Extensive monosynaptic inhibition of ventral respiratory group neurons by augmenting neurons in the Bötzinger complex in the cat

Abstract

Axonal projections and synaptic connectivity of expiratory Bötzinger neurons with an augmenting firing pattern (Bot-Aug neurons) to neurons in the ipsilateral ventral respiratory group (VRG) were studied in anaesthetized cats. Antidromic mapping revealed extensive axonal arborizations of Bot-Aug neurons (24 of 45) to the rostral or caudal VRG, with some having arbors in both regions. Of 234 pairs of neurons studied with intracellular recording and spike-triggered averaging, monosynaptic inhibitory postsynaptic potentials (IPSPs) were evoked in 49/221 VRG neurons by 38/98 Bot-Aug neurons. The highest incidence of monosynaptic inhibition was found in inspiratory bulbospinal neurons (10 of 23 tested). Evidence was also found for monosynaptic inhibition, by a separate group of Bot-Aug neurons, of expiratory bulbospinal neurons (12/58), while excitatory postsynaptic potentials (EPSPs) were identified in another two of these neurons. In addition, monosynaptic IPSPs were recorded from 13 of 53 identified laryngeal motoneurons, and from 14 of 100 respiratory propriobulbar neurons. Presumptive disynaptic IPSPs were recorded from 11 of the 221 VRG neurons. We conclude that Bot-Aug neurons exert widespread inhibition on all major neuron categories in the ipsilateral VRG, and should be regarded as an important element in shaping the spatiotemporal output pattern of both respiratory motoneurons and premotor neurons.

Multifunctional Laryngeal Premotor Neurons: Their Activities during Breathing, Coughing, Sneezing, and Swallowing

“…Figure 1C shows an example of a hyperpolarizing potential in an ELM locked to the triggering spikes of an EAUG neuron. The sharp and fast rising phase of hyperpolarization (10 -90% rise time, 0.7 ms) indicates that this hyperpolarizing potential was a monosynaptically induced IPSP (Jankowska and Roberts, 1972;Ezure and Manabe, 1989;Jiang and Lipski, 1990). The following observations also support this.…”

“…The postsynaptic potentials that show a fast rise time are thought to be evoked by direct monosynaptic neurons (Jankowska and Roberts, 1972;Ezure and Manabe, 1989;Jiang and Lipski, 1990). A reliable criterion of a monosynaptic connection is a 10 -90% rise time of a PSP of Յ0.5 ms (Kirkwood, 1979).…”

“…A reliable criterion of a monosynaptic connection is a 10 -90% rise time of a PSP of Յ0.5 ms (Kirkwood, 1979). However, many monosynaptic postsynaptic potentials have longer rise times (Jack et al, 1971;Ezure and Manabe, 1989;Jiang and Lipski, 1990;Tian et al, 1999). When the 10 -90% rise time was Ͼ0.5 ms and Յ1.2 ms, we used an additional criterion of the similarity of antidromic and orthodromic latencies as shown by Ezure and Manabe (1988).…”

“…In the present study, we simultaneously recorded the intracellular activity of the laryngeal motoneuron and the extracellular activity of its premotor neuron during fictive breathing, coughing, sneezing, and swallowing to examine whether two or more distinct rhythmic motor patterns of the larynx are driven by common premotor neurons in the respiratory neuronal network. We focused on the expiratory neuron with an augmenting firing pattern (EAUG neuron) in the region spanning the Bötzinger (BÖ T) and pre-Bötzinger (preBÖ T) complexes as an inhibitory premotor neuron of the laryngeal adductor muscle (Jiang and Lipski, 1990;Ono et al, 2006).…”

Hypercapnia modulates synaptic interaction of cultured brainstem neurons

“…These units did not seem to be recorded from axons either, as the spikes showed typical morphology of somata action potentials (Fig. 4C 1 , D 1 ) (Gustafsson and Jankowska 1976;Jiang and Lipski 1990). When they were plotted in coupling efficiency against peak-mean ratio, these large central peaks were clearly segregated from the common inputs and pericentral peaks shown above (Fig 5), suggesting that these action potentials were recorded from two neurons with electrical synapses or gap junctions as have been previously observed in brainstem neurons (Huang et al 1997;Solomon and Dean 2002;Dean et al 2002).…”