Electroresponsive properties and membrane potential trajectories of three types of inspiratory neurons in the newborn mouse brain stem in vitro

Rekling, Jens C.; Champagnat, Jean; Denavit-Saubié, Monique

doi:10.1152/jn.1996.75.2.795

Cited by 104 publications

(175 citation statements)

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“…Our data indicates that the non-LTS spiking response might be driven by residual Ih currents during the rebound depolarization. Similar contributions of Ih to rebound responses are described elsewhere in the CNS (Foehring and Waters, 1991;Rekling et al, 1996;Koch and Grothe, 2003). The developmental shift in firing patterns that we observed might simply reflect maturation of conductances underlying AP generation, or an increase in Rin because we saw no corresponding increase in Ih expression.…”

Section: Developmental Changes In Voltage-gated Currentssupporting

confidence: 83%

Postnatal maturational properties of rat parafascicular thalamic neurons recorded in vitro

Phelan

Mahler

Deere

et al. 2005

THL

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Thalamic relay neurons have homogeneous, adult-like firing properties and similar morphology by 12 days postnatally (PN 12). Parafascicular (Pf) neurons have a different morphology compared with typical thalamic relay neurons, but the development of their electrophysiological properties is not well studied. Intracellular recordings in PN 12-50 Pf neurons revealed several heterogeneous firing patterns different from those in thalamic relay neurons. Two types of cells were identified: Type I cells displayed a fast afterhyperpolarization (AHP) followed by a large-amplitude, slow AHP; whereas Type II cells had only a fast AHP. These cell types had overlapping membrane properties but differences in excitability. Some properties of Pf neurons were adult-like by PN 12, but, unlike thalamic relay neurons, there were significant maturational changes thereafter, including decreased action potential (AP) duration, increased fast AHP amplitude and increased excitability. Pf neurons did not exhibit rhythmic bursting and generally lacked low-threshold spike (LTS) responses that characterize thalamic relay neurons. Pf neurons exhibited nonlinear I-V relationships, and only a third of the cells expressed the time and voltage-dependent hyperpolarization activated (Ih) current, which declined with age. These results indicate that the morphological differences between Pf neurons and typical thalamic relay neurons are paralleled by electrophysiological differences, and that Pf membrane properties change during postnatal development.

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Section: Developmental Changes In Voltage-gated Currentssupporting

confidence: 83%

Postnatal maturational properties of rat parafascicular thalamic neurons recorded in vitro

Phelan

Mahler

Deere

et al. 2005

THL

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“…As with the preburst ramp onset mentioned above, earlier initiation of a cell's burst phase has been hypothesized to play a role in rhythmogenesis (Butera et al 1999;Ramirez et al 2004;Rekling et al 1996). A range of roundedness of burst shape (Fig.…”

Section: Discussionmentioning

confidence: 75%

Patterns of inspiratory phase-dependent activity in the in vitro respiratory network

Carroll¹,

Viemari

Ramirez

2013

Journal of Neurophysiology

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Carroll MS, Viemari JC, Ramirez JM. Patterns of inspiratory phase-dependent activity in the in vitro respiratory network. J Neurophysiol 109: 285-295, 2013. First published October 17, 2012 doi:10.1152/jn.00619.2012.-Mechanistic descriptions of rhythmogenic neural networks have often relied on ball-and-stick diagrams, which define interactions between functional classes of cells assumed to be reasonably homogenous. Application of this formalism to networks underlying respiratory rhythm generation in mammals has produced increasingly intricate models that have generated significant insight, but the underlying assumption that individual cells within these network fall into distinct functional classes has not been rigorously tested. In the present study we used multiunit extracellular recording in the in vitro pre-Bötzinger complex to identify and characterize the rhythmic activity of 951 cells. Inspiratory phasedependent activity was estimated for all cells, and the data set as a whole was analyzed with principal component analysis, nonlinear dimensionality reduction, and hierarchical clustering techniques. None of these techniques revealed categorically distinct functional cell classes, indicating instead that the behavior of these cells within the network falls along several continua of spiking behavior. neuronal networks; pre-Bötzinger complex; respiration; cell types RHYTHMIC ACTIVITY IS UBIQUITOUS in neural systems, from the slow rhythm generated by the suprachiasmatic nuclei that synchronizes mammalian circadian cycles (Dibner et al. 2010), to the broad frequency spectra covered by various oscillations generated within cortical networks (Buzsaki and Draguhn 2004;Tort et al. 2010;Wang 2010). Many of the underlying rules of rhythm generation have been established in neural circuits that generate rhythmic motor behaviors (Goulding 2009;Grillner 2006;Marder and Calabrese 1996). These motor activities are typically reciprocal in nature (e.g., expiration and inspiration, extension and flexion, protraction and retraction) and are often described by ball-and-stick 1 schematics that assume specific connectivity (sticks) between different types of cells or cell populations (balls). In these models each cell possesses functionally discrete properties firing in distinct phases with respect to a given global activity pattern (Guertin 2009; Selverston 2010). Ball-and-stick representations have been particularly powerful in invertebrate neuronal networks (Antonsen and Edwards 2003), because the firing and connectivity properties of physiologically and anatomically identified individual neurons could be reproducibly characterized across different individuals of the same species (Jing et al. 2010;Katz et al. 2010;Marder and Calabrese 1996;Newcomb et al. 2012; Ramirez, 1998;White and Nusbaum 2011). One of the many important lessons learned from these small invertebrate networks is that even in the case of a truly identified neuron, electrophysiological measures of single-cell properties do not suffice to uniquely specify a ...

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“…Whole-cell patch-clamp recordings (n ϭ 37) were performed under visual control using differential interference contrast and infrared video microscopy, an Axoclamp2A amplifier (Axon Instruments, Foster city, CA), a digitizing interface (Digidata 1322A, Axon Instruments), and the software program pClamp8 (Axon Instruments). Neurons examined were type 2 nonpacemaker inspiratory neurons (Rekling et al, 1996;Thoby-Brisson et al, 2000) located ventral to the nucleus ambiguus and within 80 -100 m of the extracellular electrode. Patch electrodes were manufactured from borosilicate glass tubes containing a filament (Clark GC 150TF, Pangbourn, UK) and filled with a solution containing (in mM): 140 K-gluconic acid, 1 CaCl 2 , 10 EGTA, 2 MgCl 2 , 4 Na 2 -ATP, 10 HEPES, pH 7.2, and 0.05 mg/l Alexa Fluor 594 (Molecular Probes, Eugene, OR).…”

Section: Methodsmentioning

confidence: 99%

“…The PBC contains all elements sufficient for generation of the respiratory rhythm in slice preparations (Smith et al, 1991), and lesioning of the PBC in vivo abolishes breathing (Koshiya and Guyenet, 1998;Ramirez et al, 1998). The PBC includes a glutamatergic network of rhythmic neurons (Bianchi et al, 1995;Ramirez et al, 1997) that express the hyperpolarization-activated cationic current I h (Rekling et al, 1996;Thoby-Brisson et al, 2000) and the substance P receptor neurokinin 1 (NK1) (Gray et al, 1999;Wang et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

Expression of Functional Tyrosine Kinase B Receptors by Rhythmically Active Respiratory Neurons in the Pre-Bötzinger Complex of Neonatal Mice

et al. 2003

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Genetic loss of brain-derived neurotrophic factor (BDNF) severely disrupts brainstem control of respiratory rhythmogenesis in newborn mice; however, the sites at which BDNF acts to regulate respiratory rhythmogenesis are unknown. Using immunochemical and multiplex RT-PCR analysis in mouse brainstem slices, we report that the BDNF receptor, Tyrosine kinase B (TrkB), is strongly expressed in the pre-Bötzinger complex (PBC), the presumed site for rhythm generation, and colocalizes with neurokinin 1 (NK1), a marker of neurons critical for breathing. The period of the respiratory rhythm generated by PBC neurons in vitro was increased by 30% after BDNF treatment (100 ng/ml) and not by nerve growth factor (100 ng/ml) or BDNF (100 ng/ml) in the presence of the tyrosine kinase inhibitor K252a (200 nM). Both synaptic and voltage-dependent properties of PBC neurons were modified by BDNF. Synaptic currents underlying spontaneous rhythmic bursts and glutamate-evoked currents were enhanced by 66 and 33%, respectively. BDNF reduced the I h current amplitude in rhythmic neurons by 46% and shifted its activation curve by Ϫ17 mV. All neurons expressing TrkB mRNA (n ϭ 8) also expressed mRNAs for the I h current [hyperpolarization-activated cyclic nucleotide-sensitive cation nonselective channel (HCN1)], and three of four NK1-positive neurons coexpressed TrkB and HCN mRNA. Six of 16 PBC neurons expressed BDNF mRNA, supporting the possibility of autocrine and paracrine actions of BDNF within the respiratory pattern generator. Our data demonstrate that BDNF can modulate respiratory network activity through TrkB signaling in rhythmic PBC neurons.

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Electroresponsive properties and membrane potential trajectories of three types of inspiratory neurons in the newborn mouse brain stem in vitro

Cited by 104 publications

References 0 publications

Postnatal maturational properties of rat parafascicular thalamic neurons recorded in vitro

Postnatal maturational properties of rat parafascicular thalamic neurons recorded in vitro

Patterns of inspiratory phase-dependent activity in the in vitro respiratory network

Expression of Functional Tyrosine Kinase B Receptors by Rhythmically Active Respiratory Neurons in the Pre-Bötzinger Complex of Neonatal Mice

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