Effects of repeated voluntary or forced exercise on brainstem serotonergic systems in rats

Arnold, Mathew R.; Greenwood, Benjamin N.; McArthur, J.A.; Clark, Peter; Fleshner, Monika; Lowry, Christopher A.

doi:10.1016/j.bbr.2019.112237

Cited by 10 publications

(7 citation statements)

References 101 publications

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“…Increasing evidences show that exercise can improve depression, anxiety, cognitive disorder, and locomotion impairment by affecting the serotonergic system (Otsuka et al, 2016 ; Ji et al, 2017 ; Arnold et al, 2020 ). Using c-Fos (a marker of acute cellular activation), Otsuka et al ( 2016 ) reported that a 30-min treadmill exercise at low speed (15 m/min) significantly enhanced the activation of 5-HT neurons in the DRN and effectively induced antidepressant/anti-anxiety properties.…”

Section: Discussionmentioning

confidence: 99%

“…Several possible reasons could account for this different observation, including the difference in animal models, the intensity and duration of exercise protocol, and the preparation for cell recording. Arnold et al found that 6-week forced exercise increased FosB/ΔFosB, a chronic 5-HT neuron activation marker, expression in 5-HT neurons of rats (Arnold et al, 2020 ). Alternatively, compared with the sedentary control group, 3-week exercise training could facilitate 5-HT neuron excitability by affecting mood or motivation.…”

Section: Discussionmentioning

confidence: 99%

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Three-Week Treadmill Exercise Enhances Persistent Inward Currents, Facilitates Dendritic Plasticity, and Upregulates the Excitability of Dorsal Raphe Serotonin Neurons in ePet-EYFP Mice

Dai

2020

Front. Cell. Neurosci.

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Exercise plays a key role in preventing or treating mental or motor disorders caused by dysfunction of the serotonergic system. However, the electrophysiological and ionic channel mechanisms underlying these effects remain unclear. In this study, we investigated the effects of 3-week treadmill exercise on the electrophysiological and channel properties of dorsal raphe nucleus (DRN). Serotonin (5-HT) neurons in ePet-EYFP mice, using whole-cell patch clamp recording. Treadmill exercise was induced in ePet-EYFP mice of P21-24 for 3 weeks, and whole-cell patch clamp recording was performed on EYFP-positive 5-HT neurons from DRN slices of P42-45 mice. Experiment data showed that 5-HT neurons in the DRN were a heterogeneous population with multiple firing patterns (single firing, phasic firing, and tonic firing). Persistent inward currents (PICs) with multiple patterns were expressed in 5-HT neurons and composed of Cav1.3 (Ca-PIC) and sodium (Na-PIC) components. Exercise hyperpolarized the voltage threshold for action potential (AP) by 3.1 ± 1.0 mV (control: n = 14, exercise: n = 18, p = 0.005) and increased the AP amplitude by 6.7 ± 3.0 mV (p = 0.031) and firing frequency by more than 22% especially within a range of current stimulation stronger than 70 pA. A 3-week treadmill exercise was sufficient to hyperpolarize PIC onset by 2.6 ± 1.3 mV (control: −53.4 ± 4.7 mV, n = 28; exercise: −56.0 ± 4.7 mV, n = 25, p = 0.050) and increase the PIC amplitude by 28% (control: 193.6 ± 81.8 pA; exercise: 248.5 ± 105.4 pA, p = 0.038). Furthermore, exercise hyperpolarized Na-PIC onset by 3.8 ± 1.8 mV (control: n = 8, exercise: n = 9, p = 0.049) and increased the Ca-PIC amplitude by 23% (p = 0.013). The exercise-induced enhancement of the PIC amplitude was mainly

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Three-Week Treadmill Exercise Enhances Persistent Inward Currents, Facilitates Dendritic Plasticity, and Upregulates the Excitability of Dorsal Raphe Serotonin Neurons in ePet-EYFP Mice

Dai

2020

Front. Cell. Neurosci.

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“…Perhaps the most unexpected outcome of this study was that physical activity status failed to robustly influence monoamine-related neurochemical responses to ethanol ingestion. This outcome was surprising because running can potently modulate monoaminergic activity and receptor plasticity throughout limbic and reward structures, which in turn can alter monoamine responses during distinct events, like exposure to stress or some drugs of abuse (Foley and Fleshner, 2008 ; Lin and Kuo, 2013 ; Clark et al, 2015 ; Arnold et al, 2020 ; Katsidoni et al, 2020 ). One possibility is that the relatively mild influence that alcohol ingestion had on monoamine and metabolite concentrations could have limited the ability to detect neurochemical changes that were further influenced by physical activity in this study.…”

Section: Discussionmentioning

confidence: 99%

The Influence of Moderate Physical Activity on Brain Monoaminergic Responses to Binge-Patterned Alcohol Ingestion in Female Mice

Buhr

Reed

Shoeman

et al. 2021

Front. Behav. Neurosci.

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Monoamine neurotransmitter activity in brain reward, limbic, and motor areas play key roles in the motivation to misuse alcohol and can become modified by exercise in a manner that may affect alcohol craving. This study investigated the influence of daily moderate physical activity on monoamine-related neurochemical concentrations across the mouse brain in response to high volume ethanol ingestion. Adult female C57BL/6J mice were housed with or without 2.5 h of daily access to running wheels for 30 days. On the last 5 days, mice participated in the voluntary binge-like ethanol drinking procedure, “Drinking in the dark” (DID). Mice were sampled immediately following the final episode of DID. Monoamine-related neurochemical concentrations were measured across brain regions comprising reward, limbic, and motor circuits using ultra High-Performance Liquid Chromatography (UHPLC). The results suggest that physical activity status did not influence ethanol ingestion during DID. Moreover, daily running wheel access only mildly influenced alcohol-related norepinephrine concentrations in the hypothalamus and prefrontal cortex, as well as serotonin turnover in the hippocampus. However, access to alcohol during DID eliminated wheel running-related decreases of norepinephrine, serotonin, and 5-HIAA content in the hypothalamus, but also to a lesser extent for norepinephrine in the hippocampus and caudal cortical areas. Finally, alcohol access increased serotonin and dopamine-related neurochemical turnover in the striatum and brainstem areas, regardless of physical activity status. Together, these data provide a relatively thorough assessment of monoamine-related neurochemical levels across the brain in response to voluntary binge-patterned ethanol drinking, but also adds to a growing body of research questioning the utility of moderate physical activity as an intervention to curb alcohol abuse.

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“…Supplementary File 2 describes a summary of the rodent model and the exercise program used in each study included in this review. Rats were the rodents used in 75.9% (41/54) of the studies ( 18 , 41 – 80 ), and mice in 24.1% (13/54) ( 81 – 93 ). In rats, the most frequent strain was Sprague-Dawley (22/54) ( 18 , 43 , 46 – 49 , 51 – 55 , 61 , 64 – 67 , 70 , 71 , 76 , 77 , 79 , 80 ), followed by Wistar (10/54) ( 44 , 45 , 57 – 60 , 63 , 68 , 69 , 73 ).…”

Section: Resultsmentioning

confidence: 99%

“…In mice, the most frequent strain was C57BL/6J (10/54) ( 81 , 82 , 84 – 89 , 92 , 93 ) and BALB/c (2/54) ( 83 , 90 ) in second place. Most of the studies used healthy animals (22/54) ( 18 , 41 , 44 , 48 , 49 , 53 , 56 , 57 , 59 , 60 , 68 , 69 , 72 – 75 , 78 , 82 , 84 , 85 , 92 ), followed by stroke models (5/54) ( 45 , 64 , 79 , 88 , 89 ). Relative to exercise frequency, 5 days per week was the most common weekly frequency and 1 session per day was the most common daily frequency.…”

Section: Resultsmentioning

confidence: 99%

A Handful of Details to Ensure the Experimental Reproducibility on the FORCED Running Wheel in Rodents: A Systematic Review

et al. 2021

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A well-documented method and experimental design are essential to ensure the reproducibility and reliability in animal research. Experimental studies using exercise programs in animal models have experienced an exponential increase in the last decades. Complete reporting of forced wheel and treadmill exercise protocols would help to ensure the reproducibility of training programs. However, forced exercise programs are characterized by a poorly detailed methodology. Also, current guidelines do not cover the minimum data that must be included in published works to reproduce training programs. For this reason, we have carried out a systematic review to determine the reproducibility of training programs and experimental designs of published research in rodents using a forced wheel system. Having determined that most of the studies were not detailed enough to be reproducible, we have suggested guidelines for animal research using FORCED exercise wheels, which could also be applicable to any form of forced exercise.

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Effects of repeated voluntary or forced exercise on brainstem serotonergic systems in rats

Cited by 10 publications

References 101 publications

Three-Week Treadmill Exercise Enhances Persistent Inward Currents, Facilitates Dendritic Plasticity, and Upregulates the Excitability of Dorsal Raphe Serotonin Neurons in ePet-EYFP Mice

Three-Week Treadmill Exercise Enhances Persistent Inward Currents, Facilitates Dendritic Plasticity, and Upregulates the Excitability of Dorsal Raphe Serotonin Neurons in ePet-EYFP Mice

The Influence of Moderate Physical Activity on Brain Monoaminergic Responses to Binge-Patterned Alcohol Ingestion in Female Mice

A Handful of Details to Ensure the Experimental Reproducibility on the FORCED Running Wheel in Rodents: A Systematic Review

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