Role of astrocytes in rhythmic motor activity

Montalant, Alexia; Carlsen, Eva Meier; Perrier, Jean-Françóis

doi:10.14814/phy2.15029

Cited by 13 publications

(9 citation statements)

References 53 publications

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“…As both hypoxia and hypercapnia modulate activities of breathing CPG, the functional role of astrocyte critically depends on the local circuit that they modulate (i.e., RTN or preBötC circuits). This diverse circuit-specific physiological function of astrocytes has been shown in other circuits, especially in circuits controlling rhythmic behaviors (Barca Mayo et al, 2019;Bellot-Saez et al, 2018;Bojarskaite et al, 2020;Broadhead & Miles, 2021;Christensen et al, 2013;Jackson et al, 2015;Jones et al, 2011;Khakh & Sofroniew, 2015;Mederos et al, 2021;Montalant et al, 2021). Not only that the function of astrocytes depends on the circuits that they are in, but also one astrocyte can release different transmitter molecules depending on neuronal signals (Covelo & Araque, 2018),…”

Section: Discussionmentioning

confidence: 90%

Astrocytic modulation of central pattern generating motor circuits

Turk

Bishop

Adeck

et al. 2022

Glia

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Central pattern generators (CPGs) generate the rhythmic and coordinated neural features necessary for the proper conduction of complex behaviors. In particular, CPGs are crucial for complex motor behaviors such as locomotion, mastication, respiration, and vocal production. While the importance of these networks in modulating behavior is evident, the mechanisms driving these CPGs are still not fully understood. On the other hand, accumulating evidence suggests that astrocytes have a significant role in regulating the function of some of these CPGs. Here, we review the location, function, and role of astrocytes in locomotion, respiration, and mastication CPGs and propose that, similarly, astrocytes may also play a significant role in the vocalization CPG.

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Section: Discussionmentioning

confidence: 90%

Astrocytic modulation of central pattern generating motor circuits

Turk

Bishop

Adeck

et al. 2022

Glia

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“…Allied to this, we cannot forget that masticatory function plays an important role in the stomatognathic system and that its central motor control, preservation of hippocampal trophism, and synaptic activity should contribute to the study of neurodegenerative diseases in an innovative and revealing way [ 21 ]. Mastication is considered a rhythmic activity like walking and breathing [ 4 ], involving muscle contraction orchestrated by networks of motoneurons called central pattern generators (CPG) that properly conduct complex behavior [ 4 , 5 ]. Knowing that most synapses in the CNS occurs in close apposition of astrocytic processes, if neurotransmitters released by neurons adhere to receptors expressed by astrocytes and activate pathways that increase calcium concentration and gliotransmitters that can modulate synaptic transmission, it is reasonable to assume that astrocyte activation impacts on motor control [ 4 , 5 ].…”

Section: Discussionmentioning

confidence: 99%

“…Neural circuits connecting oral cavity structures to the Central Nervous System (CNS) transmit proprioceptive information during mastication and reach the hippocampus via the thalamus and cerebral cortex [ 2 , 3 ]. The coordinated muscles contraction during masticatory activity dictates the timing and activation of motoneurons in the brainstem and spinal cord, which are governed by neural networks associated with central pattern generators (CPG) [ 4 , 5 ].…”

Section: Introductionmentioning

confidence: 99%

The Masticatory Activity Interference in Quantitative Estimation of CA1, CA3 and Dentate Gyrus Hippocampal Astrocytes of Aged Murine Models and under Environmental Stimulation

Leal

Junior

Arruda

et al. 2023

IJMS

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Studies indicating the influence of masticatory dysfunction, due to a soft diet or lack of molars, on impairing spatial memory and learning have led to research about neuronal connections between areas and cell populations possibly affected. In this sense, with scarce detailed data on the subfields of hippocampus in dementia neurodegeneration, there is no information about astrocytic responses in its different layers. Thus, considering this context, the present study evaluated the effects of deprivation and rehabilitation of masticatory activity, aging, and environmental enrichment on the stereological quantification of hippocampal astrocytes from layers CA1, CA3, and DG. For this purpose, we examined mature (6-month-old; 6M), and aged (18-month-old; 18M) mice, subjected to distinct masticatory regimens and environments. Three different regimens of masticatory activity were applied: continuous normal mastication with hard pellets (HD); normal mastication followed by deprived mastication with equal periods of pellets followed by soft powder (HD/SD); or rehabilitated masticatory activity with equal periods of HD, followed by powder, followed by pellets (HD/SD/HD). Under each specific regimen, half of the animals were raised in standard cages (impoverished environment (IE)) and the other half in enriched cages (enriched environment (EE)), mimicking sedentary or active lifestyles. Microscopic stereological, systematic, and random sampling approaches with an optical dissector of GFAP-immunolabeled astrocytes were done, allowing for an astrocyte numerical estimate. Stratum moleculare and hilus, from the dentate gyrus (DG) and Strata Lacunosum-Moleculare, Oriens, and Radiatum, similarly to the dentate gyrus, showed no significant change in any of the investigated variables (age, diet, or environment) in these layers. However, in Stratum radiatum, it was possible to observe significant differences associated with diet regimens and age. Therefore, diet-related differences were found when the HD 18M IE group was compared to the HD/SD/HD 18-month-old group in the same environment (IE) (p = 0.007). In the present study, we present modulatory factors (masticatory function, environmental enrichment, and aging) for the differentiated quantitative laminar response in the hippocampal regions, suggesting other studies to read the plasticity and responsiveness of astrocytes, including the molecular background.

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“…In the spinal motor network, the locomotor oscillatory rhythm is correlated with enhanced calcium (Ca 2+ ) transients in astrocytes (Broadhead & Miles, 2020), which likely triggers ATP release (Witts et al, 2015), modulating excitatory synaptic transmission (Carlsen & Perrier, 2014). Thus, growing evidence point to the contribution of gliotransmission in modulating neuronal rhythmogenesis (Montalant et al, 2021). Astrocytes can also respond to neurotransmitters and neuromodulators (Paukert et al, 2014; Rosa et al, 2015) by modifying [K + ] e , which greatly impact brain oscillations (Bellot‐Saez et al, 2018; Ding et al, 2016; Sibille et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Astrocytic Kir4.1 channels regulate locomotion by orchestrating neuronal rhythmicity in the spinal network

Barbay

Pecchi

Ducrocq

et al. 2023

Glia

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Neuronal rhythmogenesis in the spinal cord is correlated with variations in extracellular K + levels ([K + ] e ). Astrocytes play important role in [K + ] e homeostasis and compute neuronal information. Yet it is unclear how neuronal oscillations are regulated by astrocytic K + homeostasis. Here we identify the astrocytic inward-rectifying K + channel Kir4.1 (a.k.a. Kcnj10) as a key molecular player for neuronal rhythmicity in the spinal central pattern generator (CPG). By combining two-photon calcium imaging with electrophysiology, immunohistochemistry and genetic tools, we report that astrocytes display Ca 2+ transients before and during oscillations of neighboring neurons. Inhibition of astrocytic Ca 2+-transients with BAPTA decreases the barium-sensitive Kir4.1 current responsible of K + clearance. Finally, we show in mice that Kir4.1 knockdown in astrocytes progressively prevents neuronal oscillations and alters the locomotor pattern resulting in lower motor performances in challenging tasks. These data identify astroglial Kir4.1 channels as key regulators of neuronal rhythmogenesis in the CPG driving locomotion.

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Role of astrocytes in rhythmic motor activity

Abstract: This is an open access article under the terms of the Creat ive Commo ns Attri bution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 13 publications

References 53 publications

Astrocytic modulation of central pattern generating motor circuits

Astrocytic modulation of central pattern generating motor circuits

The Masticatory Activity Interference in Quantitative Estimation of CA1, CA3 and Dentate Gyrus Hippocampal Astrocytes of Aged Murine Models and under Environmental Stimulation

Astrocytic Kir4.1 channels regulate locomotion by orchestrating neuronal rhythmicity in the spinal network

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