Temperature and state dependence of dynamic phrenic oscillations in the decerebrate juvenile rat

Abstract

The aim of the present study was to determine characteristics of fast oscillations in the juvenile rat phrenic nerve (Ph) and to establish their temperature and state dependence. Two different age-matched decerebrate, baro- and chemodenervated rat preparations, in vivo and in situ arterially perfused models, were used to examine three systemic properties: 1) generation and dynamics of fast oscillations in Ph activity (both preparations), 2) responses to anoxia (both preparations), and 3) the effects of temperature on fast oscillations (in situ only). Both juvenile preparations generated power and coherence in two major bands analogous to adult medium- and high-frequency oscillations (HFO) at frequencies that increased with temperature but were lower than in adults. At < 28 degrees C, however, Ph oscillations were confined primarily to one low-frequency band (20-45 Hz). During sustained anoxia, both preparations produced stereotypical state changes from eupnea to hyperpnea to transition bursting (a behavior present only in vivo during incomplete ischemia) to gasping. Thus the juvenile rat produces a sequential pattern of responses to anoxia that are intermediate forms between those produced by neonates and those produced by adults. Time-frequency analysis determined that fast oscillations demonstrated dynamics over the course of the inspiratory burst and a state dependence similar to that of adults in vivo in which hyperpnea (and transition) bursts are associated with increases in HFO, while gasping contains no HFO. Our results confirm that both the fast oscillations in Ph activity and the coherence between Ph pairs produced by the juvenile rat are profoundly state- and temperature-dependent.

Fast oscillations during gasping and other non-eupneic respiratory behaviors: Clues to central pattern generation

“…As described earlier, HFO and MFO frequency bands are lower in the in situ arterially-perfused juvenile rat preparation, with HFO in the range 90–110 Hz and MFO in the range 40–50 Hz (Marchenko and Rogers, 2007; Solomon et al, 2003). St.…”

“…The hyperpneic phase of the transition to gasping was marked by an increase in HFO frequencies, as demonstrated in the decerebrate juvenile rat in vivo (Marchenko and Rogers, 2007), as well as replacement of the single MFO peak with two high-power bands within MFO frequency ranges in PhN, both of which exhibited higher maximal frequency peaks than eupneic MFO (Fig. 3).…”

“…Discharge of the phrenic nerve (PhN), which provides innervation to the diaphragm (the main inspiratory muscle in mammals), contains high- (HFO), medium- (MFO), and low-frequency (LFO) oscillation bands (Bruce et al, 1991; Cohen et al, 1987, 1997; Davies et al, 1985; Dittler and Garten, 1912; Huang et al, 1996; Marchenko et al, 2002; Marchenko and Rogers, 2006a,b; Richardson and Mitchell, 1982; Wyss, 1939). Due in part to differences in intrinsic membrane properties of respiratory motoneurons between different species (Berger, 1979; Dick et al, 1987; Funk and Parkis, 2002; Iscoe et al, 1976; Jodkowski et al, 1987; Purpura and Chatfield, 1952), fast oscillation ranges (Table 1) in rats (Kocsis and Gyimesi-Pelczer, 1997; Marchenko et al, 2002) are twice those (LFO ~ 20–50, MFO ~ 50–100 Hz, HFO ~ 100–200 Hz) observed in cats and rabbits (MFO ~ 20–50 Hz, HFO ~ 50–100 Hz; Ackerson and Bruce, 1983; Cohen et al, 1997; Schmid et al, 1990) and higher in the in vivo rat (Marchenko et al, 2012) than in preparations of the in situ juvenile rat (Marchenko and Rogers, 2007; Solomon et al, 2003; St. John and Leiter, 2003) and the in vitro neonatal cat (Kato et al, 1996).…”

“…In the in vivo decerebrate juvenile rat, the high-frequency band shifts toward higher frequencies during the hyperpnea and transition phases of the anoxic response and ultimately disappears during terminal gasping, where power becomes distributed in the two lower frequency bands (with 63 and 88 Hz peaks), primarily during the earlier parts of inspiration (Marchenko and Rogers, 2007). Power increases at all bands during the hyperpnea and transition phases of the anoxic response.…”

“…Changes observed in HFO during different respiratory behaviors have typically involved shifts in spectral frequency, but may also be characterized by changes in spectral power. The recent application of time-frequency analyses to represent spectra and coherence has provided increased sensitivity for detecting subtle changes (Marchenko and Rogers, 2006a,b; Marchenko and Rogers, 2007; Marchenko et al, 2012; Solomon et al, 2003) in fast oscillation dynamics associated with transitions between different respiratory behaviors, which helps inform mechanisms of central respiratory pattern generation and network reorganization during altered modes of breathing (Berger et al, 1978; Cohen et al, 1992; Galán et al, 2010; Leiter and St. John, 2004; Marchenko and Rogers, 2006a, b, 2007; Nakazawa et al, 2000; Richardson, 1986; Smith and Denny, 1990; St. John and Leiter, 2003).…”