Abstract
Breathing in mammals is hypothesized to result from the interaction of two distinct oscillators: the preBötzinger Complex (preBötC) driving inspiration and the lateral parafacial region (pFL) driving active expiration. To understand the interactions between these oscillators, we independently altered their excitability in spontaneously breathing vagotomized urethane-anesthetized adult rats. Hyperpolarizing preBötC neurons decreased inspiratory activity and initiated active expiration, ultimately progressing to apnea, i.e., cessation of both inspiration and active expiration. Depolarizing pFL neurons produced active expiration at rest, but not when inspiratory activity was suppressed by hyperpolarizing preBötC neurons. We conclude that in anesthetized adult rats active expiration is driven by the pFL but requires an additional form of network excitation, i.e., ongoing rhythmic preBötC activity sufficient to drive inspiratory motor output or increased chemosensory drive. The organization of this coupled oscillator system, which is essential for life, may have implications for other neural networks that contain multiple rhythm/pattern generators.
Highlights
Coupled oscillator neural networks driving behavior are widespread, e.g., for swimming (Grillner, 2003), and locomotion (Goulding, 2009; Talpalar et al, 2013)
We hypothesize that the respiratory rhythm central pattern generator (CPG) in mammals is comprised of two oscillators (Feldman et al, 2013): inspiratory rhythm originates in the preBotzinger Complex in the ventrolateral medulla (Smith et al, 1991) and active expiratory rhythm originates in the rostral medulla ventrolaterally adjacent to the facial nucleus (Pagliardini et al, 2011; Huckstepp et al, 2015)
In histological sections the preBotzinger Complex (preBotC) is defined as the neurokinin-1 receptor (NK1R) dense area ventral to the semi-compact nucleus ambiguous (Figure 1A,B) and the parafacial lateral (pFL) is defined as the area ventral to the lateral edge of the facial nucleus, juxtaposed to the spinal trigeminal tract (Figure 1C,D) (Huckstepp et al, 2015)
Summary
Coupled oscillator neural networks driving behavior are widespread, e.g., for swimming (Grillner, 2003), and locomotion (Goulding, 2009; Talpalar et al, 2013). We used unbiased descriptors to partition the ventral and lateral parafacial regions, designating them as parafacial lateral (pFL) and parafacial ventral (pFV) These parafacial regions are chemosensitive (Mulkey et al, 2004; Onimaru et al, 2008; Marina et al, 2010; Onimaru et al, 2012), but can be functionally separated by: i) their contribution to active expiration, with the pFV providing drive to expiration (Huckstepp et al, 2015; Silva et al, 2016) and the pFL containing a presumptive expiratory rhythm generator
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