In vitro electrophysiology of developing genioglossal motoneurons in the rat

1. Experiments were performed to determine the change in membrane properties of genioglossal (GG) motoneurons during development. Intracellular recordings were made in 127 GG motoneurons from rats postnatal ages 1-30 days. 2. The input resistance (R(in)) and the membrane time constant (τ(m)) decreased between 5-6 and 13-15 days from 84.8 ± 25.4 (SD) to 47.0 ± 18.9 MΩ (P < 0.01) and from 10.0 ± 4.2 to 7.3 ± 3.3 ms (P < 0.05), respectively. During this period, the rheobase (I(rh)) increased (P < 0.01) from 0.13 ± 0.07 to 0.27 ± 0.14 nA, and the percentage of cells exhibiting inward rectification increased from 5 to 40%. Voltage threshold (V(thr)) of the action potential remained unchanged postnatally. 3. There was also a postnatal change in the shape of the action potential. Specifically, between 1-2 and 5-6 days, there was a decrease (P < 0.05) in the spike half-width from 2.23 ± 0.53 to 1.45 ± 0.44 ms, resulting, in part, from a steepening (P < 0.05) of the slope of the falling phase of the action potential from 21.6 ± 10.1 to 32.9 ± 13.1 mV/ms. The slope of the rising phase also increased significantly (P < 0.01) between 1-2 and 13-15 days from 68.4 ± 31.0 to 91.4 ± 44.3 mV/ms. 4. The average duration of the medium afterhyperpolarization (mAHP(dur)) decreased (P < 0.05) between 1-2 (193 ± 53 ms) and 5-6 days (159 ± 43 ms). Whereas the mAHP(dur) was found to be independent of membrane potential, there was a linear relationship between the membrane potential and the amplitude of the medium AHP (mAHP(amp)). From this latter relationship, a reversal potential for the mAHP(amp) was extrapolated to be -87 mV. No evidence for the existence of a slow AHP was found in these developing motoneurons. 5. All cells analyzed (n = 74) displayed adaptation during the first three spikes. The subsequent firing pattern was classified into two groups, adapting and nonadapting. Cells at birth were all adapting, whereas all cells but two from animals 13 days and older were nonadapting. At the intermediate age (5-6 days), the minority (27%) was adapting and the majority (73%) was nonadapting. 6. The mean slope of primary range for the first interspike interval (1st ISI) was ~90 Hz/nA. This value was similar for both adapting and nonadapting cells and did not change postnatally. However, there was a significantly lower (P < 0.01) frequency of the mean ISI for adapting (27.7 ± 8.2 Hz/nA) than for nonadapting cells (36.5 ± 11.6 Hz/nA). During development, there was a trend to increase the maximum firing frequency achieved during sustained current injection. Newborn (1-2 days) motoneurons had a maximal frequency of 25.5 ± 10.1 Hz, whereas motoneurons at 19-30 days fired at 42.2 ± 19.7 Hz. 7. The mean ISI of GG motoneurons exhibited only a single linear frequency-current (f-I) relationship, whereas the 1st ISI in some cells exhibited both a primary and a secondary range. The occurrence of cells having a secondary range of the 1st ISI increased postnatally. 8. We hypothesize that there is a specific developmental sequence for the membrane properties of GG motoneurons in which channels shaping the action potential and afterpotential mature earlier than those channels governing its passive membrane properties.