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The effect of monoamines reuptake inhibitors on aerobic exercise performance in bank voles from a selection experiment.

ABSTRACT: Exercise performance depends on both physiological abilities (e.g., muscle strength) and behavioral characteristics (e.g., motivation). We tested the hypothesis that evolution of increased aerobic exercise performance can be facilitated by evolution of neuropsychological mechanisms responsible for motivation to undertake physical activity. We used a unique model system: lines of bank voles Myodes glareolus selected for high swim-induced aerobic metabolism ("aerobic" A lines). In generation 21, voles from the 4 A lines achieved a 57% higher "voluntary maximum" swim-induced aerobic metabolism (VO₂swim) than voles from 4 unselected, "control" C lines. In C lines, VO₂swim was 9% lower than the maximum forced-exercise aerobic metabolism (VO₂run; P?=?0.007), while in A lines it was even higher than VO₂run, although not significantly (4%, P?=?0.15). Thus, we hypothesized that selection changed both the aerobic capacity and the neuronal mechanisms behind motivation to undertake activity. We investigated the influence of reuptake inhibitors of dopamine (DARI), serotonin (SSRI), and norepinephrine (NERI) on VO₂swim. The drugs decreased VO₂swim both in C and A lines (% decrease compared with saline: DARI 8%, P?0.001; SSRI 6%, P?0.001; NERI 8%, P?0.001), but the proportional response differed between selection directions only for NERI (stronger effect in C lines: P?=?0.008) and the difference was marginally non-significant for SSRI (P?=?0.07) and DARI (P?=?0.06). Thus, the results suggest that all the 3 monoamines are involved in signaling pathways controlling the motivation to be active and that norepinephrine could have played a role in the evolution of increased aerobic exercise performance in our animal model.

SUBMITTER: Jaromin E

PROVIDER: S-EPMC6688583 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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The effect of monoamines reuptake inhibitors on aerobic exercise performance in bank voles from a selection experiment.

Jaromin Ewa E Sadowska Edyta T ET Koteja Paweł P

Current zoology 20180808 4

Exercise performance depends on both physiological abilities (e.g., muscle strength) and behavioral characteristics (e.g., motivation). We tested the hypothesis that evolution of increased aerobic exercise performance can be facilitated by evolution of neuropsychological mechanisms responsible for motivation to undertake physical activity. We used a unique model system: lines of bank voles <i>Myodes glareolus</i> selected for high swim-induced aerobic metabolism ("aerobic" A lines). In generatio ...[more]

PMID: 31413714

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Project description:The level of physical activity achieved in a given situation depends on both physiological abilities and behavioral characteristics (motivation). We used a unique animal model to test a hypothesis that evolution of an increased aerobic exercise performance can be facilitated by evolution of motivation to undertake physical activity, mediated by brain endocannabinoid system. Bank voles (Myodes glareolus) from "aerobic" A lines selected for 22 generations for high swim-induced aerobic metabolism (VO2swim) achieved 65% higher "voluntary maximum" VO2swim than voles from unselected, "control" C lines. In C lines, VO2swim was 24% lower than the maximum forced-running aerobic metabolism (VO2run), while in A lines VO2swim and VO2run were practically the same. Thus, the selection changed both the aerobic capacity and motivation to exercise at the top performance level. We applied a pharmacological treatment manipulation to test a hypothesis that the endocannabinoid signaling pathway 1) affects the voles performance in the aerobic exercise trials, and 2) has been modified in the selection process. Administration of the CB1 receptor antagonist (Rimonabant) did not affect the level of metabolism, but administration of the endocannabinoid reuptake inhibitor (AM404) decreased VO2swim both in A and C lines (4%, p = 0.03) and tended to decrease VO2run (2%, p = 0.07). The significant effect of AM404 suggests the involvement of endocannabinoids in signaling pathways controlling the motivation to be active. However, the response to AM404 did not differ between A and C lines (interaction effect, p ≥ 0.29). Thus, the results did not provide a support to the hypothesis that modifications of endocannabinoid signaling have played a role in the evolution of increased aerobic exercise performance in our experimental evolution model system.Summary statementThe results corroborated involvement of endocannabinoids in the regulation of physical activity, but did not support the hypothesis that modification of endocannabinoid signaling played a role in the evolution of increased aerobic exercise performance in our experimental evolution model.

Project description:As with many physiological performance traits, the capacity of endotherms to thermoregulate declines with age. Aging compromises both the capacity to conserve or dissipate heat and the thermogenesis, which is fueled by aerobic metabolism. The rate of metabolism, however, not only determines thermogenic capacity but can also affect the process of aging. Therefore, we hypothesized that selection for an increased aerobic exercise metabolism, which has presumably been a crucial factor in the evolution of endothermic physiology in the mammalian and avian lineages, affects not only the thermoregulatory traits but also the age-related changes of these traits. Here, we test this hypothesis on bank voles (Myodes glareolus) from an experimental evolution model system: four lines selected for high swim-induced aerobic metabolism (A lines), which have also increased the basal, average daily, and maximum cold-induced metabolic rates, and four unselected control (C) lines. We measured the resting metabolic rate (RMR), evaporative water loss (EWL), and body temperature in 72 young adult (4 months) and 65 old (22 months) voles at seven ambient temperatures (13-32°C). The RMR was 6% higher in the A than in the C lines, but, regardless of the selection group or temperature, it did not change with age. However, EWL was 12% higher in the old voles. An increased EWL/RMR ratio implies either a compromised efficiency of oxygen extraction in the lungs or increased skin permeability. This effect was more profound in the A lines, which may indicate their increased vulnerability to aging. Body temperature did not differ between the selection and age groups below 32°C, but at 32°C it was markedly higher in the old A-line voles than in those from other groups. As expected, the thermogenic capacity, measured as the maximum cold-induced oxygen consumption, was decreased by about 13% in the old voles from both selection groups, but the performance of old A-line voles was the same as that of the young C-line ones. Thus, the selection for high aerobic exercise metabolism attenuated the adverse effects of aging on cold tolerance, but this advantage has been traded off by a compromised coping with hot conditions by aged voles.

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The effect of monoamines reuptake inhibitors on aerobic exercise performance in bank voles from a selection experiment.

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The effect of monoamines reuptake inhibitors on aerobic exercise performance in bank voles from a selection experiment.

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