Exercise Promotes Neuroplasticity in Both Healthy and Depressed Brains: An fMRI Pilot Study

Joanne Gourgouvelis, Paul Yielder, Bernadette Murphy, Joanne Gourgouvelis, Paul Yielder, Bernadette Murphy

Abstract

Memory impairments are a frequently reported cognitive symptom in people suffering from major depressive disorder (MDD) and often persist despite antidepressant therapy. Neuroimaging studies have identified abnormal hippocampal activity during memory processes in MDD. Exercise as an ad-on treatment for MDD is a promising therapeutic strategy shown to improve mood, cognitive function, and neural structure and function. To advance our understanding of how exercise impacts neural function in MDD, we must also understand how exercise impacts healthy individuals without MDD. This pilot study used a subsequent memory paradigm to investigate the effects of an eight-week exercise intervention on hippocampal function in low-active healthy (n = 8) and low-active MDD (n = 8) individuals. Results showed a marked improvement in depression scores for the MDD group (p < 0.0001) and no change in memory performance for either group (p > 0.05). Functional imaging results showed a marginally significant decrease in hippocampal activity in both groups following the exercise intervention. Our whole brain analysis collapsed across groups revealed a similar deactivation pattern across several memory-associated regions. These results suggest that exercise may enhance neural efficiency in low-fit individuals while still resulting in a substantially greater mood effect for those suffering from MDD. This trial is registered with clinical trials.gov NCT03191994.

Figures

Figure 1
Figure 1
(a) During the encoding task, participants viewed 240 face-name pairs over two nine-minute fMRI runs. Participants were asked if they thought the name suited the face and responded using a response box. Each run included 120 face-name pairs presented for a duration of 3000 ms, jittered with 34 fixation crosses ranging from 3000–9000 ms in increments of 3000 ms. (b) The retrieval task was then performed on a laptop computer outside the MR scanner. Participants were instructed to choose which of the two names was originally paired with the face shown and then asked if they were confident with their choice. This was used to identify the correct successful encoding trials as remembered (correct) versus lucky guesses.
Figure 2
Figure 2
(a) Regions within the hippocampus found to be active in the correct > incorrect contrast for both healthy and MDD at baseline, used as an ROI to extract beta values for an analysis of activity in the hippocampus. (b) Beta values for correct > incorrect from both groups at pretreatment and posttreatment. Both groups showed a reduction in hippocampal activity within the bilateral ROI following exercise. Error bars represent standard error.
Figure 3
Figure 3
Pre to post changes in neural activity in the correct > incorrect contrast (paired sample t-test). Decreases in activity following exercise were noted in several regions, irrespective of group.
Figure 4
Figure 4
Pre-post changes found a negative relationship between changes in depression scores and activation in the right occipital, left occipital/fusiform, and left precentral gyrus, irrespective of group.

References

    1. Airaksinen E., Larsson M., Lundberg I., Forsell Y. Cognitive functions in depressive disorders: evidence from a population-based study. Psychological Medicine. 2004;34(1):83–91.
    1. Shilyansky C., Williams L. M., Gyurak A., Harris A., Usherwood T., Etkin A. Effect of antidepressant treatment on cognitive impairments associated with depression: a randomised longitudinal study. The Lancet Psychiatry. 2016;3(5):425–435.
    1. Ilsley J. E., Moffoot A. P. R., O’Carroll R. E. An analysis of memory dysfunction in major depression. Journal of the Affective Disorders. 1995;35:1–9.
    1. Sweeney J., Kmeic J., Kupfer D. Neuropsychologic impairments in bipolar and unipolar mood disorders on the CANTAB neurocognitive battery. Biological Psychiatry. 2000;48:674–685.
    1. Sperling R., Chua E., Cocchiarella A., et al. Putting names to faces: successful encoding of associative memories activates the anterior hippocampal formation. NeuroImage. 2003;20(2):1400–1410. doi: 10.1016/S1053-8119(03)00391-4.
    1. Zakzanis K. K., Leach L., Kaplan E. On the nature and pattern of neurocognitive function in major depressive disorder. Neuropsychiatry, Neuropsychology, & Behavioral Neurology. 1998;11(3):111–119.
    1. Tulving E., Markowitsch H. J. Episodic and declarative memory: role of the hippocampus. Hippocampus. 1998;8(3):198–204. doi: 10.1002/(SICI)1098-1063(1998)8:3<198::AID-HIPO2>;2-G.
    1. Burt D., Zembar M., Niederehe G. Depression and memory impairment: a meta-analysis of the association, its pattern, and specificity. Psychological Bulletin. 1995;117(2):285–305.
    1. Heckers S., Weiss A. P., Alpert N. M., Schacter D. L. Hippocampal and brain stem activation during word retrieval after repeated and semantic encoding. Cerebral Cortex. 2002;12(9):p. 900.
    1. Bray N. Learning and memory: the hippocampus encodes objects in time. Nature Reviews Neuroscience. 2014;15(5):p. 281.
    1. Köhler S., Moscovitch M., Winocur G., McIntosh A. R. Episodic encoding and recognition of pictures and words: role of the human medial temporal lobes. Acta Psychologica. 2000;105(2-3):159–179.
    1. Zola S. M., Squire L. R., Teng E., Stefanacci L., Buffalo E. A., Clark R. E. Impaired recognition memory in monkeys after damage limited to the hippocampal region. Journal of Neuroscience. 2000;20(1):p. 451.
    1. Scovile W. B., Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry. 1957;20(1):11–21.
    1. Videbech P., Ravnkilde B. Hippocampal volume and depression: a meta-analysis of MRI studies. American Journal of Psychiatry. 2004;161(11):p. 1957.
    1. McKinnon M. C., Yucel K., Nazarov A., MacQueen G. M. A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. Journal of Psychiatry & Neuroscience: JPN. 2009;34(1):p. 41.
    1. Schmaal L., Veltman D. J., van Erp T. G., et al. Subcortical brain alterations in major depressive disorder: findings from the ENIGMA major depressive disorder working group. Molecular Psychiatry. 2016;21(6):806–812. doi: 10.1038/mp.2015.69.
    1. Fairhall S. L., Sharma S., Magnusson J., Murphy B. Memory related dysregulation of hippocampal function in major depressive disorder. Biological Psychology. 2010;85(3):499–503. doi: 10.1016/j.biopsycho.2010.09.002.
    1. Milne A. M. B., MacQueen G. M., Hall G. B. C. Abnormal hippocampal activation in patients with extensive history of major depression: an fMRI study. Journal of Psychiatry & Neuroscience: JPN. 2012;37(1):p. 28.
    1. Toki S., Okamoto Y., Onoda K., et al. Hippocampal activation during associative encoding of word pairs and its relation to symptomatic improvement in depression: a functional and volumetric MRI study. Journal of Affective Disorders. 2014;152–154:462–467. doi: 10.1016/j.jad.2013.07.021.
    1. Rajkowska G., Miguel-Hidalgo J. J. Gliogenesis and glial pathology in depression. CNS & Neurological Disorders Drug Targets. 2007;6(3):219–233.
    1. Harrison P. J. The neuropathology of primary mood disorder. Brain. 2002;125(7):1428–1449.
    1. Pittenger C., Duman R. S. Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology. 2007;33(1):88–109.
    1. Stockmeier C. A., Mahajan G. J., Konick L. C., et al. Cellular changes in the postmortem hippocampus in major depression. Biological Psychiatry. 2004;56(9):640–650. doi: 10.1016/j.biopsych.2004.08.022.
    1. Qiao H., An S.-C., Ren W., Ma X.-M. Progressive alterations of hippocampal CA3-CA1 synapses in an animal model of depression. Behavioural Brain Research. 2014;275:191–200. doi: 10.1016/j.bbr.2014.08.040.
    1. Andrews G., Sanderson K., Corry J., Lapsley H. M. Using epidemiological data to model efficiency in reducing the burden of depression. The Journal of Mental Health Policy and Economics. 2000;3(4):175–186.
    1. Fava G. A., Ruini C. Long-term treatment of depression: there is more than drugs. Recenti Progressi in Medicina. 2002;93(6):p. 343.
    1. Diverty B., Beaudet M. P. Depression: an undertreated disorder. Health Reports. 1997;8(4):9–18.
    1. Insel T. R., Charney D. S. Research on major depression: strategies and priorities. The Journal of the American Medical Association. 2003;289(23):p. 3167.
    1. Babyak M., Blumenthal J. A., Herman S., et al. Exercise treatment for major depression: maintenance of therapeutic benefit at 10 months. Psychosomatic Medicine. 2000;62(21):633–638.
    1. Blumenthal J. A., Babyak M. A., Moore K. A., et al. Effects of exercise training on older patients with major depression. Archives of Internal Medicine. 1999;159(19):2349–2356.
    1. Blumenthal J. A., Babyak M. A., Doraiswamy P. M., et al. Exercise and pharmacotherapy in the treatment of major depressive disorder. Psychosomatic Medicine. 2007;69(7):p. 587. doi: 10.1097/PSY.0b013e318148c19a.
    1. Martinsen E. W., Medhus A., Sandvik L. Effects of aerobic exercise on depression: a controlled study. British Medical Journal. 1985;291(6488):p. 109.
    1. Stathopoulou G., Powers M. B., Berry A. C., Smits J. A. J., Otto M. W. Exercise interventions for mental health: a quantitative and qualitative review. Clinical Psychology: Science and Practice. 2006;13(2):179–193.
    1. Schuch F. B., Vancampfort D., Richards J., Rosenbaum S., Ward P. B., Stubbs B. Exercise as a treatment for depression: a meta-analysis adjusting for publication bias. Journal of Psychiatric Research. 2016;77:42–51. doi: 10.1016/j.jpsychires.2016.02.023.
    1. Cotman C. W., Berchtold N. C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends in Neurosciences. 2002;25(6):295–301.
    1. van Praag H., Kempermann G., Gage F. H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neuroscience. 1999;2(3):266–270. doi: 10.1038/6368.
    1. Vivar C., Potter M. C., van Praag H. All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis. Current Topics in Behavioral Neurosciences. 2013;15:189–210. doi: 10.1007/7854_2012_220.
    1. van Praag H., Shubert T., Zhao C., Gage F. H. Exercise enhances learning and hippocampal neurogenesis in aged mice. Journal of Neuroscience. 2005;25(38)
    1. van Praag H. Neurogenesis and exercise: past and future directions. Neuromolecular Medicine. 2008;10(2):128–140. doi: 10.1007/s12017-008-8028-z.
    1. Kobilo T., Liu Q.-R., Gandhi K., Mughal M., Shaham Y., van Praag H. Running is the neurogenic and neurotrophic stimulus in environmental enrichment. Learning & Memory (Cold Spring Harbor, N.Y.) 2011;18(9):605–609. doi: 10.1101/lm.2283011.
    1. Dietrich M. O., Andrews Z. B., Horvath T. L. Exercise-induced synaptogenesis in the hippocampus is dependent on UCP2-regulated mitochondrial adaptation. Journal of Neuroscience. 2008;28(42)
    1. Lopez-Lopez C., LeRoith D., Torres-Aleman I. Insulin-like growth factor I is required for vessel remodeling in the adult brain. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(26):9833–9838. doi: 10.1073/pnas.0400337101.
    1. Redila V. A., Christie A. B. R. Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience. 2006;137(4):1299–1307. doi: 10.1016/j.neuroscience.2005.10.050.
    1. Yau S.-Y., Lau B. W., Tong J. B., et al. Hippocampal neurogenesis and dendritic plasticity support running-improved spatial learning and depression-like behaviour in stressed rats. PLoS One. 2011;6(9, article e24263) doi: 10.1371/journal.pone.0024263.
    1. Erickson K. I., Voss M. W., Prakash R. S., et al. Exercise training increases size of hippocampus and improves memory. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(7):3017–3022. doi: 10.1073/pnas.1015950108.
    1. Anderson-Hanley C., Arciero P. J., Brickman A. M., et al. Exergaming and older adult cognition: a cluster randomized clinical trial. American Journal of Preventive Medicine. 2012;42(2):109–119. doi: 10.1016/j.amepre.2011.10.016.
    1. Voss M. W., Prakash R. S., Erickson K. I., et al. Plasticity of brain networks in a randomized intervention trial of exercise training in older adults. Frontiers in Aging Neuroscience. 2010;2:p. 32. doi: 10.3389/fnagi.2010.00032.
    1. Voss M. W., Heo S., Prakash R. S., et al. The influence of aerobic fitness on cerebral white matter integrity and cognitive function in older adults: results of a one-year exercise intervention. Human Brain Mapping. 2013;34(11):2972–2985. doi: 10.1002/hbm.22119.
    1. Young J., Angevaren M., Rusted J., Tabet N. Aerobic exercise to improve cognitive function in older people without known cognitive impairment. In: Young J., editor. Cochrane Database of Systematic Reviews. John Wiley & Sons, Ltd: Chichester, UK; 2015.
    1. Gates N., Fiatarone Singh M. A., Sachdev P. S., Valenzuela M. The effect of exercise training on cognitive function in older adults with mild cognitive impairment: a meta-analysis of randomized controlled trials. The American Journal of Geriatric Psychiatry. 2013;21(11):1086–1097. doi: 10.1016/j.jagp.2013.02.018.
    1. Smith P. J., Blumenthal J. A., Hoffman B. M., et al. Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosomatic Medicine. 2010;72(3):239–252. doi: 10.1097/PSY.0b013e3181d14633.
    1. Sink K. M., Espeland M. A., Castro C. M., et al. Effect of a 24-month physical activity intervention vs health education on cognitive outcomes in sedentary older adults. The Journal of the American Medical Association. 2015;314(8):p. 781.
    1. Colcombe S. J., Erickson K. I., Scalf P. E., et al. Aerobic exercise training increases brain volume in aging humans. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2006;61(11):p. 1166.
    1. Erickson K. I., Prakash R. S., Voss M. W., et al. Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus. 2009;19(10):1030–1039. doi: 10.1002/hipo.20547.
    1. Pajonk F. G., Wobrock T., Gruber O., et al. Hippocampal plasticity in response to exercise in schizophrenia. Archives of General Psychiatry. 2010;67(2):p. 133. doi: 10.1001/archgenpsychiatry.2009.193.
    1. American Psychiatric Association, and American Psychiatric Association. Task Force on DSM-IV, Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR. Washington, DC: American Psychiatric Publishing, Inc.; 2000.
    1. Beck A., Steer R., Brown G. BDI-II. Beck Depression Inventory Second Edition. Manual. San Antonio: Psychological Corporation; 1996.
    1. Nasreddine Z. S., Phillips N. A., Bédirian V., et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society. 2005;53(4):695–699. doi: 10.1111/j.1532-5415.2005.53221.x.
    1. Beck A. T., Steer R. A., Ball R., Ranieri W. F. Comparison of Beck depression inventories-IA and-II in psychiatric outpatients. Journal of Personality Assessment. 1996;67(3):588–597. doi: 10.1207/s15327752jpa6703_13.
    1. Beekley M., Brechue W., Dehoyos D. Cross-validation of the YMCA submaximal cycle ergometer test to predict VO2max. Research Quarterly for Exercise and Sport. 2004;75(3):337–342. doi: 10.1080/02701367.2004.10609165.
    1. Golding L. A., Myers C. R., Sinning W. E. Y’s way to Physical Fitness: The Complete Guide to Fitness Testing and Instruction. 3rd. Champaign, IL: Published for YMCA of the USA by Human Kinetics Publishers; 1989. pp. 106–108.
    1. Pescatello L. S., American College of Sports Medicine . ACSM’s Guidelines for Exercise Testing and Prescription. 9. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins Health; 2014.
    1. Taylor A. W. Journal of Aging and Physical Activity. 3. Vol. 12. Champaign, USA: Human Kinetics Publ INC.; 2004. Canada’s physical activity guide to healthy active living for older adults.
    1. Garber C. E., Blissmer B., Deschenes M. R., et al. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Medicine and Science in Sports and Exercise. 2011;43(7):1334–1359. doi: 10.1249/MSS.0b013e318213fefb.
    1. Stanton R., Reaburn P. Exercise and the treatment of depression: a review of the exercise program variables. Journal of Science and Medicine in Sport. 2014;17(2):177–182. doi: 10.1016/j.jsams.2013.03.010.
    1. Cooney G. Exercise for depression. Journal of Evidence-Based Medicine. 2013;6(4):307–308.
    1. Morris S. B. Estimating effect sizes from the pretest-posttest-control group designs. Organizational Research Methods. 2008;11(2):364–386.
    1. Henson R. A mini-review of fMRI studies of human medial temporal lobe activity associated with recognition memory. Quarterly Journal of Experimental Psychology B. 2005;58(3-4):340–360. doi: 10.1080/02724990444000113.
    1. Murray L. J., Ranganath C. The dorsolateral prefrontal cortex contributes to successful relational memory encoding. Journal of Neuroscience. 2007;27(20)
    1. Blumenfeld R. S., Ranganath C. Dorsolateral prefrontal cortex promotes long-term memory formation through its role in working memory organization. Journal of Neuroscience. 2006;26(3)
    1. Achim A. M., Lepage M. Neural correlates of memory for items and for associations: an event-related functional magnetic resonance imaging study. Journal of Cognitive Neuroscience. 2005;17(4):652–667. doi: 10.1162/0898929053467578.
    1. Konkel A., Cohen N. J. Relational memory and the hippocampus: representations and methods. Frontiers in Neuroscience. 2009;3(2):166–174. doi: 10.3389/neuro.01.023.2009.
    1. Paller K. A., Wagner A. D. Observing the transformation of experience into memory. Trends in Cognitive Sciences. 2002;6(2):93–102.
    1. Wagner A. D., Schacter D. L., Rotte M., et al. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science. 1998;281(5380)
    1. Mura G., Moro M. F., Patten S. B., Carta M. G. Exercise as an add-on strategy for the treatment of major depressive disorder: a systematic review. CNS Spectrums. 2014;19(6):496–508. doi: 10.1017/S1092852913000953.
    1. Wagner A. D., Davachi L. Cognitive neuroscience: forgetting of things past. Current Biology. 2001;11(23):R964–R967.
    1. Wagner A. D., Davachi L. Cognitive neuroscience: forgetting of things past. Current Biology. 2001;11(23):R964–R967.
    1. Morcom A. M., Good C. D., Frackowiak R. S. J., Rugg M. D. Age effects on the neural correlates of successful memory encoding. Brain. 2003;126(1):213–229.
    1. Kirchhoff B. A., Wagner A. D., Maril A., Stern C. E. Prefrontal-temporal circuitry for episodic encoding and subsequent memory. Journal of Neuroscience. 2000;20(16)
    1. Otten L. J., Rugg M. D. When more means less: neural activity related to unsuccessful memory encoding. Current Biology. 2001;11(19):1528–1530.
    1. Daselaar S. M., Prince S. E., Cabeza R. When less means more: deactivations during encoding that predict subsequent memory. NeuroImage. 2004;23(3):921–927. doi: 10.1016/j.neuroimage.2004.07.031.
    1. Cabeza R., Grady C. L., Nyberg L., et al. Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study. The Journal of Neuroscience. 1997;17(1):391–400.
    1. Knight R. T., Grabowecky M. F., Scabini D. Role of human prefrontal cortex in attention control. Advances in Neurology. 1995;66:21–34.
    1. Guillery R. W., Feig S. L., Lozsádi D. A. Paying attention to the thalamic reticular nucleus. Trends in Neurosciences. 1998;21(1):28–32.
    1. Sanacora G., Saricicek A. GABAergic contributions to the pathophysiology of depression and the mechanism of antidepressant action. CNS & Neurological Disorders-Drug Targets. 2007;6(2):127–140.
    1. Luscher B., Shen Q., Sahir N. The GABAergic deficit hypothesis of major depressive disorder. Molecular Psychiatry. 2011;16(4):383–406. doi: 10.1038/mp.2010.120.
    1. Cryan J. F., Kaupmann K. Don’t worry ‘B’ happy!: a role for GABAB receptors in anxiety and depression. Trends in Pharmacological Sciences. 2005;26(1):36–43. doi: 10.1016/j.tips.2004.11.004.
    1. Bajbouj M., Lisanby S. H., Lang U. E., Danker-Hopfe H., Heuser I., Neu P. Evidence for impaired cortical inhibition in patients with unipolar major depression. Biological Psychiatry. 2006;59(5):395–400. doi: 10.1016/j.biopsych.2005.07.036.
    1. Bhagwagar Z., Wylezinska M., Jezzard P., et al. Reduction in occipital cortex γ-aminobutyric acid concentrations in medication-free recovered unipolar depressed and bipolar subjects. Biological Psychiatry. 2007;61(6):806–812. doi: 10.1016/j.biopsych.2006.08.048.
    1. Sanacora G., Mason G. F., Rothman D. L., et al. Increased cortical GABA concentrations in depressed patients receiving ECT. The American Journal of Psychiatry. 2003;160(3)
    1. Hasler G., van der Veen J. W., Tumonis T., Meyers N., Shen J., Drevets W. C. Reduced prefrontal glutamate/glutamine and γ-aminobutyric acid levels in major depression determined using proton magnetic resonance spectroscopy. Archives of General Psychiatry. 2007;64(2):p. 193.
    1. Maciag D., Hughes J., O'Dwyer G., et al. Reduced density of calbindin immunoreactive GABAergic neurons in the occipital cortex in major depression: relevance to neuroimaging studies. Biological Psychiatry. 2010;67(5):465–470. doi: 10.1016/j.biopsych.2009.10.027.
    1. Rajkowska G., O’Dwyer G., Teleki Z., Stockmeier C. A., Miguel-Hidalgo J. J. GABAergic neurons immunoreactive for calcium binding proteins are reduced in the prefrontal cortex in major depression. Neuropsychopharmacology. 2007;32(2):471–482. doi: 10.1038/sj.npp.1301234.
    1. Schoenfeld T. J., Rada P., Pieruzzini P. R., Hsueh B., Gould E. Physical exercise prevents stress-induced activation of granule neurons and enhances local inhibitory mechanisms in the dentate gyrus. The Journal of Neuroscience. 2013;33(18):7770–7777. doi: 10.1523/JNEUROSCI.5352-12.2013.
    1. Fisher B. E., Wu A. D., Salem G. J., et al. The effect of exercise training in improving motor performance and corticomotor excitability in people with early Parkinson’s disease. Archives of Physical Medicine and Rehabilitation. 2008;89(7):1221–1229. doi: 10.1016/j.apmr.2008.01.013.
    1. Krafft C. E., Schwarz N. F., Chi L., et al. An 8-month randomized controlled exercise trial alters brain activation during cognitive tasks in overweight children. Obesity. 2014;22(1):232–242. doi: 10.1002/oby.20518.
    1. Nishiguchi S., Yamada M., Tanigawa T., et al. A 12-week physical and cognitive exercise program can improve cognitive function and neural efficiency in community-dwelling older adults: a randomized controlled trial. Journal of the American Geriatrics Society. 2015;63(7):1355–1363. doi: 10.1111/jgs.13481.
    1. Smith J. C., Nielson K. A., Antuono P., et al. Semantic memory functional MRI and cognitive function after exercise intervention in mild cognitive impairment. Journal of Alzheimer’s Disease. 2013;37(1):197–215. doi: 10.3233/JAD-130467.
    1. Herting M. M., Nagel B. J. Differences in brain activity during a verbal associative memory encoding task in high- and low-fit adolescents. Journal of Cognitive Neuroscience. 2013;25(4):595–612.
    1. Knaepen K., Goekint M., Heyman E. M., Meeusen R. Neuroplasticity—exercise-induced response of peripheral brain-derived neurotrophic factor. Sports Medicine. 2010;40(9):765–801. doi: 10.2165/11534530-000000000-00000.
    1. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C., Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Experimental Neurology. 2005;192(2):348–356. doi: 10.1016/j.expneurol.2004.11.016.
    1. Kubo T., Nonomura T., Enokido Y., Hatanaka H. Brain-derived neurotrophic factor (bdnf) can prevent apoptosis of rat cerebellar granule neurons in culture. Developmental Brain Research. 1995;85(2):249–258.
    1. Kellner Y., Gödecke N., Dierkes T., Thieme N., Zagrebelsky M., Korte M. The BDNF effects on dendritic spines of mature hippocampal neurons depend on neuronal activity. Frontiers in Synaptic Neuroscience. 2014;6:p. 5. doi: 10.3389/fnsyn.2014.00005.
    1. Gottmann K., Mittmann T., Lessmann V. BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses. Experimental Brain Research. 2009;199(3-4):203–234. doi: 10.1007/s00221-009-1994-z.
    1. Waterhouse E. G., An J. J., Orefice L. L., et al. BDNF promotes differentiation and maturation of adult-born neurons through GABAergic transmission. The Journal of Neuroscience. 2012;32(41):14318–14330. doi: 10.1523/JNEUROSCI.0709-12.2012.
    1. Hong E. J., McCord A. E., Greenberg M. E. A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron. 2008;60(4):610–624. doi: 10.1016/j.neuron.2008.09.024.
    1. Song L., Che W., Min-wei W., Murakami Y., Matsumoto K. Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacology Biochemistry and Behavior. 2006;83(2):186–193. doi: 10.1016/j.pbb.2006.01.004.
    1. Shirayama Y., Chen A. C. H., Nakagawa S., Russell D. S., Duman R. S. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. Journal of Neuroscience. 2002;22(8):p. 3251.
    1. Oliff H. S., Berchtold N. C., Isackson P., Cotman C. W. Exercise-induced regulation of brain-derived neurotrophic factor (BDNF) transcripts in the rat hippocampus. Molecular Brain Research. 1998;61(1):147–153.
    1. Cotman C. W., Berchtold N. C., Christie L. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends in Neurosciences. 2007;30(9):464–472. doi: 10.1016/j.tins.2007.06.011.
    1. Duman C. H., Schlesinger L., Russell D. S., Duman R. S. Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice. Brain Research. 2008;1199:148–158. doi: 10.1016/j.brainres.2007.12.047.
    1. Hamilton M. T., Healy G. N., Dunstan D. W., Zderic T. W., Owen N. Too little exercise and too much sitting: inactivity physiology and the need for new recommendations on sedentary behavior. Current Cardiovascular Risk Reports. 2008;2(4):292–298. doi: 10.1007/s12170-008-0054-8.
    1. DiMatteo M. R., Lepper H. S., Croghan T. W. Depression is a risk factor for noncompliance with medical treatment: meta-analysis of the effects of anxiety and depression on patient adherence. Archives of Internal Medicine. 2000;160(14):2101–2107.
    1. Blumenthal J. A., Smith P. J., Hoffman B. M. Opinion and evidence: is exercise a viable treatment for depression? ACSM’s Health and Fitness Journal. 2012;16(4):14–21.

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