Glutamatergic and purinergic transmitters and astrocyte modulation in the synaptic transmission in the NTS of rats exposed to short-term sustained hypoxia

Am J Physiol Regul Integr Comp Physiol. 2024 Oct 1;327(4):R423-R441. doi: 10.1152/ajpregu.00293.2023. Epub 2024 Aug 5.

Abstract

There is evidence that astrocytes modulate synaptic transmission in the nucleus tractus solitarius (NTS) interacting with glutamatergic and purinergic mechanisms. Here, using in situ working heart-brainstem preparations, we evaluated the involvement of astrocyte and glutamatergic/purinergic neurotransmission in the processing of autonomic and respiratory pathways in the NTS of control and rats exposed to sustained hypoxia (SH). Baseline autonomic and respiratory activities and the responses to chemoreflex activation (KCN) were evaluated before and after microinjections of fluorocitrate (FCt, an astrocyte metabolic inhibitor), kynurenic acid, and pyridoxalphosphate-6-azophenyl-2',4'-disulfonate (PPADS) (nonselective antagonists of glutamatergic and purinergic receptors) into the rostral aspect of the caudal commissural NTS. FCt had no effects on the baseline parameters evaluated but reduced the bradycardic response to chemoreflex activation in SH rats. FCt combined with kynurenic acid and PPADS in control rats reduced the baseline duration of expiration, which was attenuated after SH. FCt produced a large increase in PN frequency discharge in control rats, which was reduced after SH, indicating a reduction in the astrocyte modulation after SH. The data show that 1) the bradycardic component of the peripheral chemoreflex is reduced in SH rats after astrocytes inhibition, 2) the inhibition of astrocytes in the presence of double antagonists in the NTS affects the modulation of baseline duration of expiration in control but not in SH rats, and 3) the autonomic and respiratory responses to chemoreflex activation are mediated by glutamatergic and purinergic receptors in the rostral aspect of the caudal commissural NTS.NEW & NOTEWORTHY Our findings indicate that the neurotransmission of autonomic and respiratory components of the peripheral chemoreflex in the nucleus tractus solitarius (NTS) is mediated by glutamatergic and purinergic mechanisms and reveal a selective involvement of NTS astrocytes in controlling the chemoreflex parasympathetic response in rats exposed to sustained hypoxia (SH) and the baseline duration of expiration mainly in control rats, indicating a selective role for astrocytes modulation in the NTS of control and SH rats.

Keywords: ATP; NTS; astrocyte; glutamate; sustained hypoxia.

MeSH terms

  • Animals
  • Astrocytes* / drug effects
  • Astrocytes* / metabolism
  • Chemoreceptor Cells / drug effects
  • Chemoreceptor Cells / metabolism
  • Citrates / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Glutamic Acid* / metabolism
  • Hypoxia* / metabolism
  • Hypoxia* / physiopathology
  • Kynurenic Acid / pharmacology
  • Male
  • Pyridoxal Phosphate / analogs & derivatives
  • Pyridoxal Phosphate / pharmacology
  • Rats
  • Rats, Wistar
  • Receptors, Purinergic* / metabolism
  • Solitary Nucleus* / drug effects
  • Solitary Nucleus* / metabolism
  • Synaptic Transmission* / drug effects
  • Synaptic Transmission* / physiology
  • Time Factors

Substances

  • Glutamic Acid
  • Receptors, Purinergic
  • Kynurenic Acid
  • Excitatory Amino Acid Antagonists
  • fluorocitrate
  • Pyridoxal Phosphate
  • pyridoxal phosphate-6-azophenyl-2',4'-disulfonic acid
  • Citrates