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Abstract

The central representation and the goal-directed control of homeostatic bodily states are integrated in the anterior insular cortex (AIC) as core processes underlying emotion, cognition, and subjective perception. The AIC has been thought as a “node” of the saliency network with a role in coordinating brain network activity based on the detection of homeostatic changes. A recent model proposed that the left and right AIC preferentially represent parasympathetic and sympathetic activity while underlying appetitive and aversive emotions, respectively. Given the possible role of the AIC in switching brain network activities, we examined whether this asymmetry occurs in the functional relation of the AIC with the rest of the brain. We used laminar electrodes to record local field potential activity in the left and right AIC while simultaneously acquiring functional magnetic resonance imaging (fMRI) scans in four rhesus macaque monkeys. The electrode was placed in the AIC area containing the von Economo neuron (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. 2012 Neuron 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 complex nurturing and expending behaviors and feelings in a homeostatically optimal manner.