Activation of parallel fiber feedback by spatially diffuse stimuli reduces signal and noise correlations via independent mechanisms in a cerebellum-like structure.

Benjamin Simmonds,Gunnar Blohm,Maurice J Chacron

doi:10.1371/journal.pcbi.1004034

Benjamin Simmonds, Gunnar Blohm + Show 1 more

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https://doi.org/10.1371/journal.pcbi.1004034

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Journal: PLoS computational biology	Publication Date: Jan 8, 2015
Citations: 96	License type: CC BY 4.0

Affiliation: McGill University

Abstract

Correlations between the activities of neighboring neurons are observed ubiquitously across systems and species and are dynamically regulated by several factors such as the stimulus' spatiotemporal extent as well as by the brain's internal state. Using the electrosensory system of gymnotiform weakly electric fish, we recorded the activities of pyramidal cell pairs within the electrosensory lateral line lobe (ELL) under spatially localized and diffuse stimulation. We found that both signal and noise correlations were markedly reduced (>40%) under the latter stimulation. Through a network model incorporating key anatomical features of the ELL, we reveal how activation of diffuse parallel fiber feedback from granule cells by spatially diffuse stimulation can explain both the reduction in signal as well as the reduction in noise correlations seen experimentally through independent mechanisms. First, we show that burst-timing dependent plasticity, which leads to a negative image of the stimulus and thereby reduces single neuron responses, decreases signal but not noise correlations. Second, we show trial-to-trial variability in the responses of single granule cells to sensory input reduces noise but not signal correlations. Thus, our model predicts that the same feedback pathway can simultaneously reduce both signal and noise correlations through independent mechanisms. To test this prediction experimentally, we pharmacologically inactivated parallel fiber feedback onto ELL pyramidal cells. In agreement with modeling predictions, we found that inactivation increased both signal and noise correlations but that there was no significant relationship between magnitude of the increase in signal correlations and the magnitude of the increase in noise correlations. The mechanisms reported in this study are expected to be generally applicable to the cerebellum as well as other cerebellum-like structures. We further discuss the implications of such decorrelation on the neural coding strategies used by the electrosensory and by other systems to process natural stimuli.

Highlights

Understanding how the brain processes sensory information in order to lead to perception and behavior remains a central problem in neuroscience
Since experimental studies have shown that noise correlations were proportional to the amount of receptive field overlap between pyramidal cells [26], which is largely due to feedforward input from electroreceptor afferents [23], we assumed that noise correlations between our model superficial pyramidal cells (SPs) were due to the fact that they receive shared input from electroreceptor afferents and were modeled using shared noise with !c being the fraction of common feedforward noise input
In order to explain the observed reduction in noise correlations, we extended a previously published model that accurately describes how feedback can attenuate the responses of single pyramidal cells to global stimulation [32,33] to include: 1) correlated activity of multiple pyramidal cells and; 2) trial-to-trial variability in the spiking activities of individual granule cells

Summary

Introduction

Understanding how the brain processes sensory information in order to lead to perception and behavior remains a central problem in neuroscience. Mounting evidence suggests that studying correlations between neurons is required to understand the neural code [1,2,3,4]. Such correlations have been observed across systems and species and can have profound impact on neural population coding by, e.g., either decreasing or increasing information transmission depending on their sign [2,3,5,6,7]. Attentional processes can reduce correlations between neural responses [11], which is thought to reduce redundancy and maximize information transmission as originally proposed by Barlow [13,14]. Theoretical studies have proposed cellular and circuit mechanisms that can modulate correlated activity [15,16,17,18] but it is at best unclear how applicable these are in general [7]

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