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Abstract

The central representation and the goal-directed control of bodily states are integrated in the anterior insular cortex (AIC) as core processes underlying the ‘subjective’ component of emotion and cognition. The AIC is often regarded as a key “node” of the saliency network with a role in coordinating brain network activity upon the detection of homeostatic changes. A model proposed that the preferential representation of parasympathetic and sympathetic activity in the left and right AIC underlies appetitive and aversive emotions, respectively (Craig TICS 2005 9:566-71). Given the possible role of the AIC in switching brain network dynamics, we examined whether this asymmetry occurs in functional relation of the AIC with the rest of the brain. To this end we used multi contact laminar electrodes to record neural activity from the left and right AIC in parallel while simultaneously acquiring functional magnetic resonance imaging (fMRI) scans in four rhesus macaque monkeys. The electrodes were placed in the AIC area containing the von Economo neurons (or ‘VEN area’), an area shown previously to be larger and independently contain more VENs on the right than on the left side (Evrard et al. Neuron 2012 74:482-9). The ongoing spontaneous neuronal activity was analyzed focusing on the local field potential (LFP) gamma band (56-79 Hz) where frequent increases in amplitude could be observed. These gamma events were in most cases unilateral, with occurrence either in the left or in the right VEN area in the majority of the cases and only few cases where gamma band activity increased simultaneously on both sides. Following the detection of these gamma events, their occurrence was used to trigger and average the blood-oxygen-level dependent (BOLD) signal from the fMRI scans, a method called ‘neural-event-triggered fMRI’ (NET-fMRI) (Logothetis et al. Nature 2012 491:547-53). The examination and mapping of the BOLD signal change during asymmetric events revealed markedly different patterns of activation and deactivation in vast regions of the brain. These effects might substantiate a fundamental autonomic forebrain asymmetry balancing brain dynamics to produce nurturing and expending behaviors and feelings in a homeostatically optimal manner.