A theoretical framework for analyzing coupled neuronal networks: Application to the olfactory system

PLoS Comput Biol. 2017 Oct 2;13(10):e1005780. doi: 10.1371/journal.pcbi.1005780. eCollection 2017 Oct.

Abstract

Determining how synaptic coupling within and between regions is modulated during sensory processing is an important topic in neuroscience. Electrophysiological recordings provide detailed information about neural spiking but have traditionally been confined to a particular region or layer of cortex. Here we develop new theoretical methods to study interactions between and within two brain regions, based on experimental measurements of spiking activity simultaneously recorded from the two regions. By systematically comparing experimentally-obtained spiking statistics to (efficiently computed) model spike rate statistics, we identify regions in model parameter space that are consistent with the experimental data. We apply our new technique to dual micro-electrode array in vivo recordings from two distinct regions: olfactory bulb (OB) and anterior piriform cortex (PC). Our analysis predicts that: i) inhibition within the afferent region (OB) has to be weaker than the inhibition within PC, ii) excitation from PC to OB is generally stronger than excitation from OB to PC, iii) excitation from PC to OB and inhibition within PC have to both be relatively strong compared to presynaptic inputs from OB. These predictions are validated in a spiking neural network model of the OB-PC pathway that satisfies the many constraints from our experimental data. We find when the derived relationships are violated, the spiking statistics no longer satisfy the constraints from the data. In principle this modeling framework can be adapted to other systems and be used to investigate relationships between other neural attributes besides network connection strengths. Thus, this work can serve as a guide to further investigations into the relationships of various neural attributes within and across different regions during sensory processing.

MeSH terms

  • Animals
  • Cerebral Cortex / physiology
  • Computational Biology / methods*
  • Male
  • Models, Neurological
  • Nerve Net / physiology*
  • Odorants
  • Olfactory Bulb / physiology*
  • Olfactory Pathways / physiology*
  • Rats
  • Smell / physiology*

Grants and funding

This work was supported by: Simons Foundation http://www.simonsfoundation.org/, #355173 (CL) and Arkansas Biosciences Institute http://arbiosciences.org/, #0188 (SHG, WLS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.