Oscillatory integration windows in neurons.

Nitin Gupta,Swikriti Saran Singh,Mark Stopfer

doi:10.1038/ncomms13808

Abstract

Oscillatory synchrony among neurons occurs in many species and brain areas, and has been proposed to help neural circuits process information. One hypothesis states that oscillatory input creates cyclic integration windows: specific times in each oscillatory cycle when postsynaptic neurons become especially responsive to inputs. With paired local field potential (LFP) and intracellular recordings and controlled stimulus manipulations we directly test this idea in the locust olfactory system. We find that inputs arriving in Kenyon cells (KCs) sum most effectively in a preferred window of the oscillation cycle. With a computational model, we show that the non-uniform structure of noise in the membrane potential helps mediate this process. Further experiments performed in vivo demonstrate that integration windows can form in the absence of inhibition and at a broad range of oscillation frequencies. Our results reveal how a fundamental coincidence-detection mechanism in a neural circuit functions to decode temporally organized spiking.

Highlights

Oscillatory synchrony among neurons occurs in many species and brain areas, and has been proposed to help neural circuits process information
One mechanism by which oscillations have been proposed to influence coding is through the creation of cyclic integration windows—specific times within the oscillation cycle when synaptic input is most efficiently integrated by a postsynaptic neuron[9]
With simultaneous intracellular and field potential recordings we found that summation of inputs was more efficient in a specific part of the oscillatory cycle, demonstrating effective integration windows in Kenyon cells (KCs)

Summary

Introduction

Oscillatory synchrony among neurons occurs in many species and brain areas, and has been proposed to help neural circuits process information. KCs receive excitatory input from PNs followed by inhibitory input from GABAergic neurons[10,17]. Cyclic integration windows provide a possible mechanism for amplifying and privileging synchronized inputs from PNs. Spikes generated by KCs strongly phase-lock with the oscillations[6,10], but whether this occurs because KCs integrate input more effectively at some phases determined by integration windows, or because KCs receive more input at those phases, is not known. With simultaneous intracellular and field potential recordings we found that summation of inputs was more efficient in a specific part of the oscillatory cycle, demonstrating effective integration windows in KCs. with a computational model we revealed the substantial inhibition-independent contribution of noisy membrane potential fluctuations to this process. Our results establish that integration windows exist and provide a robust, simple and flexible mechanism for coincidence detection using oscillations

Methods

Results

Conclusion