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TTX-resistant NMDA receptor-mediated membrane potential oscillations in neonatal mouse Hb9 interneurons.

Masino MA, Abbinanti MD, Eian J, Harris-Warrick RM - PLoS ONE (2012)

Bottom Line: Hb9 interneurons are rhythmically active during fictive locomotor-like behavior.In contrast, exogenous serotonin and dopamine application, alone or in combination, are not sufficient.NMDA does not modulate the T-type calcium current (I(Ca(T))), which is thought to be important in generating locomotor-like activity, in Hb9 neurons.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota, United States of America. masino@umn.edu

ABSTRACT
Conditional neuronal membrane potential oscillations have been identified as a potential mechanism to help support or generate rhythmogenesis in neural circuits. A genetically identified population of ventromedial interneurons, called Hb9, in the mouse spinal cord has been shown to generate TTX-resistant membrane potential oscillations in the presence of NMDA, serotonin and dopamine, but these oscillatory properties are not well characterized. Hb9 interneurons are rhythmically active during fictive locomotor-like behavior. In this study, we report that exogenous N-Methyl-D-Aspartic acid (NMDA) application is sufficient to produce membrane potential oscillations in Hb9 interneurons. In contrast, exogenous serotonin and dopamine application, alone or in combination, are not sufficient. The properties of NMDA-induced oscillations vary among the Hb9 interneuron population; their frequency and amplitude increase with increasing NMDA concentration. NMDA does not modulate the T-type calcium current (I(Ca(T))), which is thought to be important in generating locomotor-like activity, in Hb9 neurons. These results suggest that NMDA receptor activation is sufficient for the generation of TTX-resistant NMDA-induced membrane potential oscillations in Hb9 interneurons.

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Exogenous NMDA application is sufficient to induce membrane potential oscillations in Hb9 interneurons when spike-mediated synapses are blocked with TTX. A–E,Whole-cell current-clamp recordings of membrane potential in various Hb9 interneurons under different conditions; the slow, small spikes at the tops of the oscillations are probably calcium-mediated. A, Membrane potential oscillations in the presence of a ‘cocktail’ of chemicals (21 μM NMDA, 21 μM 5-HT and 50 μM DA) that produces fictive locomotor-like activity in isolated whole-cord preparations. B, Exogenous NMDA application (21 μM) is sufficient to induce oscillations. C–E, Exogenous serotonin (5-HT, 21 μM) and dopamine (DA, 50 μM) application alone, or in combination, are not sufficient to induce Hb9 oscillations.
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pone-0047940-g001: Exogenous NMDA application is sufficient to induce membrane potential oscillations in Hb9 interneurons when spike-mediated synapses are blocked with TTX. A–E,Whole-cell current-clamp recordings of membrane potential in various Hb9 interneurons under different conditions; the slow, small spikes at the tops of the oscillations are probably calcium-mediated. A, Membrane potential oscillations in the presence of a ‘cocktail’ of chemicals (21 μM NMDA, 21 μM 5-HT and 50 μM DA) that produces fictive locomotor-like activity in isolated whole-cord preparations. B, Exogenous NMDA application (21 μM) is sufficient to induce oscillations. C–E, Exogenous serotonin (5-HT, 21 μM) and dopamine (DA, 50 μM) application alone, or in combination, are not sufficient to induce Hb9 oscillations.

Mentions: A combination (‘cocktail’) of all three neuroactive chemicals (21 μM NMDA, 21 μM 5-HT and 50 μM DA) generated membrane potential oscillations in most Hb9 interneurons (18 of 25; Fig. 1A). Bath application of NMDA alone (21 μM) produced similar oscillations in most Hb9 interneurons (40 of 61; Fig. 1B). We chose a concentration (21 μM) of NMDA shown to elicit both fictive locomotor-like activity in whole spinal cord preparations [35], [40], [51]–[53] and endogenous membrane potential oscillations in Hb9 interneurons from transverse slice preparations when applied together with 5-HT and DA [1], [6], [30]. However, neither 5-HT (21 μM; 0 of 6; Fig. 1C) nor DA (50 μM; 0 of 7; Fig. 1D) application alone, or the combination of 5-HT and DA (0 of 7; Fig. 1E), produced membrane potential oscillations. The variance of the cycle frequency did not differ between oscillations evoked by NMDA alone or the full cocktail of NMDA, 5-HT and DA (data not shown).


TTX-resistant NMDA receptor-mediated membrane potential oscillations in neonatal mouse Hb9 interneurons.

Masino MA, Abbinanti MD, Eian J, Harris-Warrick RM - PLoS ONE (2012)

Exogenous NMDA application is sufficient to induce membrane potential oscillations in Hb9 interneurons when spike-mediated synapses are blocked with TTX. A–E,Whole-cell current-clamp recordings of membrane potential in various Hb9 interneurons under different conditions; the slow, small spikes at the tops of the oscillations are probably calcium-mediated. A, Membrane potential oscillations in the presence of a ‘cocktail’ of chemicals (21 μM NMDA, 21 μM 5-HT and 50 μM DA) that produces fictive locomotor-like activity in isolated whole-cord preparations. B, Exogenous NMDA application (21 μM) is sufficient to induce oscillations. C–E, Exogenous serotonin (5-HT, 21 μM) and dopamine (DA, 50 μM) application alone, or in combination, are not sufficient to induce Hb9 oscillations.
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pone-0047940-g001: Exogenous NMDA application is sufficient to induce membrane potential oscillations in Hb9 interneurons when spike-mediated synapses are blocked with TTX. A–E,Whole-cell current-clamp recordings of membrane potential in various Hb9 interneurons under different conditions; the slow, small spikes at the tops of the oscillations are probably calcium-mediated. A, Membrane potential oscillations in the presence of a ‘cocktail’ of chemicals (21 μM NMDA, 21 μM 5-HT and 50 μM DA) that produces fictive locomotor-like activity in isolated whole-cord preparations. B, Exogenous NMDA application (21 μM) is sufficient to induce oscillations. C–E, Exogenous serotonin (5-HT, 21 μM) and dopamine (DA, 50 μM) application alone, or in combination, are not sufficient to induce Hb9 oscillations.
Mentions: A combination (‘cocktail’) of all three neuroactive chemicals (21 μM NMDA, 21 μM 5-HT and 50 μM DA) generated membrane potential oscillations in most Hb9 interneurons (18 of 25; Fig. 1A). Bath application of NMDA alone (21 μM) produced similar oscillations in most Hb9 interneurons (40 of 61; Fig. 1B). We chose a concentration (21 μM) of NMDA shown to elicit both fictive locomotor-like activity in whole spinal cord preparations [35], [40], [51]–[53] and endogenous membrane potential oscillations in Hb9 interneurons from transverse slice preparations when applied together with 5-HT and DA [1], [6], [30]. However, neither 5-HT (21 μM; 0 of 6; Fig. 1C) nor DA (50 μM; 0 of 7; Fig. 1D) application alone, or the combination of 5-HT and DA (0 of 7; Fig. 1E), produced membrane potential oscillations. The variance of the cycle frequency did not differ between oscillations evoked by NMDA alone or the full cocktail of NMDA, 5-HT and DA (data not shown).

Bottom Line: Hb9 interneurons are rhythmically active during fictive locomotor-like behavior.In contrast, exogenous serotonin and dopamine application, alone or in combination, are not sufficient.NMDA does not modulate the T-type calcium current (I(Ca(T))), which is thought to be important in generating locomotor-like activity, in Hb9 neurons.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota, United States of America. masino@umn.edu

ABSTRACT
Conditional neuronal membrane potential oscillations have been identified as a potential mechanism to help support or generate rhythmogenesis in neural circuits. A genetically identified population of ventromedial interneurons, called Hb9, in the mouse spinal cord has been shown to generate TTX-resistant membrane potential oscillations in the presence of NMDA, serotonin and dopamine, but these oscillatory properties are not well characterized. Hb9 interneurons are rhythmically active during fictive locomotor-like behavior. In this study, we report that exogenous N-Methyl-D-Aspartic acid (NMDA) application is sufficient to produce membrane potential oscillations in Hb9 interneurons. In contrast, exogenous serotonin and dopamine application, alone or in combination, are not sufficient. The properties of NMDA-induced oscillations vary among the Hb9 interneuron population; their frequency and amplitude increase with increasing NMDA concentration. NMDA does not modulate the T-type calcium current (I(Ca(T))), which is thought to be important in generating locomotor-like activity, in Hb9 neurons. These results suggest that NMDA receptor activation is sufficient for the generation of TTX-resistant NMDA-induced membrane potential oscillations in Hb9 interneurons.

Show MeSH
Related in: MedlinePlus