Correlated activity favors synergistic processing in local cortical networksin vitroat synaptically-relevant timescales

Abstract

<jats:title>ABSTRACT</jats:title><jats:p>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 3000 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.</jats:p><jats:sec><jats:title>AUTHOR SUMMARY</jats:title><jats:p>In the present work, we address the question of whether correlated activity in functional networks of cortical circuits supports neural computation. To do so, we combined network analysis with information theoretic tools to analyze the spiking activity of hundreds of neurons recorded from organotypic cultures of mouse somatosensory cortex. We found that, at timescales most relevant to direct neuronal communication, neurons with more correlated activity predicted greater computation, suggesting that correlated activity does support computation in cortical circuits. Importantly, this result reversed at timescales less relevant to direct neuronal communication, where even greater correlated activity predicted decreased computation. Thus, the relationship between correlated activity and computation depends on the timescale and the degree of correlation in neuronal interactions.</jats:p></jats:sec>

Quantifying dynamical high-order interdependencies from the O-information: an application to neural spiking dynamics

“…The relation between mutual information and synergistic information processing in spiking neurons from organotypic cultures of mouse neocortex was recently addressed in (Sherrill et al, 2020), and was found to depend on the timescale and the degree of correlation in neuronal interactions. As an example of application of dO-information, we have considered the response of a neural system to an external stimulus.…”

Information processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior

“…While the existence of synergy in biological neural networks is extremely well documented [21,24,25,26,36],…”

“…Materials & Methods). In addition, all values (AIS, mTE, and synergy) were normalized by dividing by the Shannon entropy of the receiver neuron, following [24,25,26], which provides a control for variable firing rates.…”

Neural Dependency Coding inspired Multimodal Fusion

“…Moreover, Sherrill et al (2021) recently have shown that recurrent information flow in cortical circuits leads to an increase in neural synergy and neural complexity. Sherrill et al (2020) show that correlated activity and neural synergy were positively related when multiple external correlated stimuli are provided. Thus, synergy in neural firings is a representation of the similarity between inputs.…”