Glutamatergic activities in neonatal rat spinal cord heterogeneously regulate single-fiber splanchnic nerve discharge

Ho, Chiu‐Ming; Chiang, Chun; Lee, Chia-Ming; Fan, Yu-Pei; Su, Chun-Kuei

doi:10.1016/j.autneu.2013.04.008

Cited by 5 publications

(9 citation statements)

References 26 publications

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“…En bloc preparations retaining the splanchnic sympathetic nerve–thoracic spinal cord (T1–T12) were prepared following surgical procedures as previously described (Su, 1999 ; Ho et al, 2013 ). Briefly, neonatal rats were made unconscious by hypothermia (Danneman and Mandrell, 1997 ), followed by a prompt midcollicular decerebration.…”

Section: Methodsmentioning

confidence: 99%

“…Complexity in the operation of the sympathetic-correlated neural circuit in the spinal cord is clearly revealed by the heterogeneous responses of their efferent fiber activities, when a variety of antagonists were applied to alter the endogenous receptor activities. Our previous studies demonstrate that GABAergic, glycinergic, and glutamatergic spinal neurons working, respectively, via GABA A receptors, glycine receptors, and ionotropic glutamate receptors exert functionally distinct influences on different sympathetic fiber activities (Ho et al, 2013 ; Su, 2016 ). For those fibers of low and high spontaneous activities, their firing tends to be increased and decreased, respectively, by inhibition of endogenous GABA A or glycine receptor activities.…”

Section: Introductionmentioning

confidence: 99%

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Nitric Oxide Orchestrates a Power-Law Modulation of Sympathetic Firing Behaviors in Neonatal Rat Spinal Cords

Chen

2018

Front. Physiol.

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Nitric oxide (NO) is a diffusible gas and has multifarious effects on both pre- and postsynaptic events. As a consequence of complex excitatory and inhibitory integrations, NO effects on neuronal activities are heterogeneous. Using in vitro preparations of neonatal rats that retain the splanchnic sympathetic nerves and the thoracic spinal cord as an experimental model, we report here that either enhancement or attenuation of NO production in the neonatal rat spinal cords could increase, decrease, or not change the spontaneous firing behaviors recorded from splanchnic sympathetic single fibers. To elucidate the mathematical features of NO-mediated heterogeneous responses, the ratios of changes in firing were plotted against their original firing rates. In log-log plots, a linear data distribution demonstrated that NO-mediated heterogeneity in sympathetic firing responses was well described by a power function. Selective antagonists were applied to test if glycinergic, GABAergic, glutamatergic, and cholinergic neurotransmission in the spinal cord are involved in NO-mediated power-law firing modulations (plFM). NO-mediated plFM diminished in the presence of mecamylamine (an open-channel blocker of nicotinic cholinergic receptors), indicating that endogenous nicotinic receptor activities were essential for plFM. Applications of strychnine (a glycine receptor blocker), gabazine (a GABAA receptor blocker), or kynurenate (a broad-spectrum ionotropic glutamate receptor blocker) also caused plFM. However, strychnine- or kynurenate-induced plFM was diminished by L-NAME (an NO synthase inhibitor) pretreatments, indicating that the involvements of glycine or ionotropic glutamate receptor activities in plFM were secondary to NO signaling. To recapitulate the arithmetic natures of the plFM, the plFM were simulated by firing changes in two components: a step increment and a fractional reduction of their basal firing activities. Ionotropic glutamate receptor activities were found to participate in plFM by both components. In contrast, GABAA receptor activities are involved in the component of fractional reduction only. These findings suggest that NO orchestrates a repertoire of excitatory and inhibitory neurotransmissions, incurs a shunting effect on postsynaptic membrane properties, and thus, alters sympathetic firing in a manner of plFM. We propose that the plFM mediated by NO forms a basic scheme of differential controls for heterogeneous sympathetic regulation of visceral functions.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Nitric Oxide Orchestrates a Power-Law Modulation of Sympathetic Firing Behaviors in Neonatal Rat Spinal Cords

Chen

2018

Front. Physiol.

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“…Dissociation of the nerve bundles was performed by incubating the splanchnic nerves for ~90 min in a glass micropipette containing 0.5% collagenase (Type IV collagenase, C5138, Sigma-Aldrich, buffered by Hanks' Balanced Salt Solution, 14185-052, Invitrogen Corporation). Dissociated nerve fascicles showing a nerve stub with split ends were easily obtained after the incubation (Ho et al, 2013). …”

Section: Methodsmentioning

confidence: 99%

“…We used a splanchnic sympathetic nerve-thoracic spinal cord preparation that can spontaneously generate rhythmic SND in vitro as an experimental model (Su, 1999). Collagenase was used for in situ dissociation of the splanchnic nerve bundles (Ho et al, 2013). The dissociated nerve fascicles were then brought into a suction electrode to record several fiber activities, the so-called “oligofiber recording.”…”

Section: Introductionmentioning

confidence: 99%

Computational solution of spike overlapping using data-based subtraction algorithms to resolve synchronous sympathetic nerve discharge

Chiang

Lee

et al. 2013

Front. Comput. Neurosci.

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Sympathetic nerves conveying central commands to regulate visceral functions often display activities in synchronous bursts. To understand how individual fibers fire synchronously, we establish "oligofiber recording techniques" to record "several" nerve fiber activities simultaneously, using in vitro splanchnic sympathetic nerve-thoracic spinal cord preparations of neonatal rats as experimental models. While distinct spike potentials were easily recorded from collagenase-dissociated sympathetic fibers, a problem arising from synchronous nerve discharges is a higher incidence of complex waveforms resulted from spike overlapping. Because commercial softwares do not provide an explicit solution for spike overlapping, a series of custom-made LabVIEW programs incorporated with MATLAB scripts was therefore written for spike sorting. Spikes were represented as data points after waveform feature extraction and automatically grouped by k-means clustering followed by principal component analysis (PCA) to verify their waveform homogeneity. For dissimilar waveforms with exceeding Hotelling's T 2 distances from the cluster centroids, a unique data-based subtraction algorithm (SA) was used to determine if they were the complex waveforms resulted from superimposing a spike pattern close to the cluster centroid with the other signals that could be observed in original recordings. In comparisons with commercial software, higher accuracy was achieved by analyses using our algorithms for the synthetic data that contained synchronous spiking and complex waveforms. Moreover, both T 2 -selected and SA-retrieved spikes were combined as unit activities. Quantitative analyses were performed to evaluate if unit activities truly originated from single fibers. We conclude that applications of our programs can help to resolve synchronous sympathetic nerve discharges (SND).

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“…Heterogeneity in drug-induced firing responses is basal activity-dependent [23,[26][27][28]. In other words, an antagonist application tends to suppress those sympathetic fibers with higher basal firing rates and boost those with lower ones.…”

Section: A Quantitative Expression Of the Neural Network Activity By LVmentioning

confidence: 99%

Central visceral commands formatted as the slow rhythms encoded in the temporal structures of the sympathetic firing originated from the neonatal rat spinal cord in vitro

2022

Preprint

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Central sympathetic neural circuits continuously generate efferent commands to sustain rhythmic operations of their peripheral effectors. However, beyond the firing rates, in what configuration an effective visceral command is formatted by the spiking activities was largely unknown. This study used an in vitro splanchnic nerve–spinal cord preparation of the neonatal rats as an experimental model and recorded spontaneous efferent activities from single sympathetic fibers. The patterns of the fiber activities were quantitatively evaluated by a metric, the so-called local variation (Lv). Lv was derived from calculating the relative differences between adjacent interspike intervals (ISIs), and thus, described the spiking patterns from a regular spiking with Lv = 0 to that spiking in bursts with Lv >1. Along the time course, the dynamic components of Lv (dLv) displayed quasiperiodic oscillations. Continuous wavelet analysis showed that dLv oscillations registered a dominant power rhythm at ~7 mHz. This slow rhythmicity was heterogeneously altered by application of various antagonists that interrupted endogenous neurotransmitter activities mediated by ionotropic glutamate receptors or GABA A receptors in the spinal cord. Thus, the oscillation of dLv manifested itself as a feature of neural network operation. On the assumption that the total power of the dLv oscillations reflects an activity status of neural network operation, the antagonist-induced change of the power fits well with a concomitant ISI change in a negative sigmoid relationship, which explains the heterogeneity of the antagonist-induced firing responses. In conclusion, dLv oscillations reflect a dynamic status of neural network operation. The slow rhythms embedded in the dLv oscillations are likely acting as an information coder and convey effective central visceral commands that can be followed by their downstream effectors.

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Glutamatergic activities in neonatal rat spinal cord heterogeneously regulate single-fiber splanchnic nerve discharge

Cited by 5 publications

References 26 publications

Nitric Oxide Orchestrates a Power-Law Modulation of Sympathetic Firing Behaviors in Neonatal Rat Spinal Cords

Nitric Oxide Orchestrates a Power-Law Modulation of Sympathetic Firing Behaviors in Neonatal Rat Spinal Cords

Computational solution of spike overlapping using data-based subtraction algorithms to resolve synchronous sympathetic nerve discharge

Central visceral commands formatted as the slow rhythms encoded in the temporal structures of the sympathetic firing originated from the neonatal rat spinal cord in vitro

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