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

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

doi:10.1162/netn_a_00141

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

Netw Neurosci. 2020 Jul 1;4(3):678-697. doi: 10.1162/netn_a_00141. eCollection 2020.

Authors

Samantha P Sherrill¹, Nicholas M Timme², John M Beggs³, Ehren L Newman¹

Affiliations

¹ Department of Psychological and Brain Sciences and Program in Neuroscience, Indiana University Bloomington, Bloomington, IN, USA.
² Department of Psychology, Indiana University-Purdue University Indianapolis, Indianapolis, IN, USA.
³ Department of Physics & Program in Neuroscience, Indiana University Bloomington, Bloomington, IN, USA.

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.

Keywords: Computation; Correlated activity; Cortex; Effective connectivity; In vitro networks; Information theory; Neural information processing; Synergy.