Distinct purinergic receptor-mediated currents of rat oculomotor integrator neurons characterized by different firing patterns

J Neurophysiol. 2021 Oct 1;126(4):1045-1054. doi: 10.1152/jn.00209.2021. Epub 2021 Aug 25.

Abstract

The prepositus hypoglossi nucleus (PHN) and the interstitial nucleus of Cajal (INC) are oculomotor neural integrators involved in the control of horizontal and vertical gaze, respectively. We previously reported that local application of adenosine 5'-trisphosphate (ATP) to PHN neurons induced P2X receptor-mediated fast inward currents, P2Y receptor-mediated slow inward currents, and/or adenosine P1 receptor-mediated slow outward currents. In contrast to the findings on PHN neurons, the expression of functional purinergic receptors in INC neurons has not been examined. In this study, we investigated ATP-induced current responses in INC neurons and the distributions of the three current types across distinct firing patterns in PHN and INC neurons using whole cell recordings of rat brainstem slices. The application of ATP induced all three current types in INC neurons. Pharmacological analyses indicated that the fast inward and slow outward currents were mainly mediated by the P2X and P1 subtypes, respectively, corresponding to the receptor subtypes in PHN neurons. However, agonists of the P2Y subtype did not induce the slow inward current in INC neurons, suggesting that other subtypes or mechanisms are responsible for this current. Analysis of the distribution of the three current types in PHN and INC neurons revealed that the proportions of the currents were distinctly dependent on the firing patterns of PHN neurons whereas the proportion of the fast inward current was higher during all firing patterns of INC neurons. The different distributions of ATP-induced currents suggest distinct modes of purinergic modulation specific to horizontal and vertical integrators.NEW & NOTEWORTHY The roles of purinergic signaling on vertical (mediated by the interstitial nucleus of Cajal; INC) and horizontal (prepositus hypoglossal nucleus; PHN) gaze control are not understood. Here, we report three current types induced by ATP in INC neurons; the distribution of these current types across different types of INC neurons is different from that in PHN neurons. These results suggest distinct modes of purinergic modulation in horizontal and vertical gaze control centers.

Keywords: ATP; adenosine; interstitial nucleus of Cajal; prepositus hypoglossi nucleus; whole cell recording.

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Animals
  • Electrophysiological Phenomena / physiology*
  • Eye Movements / physiology*
  • Female
  • Male
  • Neurons / physiology*
  • Patch-Clamp Techniques
  • Rats
  • Rats, Long-Evans
  • Receptors, Purinergic P2X / metabolism*
  • Receptors, Purinergic P2Y / metabolism*
  • Tegmentum Mesencephali / physiology*

Substances

  • Receptors, Purinergic P2X
  • Receptors, Purinergic P2Y
  • Adenosine Triphosphate