Dorsal and median raphe neuronal firing dynamics characterized by nonlinear measures

PLoS Comput Biol. 2024 May 28;20(5):e1012111. doi: 10.1371/journal.pcbi.1012111. eCollection 2024 May.

Abstract

The dorsal (DRN) and median (MRN) raphe are important nuclei involved in similar functions, including mood and sleep, but playing distinct roles. These nuclei have a different composition of neuronal types and set of neuronal connections, which among other factors, determine their neuronal dynamics. Most works characterize the neuronal dynamics using classic measures, such as using the average spiking frequency (FR), the coefficient of variation (CV), and action potential duration (APD). In the current study, to refine the characterization of neuronal firing profiles, we examined the neurons within the raphe nuclei. Through the utilization of nonlinear measures, our objective was to discern the redundancy and complementarity of these measures, particularly in comparison with classic methods. To do this, we analyzed the neuronal basal firing profile in both nuclei of urethane-anesthetized rats using the Shannon entropy (Bins Entropy) of the inter-spike intervals, permutation entropy of ordinal patterns (OP Entropy), and Permutation Lempel-Ziv Complexity (PLZC). Firstly, we found that classic (i.e., FR, CV, and APD) and nonlinear measures fail to distinguish between the dynamics of DRN and MRN neurons, except for the OP Entropy. We also found strong relationships between measures, including the CV with FR, CV with Bins entropy, and FR with PLZC, which imply redundant information. However, APD and OP Entropy have either a weak or no relationship with the rest of the measures tested, suggesting that they provide complementary information to the characterization of the neuronal firing profiles. Secondly, we studied how these measures are affected by the oscillatory properties of the firing patterns, including rhythmicity, bursting patterns, and clock-like behavior. We found that all measures are sensitive to rhythmicity, except for the OP Entropy. Overall, our work highlights OP Entropy as a powerful and useful quantity for the characterization of neuronal discharge patterns.

MeSH terms

  • Action Potentials* / physiology
  • Animals
  • Computational Biology
  • Male
  • Models, Neurological*
  • Neurons* / physiology
  • Nonlinear Dynamics*
  • Raphe Nuclei / physiology
  • Rats
  • Rats, Sprague-Dawley

Grants and funding

This study was supported by the “Programa de Desarrollo de Ciencias Básicas, PEDECIBA” (https://www.pedeciba.edu.uy/es/area/biologia/) and the “Comisión Sectorial de Investigación Científica” (CSIC) I + D grupos 2022-22620220100148 grant from Uruguay (https://www.csic.edu.uy/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.