Electrophysiological properties of developing phrenic motoneurons in the cat

Intracellular recordings were made in 427 phrenic motoneurons from kittens (in four stages of postnatal development, ranging from 2 to 14 wk) and in 72 motoneurons from adult cats. These experiments were performed to determine how the pattern of spontaneous discharge changes in phrenic motoneurons during development and how these changes might be influenced by alterations in the electrophysiological properties of these neurons. The mean axonal conduction velocity increased significantly (P < 0.0001) throughout this period of development, with the most rapid increase occurring between weeks 2 and 5 (18.5 ± 5.4 and 32.4 ± 5.6 m/s, respectively, mean ± SD). There was no change in the magnitude of the membrane potential, antidromic action potential, or positive overshoot; whereas there was a decrease in the half-width of the action potential from 2 (652 ± 184 ms) to 14 (525 ± 116 ms) wk postnatal. The mean duration of the afterhyperpolarization (AHP(dur)) decreased from 69 ± 20 ms at 2 wk to 60 ± 16 ms by 9 wk, then increased to 66 ± 18 ms by 14 wk of age and to 75 ± 21 ms in the adult. The mean amplitude of the afterhyperpolarization (AHP(amp)) in the 2-wk-old group (4.9 ± 1.8 mV) was larger than that at weeks 5 (3.9 ± 1.7 mV) and 9 (3.9 ± 1.6 mV), whereas the mean AHP(amp) of the adult (3.1 ± 1.2 mV) was significantly smaller than the mean of any younger group. A significant negative correlation was found between AHP(dur) and axonal conduction velocity in all age groups studied, including the adult. During the course of postnatal development, the percentage of the motor pool that was activated during inspiration decreased. At 2 wk, almost all cells studied (94%) discharged either early or late within the inspiratory cycle, whereas, at 5 wk, these active cells accounted for only 57% of the population, with the balance of cells remaining inactive or quiescent during the cycle. These changes in the proportion of cells with different discharge patterns were paralleled by significant alterations in the membrane properties of the motoneurons. The greatest changes in membrane properties occur between weeks 2 and 5. The mean rheobase (I(rh)) increased from 2.4 ± 1.2 to 6.0 ± 3.2 nA during this period, whereas the mean input resistance (R(n)) decreased from 4.1 ± 0.7 to 1.9 ± 1.0 MΩ. The mean I(rh) increased almost fourfold between weeks 2 and 14 (9.5 ± 7.0 nA), and the mean R(n) at 14 wk (1.3 ± 0.6 MΩ) was less than one-third of that at 2 wk of age. In the 2-wk-old kittens, mean I(rh) was significantly less and mean R(n) greater than that measured in the older animals. Both mean R(n) and I(rh) achieved their adult values by 14 wk of age. The mean threshold voltage (V(thr)) at 2 wk (-53.0 ± 4.1 mV) was significantly more negative than that found at 5 (-49.7 ± 3.6 mV) or 9 wk (-50.3 ± 3.7 mV), and the mean depolarization voltage (V(dep)) at 2 wk (10.6 ± 4.8 mV) was significantly less than that found at 5 wk (13.8 ± 4.1 mV). No differences were found in the mean V(thr) or V(dep) at ages 5 wk and older. The increase in I(rh) was greatest among the quiescent cells and least in the cells activated early in inspiration. These changes in I(rh) during development can account for the changes in the proportion of phrenic motoneurons firing at different times during the inspiratory cycle. We conclude that the membrane properties of phrenic motoneurons in the newborn tend to ensure the activation of most phrenic motoneurons, and therefore diaphragmatic motor units, by the central respiratory drive generated in these hyperoxic, hypercapnic animals.