TTX-Resistant NMDA Receptor-Mediated Membrane Potential Oscillations in Neonatal Mouse Hb9 Interneurons

Masino, Mark A.; Abbinanti, Matthew D.; Eian, J.; Harris-Warrick, Ronald M.

doi:10.1371/journal.pone.0047940

Cited by 18 publications

(16 citation statements)

References 64 publications

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“…Application of 5-HT is also known to slow down the locomotor frequency (Harris-Warrick and Cohen 1985). A modulation of TTX-resistant NMDA oscillations by 5-HT occurs in several species, including rodents (Hsiao et al 2002;MacLean et al 1998;MacLean and Schmidt 2001;Masino et al 2012;Schmidt et al 1998), amphibians (Reith and Sillar 1998;Scrymgeour-Wedderburn et al 1997;Sillar and Simmers 1994a;Sillar et al 1992), and lamprey [present study and El Manira et al (1994); Wallén et al (1989)]. …”

Section: Discussionmentioning

confidence: 59%

“…NMDA can induce pacemaker-like oscillations in different neurons in the lamprey spinal cord and in other species (Hochman et al 1994;Li et al 2010;Masino et al 2012;Sigvardt et al 1985;Wallén and Grillner 1987) after a blockade of interaction between the cells with tetrodotoxin. The generation of these plateaus depends on an interaction between a number of ion channels.…”

Section: Discussionmentioning

confidence: 99%

“…NMDA receptor-mediated, TTX-resistant membrane potential oscillations can contribute to the generation of locomotor activity and have also been demonstrated in other species, including rodents (Hochman et al 1994;MacLean et al 1997;Masino et al 2012;Schmidt et al 1998) and amphibians (Li et al 2010;Reith and Sillar 1998;Scrymgeour-Wedderburn et al 1997). In the lamprey, these oscillations vary in a characteristic way between different spinal cord preparations.…”

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confidence: 91%

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Endogenous release of 5-HT modulates the plateau phase of NMDA-induced membrane potential oscillations in lamprey spinal neurons

Wang

Grillner

Wallén

2014

Journal of Neurophysiology

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The lamprey central nervous system has been used extensively as a model system for investigating the networks underlying vertebrate motor behavior. The locomotor networks can be activated by application of glutamate agonists, such as N-methyl-D-aspartic acid (NMDA), to the isolated spinal cord preparation. Many spinal neurons are capable of generating pacemaker-like membrane potential oscillations upon activation of NMDA receptors. These oscillations rely on the voltage-dependent properties of NMDA receptors in interaction with voltage-dependent potassium and calcium-dependent potassium (K(Ca)) channels, as well as low voltage-activated calcium channels. Upon membrane depolarization, influx of calcium will activate K(Ca) channels, which in turn, will contribute to repolarization and termination of the depolarized phase. The appearance of the NMDA-induced oscillations varies markedly between spinal cord preparations; they may either have a pronounced, depolarized plateau phase or be characterized by a short-lasting depolarization lasting approximately 200-300 ms without a plateau. Both types of oscillations increase in frequency with increased concentrations of NMDA. Here, we characterize these two types of membrane potential oscillations and show that they depend on the level of endogenous release of 5-HT in the spinal cord preparations. In the lamprey, 5-HT acts to block voltage-dependent calcium channels and will thereby modulate the activity of K(Ca) channels. When 5-HT antagonists were administered, the plateau-like oscillations were converted to the second type of oscillations lacking a plateau phase. Conversely, plateau-like oscillations can be induced or prolonged by 5-HT agonists. These properties are most likely of significance for the modulatory action of 5-HT on the spinal networks for locomotion.

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Section: Discussionmentioning

confidence: 59%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 91%

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Endogenous release of 5-HT modulates the plateau phase of NMDA-induced membrane potential oscillations in lamprey spinal neurons

Wang

Grillner

Wallén

2014

Journal of Neurophysiology

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“…Anatomical analysis suggests that they are premotor interneurons receiving inputs from sensory afferents and having axonal projections terminating directly onto motoneurons (83,259,297,474,490). These interneurons also display pacemaker properties mediated by activation of persistent sodium currents (61,62,446,490) them to generate rhythmicity in the absence of fast excitatory and inhibitory synaptic transmission (12,327). While these Hb9 interneurons were rhythmically active during drug-induced locomotor-like activity in vitro, the onset of their activity occurred after that of motoneurons, which prompted uncertainty whether these interneurons could be driving locomotor activity (297).…”

Section: Rhythm Generationmentioning

confidence: 99%

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Grillner

Manira

2020

Physiological Reviews

383

395

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The vertebrate control of locomotion involves all levels of the nervous system from cortex to the spinal cord. Here, we aim to cover all main aspects of this complex behavior, from the operation of the microcircuits in the spinal cord to the systems and behavioral levels and extend from mammalian locomotion to the basic undulatory movements of lamprey and fish. The cellular basis of propulsion represents the core of the control system, and it involves the spinal central pattern generator networks (CPGs) controlling the timing of different muscles, the sensory compensation for perturbations, and the brain stem command systems controlling the level of activity of the CPGs and the speed of locomotion. The forebrain and in particular the basal ganglia are involved in determining which motor programs should be recruited at a given point of time and can both initiate and stop locomotor activity. The propulsive control system needs to be integrated with the postural control system to maintain body orientation. Moreover, the locomotor movements need to be steered so that the subject approaches the goal of the locomotor episode, or avoids colliding with elements in the environment or simply escapes at high speed. These different aspects will all be covered in the review.

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“…It is possible that both mechanisms are used in the same neurons. For example, according to one group of authors, the endogenous rhythmic activity of Hb9 interneurons is linked with activation of NMDA receptors [Masino et al, 2012], while data from other authors indicate that this Fig. 7.…”

Section: Mechanisms Of Operation Of Central Pattern Generatorsmentioning

confidence: 98%

Central Pattern Generators: Mechanisms of Operation and Their Role in Controlling Automatic Movements

Arshavsky

Deliagina

Orlovsky

2016

Neurosci Behav Physi

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Central pattern generators consist of sets of interconnected neurons able to generate a basic motor output pattern underlying automatic movements (respiration, locomotion, chewing, swallowing, etc.) without any afferent signals from the executive motor apparatus. They are divided into constitutive pattern generators, which are active throughout life (the respiratory generator), and conditional pattern generators, which control episodic movements (locomotion, chewing, swallowing, etc.). As the motor output of a pattern generator is defi ned by its internal organization, the activity of conditional pattern generators is initiated by a simple command arriving from the higher centers. The structural-functional organization of the locomotor pattern generators in the marine mollusk Clione, the lamprey, the frog embryo, and laboratory mammals (cats, mice, and rats) are described, along with pattern generators controlling respiratory and swallowing movements in mammals and pattern generators for discharges of the electric organs of gymnotiform fi sh. Generation of the rhythmic motor output is shown in all cases to be based on the endogenous (pacemaker) activity of specifi c groups of interneurons and interneural interactions. These two interacting mechanisms supplement each other, ensuring the reliable operation of pattern generators. The question of whether experience gained from studies of central pattern generators can be used for understanding the mechanisms of more complex brain functions, including cognitive functions, is discussed.

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TTX-Resistant NMDA Receptor-Mediated Membrane Potential Oscillations in Neonatal Mouse Hb9 Interneurons

Cited by 18 publications

References 64 publications

Endogenous release of 5-HT modulates the plateau phase of NMDA-induced membrane potential oscillations in lamprey spinal neurons

Endogenous release of 5-HT modulates the plateau phase of NMDA-induced membrane potential oscillations in lamprey spinal neurons

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Central Pattern Generators: Mechanisms of Operation and Their Role in Controlling Automatic Movements

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