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The Journal of Neuroscience, March 5, 2008, 28(10):2353-2365; doi:10.1523/JNEUROSCI.3553-07.2008

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Behavioral/Systems/Cognitive
Functional Imaging, Spatial Reconstruction, and Biophysical Analysis of a Respiratory Motor Circuit Isolated In Vitro

Hidehiko Koizumi,^1,2 * Christopher G. Wilson,^1,3,4 * Stephen Wong,^1,5 Tadashi Yamanishi,¹ Naohiro Koshiya,⁶ and Jeffrey C. Smith¹

¹Cellular and Systems Neurobiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892, ²Osaka University Graduate School of Dentistry, Osaka 565-0871, Japan, Departments of ³Pediatrics and ⁴Neurosciences, Case Western Reserve University, Cleveland, Ohio 44106, ⁵Howard Hughes Medical Institute, Bethesda, Maryland 20814, and ⁶Blanchette Rockefeller Neurosciences Institute, Johns Hopkins Campus, Rockville, Maryland 20850

Correspondence should be addressed to Dr. Jeffrey C. Smith, Porter Neuroscience Research Center, Building 35, Room 3C-917, 35 Convent Drive, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892. Email: jsmith{at}helix.nih.gov

We combined real-time calcium-based neural activity imaging with whole-cell patch-clamp recording techniques to map the spatial organization and analyze electrophysiological properties of respiratory neurons forming the circuit transmitting rhythmic drive from the pre-Bötzinger complex (pre-BötC) through premotoneurons to hypoglossal (XII) motoneurons. Inspiratory pre-BötC neurons, XII premotoneurons (preMNs), and XII motoneurons (MNs) were retrogradely labeled with Ca²⁺-sensitive dye in neonatal rat in vitro brainstem slices. PreMN cell bodies were arrayed dorsomedially to pre-BötC neurons with little spatial overlap; axonal projections to MNs were ipsilateral. Inspiratory MNs were distributed in dorsal and ventral subnuclei of XII. Voltage-clamp recordings revealed that two currents, persistent sodium current (NaP) and K⁺-dominated leak current (Leak), primarily contribute to preMN/MN subthreshold current–voltage relationships. NaP or Leak conductance densities in preMNs and MNs were not significantly different. We quantified preMN and MN action potential time course and spike frequency–current (f–I) relationships and found no significant differences in repetitive spiking dynamics, steady-state f–I gains, and afterpolarizing potentials. Rhythmic synaptic drive current densities were similar in preMNs and MNs. Our results indicate that, despite topographic and morphological differences, preMNs and MNs have some common intrinsic membrane, synaptic integration, and spiking properties that we postulate ensure fidelity of inspiratory drive transmission and conversion of synaptic drive into (pre)motor output. There also appears to be a common architectonic organization for some respiratory drive transmission circuits whereby many preMNs are spatially segregated from pre-BötC rhythm-generating neurons, which we hypothesize may facilitate downstream integration of convergent inputs for premotor pattern formation.

Key words: breathing; brainstem; calcium imaging; rhythm; pre-Bötzinger complex; premotoneurons

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Received Jan. 28, 2007; revised Jan. 11, 2008; accepted Jan. 13, 2008.

Correspondence should be addressed to Dr. Jeffrey C. Smith, Porter Neuroscience Research Center, Building 35, Room 3C-917, 35 Convent Drive, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892. Email: jsmith{at}helix.nih.gov

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