Cytoarchitecture of Pneumotaxic Integration of Respiratory and Nonrespiratory Information in the Rat

Abstract

The "pneumotaxic center" in the Kölliker-Fuse and medial parabrachial nuclei of dorsolateral pons (dl-pons) plays an important role in respiratory phase switching, modulation of respiratory reflex, and rhythmogenesis. Recent electrophysiological and neural tracing data implicate additional pneumotaxic nuclei in (and a broader role for) the dl-pons in integrating respiratory and nonrespiratory information. Here, we examined the cytoarchitecture of the greater pneumotaxic center and its integrating function by using combined extracellular recording and juxtacellular labeling of unit respiratory rhythmic neurons in dl-pons in urethane-anesthetized, vagotomized, paralyzed, and servo-ventilated adult Sprague Dawley rats. Perievent histogram analysis identified four major types of neuronal discharge patterns: inspiratory, expiratory (with three subdivisions), inspiratory-expiratory, and expiratory-inspiratory phase spanning, sometimes with mild tonic background activity. Most recorded neurons were localized in the Kölliker-Fuse and medial parabrachial nuclei, but some were also found in lateral parabrachial nucleus, intertrigeminal nucleus, principal trigeminal sensory nucleus, and supratrigeminal nucleus. The majority of labeled neurons had large and spatially extended dendritic trees that spanned several of these dl-pons subnuclei, often with terminal dendrites ending in the ventral spinocerebellar tract. The distal sections of the primary and higher-order dendrites exhibited rich varicosities, sometimes with dendritic spines. Axons of some labeled neurons were traced all the way to the ventrolateral pons (vl-pons). These findings extend and generalize the classical definition of the pneumotaxic center to include extensive somatic-axonal-dendritic integration of complex descending and ascending respiratory information as well as nociceptive and possibly musculoskeletal and trigeminal information in multiple dl-pons and vl-pons structures in the rat.