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.

Highlights

  • As experimental tools advance, measuring whole-brain dynamics with single-neuron resolution becomes closer to reality [1,2,3,4]

  • Our main result is the development of a theoretical framework to infer hard-to-measure connection strengths in a minimal firing rate model, constrained by spike count statistics from simultaneous array recordings

  • We show that a general leaky integrate-and-fire (LIF) spiking neuron model of the coupled olfactory bulb (OB)-piriform cortex (PC) system can satisfy all 12 data constraints

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Summary

Introduction

As experimental tools advance, measuring whole-brain dynamics with single-neuron resolution becomes closer to reality [1,2,3,4]. We used two micro-electrode arrays to simultaneously record from olfactory bulb (OB) and anterior piriform cortex (PC) Constrained by these experimental data, we developed computational models and theory to investigate interactions within and between OB and PC. Each region contains multiple individual populations, each of which is modeled with a firing rate model [14]; even this minimal model involves several coupled stochastic differential equations (here, six) and has a large-dimensional parameter space Analysis of this system would be unwieldy in general; we address this by developing a novel method to compute firing statistics that is computationally efficient, captures the results of Monte Carlo simulations, and can provide analytic insight. These equations were derived using an approximation based on asymptotic expansions (see Materials and methods: Approximation of Firing Statistics in the Firing Rate Model for details)

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