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Computation is concentrated in rich clubs of local cortical networks.

ABSTRACT: To understand how neural circuits process information, it is essential to identify the relationship between computation and circuit organization. Rich clubs, highly interconnected sets of neurons, are known to propagate a disproportionate amount of information within cortical circuits. Here, we test the hypothesis that rich clubs also perform a disproportionate amount of computation. To do so, we recorded the spiking activity of on average ∼300 well-isolated individual neurons from organotypic cortical cultures. We then constructed weighted, directed networks reflecting the effective connectivity between the neurons. For each neuron, we quantified the amount of computation it performed based on its inputs. We found that rich-club neurons compute ∼160% more information than neurons outside of the rich club. The amount of computation performed in the rich club was proportional to the amount of information propagation by the same neurons. This suggests that in these circuits, information propagation drives computation. In total, our findings indicate that rich-club organization in effective cortical circuits supports not only information propagation but also neural computation.

SUBMITTER: Faber SP

PROVIDER: S-EPMC6370472 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Computation is concentrated in rich clubs of local cortical networks.

Faber Samantha P SP Timme Nicholas M NM Beggs John M JM Newman Ehren L EL

Network neuroscience (Cambridge, Mass.) 20190201 2

To understand how neural circuits process information, it is essential to identify the relationship between computation and circuit organization. Rich clubs, highly interconnected sets of neurons, are known to propagate a disproportionate amount of information within cortical circuits. Here, we test the hypothesis that rich clubs also perform a disproportionate amount of computation. To do so, we recorded the spiking activity of on average ∼300 well-isolated individual neurons from organotypic c ...[more]

PMID: 30793088

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Project description:BackgroundGeneral anesthesia (GA) provides an invaluable experimental tool to understand the essential neural mechanisms underlying consciousness. Previous neuroimaging studies have shown the functional integration and segregation of brain functional networks during anesthetic-induced alteration of consciousness. However, the organization pattern of hubs in functional brain networks remains unclear. Moreover, comparisons with the well-characterized physiological unconsciousness can help us understand the neural mechanisms of anesthetic-induced unconsciousness.MethodsResting-state functional magnetic resonance imaging was performed during wakefulness, mild propofol-induced sedation (m-PIS), and deep PIS (d-PIS) with clinical unconsciousness on 8 healthy volunteers and wakefulness and natural sleep on 9 age- and sex-matched healthy volunteers. Large-scale functional brain networks of each volunteer were constructed based on 160 regions of interest. Then, rich-club organizations in brain functional networks and nodal properties (nodal strength and efficiency) were assessed and analyzed among the different states and groups.ResultsRich-clubs in the functional brain networks were reorganized during alteration of consciousness induced by propofol. Firstly, rich-club nodes were switched from the posterior cingulate cortex (PCC), angular gyrus, and anterior and middle insula to the inferior parietal lobule (IPL), inferior parietal sulcus (IPS), and cerebellum. When sedation was deepened to unconsciousness, the rich-club nodes were switched to the occipital and angular gyrus. These results suggest that the rich-club nodes were switched among the high-order cognitive function networks (default mode network [DMN] and fronto-parietal network [FPN]), sensory networks (occipital network [ON]), and cerebellum network (CN) from consciousness (wakefulness) to propofol-induced unconsciousness. At the same time, compared with wakefulness, local connections were switched to rich-club connections during propofol-induced unconsciousness, suggesting a strengthening of the overall information commutation of networks. Nodal efficiency of the anterior and middle insula and ventral frontal cortex was significantly decreased. Additionally, from wakefulness to natural sleep, a similar pattern of rich-club reorganization with propofol-induced unconsciousness was observed: rich-club nodes were switched from the DMN (including precuneus and PCC) to the sensorimotor network (SMN, including part of the frontal and temporal gyrus). Compared with natural sleep, nodal efficiency of the insula, frontal gyrus, PCC, and cerebellum significantly decreased during propofol-induced unconsciousness.ConclusionsOur study demonstrated that the rich-club reorganization in functional brain networks is characterized by switching of rich-club nodes between the high-order cognitive and sensory and motor networks during propofol-induced alteration of consciousness and natural sleep. These findings will help understand the common neurological mechanism of pharmacological and physiological unconsciousness.

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Computation is concentrated in rich clubs of local cortical networks.

Publications

Computation is concentrated in rich clubs of local cortical networks.

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