00 (14.97) 873.40 (3.04) 863.95 (32.00 (3.23) 593.004. ∗ p ≤ 0. verbal long-term free recall (VLMT late recall.90 (4. 25th percentile.30 (8.09) 14.59) Gray matter volume (mm3 ) 601. The BDNF levels seen in the comparison of the baseline to the 18-month data in significantly increased in the dance group after 6 months of training both groups.17 (1284.50 (277.009.28) 1725.244).24) 43.75 (288.16 (40. η2 = 0.05. verbal long-term recognition (VLMT recognition.220) and attention reaction time (subtest flexibility.156.86) 12.438. a similar TABLE 2 | Means and (SD) for fitness. F (2.25 (3.21) 73. 75th percentile.83 (778.04) 1610.19) = 6.27) 1861. Thus. the volumes in the left precentral gyrus of the precentral gyrus.30) 1.08 (2.54) 602.73) VLMT recognition (points) 10.92 (8. left precentral gyrus and the right parahippocampal. There was no change over the entire time course in the sport group (Friedman test. In the conventional sport group.34) 9. Furthermore.89 (1.00) 53.80 (2. the PWC 130 score did not increase significantly throughout the time course of either intervention.22 (5. p < 0. whereas the change in after 18 months.86) 53. whereas interval only (Figure 3).70 (3.00 (1.89 (34.049. (Mann-Whitney U-test. DISCUSSION In this study. η2 = 0. the volume increase in the precentral the dancers. p < 0.15) 12.50 (12. p = 0.75 (40.28 (0.27 (33. As a main finding.Müller et al. Post The dance program was a newly designed intervention that hoc t-tests between the baseline and 6-month data showed required constantly learning new dance choreographies.59 (1116. Post hoc pairwise comparisons showed significant FIGURE 2 | Intraindividual changes in BDNF plasma levels after improvements from baseline to 18 months and from 6 to intervention.319).92 (3.08 (10.001.17) BDNF plasma 1469. the dancers exhibited a significant gray matter dancers had increased more than those in the sport group.15) 901.00 (12.44) 585.387.21) 11.19) = 5. Dance group Sport group Variable Baseline 6 months 18 months Baseline 6 months 18 months Relative physical capacity (Watt/kg) 1.25 (3. η2 = 0. p = 0.33) 1.31) Resting heart frequency (min−1 ) 77.87) 2189.19) = 3.75) Frontiers in Aging Neuroscience | www. F (2. BDNF whereas a significant change over the entire time course was observed in the dance group (Friedman test. we compared the effects of participation in MRI either a dance program or a conventional physical fitness sport A significant group × time interaction was observed in the program on brain function and volume in healthy seniors.33) 1.253).19 (0.57 (1038. In the comparison exercises. No significant time × group interactions emerged.92 (168.39 (0.75 (15.69) 2170.26) 597. Neuropsychological Tests A significant main effect of time was observed for verbal short-term memory (VLMT early recall. The intraindividual changes in BDNF the parahippocampal gyrus occurred during the later training level revealed a significant increase in the dancing group.66) 72.58 (241.70 (162. a significant improvement was training. which After another 12 months of training. F (2. η2 = 0.94) 9. F (2.org 4 March 2017 | Volume 9 | Article 56 . the onset of training as well as 6 months and 18 months after the onset of training.08) 8.489).70 (234. after 6 months of training and after 18 months of Regarding TAP reaction times.19 (0.38) 1. Absolute BDNF plasma levels are summarized in Table 2. Plasma levels of BDNF were analyzed in blood samples before median.83 (10. volume increase in the right parahippocampal gyrus. cognitive functioning.68) 56. BDNF plasma levels were analyzed in blood samples of participants performing a dancing training program or a sport training program 18 months in all three VLMT subcategories in both groups.028).17 (2.352.62) 772. BDNF levels increased during the first 6 months gyrus emerged after 6 months and remained stable over the of dance training and returned to the pre-treatment values remaining dance training interval.004) and declined nearly to baseline of the pretreatment value after 18 months of dancing training. p = 0. Dance Induced Brain Plasticity baseline.20) 11.10 (8. p = 0. we observed that after 6 months of the baseline and the 18-month data in addition to the of training.965) TAP flexibility reaction time (ms) 978.64) 76.58) VLMT early recall (points) 47. Box plots: minimum.29) 1. BDNF plasma levels and total gray matter volume within training groups over the intervention.42) 11.

therefore. because it is interconnected by the perforant attributed to improvements in physical fitness but instead tract both to regions of the frontal lobe. whereas changes in the neuropil occur much slower The parahippocampal gyrus is part of the outer arc of the (Black et al. Reflecting on these developed at different times. to coordinate the whole body and to navigate in parahippocampal regions (Tisserand et al. (2006) have in the motor areas after 6 months (see also Rehfeld et al.e. the central These features included the requirement to constantly learn structure in episodic memory encoding and spatial navigation. 2016). reported dance-induced activations in the putamen. rapid increases in gray matter limbic system and plays an important role in working memory volume in the prefrontal regions have been observed after only and episodic memory retrieval (Pantel et al. the dance-related volume increase mechanisms. Hence. memory). The between coordination demands (e. Brown et al.. The observation that Brain Changes engaging in a dance program for a longer period can induce The precentral gyrus is essential for the control of voluntary neuroplastic processes in this crucial memory region. testing for greater volume changes in the dance compared with the sport group. based on the complex and ever-changing movement patterns that the dancers had to perform. These movements required Temporal Dynamics of Gray Matter Brain the simultaneous coordination of several parts of the body in Plasticity different directions and adjustment to the varying rhythms of The observed volume increases in the two brain regions the music (polycentric and polyrhythmic). to integrate multisensory Many VBM studies have reported an age-related volume loss in information. the observed effects could not be of the present.. (2011) have suggested that parahippocampal atrophy is an early biomarker of AD... 2002). 1990)..frontiersin. motor functions. which are associated seemed to be related to the specific features of the dance program.05. therefore. 2008. the primary which remained stable during the subsequent 12 months. Other studies have indicated an association emerged later and was observed only in the 18-month data. regions may be related to differences in the underlying cellular Taubert et al. new choreographies (i. juggling) and different temporal dynamics in the evolution of the two brain neuroplasticity in the precentral region (Boyke et al.org 5 March 2017 | Volume 9 | Article 56 .Müller et al. balancing.g. 2003). the parahippocampal gyrus constitutes fitness levels over the course of the interventions remained the interface between memory and the experiential consciousness constant in both groups... rapidly. increase in BDNF was not evident. 2010). y = −18. have been strategies. as dance-associated volume increase in the parahippocampal gyrus shown by PET. The box plots show the relative gray matter changes in the peak voxel. In humans. According 2 weeks of motor learning in younger adults (Taubert et al.. Dancing led to a volume increase complex coordination requirements. The motor cortex and the supplementary motor area (SMA). and to the hippocampus. space. y = −26. 2012) occur literature. z = −20). A significant increase in gray matter was found in the precentral gyrus (Montreal Neurological Institute (MNI)-coordinates: x = −16. Because the cardiovascular to Bliss and Lomo (1973). ∗ p ≤ 0. Animal research has suggested that angiogenesis in this area was consistent with expectations based on the and the formation of new dendrites (Thomas et al.. Dance Induced Brain Plasticity FIGURE 3 | Time by group interaction analysis. Echávarri et al. Furthermore. z = 77) and in the parahippocampal gyrus gyrus (MNI-coordinates: x = 34.. with working memory. Frontiers in Aging Neuroscience | www. The increase in gray matter volume in the particularly encouraging in terms of developing prevention precentral gyrus in the dance group may.

brain.. Dance Induced Brain Plasticity 2010). 2014). BDNF formation in professional dancers and slackliners compared changes have also been associated with physical activity.. KR designed and performed the research. However. because less cortical control is needed after the motor be considered.frontiersin. Others have reported superior of preventing gray matter and cognitive decline in the elderly.. Frontiers in Aging Neuroscience | www. 2014). analyzed the data. 2011) should volume. However. in contrast to previous ones (Erickson et al. Based on these initial conditions a BDNF increase in the first 6 months. 18 months. However. at least within circuits to different stressors (Barulli and Stern. in our study. (2010) are not must be other factors involved in adult brain plasticity observed. Regarding attention performance. and not all sectional observational studies which compared the brains studies have observed a BDNF increase after cardiovascular of professional dancers to those of non-professionals. Freret et al.. 2011. which may explain why. Later. challenges. insulin-like growth Niemann et al. However. our study are in contrast to the results of Hänggi et al. which may have the opposite effects on cortical plasticity also concept of brain reserve (Satz et al. this technique does not allow causal wrote the article. animal research has addition. 2006).org 6 March 2017 | Volume 9 | Article 56 . (2011). no randomized study to recommend dancing programs as a means group differences emerged. to recruitment of additional neural resources.. 2013. diseases such as Alzheimer’s. social with non-professionals. Cognitive functions also showed nonlinear development. However. 2008). however. Finally. which combines physical. no cortical volume decreases were observed in our 2015). older adults) and our special designed dancing training BDNF levels returned to baseline in the following 12 months program. We presume groups (Rehfeld et al. study. In training (Vital et al. 2012. 1990). present between groups.. this is the first longitudinal. Together. these studies were cross. which revealed that professional ballet dancers have et al. Maass (2010). the article. TB and JK designed the just a few of the mechanisms that have been suggested to research. interaction and positive stress (Mattson. analyzed the data. it is possible that effects of specialization induced the parahippocampal gyrus. These findings support prior that this advantage is related to the multimodal nature of reports regarding the beneficial effects of physical interventions dancing. in contrast to the brain data.. 2016). which required constantly new learning of movement while volume increases were simultaneously observed in patterns. therefore. NGM designed the research. growth factors such as BDNF. prolonged training leads to Regarding neurobiological mechanisms of exercised-induced automatization. 2014). Putamen and superior frontal gyrus and the results during the interventions. The latter observation was probably of Hüfner et al. synaptogenesis and angiogenesis are MD: data collection. 2008). our dance group consisted of old aged novices. wrote be the basis of brain volume changes (Zatorre et al. in cognitive ability data. 2012). The concept of brain reserve describe individual skills have been fully established (Taube. effects of combined cognitive and physical training as Further research is needed to clarify in greater detail the temporal opposed to single interventions (Oswald et al. AH and VL designed the research. 2014). Underlying Cellular and Molecular AUTHOR CONTRIBUTIONS Mechanisms of Gray Matter Plasticity Although VBM is an imaging modality that reveals volume PM designed and performed the research.Müller et al. thus explaining why only dancers showed with long-term experience. was specially designed to avoid which provide greater dynamic capacity for remodeling cortical such automatization. less neuronal resources may have been more crucial during dancing than during are needed which may lead to volume decreases in those fitness activities. which several brain regions including the anterior hippocampal we aimed to maintain in the aerobic zone. indicates that there volume decreases as reported by Hänggi et al. when the named additional factors that drive BDNF secretion the skill becomes more automatic. changes in the brain. the aforementioned volume increases from (Kirk-Sanchez and McGough. significant intervention could be superior to repetitive physical exercise in improvements were observable after only 6 months in both inducing neuroplasticity in the aging human brain.. Neurogenesis. Our dance differences in an increased baseline adaptive neuroplasticity.. The observation that (novices.. 2015). To induce neuroplasticity in the hippocampus. To our knowledge. which report reduced volumes in related to our control of the individual heart frequency. factor (IGF) and nerve growth factor (NGF) are being studied Interestingly. suggested that coordination but not endurance training induces It has been shown that learning of a new skill first leads synaptogenesis and glial changes (Black et al. processes. training program. conclusions regarding the underlying neurophysiological MS analyzed the data.. We dynamics and the underlying neurobiological mechanisms of will extend our interventions further to test whether group dance-induced neuroplasticity and whether this intervention differences in cognition might emerge at even later time truly has the potential to reduce the risk of neurodegenerative points.. and the fitness levels did not change SMA. than the ones represented by BDNF levels in the peripheral It is generally thought that motor training initially induces blood. longer As mediators of the effects of cardiovascular fitness on the training periods have been recommended (Erickson et al. article revision. no differences in cardiovascular fitness were decreased gray matter volumes in the left premotor cortex. Perspectives whereby verbal memory increased only during the second The results of our study suggest that a long-term dancing training period. cognitive and coordinative on neuropsychological tests (Bamadis et al. brain volume increases.

A. Neurol.14. (2013). C. Chaddock. Sobieray.24. J. The verbal learning and retention Taubert. Schmicker.1007/s00429-010-0283-8 effects of single versus combined cognitive and physical training with older Edelmann. L. A. Sanz Arigita... H. Neuropharmacology 76.. P. 33. 615–621.org 7 March 2017 | Volume 9 | Article 56 ... W. B.00170 an early biomarker of Alzheimer’s disease. P. Fenn.1113/jphysiol. 127–138.. doi: 10. Essig. J. G. Lessmann. T. Am..5568 synaptic BDNF secretion: an update.2014. (2012). and kinetics of 5568–5572.1073/pnas. Hardy. L. doi: 10. Neurosci. whereas motor activity causes doi: 10. E. Arch.neuroimage.. 179–192.. S. doi: 10.. S. Rehfeld.. (2011). (2005).3390/brainsci2040684 jsams. Sci. Satz. B. K. (1973).. motor. and Dinse. (2009). A.1016/j. Pruessner.neuroimage.. 855–865. A. 7031–7035.. and Schröde. Neurosci. 379–382. K. and Lomo. 213–222. Shubert. A. 11670–11677.. Neumann. (Vienna) 122. 97–112.. (2008).1015950108 Park.. 331–356. doi: 10. Koeneke. D..1016/j. A.. P. 307–315.. C. Eur. Physical exercise and cognitive Black..0742-08.. neurons in adult mice living in an enriched environment. Six learning and hippocampal neurogenesis in aged mice. Not only cardiovascular. Ageing 3. Kuhn.008 Rehfeld. J.. F. Kaufmann. T. P. Dtsch.. (2002). J. L. Thomas. C. Arch. (2008).030 Helmstaedter. J. Gregory. Scalf.09. S. Billard. 7–23. E. 1157–1167. locations. compensation.. Aging 9. J. D. induced brain structure changes in the elderly. Peter.. V. The neuronal basis of human and disease. Goerke.10. R. and Johansen-Berg. J. M.. (2014)..06. C. doi: 10.03. Exercise enhances Kattenstroth. U.. A. Kalisch..87. C..2014. sensorimotor. Kolankowska.1038/ plasticity. T.2008 Mattson.. performance in the elderly: current perspectives. V. Müller.2000. in BDNF secretion and action in synaptic plasticity. L. et al. U S A 108. Efficiency. M.11.3389/fnagi. and brain health: what is the role of exercise training in the prevention cognitive function in older people.379 Proc. of dementia? Brain Sci. K. Neural..1007/s10433-006-0035-z 610–627.. M. doi: 10. deficits in subjects with aging-associated cognitive decline. B. doi: 10. Gaudreau. individuals with multi-year dancing activities. Biol. Anwander.1016/s1053-8119(02)91173-0 heart rate: a longitudinal study. Zhao. and Brigadski. (2011). doi: 10. M. P.012 Kirk-Sanchez. Res. 160. doi: 10.. J. M. and Voelcker-Rehage.. doi: 10. and Müller. J. 21–30. Büchel. L. (2010).2009. D. Sci. G.. M. F. J.’’ in Proceeding-International Conference of doi: 10. doi: 10.. Med. A. C. C. cognitive et al.1196/annals. Hökelmann. Sci.. Dance Induced Brain Plasticity REFERENCES performance in elderly without affecting cardio-respiratory functions. S55–S61. Driemeyer. 35. A. (2016). S.. Neuroimage 131. J. Oswald. Training. doi: 10. J. Brain and (2015). (2016). Effect of intermittent normobaric hypoxia on aerobic capacity and function. Pre.. doi: 10. Parker.1073/pnas. Neurosci.1093/gerona/ doi: 10. Weinstein. 28. 493–495. Kaufmann.2567-10.. Voss. and Friston. Med..2005 Frontiers in Aging Neuroscience | www.2013.004 transmission in the dentate of the aneasthetized rabbit following stimulation Maass. Aalten.1176/appi. 43.. 65. Clin.05. K. Long-lasting potentiation of synaptic neures. et al. Schumann-Bard. E. M. doi: 10. Neurosci. Neuropsychol. Acad.. T. Jacobs. Hum. W. H. J.012 Hänggi. Anderson. Huang.1523/JNEUROSCI. M. and Reichardt.. J. (2014). dancers. Physiol.. N Y Acad. Mechanisms underlying the neuroprotective effect of brain reserve cognitive reserve: mediator(s) and construct validity. B. (2014). Hamilton. Alcantara. C. Ann.1016/j. W. J. J.2016. J. Lessmann. The effects of training on morphometry. Visser.1002/hipo.1093/cercor/bhj057 Müller. 684–708. Nat. R.20801 in aging: an MRI study to compare volumetric approaches and voxel-based Karvonen. E. Hüfner. Clin. Front. J. and cognitive performance in elderly Bamadis. (1957). J. L.. Cereb. Erickson. 51–62. 386. and Alzheimer’s disease. Bezzola.1523/JNEUROSCI. J. Interv. J.. and Dinse.. Learning causes synaptogenesis. Acad.1973. brain development and function.2012. A. and May. V. Leßmann. Nature. Ruscheweyh. Aging Neurosci. doi: 10. a critique. A. Klados. Binetti. Transm. N. doi: 10.. 3017–3022.3389/fpsyg. (2014). Aerobic exercise training increases brain volume in aging auf die graue Hirnsubstanz gesunder Senioren. Martinez.. N.. T.Müller et al. A. P. Exp.5960/dzsm. (2011).tics. 11–22. doi: 10. Gaser. R.. and Jäncke. 10. et al.. Aging Neurosci. 2756–2763. Neurotrophins: roles in J. et al. and McGough. H. of a dance vs.. plasticity: emerging concepts in cognitice reserve. Prakash. but also coordinative exercise increases hippocampal volume in older adults... T... a fitness training on brain plasticity.. Physical activity. Aging Neurosci. H.2010. and Thompson. A. and Poo. et al. Gronenschild. M. L.00005 Ashburner. against late life depression.2013. (2016).. A. and Hagen.. D. (2008). 24. Kalisch. T.. 61. R. Neuroimage 17.. capacity. (2010). (2006).. E. 14. Freret. and cognitive 8680–8685. A. 46.1523/JNEUROSCI.. hippocampal perfusion and volumes Boyke.1731-05. and Gage. Styliadis. D. and Greenough. Funct.S39506 angiogenesis. A review of physical and cognitive interventions in aging. Hippocampus 21. M. Echávarri. Bliss. longitudinal group comparison. 273–277.02.. Brain Mapp. A. T.. J. W. G.. Neurosci.005 dance.. van Praag. P. 31. Sportmed. 25. 2. H. Prakash. Linn. Physical activity. J. Rev. S. P. and Lopez. K. McAuley. Rev. A. P. doi: 10. Bandettini.1166 Niemann.. Schlee. Rupprecht.2. Physical activity and memory functions: are neurotrophins and and attention in healthy seniores: a new approach with SPM 12 for pairwise cerebral gray matter volume the missing link? Neuroimage 49. H. Lüders.043 Pantel.. 215. (2006).1038/386493a0 502–509. 1144. A. J. Cortex 16. J. Neurosci. 5:5. E.neuro.. M. 30. J. Gerontol. Hamacher.2010. Flanagin. doi: 10. More hippocampal Barulli. J.2013. Kentala. A... J. V..160. Sport 19.. M.. E.. Psychiatry (2011). H. W. S. M. ‘‘Effects Flöel. J. Isermann.1006/nimg. D. A.. Psychiatr. V. Kattenstroth. Relationship between peripheral IGF-1.677 The effects of aerobic activity on brain structure. C. B. doi: 10.0582 (2010). Winter. Szabo. test.1016/j.019 Kempermann. Uyling. T. formation in professional dancers and slackliners. T.. M. (2013).1007/s12662-016-0411-6 61... humans.. C. and Mustala. H.08. Godde. Willemer. 677–736. J.. Natl. Med. M. et al. (2000). J. Basak. D...20928 2012. and Popa-Wagner. T.frontiersin. J...1. 121–130. Sci. 3:86. C. I. B. (2010). (2012).. Rev. Evans. F.. I. Holt. Vivas. R. and Durwen.2012. Düzel. S.. 63. O. Y.3389/fnagi. B. Z. (1997). R...00086 et al.1016/j. Differential doi: 10.. G. C. (2003). B. 6:170. balance performance et al..1016/j.. Isaacs.. Stephan. 17. 657–669. doi: 10. L.. D. Kratz. Res. Structural Taube. Brigadski.. Tegethoff. Front. P. Glutamate and neurotrophic factors in neuronal plasticity Brown. Neurophysiological adaptations in response to neuroplasticity in the sensorimotor network of professional female ballet balance training. Frantzidis. C.493151 doi: 10. M. Exp. B.1016/j. Natl.2015. and Brigadski. Krüger. A. (2006).. K. K. Neurotrophin regulation of neural circuit Erickson. Mechanisms.. L. maintenance.neubiorev. (2012). nrn3379 arcmed. Voxel-based morphometry—the methods..00031 Biobehav. Neuroimage 11. Villringer. C.1080/13803395... Draganski.and postsynaptic twists adults: the SimA study in a 5-year perspective. doi: 10. Biol. and Stern. I. of the perforant path.1146/annurev.. M. Dennis. (1985) 141. M. K. Annu. Kim.1418. Becke. and Parsons. Regional frontal cortical volumes decrease differentially doi: 10. J..2009.... M. Völker. Med. I. Psychol. E.1007/s00702-013-1154-2 Schega. Jolles. (2015). 805–821. K. C.und eines Gesundheitssporttrainings et al. S. Colcombe. P.1002/hbm. T. Sci. A. learning related changes in cortical areas and associated fiber connections.. doi: 10.. H. doi: 10. (1990). Horstmann. doi: 10. 142–154. R. Neurosci.. 44. Brain Struct.. A useful and differentiated tool in evaluating verbal memory performance. Sci. Y. Sci.. months of dance intervention enhances postural. B. H. A..3389/fnagi. VEGF and BDNF levels and sp010273 exercise-related changes in memory. Parahippocampal volume Erickson. Dynamic properties of human brain structure: Schweiz. in cerebellar cortex of adult rats. and Rassovsky. K.. 232. Trends Cogn. doi: 10. in older adults. Gunzelmann. et al. Sportwiss. M. (2001).. Effekte eine Tanz... 265–271. I. U S A 87. doi: 10. H. J. Front. doi: 10..2010 neuronal development and function.. F. 206–220. van Boxtel. 1166–1170. Ann.1016/j. and Gage.. Atrophy in the parahippocampal gyrus as Front. 941–945.neuropharm.084 doi: 10. 2:31. Proc. doi: 10. M..043 Sports and Neuroscience (Magdeburg).2147/CIA. K.ajp.. 1196–1206. Structural and functional plasticity of the hippocampal Tisserand. B. P. Cole. Hökelmann. (1990). K. doi: 10. J.. Exercise training increases size of hippocampus and improves memory.. (2013). O. Superior sensory.

234–239.Müller et al. 348. T. F. R.1038/nn. Kuslansky. Physical exercise and vascular endothelial conducted in the absence of any commercial or financial relationships that could growth factor (VEGF) in elderly: a systematic review.. et al. J. Handbuch—Teil1. Rehfeld.neubiorev. provided the original author(s) or Zatorre. and Johansen-Berg.028 and reproduction in other forums is permitted. Hökelmann. Teodorov... E. Lipton. M.2013. distribution 01.. B. doi: 10. 2268–2295. C. C.04. B.. Stein. A. Arantes. Geriatr. J. (2014).. Version 1. The use. Dance Induced Brain Plasticity Verghese. Conflict of Interest Statement: The authors declare that the research was Santos-Galduróz. No use.. de Melo Coelho.frontiersin. Fields. Hall. D. J. Rev. R. Lessmann. distribution or reproduction 15.1056/NEJMoa022252 Vital. G. Leisure activities and the risk of dementia in the elderly.3045 is permitted which does not comply with these terms. J.. B.. Frontiers in Aging Neuroscience | www. (2012). G. J.. N. Structural and functional Copyright © 2017 Müller. (TAP). M. doi: 10. terms of the Creative Commons Attribution License (CC BY). A. Neurosci. Kaufmann and Müller. be construed as a potential conflict of interest. Zimmermann..011 Voelcker-Rehage. P. and Fimm. (2013).1016/j. Med. et al. Arch. Dordevic. Dervy. H.7.2014. accordance with accepted academic practice. Katz. Engl. C..1016/j. doi: 10. Biobehav. F. Gerontol. brain changes related to different types of physical activity across the life Brigadski.archger. R..org 8 March 2017 | Volume 9 | Article 56 . Würselen: Psytest. 59. (2002). This is an open-access article distributed under the span. 2508–2516. doi: 10. R.. Testbatterie zur Aufmerksamkeitsprüfung (2003). 528–536. M. Nat. 37. Plasticity in gray and licensor are credited and that the original publication in this journal is cited. Neurosci. C. Schmicker. and Niemann. F... in white: neuroimaging changes in brain structure during learning.