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This review discusses the potential role that glial cells may play in influencing the relationship between exercise and episodic memory function. A narrative review methodology is employed. Herein, the different types of glial cells, their implications in subserving episodic memory function, and how exercise can modulate glial cell activity, particularly astrocyte functionality, are discussed. Although additional experimental work is needed, astrocytes appear to play an important role in the exercise–memory interaction. Exercise may increase astrocytic size, attenuate astrogliodegeneration, improve astrocytic aquaporin-4 expression, and increase astrocytic transporter levels. These effects, in turn, may help to increase the number of synapses that neurons form, increase the number of synaptic structures, and increase presynaptic function and postsynaptic receptor localization. Ultimately, these effects may help influence long-term potentiation and episodic memory function.
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Adamsky A , Kol A , Kreisel T , Doron A , Ozeri-Engelhard N , Melcer T , Refaeli R , Horn H , Regev L , Groysman M , London M , Goshen I : Astrocytic activation generates de novo neuronal potentiation and memory enhancement. Cell 174, 59–71.e14 (2018)
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Ashton RS , Conway A , Pangarkar C , Bergen J , Lim KI , Shah P , Bissell M , Schaffer DV : Astrocytes regulate adult hippocampal neurogenesis through ephrin-B signaling. Nat. Neurosci. 15, 1399–1406 (2012)
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Ayadi AE , Zigmond MJ , Smith AD : IGF-1 protects dopamine neurons against oxidative stress: association with changes in phosphokinases. Exp. Brain Res. 234, 1863–1873 (2016)
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Baldwin KT , Eroglu C : Molecular mechanisms of astrocyte-induced synaptogenesis. Curr. Opin. Neurobiol. 45, 113–120 (2017)
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Beauquis J , Pavia P , Pomilio C , Vinuesa A , Podlutskaya N , Galvan V , Saravia F : Environmental enrichment prevents astroglial pathological changes in the hippocampus of APP transgenic mice, model of Alzheimer’s disease. Exp. Neurol. 239, 28–37 (2013)
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Bolborea M , Dale N : Hypothalamic tanycytes: potential roles in the control of feeding and energy balance. Trends Neurosci. 36, 91–100 (2013)
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Brockett AT , LaMarca EA , Gould E : Physical exercise enhances cognitive flexibility as well as astrocytic and synaptic markers in the medial prefrontal cortex. PLoS One 10, e0124859 (2015)
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Choi SH , Bylykbashi E , Chatila ZK , Lee SW , Pulli B , Clemenson GD , Kim E , Rompala A , Oram MK , Asselin C , Aronson J , Zhang C , Miller SJ , Lesinski A , Chen JW , Kim DY , van Praag H , Spiegelman BM , Gage FH , Tanzi RE : Combined adult neurogenesis and BDNF mimic exercise effects on cognition in an Alzheimer’s mouse model. Science 361, eaan8821 (2018)
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Chung WS , Allen NJ , Eroglu C : Astrocytes control synapse formation, function, and elimination. Cold Spring Harb. Perspect. Biol. 7, a020370 (2015)
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Corbin EA , Millet LJ , Keller KR , King WP , Bashir R : Measuring physical properties of neuronal and glial cells with resonant microsensors. Anal. Chem. 86, 4864–4872 (2014)
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Covelo A , Araque A : Stimulating astrocytes to remember. Cell 174, 12–13 (2018)
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de Senna PN , Bagatini PB , Galland F , Bobermin L , do Nascimento PS , Nardin P , Tramontina AC , Goncalves CA , Achaval M , Xavier LL : Physical exercise reverses spatial memory deficit and induces hippocampal astrocyte plasticity in diabetic rats. Brain Res. 1655, 242–251 (2017)
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Escartin C , Murai KK : Imaging and monitoring astrocytes in health and disease. Front. Cell. Neurosci. 8, 74 (2014)
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Fiacco TA , McCarthy KD : Multiple lines of evidence indicate that gliotransmission does not occur under physiological conditions. J. Neurosci. 38, 3–13 (2018)
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Frith E , Loprinzi PD : Physical activity and individual cognitive function parameters: unique exercise-induced mechanisms. JCBPR 7, 92–106 (2018)
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Frith E , Sng E , Loprinzi PD : Randomized controlled trial evaluating the temporal effects of high-intensity exercise on learning, short-term and long-term memory, and prospective memory. Eur. J. Neurosci. 46, 2557–2564 (2017)
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Fulmer CG , VonDran MW , Stillman AA , Huang Y , Hempstead BL , Dreyfus CF : Astrocyte-derived BDNF supports myelin protein synthesis after cuprizone-induced demyelination. J. Neurosci. 34, 8186–8196 (2014)
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Ginhoux F , Greter M , Leboeuf M , Nandi S , See P , Gokhan S , Mehler MF , Conway SJ , Ng LG , Stanley ER , Samokhvalov IM , Merad M : Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841–845 (2010)
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Green D , Loprinzi PD : Experimental effects of acute exercise on prospective memory and false memory. Psychol. Rep. 33294118782466 (2018) [Epub ahead of print]
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Greener M : Don’t underestimate glial cells. Prog. Neurol. Psychiatry 19, 5–8 (2015)
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He XF , Liu DX , Zhang Q , Liang FY , Dai GY , Zeng JS , Pei Z , Xu GQ , Lan Y : Voluntary exercise promotes glymphatic clearance of amyloid beta and reduces the activation of astrocytes and microglia in aged mice. Front. Mol. Neurosci. 10, 144 (2017)
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Latimer CS , Searcy JL , Bridges MT , Brewer LD , Popovic J , Blalock EM , Landfield PW , Thibault O , Porter NM : Reversal of glial and neurovascular markers of unhealthy brain aging by exercise in middle-aged female mice. PLoS One 6, e26812 (2011)
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Lloyd BA , Hake HS , Ishiwata T , Farmer CE , Loetz EC , Fleshner M , Bland ST , Greenwood BN : Exercise increases mTOR signaling in brain regions involved in cognition and emotional behavior. Behav. Brain Res. 323, 56–67 (2017)
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Loprinzi PD : IGF-1 in exercise-induced enhancement of episodic memory. Acta Physiol. (Oxf). e13154 (2018)
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Loprinzi PD , Edwards MK : Exercise and cognitive-related semantic memory function. JCBPR 7, 51–52 (2018)
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Loprinzi PD , Edwards MK : Exercise and implicit memory: a brief systematic review. Psychol. Rep. 121, 1072–1085 (2017)
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Loprinzi PD , Edwards MK , Frith E : Potential avenues for exercise to activate episodic memory-related pathways: a narrative review. Eur. J. Neurosci. 46, 2067–2077 (2017)
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Loprinzi PD , Frith E : A brief primer on the mediational role of BDNF in the exercise-memory link. Clin. Physiol. Funct. Imaging, 39(1), 9–14 (2018)
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Loprinzi PD , Frith E , Edwards MK : Exercise and emotional memory: a systematic review. J. Cogn. Enhanc. 1–10 (2018)
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Loprinzi PD , Frith E , Edwards MK : Resistance exercise and episodic memory function: a systematic review. Clin. Physiol. Funct. Imaging, 38(6), 923–929 (2018)
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Loprinzi PD , Frith E , Edwards MK , Sng E , Ashpole N : The effects of exercise on memory function among young to middle-aged adults: systematic review and recommendations for future research. Am. J. Health Promot. 32, 691–704 (2017)
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Loprinzi PD , Ponce P , Frith E : Hypothesized mechanisms through which acute exercise influences episodic memory. Physiol. Int. 105, 1–13 (2018)
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Matsui T , Omuro H , Liu YF , Soya M , Shima T , McEwen BS , Soya H : Astrocytic glycogen-derived lactate fuels the brain during exhaustive exercise to maintain endurance capacity. Proc. Natl. Acad. Sci. U. S. A. 114, 6358–6363 (2017)
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Moreno-Collazos JM , Orti ES : The effect of physical exercise on neurogenesis factor production in glial cells. Curr. Pharm. Des. 24, 46–55 (2018)
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Nagelhus EA , Amiry-Moghaddam M , Bergersen LH , Bjaalie JG , Eriksson J , Gundersen V , Leergaard TB , Morth JP , Storm-Mathisen J , Torp R , Walhovd KB , Tonjum T : The glia doctrine: addressing the role of glial cells in healthy brain ageing. Mech. Ageing Dev. 134, 449–459 (2013)
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O’Brien ER , Howarth C , Sibson NR : The role of astrocytes in CNS tumors: pre-clinical models and novel imaging approaches. Front. Cell. Neurosci. 7, 40 (2013)
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Ponce P , Loprinzi PD : A bi-directional model of exercise and episodic memory function. Med. Hypotheses 117, 3–6 (2018)
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Quesseveur G , David DJ , Gaillard MC , Pla P , Wu MV , Nguyen HT , Nicolas V , Auregan G , David I , Dranovsky A , Hantraye P , Hen R , Gardier AM , Deglon N , Guiard BP : BDNF overexpression in mouse hippocampal astrocytes promotes local neurogenesis and elicits anxiolytic-like activities. Transl. Psychiatry 3, e253 (2013)
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Rodriguez JJ , Terzieva S , Olabarria M , Lanza RG , Verkhratsky A : Enriched environment and physical activity reverse astrogliodegeneration in the hippocampus of AD transgenic mice. Cell Death Dis. 4, e678 (2013)
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Siddiqui A , Loprinzi PD : Experimental investigation of the time course effects of acute exercise on false episodic memory. J. Clin. Med. 7, 157 (2018)
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Sng E , Frith E , Loprinzi PD : Experimental effects of acute exercise on episodic memory acquisition: decomposition of multi-trial gains and losses. Physiol. Behav. 186, 82–84 (2018)
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Sng E , Frith E , Loprinzi PD : Temporal effects of acute walking exercise on learning and memory function. Am. J. Health Promot. 32, 1518–1525 (2017)
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Tsai SF , Chen PC , Calkins MJ , Wu SY , Kuo YM : Exercise counteracts aging-related memory impairment: a potential role for the astrocytic metabolic shuttle. Front. Aging Neurosci. 8, 57 (2016)
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Uda M , Ishido M , Kami K , Masuhara M : Effects of chronic treadmill running on neurogenesis in the dentate gyrus of the hippocampus of adult rat. Brain. Res. 1104, 64–72 (2006)
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Verkhratsky A , Nedergaard M : Astroglial cradle in the life of the synapse. Philos. Trans. R Soc. Lond. B Biol. Sci. 369, 20130595 (2014)
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Yanes D , Loprinzi PD : Experimental effects of acute exercise on iconic memory, short-term episodic, and long-term episodic memory. J. Clin. Med. 7, E146 (2018)
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Ziegler-Waldkirch S , d’Errico P , Sauer JF , Erny D , Savanthrapadian S , Loreth D , Katzmarski N , Blank T , Bartos M , Prinz M , Meyer-Luehmann M : Seed-induced Aβ deposition is modulated by microglia under environmental enrichment in a mouse model of Alzheimer’s disease. EMBO J. 37, 167–182 (2018)
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Zorec R , Horvat A , Vardjan N , Verkhratsky A : Memory formation shaped by Astroglia. Front. Integr. Neurosci. 9, 56 (2015)
Editor-in-Chief
László ROSIVALL (Semmelweis University, Budapest, Hungary)
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Anna BERHIDI (Semmelweis University, Budapest, Hungary)
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- Ákos KOLLER (Semmelweis University, Budapest, Hungary)
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- Magdolna DANK (Semmelweis University, Budapest, Hungary)
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- Zoltán GIRICZ (Semmelweis University, Budapest, Hungary and Pharmahungary Group, Szeged, Hungary)
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