Hypoxia-induced short-term potentiation (STP) of respiratory motor output is manifested by a progressive increase in activity after the acute hypoxic response and a gradual decrease in activity on termination of hypoxia. We hypothesized that STP would be differentially expressed between physiologically defined phrenic motoneurons (PhrMNs). Phrenic nerve "single fiber" recordings were used to characterize PhrMN discharge in anesthetized, vagotomized and ventilated rats. PhrMNs were classified as early (Early-I) or late inspiratory (Late-I) according to burst onset relative to the contralateral phrenic neurogram during normocapnic baseline conditions. During hypoxia (F(I)O(2) = 0.12-0.14, 3 min), both Early-I and Late-I PhrMNs abruptly increased discharge frequency. Both cell types also showed a progressive increase in frequency over the remainder of hypoxia. However, Early-I PhrMNs showed reduced overall discharge duration and total spikes/breath during hypoxia, whereas Late-I PhrMNs maintained constant discharge duration and therefore increased the number of spikes/breath. A population of previously inactive (i.e., silent) PhrMNs was recruited 48 +/- 8 s after hypoxia onset. These PhrMNs had a Late-I onset, and the majority (8/9) ceased bursting promptly on termination of hypoxia. In contrast, both Early-I and Late-I PhrMNs showed post-hypoxia STP as reflected by greater discharge frequencies and spikes/breath during the post-hypoxic period (P < 0.01 vs. baseline). We conclude that the expression of phrenic STP during hypoxia reflects increased activity in previously active Early-I and Late-I PhrMNs and recruitment of silent PhrMNs. post-hypoxia STP primarily reflects persistent increases in the discharge of PhrMNs, which were active before hypoxia.