OBM Neurobiology is an international peer-reviewed Open Access journal published quarterly online by LIDSEN Publishing Inc. By design, the scope of OBM Neurobiology is broad, so as to reflect the multidisciplinary nature of the field of Neurobiology that interfaces biology with the fundamental and clinical neurosciences. As such, OBM Neurobiology embraces rigorous multidisciplinary investigations into the form and function of neurons and glia that make up the nervous system, either individually or in ensemble, in health or disease. OBM Neurobiology welcomes original contributions that employ a combination of molecular, cellular, systems and behavioral approaches to report novel neuroanatomical, neuropharmacological, neurophysiological and neurobehavioral findings related to the following aspects of the nervous system: Signal Transduction and Neurotransmission; Neural Circuits and Systems Neurobiology; Nervous System Development and Aging; Neurobiology of Nervous System Diseases (e.g., Developmental Brain Disorders; Neurodegenerative Disorders).

OBM Neurobiology publishes research articles, technical reports and invited topical reviews. Although the OBM Neurobiology Editorial Board encourages authors to be succinct, there is no restriction on the length of the papers. Authors should present their results in as much detail as possible, as reviewers are encouraged to emphasize scientific rigor and reproducibility.

Indexing: DOAJ-Directory of Open Access Journals.

Archiving: full-text archived in CLOCKSS.

Rapid publication: manuscripts are undertaken in 7 days from acceptance to publication (average values for papers published in this journal in the first half of 2019, 1-2 days of FREE language polishing time is also included in this period).

Free Publication in 2020
Current Issue: 2020  Archive: 2019 2018 2017
Open Access Review
The Effects of Exercise on Long-Term Potentiation: A Candidate Mechanism of the Exercise-Memory Relationship

Paul D. Loprinzi *

Exercise & Memory Laboratory, Department of Health, Exercise Science and Recreation Management, The University of Mississippi, University, MS 38677, USA

Correspondence: Paul D. Loprinzi

Academic Editor: Bart Ellenbroek

Received: March 30, 2019 | Accepted: May 08, 2019 | Published: May 10, 2019

OBM Neurobiology 2019, Volume 3, Issue 2, doi:10.21926/obm.neurobiol.1902026

Recommended citation: Loprinzi PD. The Effects of Exercise on Long-Term Potentiation: A Candidate Mechanism of the Exercise-Memory Relationship. OBM Neurobiology 2019;3(2):13; doi:10.21926/obm.neurobiol.1902026.

© 2019 by the authors. This is an open access article distributed under the conditions of the Creative Commons by Attribution License, which permits unrestricted use, distribution, and reproduction in any medium or format, provided the original work is correctly cited.


Objective: The objective of this paper was to evaluate the extent to which exercise may influence long-term potentiation (LTP), a key cellular correlate of episodic memory function.

Methods: Studies were identified using electronic databases, including PubMed, PsychInfo, Sports Discus and Google Scholar.

Results: The computerized searches revealed 20 articles meeting the study criteria. Among these 20 evaluated articles, 17 were conducted in an animal model and 3 among humans. All 17 of these studies, with the exception of one, provided evidence that exercise enhances LTP. Each of the three human studies demonstrated evidence that exercise was favorably associated with LTP or LTP-like mechanisms. In animal models, exercise reliability increases LTP and lowers the threshold for LTP induction.

Conclusion: Chronic exercise appears to robustly enhance LTP. The mechanisms of this effect are multifold and include, for example, exercise modulation of the structure and function of NMDA receptors.


Encoding; consolidation; NMDA

1. Introduction

Long-term potentiation (LTP) [1] is considered a cellular correlate of episodic memory function [2,3,4], involving an enhanced functional connectivity among neurons, characteristically shown by sustained excitatory post-synaptic potentiation (EPSP). Two factors that induce LTP are the frequency and intensity of the stimulation. The intensity of the stimulation increases the amplitude of the EPSP, whereas the frequency of the stimulation facilitates an additive effect on EPSP. In animal models, LTP is often induced via a three-step process, including 1) stimulating the axon (e.g., Schaffer collaterals) and then recording the post-synaptic EPSP, with the baseline period of axon stimulation occurring approximately once every 10-seconds, 2) a conditioning stimulus at a higher intensity to induce plasticity, and 3) re-stimulation of the axon followed by post-synaptic EPSP recording. If the post-conditioning EPSP in step 3 is greater than that recorded in step 1, then evidence of LTP is present. As noted below, LTP is largely dependent on kinase activation and protein synthesis.

In brief, LTP consists of an early (E-LTP) and late (L-LTP) phase, including non-protein synthesis and protein synthesis mechanisms, respectively. LTP-related mechanisms likely occur at both the pre- and post-synaptic neuron [5]. On the pre-synaptic neuron, related mechanisms may include, for example, increased neurotransmitter release, increase number of neurotransmitters in the vesicle, and increased probability of vesicle fusion. In E-LTP, pre-synaptic action potential increases Ca2+ (calcium) influx, facilitating vesicle docking. A neurotransmitter (e.g., glutamate) binds to an AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid) receptor, facilitating Na+ (sodium) influx and K+ (potassium) efflux, inducing cell depolarization. Ca2+ enters through NMDA (N-methyl-D-aspartate) via electrostatic repulsion, which phosphorylates AMPA receptors via protein kinases. Further, NMDA activation can facilitate membrane insertion of new AMPA receptors [6]. In L-LTP, cAMP (cyclic adenosine monophosphate)-dependent protein kinase and mitogen-activated protein kinase (MAPK) are activated, which upregulate transcription factors (e.g., CREB; cAMP response element binding protein) to facilitate synaptic plasticity by necessary synaptic proteins.

Recent work demonstrates that acute and chronic exercise may subserve episodic memory function [7,8,9,10,11,12,13,14,15,16]. Regarding acute exercise, the timing of the bout of exercise plays a critical role in influencing episodic memory performance [17]. Generally, when the acute bout of exercise occurs shortly before memory encoding or during memory consolidation, episodic memory is enhanced, whereas when it occurs during memory encoding, episodic memory is impaired. However, as detailed elsewhere, the intensity of exercise and the memory type may moderate these effects [18]. The potential mechanisms of this acute exercise effect are multifold [2,19,20], including, for example, exercise-induced LTP, via muscle spindle and vagus nerve activation, inducing hippocampal neuronal excitability. Chronic exercise, however, is likely to influence long-term memory function via structural and functional changes that are influenced by molecular and cellular mechanisms. For example, chronic exercise-induced molecular changes (e.g., increased brain-derived neurotrophic factor, vascular endothelial growth factor, and insulin-like growth factor) may alter cellular adaptations (e.g., gliogenesis, neurogenesis, synaptogenesis, and angiogenesis), which may influence episodic memory via structural and functional outcomes (e.g., increased white and grey matter, increased receptor and neural activity) [21]. These acute and chronic exercise-induced alterations may influence LTP, and in turn, enhance episodic memory function.

However, no reviews have specifically focused on the acute and chronic effects of exercise on LTP. Thus, the purpose of this brief review was to evaluate the extent to which exercise may induce LTP. This will provide insights on the potential underlying mechanisms through which exercise may influence episodic memory function. As stated, narrative reviews have suggested that LTP may mediate the effects of exercise on episodic memory, but to date, no systematic review has evaluated this possibility.

2. Methods

Studies were identified using electronic databases, including PubMed, PsychInfo, Sports Discus and Google Scholar. Computerized searches were conducted from inception to February, 2019. The search terms included: exercise, physical activity, running, LTP, and long-term potentiation (and their combinations). For example, “exercise AND LTP”, “physical activity AND LTP”, “running AND LTP”, and “exercise AND long-term potentiation.”

To be eligible for inclusion in this review, studies had to:

  • Be published in English.
  • Include a measure of exercise as the independent variable.
  • Directly measure LTP or LTP-like mechanisms (e.g., measured EPSP or a stimulus-induced event-related potential).

3. Results

The computerized searches revealed 252 unique articles. The title and abstract of each of these articles were reviewed. Among these 252 articles, 25 appeared to meet the study criteria. The full-text of these 25 articles were retrieved and read in full. Among these, 20 articles met the study criteria listed above. Among these 20 evaluated articles, 17 were conducted in an animal model and 3 among humans.

Table 1 displays the results for the 17 animal studies. The animal experiments included varied exercise protocols, ranging from an acute bout of walking to up to 4-months of voluntary running. The LTP induction protocol also varied, including, for example, low-frequency stimulation protocols, single high-frequency stimulations, and multiple high-frequency stimulations. All 17 of these studies, with the exception of one [22], provided some evidence that exercise enhanced LTP.

Table 2 displays the results for the 3 human studies. All 3 studies employed young adult samples. One study employed an exhaustive bout of acute exercise [23]; another employed a high-intensity 20-minute cycling session [24]; and another stratified participants into being active or inactive based on self-report [25]. Two of these studies employed a paired associate stimulation protocol [23,24], with the other utilizing a visual stimuli to induce visual cortex LTP [25]. Each of these three studies demonstrated evidence to suggest that exercise was favorably associated with LTP-like mechanisms.

Table 1 Extraction table of the evaluated studies among animals.

Table 2 Extraction table of the evaluated studies among humans.

4. Discussion

4.1 Overall Summary

Emerging research suggests that exercise (both acute and chronic) can subserve memory function [2,5]. Long-term potentiation (LTP) is considered a cellular correlate of episodic memory function [42]. No reviews, to date, have evaluated the extent to which exercise may enhance LTP. All of this served as the motivation for the present review, which was to evaluate the extent to which exercise is associated with LTP. The main finding from this brief review was that there is consistent evidence in animal models demonstrating that chronic exercise may enhance LTP, with some evidence, among humans, to suggest that acute exercise may enhance LTP. Notably, the exercise protocol for these chronic training studies varied considerably (e.g., 6 days to 6-weeks of exercise; walking, running, and swimming protocols). Despite the variability in the exercise paradigm, there were consistent findings, demonstrating a robust effect of exercise on LTP in animal models. The human findings also support these results, but additional work in this area among humans is needed. Specifically, additional work in humans is needed to evaluate whether exercise duration (e.g., acute vs. chronic) has a differential effect on LTP. In totality, despite the variation in exercise protocols in the animal studies (e.g., 6 days to 6-weeks of exercise; walking, running, and swimming protocols) and human studies (e.g., acute bout of exercise, or using habitual exercise patterns to classify individuals as active or inactive), across both populations, there was consistent evidence of an exercise-induced LTP effect. This, ultimately, suggests that exercise robustly influences LTP. The narrative that follows will highlight key observations from the evaluated studies, for both the animal and human studies, as well as discuss candidate mechanisms through which exercise may enhance LTP.

4.2 Non-Human Studies

A key observation of the evaluated animal studies was that exercise, either before or during LTP induction, enhanced LTP. A likely mechanism explaining this observation is through exercise-induced alterations in NMDA structure and function. Dietrich et al. [43] reported that the level of phosphorylation of NR1 and NR2 subunits of the rat cerebral cortex NMDA receptor was increased with voluntary wheel running for one month. Further, the NMDA receptor channel open rate was increased with running. Molteni et al. [44] also showed that voluntary wheel running increased the expression of NR1, NR2A, and NR2B mRNA in the rat hippocampus after 3 and 7 days of running. Importantly, exercise-induced NMDA receptor expression increases not only in the hippocampus, but in the prefrontal cortex as well [45], which is an important brain structure involved in memory function [46].

Exercise has been shown to increase BDNF levels [20] and BNDF (brain-derived neurotrophic factor) may help upregulate the expression and function of the NMDA receptor [47,48,49]. BDNF also buffers against depotentiation [50]. Downstream of the BDNF/TrkB (Tropomyosin receptor kinase B) signaling pathway, PI3K-AKT activation is thought to contribute to the maintenance of LTP via NMDAR activity [51]. That is, substrates of AKT (e.g., girdin; actin-binding protein) may interact with kinases and NMDA subunits, leading to phosphorylation of NMDA receptors. Importantly, physical exercise has been shown to alter the kinetics of TrkB phosphorylation induced by exogenous BDNF, with sustained TrkB signaling acting as a key mechanism underlying the synergistic effects of neuronal activity and BDNF [52]. Neurogenesis may also be a mechanism through which chronic exercise may increase LTP, as newly generated neurons can be more easily activated and more readily to produce LTP [53]. Relatedly, exercise-related, BDNF-induced neurogenesis influences synaptic development, and in turn, likely plays an important role in LTP production. Other candidate mechanisms include exercise-related alterations in cholinergic activity [27], mineralocorticoid/glucocorticoid receptor expression [29], cAMP signaling [37], and inflammatory cytokines [38].

In addition to exercise subserving LTP via NMDA-related mechanisms, exercise may maintain this beneficial effect even in the presence of a neuronal insult. For example, from various determinants, such as epilepsy or sleep deprivation, exercise has been shown to revert the reduced CA1 (Cornu Ammonis-1) LTP [54,55]. Similarly, when exercise and stress occurs concurrently, exercise is able to combat the stress so that the dorsal hippocampus can experience normal levels of LTP [40]. Additionally, in Alzheimer’s disease (AD) models, Aβ impairs CREB phosphorylation, and this impairment is prevented by regular exercise, which also relieves the AD-induced suppression of BDNF [35]. Relatedly, exercise has been shown to increase LTP across the entire lifespan, including aging populations [41].

Although the current evidence suggests that acute and chronic exercise can enhance LTP, exercise withdrawal may reverse the exercise-LTP beneficial effects [36]. Further, extremely high levels of exercise or exhaustive exercise has not been shown to enhance LTP among mice, which is thought to occur from the reduction of NMDA/AMPA levels, which may lead to less Ca2+ influx [22]. However, this finding has not been replicated in humans, as in young adult humans, a maximal bout of acute exercise has been shown to enhance LTP-like neuroplasticity and promote implicit motor learning [23].

4.3 Human Studies

Three human studies evaluated the effects of exercise on LTP [23,24,25], two of which employed an acute bout of exercise, whereas one study evaluated whether LTP was different among active and inactive individuals [25]. Mang et al. [23] employed an exhaustive exercise test on a cycle ergometer and induced LTP via transcranial magnetic stimulation (TMS). Exercise prior to the TMS showed greater paired associate stimulation (PAS) when compared to a non-exercise stimulus. Relatedly, in a similar young adult population, Singh et al. [24] showed that PAS-induced increases in motor cortical excitability were enhanced when a 20-min cycle session occurred before the stimulation. Lastly, Smallwood et al. [25] showed that, among young adults, visually-evoked (later phase) LTP-like responses in the occipital cortex where higher in habitually active individuals when compared to their less active counterparts. Specifically, the active group demonstrated a greater increase in the amplitude of the N1b following tetanus.

4.4 Limitations

Limitations of this review include the use of a single author to screen and retrieve articles for this review. Thus, not all aspects of a systematic review were able to be adhered to. Further, given the heterogeneity in the study designs, I did not employ a meta-analysis. Such limitations should be considered when interpreting the findings from this review as well as inform future reviews on this topic.

5. Conclusion

In conclusion, this brief review demonstrates that, in animal models, exercise reliability increases LTP and lowers the threshold for LTP induction. The mechanisms of this effect are multifold and include, for example, exercise modulation of the function of NMDA receptors. Additional creative work in humans is needed to continue to evaluate the extent to which exercise may subserve LTP in adults. Such work should continue to investigate both acute and chronic exercise paradigms. Acute exercise studies should evaluate whether there is an exercise intensity-dependent effect on LTP and whether certain molecular proteins (e.g., BDNF) mediate this effect.


I declare no conflicts of interest and no funding was used to prepare this manuscript.

Author Contributions

The author did all the research work of this study.


  1. Bliss TV, Gardner-Medwin AR. Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol. 1973; 232: 357-374. [CrossRef]
  2. Loprinzi PD, Edwards MK, Frith E. Potential avenues for exercise to activate episodic memory-related pathways: A narrative review. Eur J Neurosci. 2017; 46: 2067-2077. [CrossRef]
  3. Panja D, Bramham CR. Bdnf mechanisms in late ltp formation: A synthesis and breakdown. Neuropharmacology. 2014; 76 Pt C: 664-676. [CrossRef]
  4. McGaugh JL. Memory--a century of consolidation. Science. 2000; 287: 248-251. [CrossRef]
  5. Loprinzi PD, Ponce P, Frith E. Hypothesized mechanisms through which acute exercise influences episodic memory. Physiol Int. 2018; 105: 285-297. [CrossRef]
  6. Lu W, Man H, Ju W, Trimble WS, MacDonald JF, Wang YT. Activation of synaptic nmda receptors induces membrane insertion of new ampa receptors and ltp in cultured hippocampal neurons. Neuron. 2001; 29: 243-254. [CrossRef]
  7. 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. 2018; 32: 691-704. [CrossRef]
  8. Loprinzi PD, Frith E. The role of sex in memory function: Considerations and recommendations in the context of exercise. J Clin Med. 2018; 7. [CrossRef]
  9. Loprinzi PD, Herod SM, Cardinal BJ, Noakes TD. Physical activity and the brain: A review of this dynamic, bi-directional relationship. Brain Res. 2013; 1539: 95-104. [CrossRef]
  10. Ponce P, Loprinzi PD. A bi-directional model of exercise and episodic memory function. Med Hypotheses. 2018; 117: 3-6. [CrossRef]
  11. 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. 2017; 46: 2557-2564. [CrossRef]
  12. Frith E, Sng E, Loprinzi PD. Randomized controlled trial considering varied exercises for reducing proactive memory interference. J Clin Med. 2018; 7. [CrossRef]
  13. Haynes IV J, Frith E, Loprinzi PD. The experimental effects of acute exercise on episodic memory function: Considerations for the timing of exercise. Psychol Rep. 2018. [CrossRef]
  14. Siddiqui A, Loprinzi PD. Experimental investigation of the time course effects of acute exercise on false episodic memory. J Clin Med. 2018; 7. [CrossRef]
  15. Sng E, Frith E, Loprinzi PD. Experimental effects of acute exercise on episodic memory acquisition: Decomposition of multi-trial gains and losses. Physiol Behav. 2018; 186: 82-84. [CrossRef]
  16. Yanes D, Loprinzi PD. Experimental effects of acute exercise on iconic memory, short-term episodic, and long-term episodic memory. J Clin Med. 2018; 7. [CrossRef]
  17. Loprinzi PD, Blough J, Crawford L, Ryu S, Zou L, Li H. The temporal effects of acute exercise on episodic memory function: Systematic review with meta-analysis. Brain Sci. 2019; 9: 87. [CrossRef]
  18. Loprinzi PD. Intensity-specific effects of acute exercise on human memory function: Considerations for the timing of exercise and the type of memory. Health Promot Perspect. 2018; 8: 255-262. [CrossRef]
  19. Loprinzi PD. Igf-1 in exercise-induced enhancement of episodic memory. Acta Physiol (Oxf). 2018: e13154. [CrossRef]
  20. Loprinzi PD, Frith E. A brief primer on the mediational role of bdnf in the exercise-memory link. Clin Physiol Funct Imaging. 2018. [CrossRef]
  21. El-Sayes J, Harasym D, Turco CV, Locke MB, Nelson AJ. Exercise-induced neuroplasticity: A mechanistic model and prospects for promoting plasticity. Neuroscientist. 2019; 25: 65-85. [CrossRef]
  22. Ma J, Chen H, Liu X, Zhang L, Qiao D. Exercise-induced fatigue impairs bidirectional corticostriatal synaptic plasticity. Front Cell Neurosci. 2018; 12: 14. [CrossRef]
  23. Mang CS, Snow NJ, Campbell KL, Ross CJ, Boyd LA. A single bout of high-intensity aerobic exercise facilitates response to paired associative stimulation and promotes sequence-specific implicit motor learning. J Appl Physiol (1985). 2014; 117: 1325-1336. [CrossRef]
  24. Singh AM, Neva JL, Staines WR. Acute exercise enhances the response to paired associative stimulation-induced plasticity in the primary motor cortex. Exp Brain Res. 2014; 232: 3675-3685. [CrossRef]
  25. Smallwood N, Spriggs MJ, Thompson CS, Wu CC, Hamm JP, Moreau D, et al. Influence of physical activity on human sensory long-term potentiation. J Int Neuropsych Soc. 2015; 21: 831-840. [CrossRef]
  26. van Praag H, Christie BR, Sejnowski TJ, Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. P Natl Acad Sci USA. 1999; 96: 13427-13431. [CrossRef]
  27. Leung LS, Shen B, Rajakumar N, Ma J. Cholinergic activity enhances hippocampal long-term potentiation in ca1 during walking in rats. J Neurosci. 2003; 23: 9297-9304. [CrossRef]
  28. Farmer J, Zhao X, van Praag H, Wodtke K, Gage FH, Christie BR. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male sprague-dawley rats in vivo. Neuroscience. 2004; 124: 71-79. [CrossRef]
  29. Ahmed T, Frey JU, Korz V. Long-term effects of brief acute stress on cellular signaling and hippocampal ltp. J Neurosci. 2006; 26: 3951-3958. [CrossRef]
  30. O'Callaghan RM, Ohle R, Kelly AM. The effects of forced exercise on hippocampal plasticity in the rat: A comparison of ltp, spatial- and non-spatial learning. Behav Brain Res. 2007; 176: 362-366. [CrossRef]
  31. Vasuta C, Caunt C, James R, Samadi S, Schibuk E, Kannangara T, et al. Effects of exercise on nmda receptor subunit contributions to bidirectional synaptic plasticity in the mouse dentate gyrus. Hippocampus. 2007; 17: 1201-1208. [CrossRef]
  32. Patten AR, Sickmann H, Hryciw BN, Kucharsky T, Parton R, Kernick A, et al. Long-term exercise is needed to enhance synaptic plasticity in the hippocampus. Learn Memory. 2013; 20: 642-647. [CrossRef]
  33. Yu Q, Li X, Wang J, Li Y. Effect of exercise training on long-term potentiation and nmda receptor channels in rats with cerebral infarction. Exp Ther Med. 2013; 6: 1431-1436. [CrossRef]
  34. Miladi-Gorji H, Rashidy-Pour A, Fathollahi Y, Semnanian S, Jadidi M. Effects of voluntary exercise on hippocampal long-term potentiation in morphine-dependent rats. Neuroscience. 2014; 256: 83-90. [CrossRef]
  35. Dao AT, Zagaar MA, Levine AT, Alkadhi KA. Comparison of the effect of exercise on late-phase ltp of the dentate gyrus and ca1 of alzheimer's disease model. Mol Neurobiol. 2016; 53: 6859-6868. [CrossRef]
  36. Radahmadi M, Hosseini N, Alaei H. Effect of exercise, exercise withdrawal, and continued regular exercise on excitability and long-term potentiation in the dentate gyrus of hippocampus. Brain Res. 2016; 1653: 8-13. [CrossRef]
  37. Zheng F, Zhang M, Ding Q, Sethna F, Yan L, Moon C, et al. Voluntary running depreciates the requirement of ca2+-stimulated camp signaling in synaptic potentiation and memory formation. Learn Mem. 2016; 23: 442-449. [CrossRef]
  38. D'Arcangelo G, Triossi T, Buglione A, Melchiorri G, Tancredi V. Modulation of synaptic plasticity by short-term aerobic exercise in adult mice. Behav Brain Res. 2017; 332: 59-63. [CrossRef]
  39. Cheng M, Cong J, Wu Y, Xie J, Wang S, Zhao Y, et al. Chronic swimming exercise ameliorates low-soybean-oil diet-induced spatial memory impairment by enhancing bdnf-mediated synaptic potentiation in developing spontaneously hypertensive rats. Neurochem Res. 2018; 43: 1047-1057. [CrossRef]
  40. Miller RM, Marriott D, Trotter J, Hammond T, Lyman D, Call T, et al. Running exercise mitigates the negative consequences of chronic stress on dorsal hippocampal long-term potentiation in male mice. Neurobiol Learn Mem. 2018; 149: 28-38. [CrossRef]
  41. Tsai SF, Ku NW, Wang TF, Yang YH, Shih YH, Wu SY, et al. Long-term moderate exercise rescues age-related decline in hippocampal neuronal complexity and memory. Gerontology. 2018: 1-11. [CrossRef]
  42. Poo MM, Pignatelli M, Ryan TJ, Tonegawa S, Bonhoeffer T, Martin KC, et al. What is memory? The present state of the engram. BMC Biol. 2016; 14: 40. [CrossRef]
  43. Dietrich MO, Mantese CE, Porciuncula LO, Ghisleni G, Vinade L, Souza DO, et al. Exercise affects glutamate receptors in postsynaptic densities from cortical mice brain. Brain Res. 2005; 1065: 20-25. [CrossRef]
  44. Molteni R, Ying Z, Gomez-Pinilla F. Differential effects of acute and chronic exercise on plasticity-related genes in the rat hippocampus revealed by microarray. Eur J Neurosci. 2002; 16: 1107-1116. [CrossRef]
  45. Park JK, Lee SJ, Kim TW. Treadmill exercise enhances nmda receptor expression in schizophrenia mice. J Exerc Rehabil. 2014; 10: 15-21. [CrossRef]
  46. Preston AR, Eichenbaum H. Interplay of hippocampus and prefrontal cortex in memory. Current biology : CB. 2013; 23: R764-773. [CrossRef]
  47. Clarke RJ, Johnson JW. Voltage-dependent gating of nr1/2b nmda receptors. J Physiol. 2008; 586: 5727-5741. [CrossRef]
  48. Caldeira MV, Melo CV, Pereira DB, Carvalho RF, Carvalho AL, Duarte CB. Bdnf regulates the expression and traffic of nmda receptors in cultured hippocampal neurons. Mol Cell Neurosci. 2007; 35: 208-219. [CrossRef]
  49. Kim JH, Roberts DS, Hu Y, Lau GC, Brooks-Kayal AR, Farb DH, et al. Brain-derived neurotrophic factor uses creb and egr3 to regulate nmda receptor levels in cortical neurons. J Neurochem. 2012; 120: 210-219. [CrossRef]
  50. Radecki DT, Brown LM, Martinez J, Teyler TJ. Bdnf protects against stress-induced impairments in spatial learning and memory and ltp. Hippocampus. 2005; 15: 246-253. [CrossRef]
  51. Nakai T, Nagai T, Tanaka M, Itoh N, Asai N, Enomoto A, et al. Girdin phosphorylation is crucial for synaptic plasticity and memory: A potential role in the interaction of bdnf/trkb/akt signaling with nmda receptor. J Neurosci. 2014; 34: 14995-15008. [CrossRef]
  52. Guo W, Ji Y, Wang S, Sun Y, Lu B. Neuronal activity alters bdnf-trkb signaling kinetics and downstream functions. J Cell Sci. 2014; 127: 2249-2260. [CrossRef]
  53. Trivino-Paredes J, Patten AR, Gil-Mohapel J, Christie BR. The effects of hormones and physical exercise on hippocampal structural plasticity. Front Neuroendocrin. 2016; 41: 23-43. [CrossRef]
  54. Arida RM, Sanabria ER, da Silva AC, Faria LC, Scorza FA, Cavalheiro EA. Physical training reverts hippocampal electrophysiological changes in rats submitted to the pilocarpine model of epilepsy. Physiol Behav. 2004; 83: 165-171. [CrossRef]
  55. Zagaar M, Dao A, Levine A, Alhaider I, Alkadhi K. Regular exercise prevents sleep deprivation associated impairment of long-term memory and synaptic plasticity in the ca1 area of the hippocampus. Sleep. 2013; 36: 751-761. [CrossRef]
Download PDF
0 0