Correlated activity favors synergistic processing in local cortical networks in vitro at synaptically relevant timescales.

Nicholas M Timme,John M Beggs,Samantha P Sherrill,Ehren L Newman

doi:10.1162/netn_a_00141

Abstract

Neural information processing is widely understood to depend on correlations in neuronal activity. However, whether correlation is favorable or not is contentious. Here, we sought to determine how correlated activity and information processing are related in cortical circuits. Using recordings of hundreds of spiking neurons in organotypic cultures of mouse neocortex, we asked whether mutual information between neurons that feed into a common third neuron increased synergistic information processing by the receiving neuron. We found that mutual information and synergistic processing were positively related at synaptic timescales (0.05–14 ms), where mutual information values were low. This effect was mediated by the increase in information transmission—of which synergistic processing is a component—that resulted as mutual information grew. However, at extrasynaptic windows (up to 3,000 ms), where mutual information values were high, the relationship between mutual information and synergistic processing became negative. In this regime, greater mutual information resulted in a disproportionate increase in redundancy relative to information transmission. These results indicate that the emergence of synergistic processing from correlated activity differs according to timescale and correlation regime. In a low-correlation regime, synergistic processing increases with greater correlation, and in a high-correlation regime, synergistic processing decreases with greater correlation.

Highlights

What role does the correlated activity among cortical neurons play in neural information processing? Correlated activity is ubiquitous throughout the brain, emerging from both external stimuli and internal dynamics
We quantified the amount of computation performed by the receiver on the inputs using “synergy,” a term derived from partial information decomposition
The correlation between multivariate transfer entropy (mvTE) and synergy was significantly greater at synaptic compared with extrasynaptic timescales (Zr.s. = 9.99, p < 1 × 10−22, n = 150 networks; Figure 5D). These results indicate that the growth of information transmission with correlated activity that contributed to increased synergistic processing at synaptic timescales was lost at extrasynaptic timescales

Summary

Introduction

What role does the correlated activity among cortical neurons play in neural information processing? Correlated activity is ubiquitous throughout the brain, emerging from both external stimuli and internal dynamics. The synchronization of neuronal spiking is linked to higher order cognitive and behavioral processes (Grammont & Riehle, 1999; Riehle et al, 1997; Vinck et al, 2015) From this perspective, correlation is favorable for information processing. Even within the cognitive rhythms community there is recognition that excess correlation can be unfavorable and that, in some circumstances, desynchronization supports information processing better than synchronization (e.g., Bastos et al, 2015; Hanslmayr et al, 2012; van Winsun et al, 1984). The discrepancy between this and the standard view of the cognitive rhythms community warrants reconciliation (Hanslmayr, Staresina, & Bowman, 2016)

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Discussion

Conclusion