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Review
.2009 Sep 12;364(1529):2517-26.
doi: 10.1098/rstb.2009.0074.

Pontine respiratory activity involved in inspiratory/expiratory phase transition

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Review

Pontine respiratory activity involved in inspiratory/expiratory phase transition

Michael Mörschel et al. Philos Trans R Soc Lond B Biol Sci..

Abstract

Control of the timing of the inspiratory/expiratory (IE) phase transition is a hallmark of respiratory pattern formation. In principle, sensory feedback from pulmonary stretch receptors (Breuer-Hering reflex, BHR) is seen as the major controller for the IE phase transition, while pontine-based control of IE phase transition by both the pontine Kölliker-Fuse nucleus (KF) and parabrachial complex is seen as a secondary or backup mechanism. However, previous studies have shown that the BHR can habituate in vivo. Thus, habituation reduces sensory feedback, so the role of the pons, and specifically the KF, for IE phase transition may increase dramatically. Pontine-mediated control of the IE phase transition is not completely understood. In the present review, we discuss existing models for ponto-medullary interaction that may be involved in the control of inspiratory duration and IE transition. We also present intracellular recordings of pontine respiratory units derived from an in situ intra-arterially perfused brainstem preparation of rats. With the absence of lung inflation, this preparation generates a normal respiratory pattern and many of the recorded pontine units demonstrated phasic respiratory-related activity. The analysis of changes in membrane potentials of pontine respiratory neurons has allowed us to propose a number of pontine-medullary interactions not considered before. The involvement of these putative interactions in pontine-mediated control of IE phase transitions is discussed.

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Figures

Figure 1.
Figure 1.
Discharge patterns of pontine and medullary respiratory neurons. (a) Peri-stimulus triggered histogram (PSTH) derived from at least 10 consecutive respiratory cycles shows the discharge pattern of a pontine decrementing inspiratory with post-I after discharge (left-hand side) and late-inspiratory/post-I (right-hand side) phase-spanning neurons. (b) PSTHs of pontine (left-hand side) and medullary (right-hand side), (i)–(ii) post-I neurons (both with (i) long decrementing discharge and (ii) with short discharge) and (iii) constant expiratory neurons (con-E). PNA, phrenic nerve activity.
Figure 2.
Figure 2.
Voltage characteristics of key pontine and medullary neurons for IE phase transitions. (a) Pontine early-I neuron, (b) pontine IE phase-spanning neuron, (c) a second IE phase-spanning neuron that clearly showed augmenting excitatory post-synaptic potentials (EPSPs) with the onset of inspiration, (d) medullary late-I neuron, (e) medullary decrementing post-I neuron, and (f) pontine decrementing post-I neuron. Note that pontine IE neurons showed augmenting EPSPs during inspiration, while late-I medullary neurons were inhibited during 70 per cent of inspiratory phase and received excitatory synaptic input only during the late-I phase.
Figure 3.
Figure 3.
Hypothetical network model for pontine-mediated IE phase transition. For the theoretical model presented, the following predictions were made: the pontine early-I population receives excitatory synaptic input (efference copy 1) from I-driver neurons located in the pre-Bötzinger complex. The pontine early-I populations are inhibitory interneurons of the pons. The pontine early-I neurons inhibit the pontine IE phase-spanning neuron and pontine post-I pre-motoneurons (post-I) to prevent the initiation of phase transition during early and mid-inspiration (a). With ongoing inspiration, the pontine I/E neurons receive increasing excitatory drive (efference copy 2) from medullary aug-I pre-motor neurons that override the inhibition of early-I, causing firing onset around late inspiration. The pontine IE neurons are, in turn, excitatory interneurons that activate the medullary late-I neurons to initiate the IE phase transition (b). Finally, the inhibitory late-I neurons of the medulla terminate the activity of the medullary early-I neurons and release the medullary post-I population (inhibitory interneurons) from synaptic inhibition. These inhibitory post-I neurons inhibit all the inspiratory population (medullary and pontine). Consequently, the pontine and medullary post-I pre-motor population start firing. According to our previous publication (Dutschmannet al. 2008), we suggest that the pontine population could dominate the medullary populations (c). The effect of post-synaptic blockade of glutamatergic neurotransmission (e.g. NMDA-R antagonism) within the dorsolateral pons is illustrated in (d). Local blockade of excitatory synaptic interaction (black circles) in the pons suppresses theefference copies 1–2, causing blockade of the descending excitatory synaptic input from the pontine IE neurons to the medullary late-I population. This abolishes the pontine-mediated timing of the IE phase transition causing arrest in the inspiratory phase (apneusis). Note that other expiratory neurons that could be involved in the termination of the inspiratory burst are not considered in the theoretical sketch. Red circles, inhibitory interneurons; red lines, the associated connectivity; green circles without frame, excitatory interneurons; green circles with black frame, pre-motor neurons; green lines, excitatory connectivity. The right-hand frames of (a–d) illustrate the motor outputs of the phrenic nerve (PNA) and recurrent laryngeal nerve (RCNA). The green line indicates the point in time of the three-phase respiratory cycle (I, inspiration; PI, post-inspiration; E2, late expiration) that corresponds to the illustrated ponto-medullary synaptic interactions.
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