Edited by: Rodrigo Iturriaga, P Universidad Católica Chile, Chile
Reviewed by: Machiko Shirahata, Johns Hopkins University, USA; Ana Rita Nunes, Centro de Estudos de Doenças Crónicas, Portugal
*Correspondence: Mauricio A. Retamal, Facultad de Medicina, Centro de Fisiología Celular e Integrativa, Clínica Alemana Universidad del Desarrollo, Av Las Condes 12438, Santiago 7690000, Chile e-mail:
Julio Alcayaga, Laboratorio de Fisiología Celular, Departamento de Biología, Facultad de Ciencias, Universidad de Chile, Las Palmeras 3425, Santiago 7800003, Chile e-mail:
This article was submitted to Integrative Physiology, a section of the journal Frontiers in Physiology.
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The petrosal ganglion (PG) is a peripheral sensory ganglion, composed of pseudomonopolar sensory neurons that innervate the posterior third of the tongue and the carotid sinus and body. According to their electrical properties PG neurons can be ascribed to one of two categories: (i) neurons with action potentials presenting an inflection (hump) on its repolarizing phase and (ii) neurons with fast and brisk action potentials. Although there is some correlation between the electrophysiological properties and the sensory modality of the neurons in some species, no general pattern can be easily recognized. On the other hand, petrosal neurons projecting to the carotid body are activated by several transmitters, with acetylcholine and ATP being the most conspicuous in most species. Petrosal neurons are completely surrounded by a multi-cellular sheet of glial (satellite) cells that prevents the formation of chemical or electrical synapses between neurons. Thus, PG neurons are regarded as mere wires that communicate the periphery (i.e., carotid body) and the central nervous system. However, it has been shown that in other sensory ganglia satellite glial cells and their neighboring neurons can interact, partly by the release of chemical neuro-glio transmitters. This intercellular communication can potentially modulate the excitatory status of sensory neurons and thus the afferent discharge. In this mini review, we will briefly summarize the general properties of PG neurons and the current knowledge about the glial-neuron communication in sensory neurons and how this phenomenon could be important in the chemical sensory processing generated in the carotid body.
The petrosal ganglion (PG) contains the soma of pseudomonopolar sensory neurons (Ramón y Cajal,
Intracellular recordings show two major populations of neurons according to their action potential (AP) waveform: neurons with APs presenting an inflection (hump) on its repolarizing phase (Figure
The central axotomy has no significant effect on PG neurons that present a hump in the AP, irrespective of their peripheral projection. However, peripheral axotomy decreases the conduction velocity, after hyperpolarization amplitude but increases AP duration without modifying resting membrane potential (Vm) or input resistance (Rin) (Belmonte et al.,
Cat PG neurons projecting through the CSN with myelinated axons can also be categorized according to their AP waveform. Thus, sensory neurons connected to the CB present humped APs with longer hyperpolarizations and phasic responses (Belmonte and Gallego,
Patch clamp recordings of rat isolated chemosensory neurons indicate that they present both transient and persistent TTX-sensitive Na+ currents. Conversely, non-chemosensory PG neurons persistent Na+ current is TTX-insensitive (Cummins et al.,
Mechanosensory neurons appear to comprise a population of large, fast conducting neurons that present fast APs with short hyperpolarizations, generated by a TTX sensitive Na+-current and a TEA-sensitive K+-current, respectively. On the other hand, chemosensory neurons present APs of longer duration and long lasting hyperpolarization, resulting from the presence of Ca2+-currents and a Ca2+-dependent K+-current, respectively, as well as other K+-currents.
Many transmitter molecules have been indicated to participate in the generation and/or modulation of carotid chemosensory activity (González et al.,
Cat and rabbit PG neurons projecting through the CSN increase their AP discharge frequency in response to acetylcholine (ACh), effect blocked by nicotinic ACh receptor (nAChR) antagonists (Alcayaga et al.,
In cultured PG neurons ACh and nicotine induces depolarization (Zhong and Nurse,
In a reconstituted system, containing rat NPJc neurons and CB cells, the basal neuronal activity as well as hypoxia induced increases in neuronal activity are partially blocked by nAChRs antagonists (Zhong et al.,
The rabbit and cat PG neurons projecting through the CSN increase their spiking activity in response to ATP in a dose dependent manner (Alcayaga et al.,
Whole cell recordings of cultured cat PG neurons show that ATP induces a dose dependent depolarization that increased the discharge frequency and a sustained inward current at a holding potential near the resting Vm (−60 mV) (Alcayaga et al.,
Recordings of identified cat chemosensory neurons (Varas et al.,
Dopamine is another neurotransmitter involved in the CB-petrosal neuron communication. The presence of D1- and D2-dopamine receptor mRNA in rat and cat PG (Schamel and Verna,
The aforementioned data indicate that PG neurons that project to the CB are excited, at least, by ACh and ATP and those responses can also be modulated by, dopamine. However, the lack of complete elimination of responses to hypoxia
As mentioned before, PG neurons express several different types of receptors -including ionotropic and metabotropic- in their somas. Rabbit's but not rat's petrosal neurons change their response to neurotransmitters as a consequence of normobaric chronic hypoxia (Iturriaga and Alcayaga,
An increasing body of evidence shows that there is information processing into sensory ganglia related to the appearance and/or maintenance of chronic pain. Thus, satellite glial cells (SGCs) of trigeminal and dorsal root ganglion are activated in response to neuronal damage and/or to inflammatory process. This activation -correlated with an increased sensory neurons activity- (Blum et al.,
Since there are no works showing information processing in the PG, it is necessary to perform experiments in order to explore the possibility that SGCs and petrosal neurons communicate. This could be due to the release of neuro- and/or glio-transmitters through Cx hemichannels or Panx channels, as suggested by Retamal et al. (
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
This work was funded by grants FONDECYT #1120214 (Mauricio A. Retamal), 1090157 (Julio Alcayaga) and 1130177 (Julio Alcayaga), and Anillo #ACT1104 (Mauricio A. Retamal).