Electroresponsive properties and membrane potential trajectories of three types of inspiratory neurons in the newborn mouse brain stem in vitro

被引:99
作者
Rekling, JC [1 ]
Champagnat, J [1 ]
DenavitSaubie, M [1 ]
机构
[1] CNRS,INST ALFRED FESSARD,F-91198 GIF SUR YVETTE,FRANCE
关键词
D O I
10.1152/jn.1996.75.2.795
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
1. The electrophysiological properties of inspiratory neurons were studied in a rhythmically active thick-slice preparation of the newborn mouse brain stem maintained in vitro. Whole cell patch recordings were performed from 60 inspiratory neurons within the rostral ventrolateral part of the slice with the aim of extending the classification of inspiratory neurons to include analysis of active membrane properties. 2. The slice generated a regular rhythmic motor output recorded as burst of action potentials on a XII nerve root with a peak to peak time of 11.5 +/- 3.4 s and a duration of 483 +/- 54 ms (means +/- SD, n = 50). Based on the electroresponsive properties and membrane potential trajectories throughout the respiratory cycle, three types of inspiratory neurons could be distinguished. 3. Type-1 neurons were spiking in the interval between the inspiratory potentials (n = 9) or silent with a resting membrane potential of -48.6 +/- 10.1 mV and an input resistance of 306 +/- 130 M Omega (n = 15). The spike activity between the inspiratory potentials was burst-like with spikes riding on top of an underlying depolarization (n = 11) or regular with no evidence of bursting (n = 12). Hyperpolarization of the neurons below threshold for spike initiation did not reveal any underlying phasic synaptic activity, that could explain the bursting behavior. 4. Type-1 neurons showed delayed excitation after hyperpolarizing square current pulses or when the neurons were depolarized from a hyperpolarized level. This membrane behavior resembles the response seen in other CNS neurons expressing an I-A. The response to 1-s long depolarizing pulses with a large current strength showed signs of activation of an active depolarizing membrane response leading to a transient reduction in the spike amplitude. The relationship between the membrane potential and the amplitude of square current pulses (V-m-I) showed a small upward rectification below -70 mV, and spike adaptation throughout a 1-s pulse had a largely linear time course. 5. Type-1 neurons depolarized and started to fire spikes 398 +/- 102 ms (n = 20) before the upstroke of the integrated XII nerve discharge. The inspiratory potential was followed by fast hyperpolarization, a short fast-repolarizing phase (1,040 +/- 102 ms, n = 5) and a longer slow-repolarizing phase (lasting until the next inspiratory discharge). 6. Type-2 neurons were spiking in the interval between the inspiratory potentials with no evidence of bursting behavior and had an input resistance of 296 +/- 212 M Omega (n = 26), The response to hyperpolarizing pulses revealed an initial sag and postinhibitory rebound depolarization. This membrane behavior resembles the response seen in other CNS neurons expressing an I-h. The V-m-I relationship was linear at depolarized potentials and showed a marked upward rectification below -69 mV. Spike trains elicited by 1-s long pulses showed a pronounced early and late adaptation. 7. Type-2 neurons depolarized and started to fire spikes 171 +/- 87 ms (n = 23) before the upstroke of the integrated XII nerve discharge. The inspiratory potential had a variable amplitude from cell to cell and was followed by a short hyperpolarization in the cells displaying a large amplitude inspiratory potential. 8. Type-3 neurons were spiking in the interval between the inspiratory potentials with no evidence of bursting behavior (n = 5) or silent with a resting membrane potential of -50.4 +/- 2.7 mV and an input resistance of 126 +/- 34 M Omega (n = 10). The response to current pulses revealed a low-threshold depolarization elicited by depolarizing pulses from a hyperpolarized level or after hyperpolarizing pulses from rest. This membrane behavior resembles the response seen in other CNS neurons expressing a low-voltage-activated Ca2+ current. The V-m-I relationship showed a small upward rectification below -70 mV and the spike train throughout a 1-s pulse showed a pronounced early and late adaptation. 9. Type-3 neurons depolarized 100 +/- 40 ms (n = 9) before the upstroke of the integrated XII nerve discharge. The inspiratory potential was followed by a small amplitude afterdepolarization at resting membrane potential. 10. In conclusion, three types of inspiratory neurons in the newborn mouse ventrolateral brain stem display a number of active membrane responses, which seem to shape the membrane potential trajectory before, during, and after the inspiratory potentials. The differential timing of synaptic activity preceding the XII nerve discharge demonstrates a sequence of activation in relation to the inspiratory burst, where type-1 neurons are activated well before type-2 neurons, which are activated before type-3 neurons suggesting that type-1 neurons may be more closely involved in the generation of the respiratory rhythm.
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页码:795 / 810
页数:16
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