Exercise and the Brain: Lessons From Invertebrate Studies
Frontiers in Behavioral Neuroscience
https://doi.org/10.3389/FNBEH.2022.928093Abstract
Benefits of physical exercise for brain functions are well documented in mammals, including humans. In this review, we will summarize recent research on the effects of species-specific intense locomotion on behavior and brain functions of different invertebrates. Special emphasis is made on understanding the biological significance of these effects as well as underlying cellular and molecular mechanisms. The results obtained in three distantly related clades of protostomes, Nematodes, Molluscs and Artropods, suggest that influence of intense locomotion on the brain could have deep roots in evolution and wide adaptive significance. In C. elegans, improved learning, nerve regeneration, resistance to neurodegenerative processes were detected after physical activity; in L. stagnalis—facilitation of decision making in the novel environment, in Drosophila—increased endurance, improved sleep and feeding behavior, in G. bimaculatus—improved orientation in conspecific phonotaxis, enhanced ag...
References (61)
- Adamo, S. A., Linn, C. E., and Hoy, R. R. (1995). The role of neurohormonal octopamine during ''fight or flight'' behaviour in the field cricket Gryllus bimaculatus. J. Exp. Biol. 198, 1691-1700. doi: 10.1242/jeb.198.8.1691
- Aonuma, H., Mezheritskiy, M., Boldyshev, B., Totani, Y., Vorontsov, D., Zakharov, I., et al. (2020). The role of serotonin in the influence of intense locomotion on the behavior under uncertainty in the mollusk Lymnaea stagnalis. Front. Physiol. 11:221. doi: 10.3389/fphys. 2020.00221
- Babcock, D.T., and Ganetzky, B. (2014). An improved method for accurate and rapid measurement of flight performance in Drosophila. J. Vis. Exp. 84:e51223. doi: 10.3791/51223
- Beckett, M. W., Ardern, C. I., and Rotondi, M. A. (2015). A meta-analysis of prospective studies on the role of physical activity and the prevention of Alzheimer's disease in older adults. BMC Geriatr. 15, 1-7. doi: 10.1186/s12877- 015-0007-2
- Berlandi, J., Lin, F., Ambrée, O., Rieger, D., Paulus, W., Jeibmann, A., et al. (2017). Swing Boat: inducing and recording locomotor activity in a Drosophila melanogaster model of Alzheimer's disease. Front. Behav. Neurosci. 11:159. doi: 10.3389/fnbeh.2017.00159
- Bramble, D. M., and Lieberman, D. E. (2004). Endurance running and the evolution of Homo. Nature 432, 345-352. doi: 10.1038/nature03052
- Burger, J., Kolss, M., Pont, J., and Kawecki, T. J. (2008). Learning ability and longevity: a symmetrical evolutionary trade-off in Drosophila. Evolution 62, 1294-1304. doi: 10.1111/j.1558-5646.2008.00376.x
- Chaudhari, S. N., and Kipreos, E. T. (2017). Increased mitochondrial fusion allows the survival of older animals in diverse. C. elegans longevity pathways. Nat. Commun. 8:182. doi: 10.1038/s41467-017-00274-4
- Chistopol'skii, I. A., and Sakharov, D. A. (2003). Non-synaptic integration of the cell bodies of neurons into the central nervous system of the snail. Neurosci. Behav. Physiol. 33, 295-300. doi: 10.1023/a:1022163701311
- Chuang, H. S., Kuo, W. J., Lee, C. L., Chu, I. H., and Chen, C. S. (2016). Exercise in an electrotactic flow chamber ameliorates age-related degeneration in Caenorhabditis elegans. Sci. Rep. 6:28064. doi: 10.1038/srep28064
- Cobb, T., Sujkowski, A., Morton, C., Ramesh, D., and Wessells, R. (2020). Variation in mobility and exercise adaptations between Drosophila species. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 206, 611-621. doi: 10.1007/s00359-020-01421-x
- Costa Daniele, T. M., de Bruin, P. F. C., de Matos, R. S., de Bruin, G. S., Chaves Junior, C. M., de Bruin, V. M. S., et al. (2020). Exercise effects on brain and behavior in healthy mice, Alzheimer's disease and Parkinson's disease model-a systematic review and meta-analysis. Behav. Brain Res. 383:112488. doi: 10.1016/j.bbr.2020.112488
- Damschroder, D., Reynolds, C., and Wessells, R. (2018). Drosophila tafazzin mutants have impaired exercise capacity. Physiol. Rep. 6:e13604. doi: 10.14814/phy2.13604
- Dingle, H. (1972). Migration strategies of insects. Science 175, 1327-1335. doi: 10.1126/science.175.4028.1327
- Dyakonova, T. L., Sultanakhmetov, G. S., Mezheritskiy, M. I., Sakharov, D. A., and Dyakonova, V. E. (2019). Storage and erasure of behavioral experiences at the single neuron level. Sci. Rep. 9:14733. doi: 10.1038/s41598-019-51331-5
- Dyakonova, V. E. (2020). Neuronal counter of the life span: does it exist? Russ. J. Dev. Biol. 51, 197-200. doi: 10.1134/S1062360420030066
- Dyakonova, V. E., Hernádi, L., Ito, E., Dyakonova, T. L., Chistopolsky, I. A., Zakharov, I. S., et al. (2015a). The activity of isolated neurons and the modulatory state of an isolated nervous system represent a recent behavioural state. J. Exp. Biol. 218, 1151-1158. doi: 10.1242/jeb.111930
- Dyakonova, V. E., Hernádi, L., Ito, E., Dyakonova, T. L., Zakharov, I. S., Sakharov, D. A., et al. (2015b). The activity of isolated snail neurons controlling locomotion is affected by glucose. Biophysics 11, 55-60. doi: 10.2142/biophysics.11.55
- Dyakonova, V. E., and Krushinsky, A. L. (2008). Previous motor experience enhances courtship behavior in male cricket Gryllus bimaculatus. J. Insect Behav. 21, 172-180. doi: 10.1007/s10905-008-9117-4
- Epp, J. R., Silva, M. R., Köhler, S., Josselyn, S. A., and Frankland, P. W. (2016). Neurogenesis-mediated forgetting minimizes proactive interference. Nat. Commun. 7:10838. doi: 10.1038/ncomms10838
- Farooqui, T. (2007). Octopamine-mediated neuromodulation of insect senses. Neurochem. Res. 32, 1511-1529. doi: 10.1007/s11064-007-9344-7
- Gargano, J. W., Martin, I., Bhandari, P., and Grotewiel, M. S. (2005). Rapid iterative negative geotaxis (RING): a new method for assessing age-related locomotor decline in Drosophila. Exp. Gerontol. 40, 386-395. doi: 10.1016/j. exger.2005.02.005
- Gillette, R. (2006). Evolution and function in serotonergic systems. Integr. Comp. Biol. 46, 838-846. doi: 10.1093/icb/icl024
- Giurfa, M. (2006). Associative learning: the instructive function of biogenic amines. Curr. Biol. 16, 892-895. doi: 10.1016/j.cub.2006.09.021
- Harrison, J. F., and Roberts, S. P. (2000). Flight respiration and energetics. Annu. Rev. Physiol. 62, 179-205. doi: 10.1146/annurev.physiol.62.1.179
- Hartman, J. H., Smith, L. L., Gordon, K. L., Laranjeiro, R., Driscoll, M., Sherwood, D. R., et al. (2018). Swimming exercise and transient food deprivation in Caenorhabditis elegans promote mitochondrial maintenance and protect against chemical-induced mitotoxicity. Sci. Rep. 8:8359. doi: 10.1038/s41598-018-26552-9
- Heijnen, S., Hommel, B., Kibele, A., and Colzato, L. S. (2016). Neuromodulation of aerobic exercise-a review. Front. Psychol. 6:1890. doi: 10.3389/fpsyg.2015. 01890
- Hofmann, H. A., and Stevenson, P. A. (2000). Flight restores fight in crickets. Nature 403:613. doi: 10.1038/35001137
- Hughes, K. J., Rodriguez, A., Flatt, K. M., Ray, S., Schuler, A., Rodemoyer, B., et al. (2019). Physical exertion exacerbates decline in the musculature of an animal model of Duchenne muscular dystrophy. Proc. Natl. Acad. Sci. U S A 116, 3508-3517. doi: 10.1073/pnas.1811379116
- Jung, S. N., Borst, A., and Haag, J. (2011). Flight activity alters velocity tuning of fly motion-sensitive neurons. J. Neurosci. 31, 9231-9237. doi: 10.1523/JNEUROSCI.1138-11.2011
- Kondo, M., and Shimada, S. (2015). Serotonin and exercise-induced brain plasticity. Neurotransmitter 2:e793. doi: 10.14800/nt.793
- Korshunova, T. A., Vorontsov, D. D., and Dyakonova, V. E. (2016). Previous motor activity affects transition from uncertainty to decision- making in snails. J. Exp. Biol. 219, 3635-3641. doi: 10.1242/jeb. 146837
- Kumar, S., Behera, S., Basu, A., Dey, S., and Ghosh-Roy, A. (2021). Swimming exercise promotes post-injury axon regeneration and functional restoration through AMPK. eNeuro 8:ENEURO.0414-20.2021. doi: 10.1523/ENEURO. 0414-20.2021
- Laranjeiro, R., Harinath, G., Burke, D., Braeckman, B. P., and Driscoll, M. (2017). Single swim sessions in C. elegans induce key features of mammalian exercise. BMC Biol. 15:30. doi: 10.1186/s12915-017-0368-4
- Laranjeiro, R., Harinath, G., Hewitt, J. E., Hartman, J. H., Royal, M. A., Meyer, J. N., et al. (2019). Swim exercise in. Caenorhabditis elegans extends neuromuscular and gut healthspan, enhances learning ability and protects against neurodegeneration. Proc. Natl. Acad. Sci. U S A 116, 23829-23839. doi: 10.1073/pnas.1909210116
- Lieberman, D. E. (2012). Human evolution: those feet in ancient times. Nature 483, 550-551. doi: 10.1038/483550a
- Lorenz, M. W. (2007). Oogenesis-flight syndrome in crickets: age-dependent egg production, flight performance and biochemical composition of the flight muscles in adult female Gryllus bimaculatus. J. Insect. Physiol. 8, 819-832. doi: 10.1016/j.jinsphys.2007.03.011
- Mezheritskiy, M., Vorontsov, D., Lapshin, D., and Dyakonova, V. (2020). Previous flight facilitates partner finding in female crickets. Sci. Rep. 10:22328. doi: 10.1038/s41598-020-78969-w
- Murashov, A. K., Pak, E. S., Lin, C. T., Boykov, I. N., Buddo, K. A., Mar, J., et al. (2020). Preference and detrimental effects of high fat, sugar and salt diet in wild-caught Drosophila simulans are reversed by flight exercise. FASEB Bioadv. 3, 49-64. doi: 10.1096/fba.2020-00079
- Nolen, T. G., and Hoy, R. R. (1986). Phonotaxis in flying crickets. I. Attraction to the calling song and avoidance of bat-like ultrasound are discrete behaviors. J. Comp. Physiol. A. 159, 423-439. doi: 10.1007/BF0 0604163
- Park, S., Artan, M., Han, S. H., Park, H. H., Jung, Y., Hwang, A. B., et al. (2020). VRK-1 extends life span by activation of AMPK via phosphorylation. Sci. Adv. 6:eaaw7824. doi: 10.1126/sciadv.aaw7824
- Piazza, N., Gosangi, B., Devilla, S., Arking, R., and Wessells, R. (2009). Exercise- training in young Drosophila melanogaster reduces age-related decline in mobility and cardiac performance. PLoS One 4:e5886. doi: 10.1371/journal. pone.0005886
- Raichlen, D. A., and Alexander, G. E. (2017). Adaptive capacity: an evolutionary neuroscience model linking exercise, cognition and brain health. Trends Neurosci. 40, 408-421. doi: 10.1016/j.tins.2017.05.001
- Rivi, V., Benatti, C., Colliva, C., Radighieri, G., Brunello, N., Tascedda, F., et al. (2019). Lymnaea stagnalis as model for translational neuroscience research: from pond to bench. Neurosci. Biobehav. Rev. 108, 602-616. doi: 10.1016/j. neubiorev.2019.11.020
- Ryglewski, S., Duch, C., and Altenhein, B. (2017). Tyramine actions on Drosophila flight behavior are affected by a glial dehydrogenase/reductase. Front. Syst. Neurosci. 11:68. doi: 10.3389/fnsys.2017.00068
- Sergejeva, M. V., and Popov, A. V. (1994). Ontogeny of positive phonotaxis in female crickets, Gryllus bimaculatus. De Geer: dynamics of sensitivity, frequency-intensity domain and selectivity to temporal pattern of the male calling song. J. Comp. Physiol. A. 174, 381-389.
- Shiga, S., Kogawauchi, S., Yasuyama, K., and Yamaguchi, T. (1991). Flight behaviour and selective degeneration of flight muscles in the adult cricket (Gryllus bimaculatus). J. Exp. Biol. 155, 661-667. doi: 10.1242/jeb. 155.1.661
- Stevenson, P. A., Dyakonova, V. E., Rillich, J., and Schildberger, K. (2005). Octopamine and experience-dependent modulation of aggression in crickets. J. Neurosci. 25, 1431-1441. doi: 10.1523/JNEUROSCI.4258-04.2005
- Stevenson, P. A., Hofmann, H., Schoch, K., and Schildberger, K. (2000). The fight and flight responses of crickets depleted of biogenic amines. J. Neurobiol. 43, 107-120.
- Sujkowski, A., Bazzell, B., Carpenter, K., Arking, R., and Wessells, R. J. (2015). Endurance exercise and selective breeding for longevity extend Drosophila healthspan by overlapping mechanisms. Aging (Albany NY) 7, 535-552. doi: 10.18632/aging.100789
- Sujkowski, A., Gretzinger, A., Soave, N., Todi, S. V., and Wessells, R. (2020). Alpha-and beta-adrenergic octopamine receptors in muscle and heart are required for Drosophila exercise adaptations. PLoS Genet. 16:e1008778. doi: 10.1371/journal.pgen.1008778
- Sujkowski, A., Ramesh, D., Brockmann, A., and Wessells, R. (2017). Octopamine drives endurance exercise adaptations in Drosophila. Cell Rep. 21, 1809-1823. doi: 10.1016/j.celrep.2017.10.065
- Vorontsov, D. D., and Dyakonova, V. E. (2017). Light-dark decision making in snails: Do preceding light conditions matter? Commun. Int. Biol. 10:e1356515. doi: 10.1080/19420889.2017.1356515
- Walker, T. J. (1986). Monitoring the flights of field crickets (Gryllus spp) and a tachinid fly (Euphasiopteryx ochracea) in north Florida. Fla Enthomol. 69, 678-685.
- Watanabe, L. P., and Riddle, N. C. (2019). New opportunities. Drosophila as a model system for exercise research. J. Appl. Physiol. 127, 482-490. doi: 10. 1152/japplphysiol.00394.2019
- Watanabe, L. P., and Riddle, N. C. (2021). GWAS reveal a role for the central nervous system in regulating weight and weight change in response to exercise. Sci. Rep. 11:5144. doi: 10.1038/s41598-021 -84534-w
- Wen, D. T., Zheng, L., Ni, L., Wang, H., Feng, Y., Zhang, M., et al. (2016). The expression of CG9940 affects the adaptation of cardiac function, mobility and lifespan to exercise in aging Drosophila. Exp. Gerontol. 83, 6-14. doi: 10.1016/j. exger.2016.07.006
- Yang, Y., Lagisz, M., Foo, Y. Z., Noble, D. W. A., Anwer, H., Nakagawa, S., et al. (2021). Beneficial intergenerational effects of exercise on brain and cognition: a multilevel meta-analysis of mean and variance. Biol. Rev. 96, 1504-1527. doi: 10.1111/brv.12712
- Yin, M. M., Wang, W., Sun, J., Liu, S., Liu, X. L., Niu, Y. M., et al. (2013). Paternal treadmill exercise enhances spatial learning and memory related to hippocampus among male offspring. Behav. Brain Res. 253, 297-304. doi: 10.1016/j.bbr.2013.07.040
- Zheng, L., Feng, Y., Wen, D. T., Wang, H., and Wu, X. S. (2015). Fatiguing exercise initiated later in life reduces incidence of fibrillation and improves sleep quality in Drosophila. Age (Dordr) 37:77. doi: 10.1007/s11357-015 -9816-7
- Zullo, J. M., Drake, D., Aron, L., O'Hern, P., Dhamne, S. C., Davidsohn, N., et al. (2019). Regulation of lifespan by neural excitation and REST. Nature 574, 359-364. doi: 10.1038/s41586-019-1647-8