On the Run for Hippocampal Plasticity
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Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press On the Run for Hippocampal Plasticity C’iana Cooper,1 Hyo Youl Moon,1,2 and Henriette van Praag1 1Neuroplasticity and Behavior Unit, Laboratory of Neurosciences, National Institute on Aging, National Institutes of Health, Biomedical Research Center, Baltimore, Maryland 21224 2Institute of Sport Science, Seoul National University, Gwanak-ro, Gwanak-gu, Seoul 08826, Republic of Korea Correspondence: [email protected] Accumulating research in rodents and humans indicates that exercise benefits brain function and may prevent or delay onset of neurodegenerative conditions. In particular, exercise modifies the structure and function of the hippocampus, a brain area important for learning and memory. This review addresses the central and peripheral mechanisms underlying the beneficial effects of exercise on the hippocampus. We focus on running-induced changes in adult hippocampal neurogenesis, neural circuitry, neurotrophins, synaptic plasticity, neurotransmitters, and vasculature. The role of peripheral factors in hippocampal plasticity is also highlighted. We discuss recent evidence that systemic factors released from peripher- al organs such as muscle (myokines), liver (hepatokines), and adipose tissue (adipokines) during exercise contribute to hippocampal neurotrophin and neurogenesis levels, and memory function. A comprehensive understanding of the body–brain axis is needed to elucidate how exercise improves hippocampal plasticity and cognition. here is a global increase in physical inactivity for learning and memory and exhibits extensive T(Guthold et al. 2008; Dumith et al. 2011; functional plasticity in response to exercise. In Hallal et al. 2012; Kohl et al. 2012). Sedentary the dentate gyrus (DG) of the hippocampus, the behavior is associated with increased risk of production of new neurons is increased by vol- cognitive decline, whereas exercise boosts brain untary wheel running in rodents in association function (Duzel et al. 2016). Moreover, multiple with enhanced synaptic plasticity and memory neurological and neurodegenerative diseases, function (van Praag et al. 1999a,b; Vivar et al. and conditions such as stroke, traumatic brain 2013; Voss et al. 2013). We will discuss local www.perspectivesinmedicine.org injury, and substance addiction, which lack ef- factors in the hippocampus such as neurotro- fective medications, are ameliorated by exercise phins and neurotransmitters as well as distal (Table 1). Research into the underlying cellular peripheral components (myokines, hepatokines, mechanisms has shown that in rodents running and adipokines) that may mediate changes in results in structural, neurochemical, mitochon- neural plasticity as a result of exercise (Fig. 1). drial, and vascular changes in the brain (Neeper et al. 1996; Eadie et al. 2005; Stranahan et al. EXERCISE AND THE HIPPOCAMPUS 2007; Dietrich et al. 2008; van Praag, 2008; Du- zel et al. 2016). In this review, we will focus on The hippocampus is critical for the acquisition the hippocampus, a brain area that is essential of new memories (Squire 1992; Riedel et al. 1999; Editors: Juleen R. Zierath, Michael J. Joyner, and John A. Hawley Additional Perspectives on The Biology of Exercise available at www.perspectivesinmedicine.org Copyright # 2017 Cold Spring Harbor Laboratory Press; all rights reserved Advanced Online Article. Cite this article as Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a029736 1 Downloaded from www.perspectivesinmedicine.org http://perspectivesinmedicine.cshlp.org/ C. Cooper et al. 2 Table 1. Exercise and neurological disorders across humans and animal model studies, with focus on the hippocampus Disease Humans Animals Hippocampus References Alzheimer’s Global cognition Learning and memory Ab load, APP Heyn et al. 2004; Adlard et al. 2005; disease Anxiety or $Tau AT 100 epitope Lautenschlager et al. 2008; Baker et al. 2010; Advanced Online Article. Cite this article as Sensorimotor function IL-1b, TNF-a Belarbi et al. 2011; Garcia-Mesa et al. 2011; Exploratory behavior LT P Liu et al. 2011; Rodrı´guez et al. 2011; Marlatt Neurogenesis et al. 2013; Zhao et al. 2015 Anxiety State anxiety Anxiety-like behaviors Glucocorticoid receptors Oldridge et al. 1991, 1995; Dishman 1997; Sleep quality Fear relapse BDNF Broocks et al. 1998; Russo-Neustadt et al. Corticosterone response Inhibitory interneuron 1999; Bandelow et al. 2000; Greenwood et al. Social avoidance behavior mechanisms (ventral 2003, 2008, 2013; Fulk et al. 2004; Broman- Learning impairments hippocampus) Fulks and Storey 2008; Smits et al. 2008; onSeptember26,2021-PublishedbyColdSpringHarborLaboratory Sympathetic nervous system Melanin-concentrating Carmeli et al. 2009; Wedekind et al. 2010; Press activation hormone Herring et al. 2011, 2015; Goldin et al. 2012; Improved diurnal rhythms Serotonin responsiveness Jazaieri et al. 2012; Goldin et al. 2013; to stressors Hovland et al. 2013; Schoenfeld et al. 2013; Cold Spring Harb Perspect Med Patki et al. 2014; Mika et al. 2015; Otsuka et al. 2015; Pan-Vazquez et al. 2015; Kim and Han 2016 Autism Stereotypic behavior Aggressive tendencies Neurogenesis Kern et al. 1982; Levinson and Reid 1993; Cognition and attention Spatial learning Reelin Rosenthal-Malek and Mitchell 1997; Prupas or $ Social–emotional Motor coordination and BDNF and Reid 2001; Bass et al. 2009; Pan 2010; functioning balance LT P Nicholson et al. 2011; Oriel et al. 2011; Rosenblatt et al. 2011; Bahrami et al. 2012; Gabriels et al. 2012; Kim et al. 2013; doi: 10.1101 Movahedi et al. 2013; Seo et al. 2013; Ward et al. 2013 Alcoholism Drinking days and heavy Alcohol preference and BDNF Sinyor et al. 1982; Crews et al. 2004; drinking days consumption Neurogenesis Vedamurthachar et al. 2006; Coiro et al. 2007; / cshperspect.a029736 Days abstinent Alcohol withdrawal score Brown et al. 2009, 2014b; Ehringer et al. 2009; and $ Depression, anxiety, Blood cortisol Klintsova et al. 2012; Motaghinejad et al. and abstinence self-efficacy 2014, 2015; Gallego et al. 2015 Blood cortisol and ACTH compared with controls Continued Downloaded from www.perspectivesinmedicine.org http://perspectivesinmedicine.cshlp.org/ Advanced Online Article. Cite this article as Table 1. Continued Disease Humans Animals Hippocampus References Dementia Balance Cognitive impairment Neurogenesis Van de Winckel et al. 2004; Christofoletti et al. Agitation/aggression/ BDNF 2008; Eggermont et al. 2009a,b; Conradsson disinhibition et al. 2010; Hwang and Choi 2010; Kemoun Apathy et al. 2010; Venturelli et al. 2011; Volkers and or $ Cognitive function Scherder 2011; Forbes et al. 2015; Telenius Ability to perform activities et al. 2015a,b; Choi et al. 2016 of daily living or $ Depressive symptoms onSeptember26,2021-PublishedbyColdSpringHarborLaboratory Cold Spring Harb Perspect Med Depression Depression symptoms Depressive symptoms ( Toll-like receptor 4 Craft and Landers 1998; Stathopoulou et al. Coping strategies immobility time in forced IL-1b and IL-18 2006; Daley 2008; Foley et al. 2008; Rethorst Press Episodic memory swim test; sucrose Neurogenesis et al. 2009; De Zeeuw et al. 2010; Forsman preference) VEGF, BDNF et al. 2011; Krogh et al. 2011; Kiuchi et al. $ 5-HT 2012; Cooney et al. 2013; Danielsson et al. Noradrenaline 2013; Lee et al. 2013; Silveira et al. 2013; Josefsson et al. 2014; Lu et al. 2014; Sadeghi et al. 2016a,b Epilepsy Seizure threshold Seizure frequency PVþ interneurons Gotze et al. 1967; Nakken et al. 1990; Eriksen doi: 10.1101 or $ Seizure frequency Seizure intensity CA1 hyper- et al. 1994; Arida et al. 1999; McAuley et al. EEG epileptiform Susceptibility to kindling and responsiveness 2001; Heise et al. 2002; Arida et al. 2004, On the Run for Hippocampal Plasticity discharges chemically induced seizures LT P 2007, 2008, 2009, 2010; Rambo et al. 2009; / Seizures during mental and Reiss et al. 2009; Tutkunet al. 2010; Eom et al. cshperspect.a029736 physical activity 2016 Comorbidities (depression, anxiety) Vigilance and attention Huntington’s Motor function (gait Corticostriatal connectivity Neurogenesis Pang et al. 2006; van Dellen et al. 2008; Cepeda disease speed and balance) and or Gait function and motor et al. 2010; Potter et al. 2010; Renoir et al. coordination coordination 2012; Busse et al. 2013; Harrison et al. 2013; Cognitive measures or Cognitive dysfunction Khalil et al. 2013; Kloos et al. 2013 Delays circadian dysfunction Continued 3 Downloaded from www.perspectivesinmedicine.org http://perspectivesinmedicine.cshlp.org/ C. Cooper et al. 4 Table 1. Continued Disease Humans Animals Hippocampus References Advanced Online Article. Cite this article as Multiple sclerosis $ or Moderately relapse Delay disease onset Le Page et al. 1994, 1996; Motl and Snook 2008; rates Demyelination Motl et al. 2008; Rossi et al. 2009; Motl and $ Markers of immune Duration of relapse Pilutti 2012; Patel and White 2013; Benson function Physical disability et al. 2015; Pryor et al. 2015; Alvarez- Physical disability $ or Inflammatory response Saavedra et al. 2016; Souza et al. 2016 progression Dendritic spine loss MRI brain lesion volumes Synaptic deficits Neuroperformance NGF, BDNF onSeptember26,2021-PublishedbyColdSpringHarborLaboratory (walking speed and Pain hypersensitivity Press endurance) Oxidative stress Parkinson’s disease Motor function (gait, Spatial