The human insula reimagined: Single neurons respond to simple sounds during passive listening

Abstract

The insula is critical for integrating sensory information from the body with that arising from the environment. Although previous studies suggested that posterior insula is sensitive to sounds, these studies usually involved behaviorally relevant stimuli. Further, auditory response properties of the human insula have not previously been studied on the single-neuron level. Here, we provide the first report of a population of human single neuron data from both anterior and posterior insula and provide comparative data from the primary auditory cortex, recorded intracranially from human participants during passive listening. In each condition, more than 340 single neurons were recorded in 12 participants of either sex. Almost a third of neurons in posterior insula and a smaller subset in anterior insula responded to simple tones and clicks. Responsive neurons were distributed throughout posterior and anterior insula and showed preferred frequency tuning. Onset latencies in insula were short, but response durations were significantly shorter than primary auditory cortex. Overall, these data show that insula neurons respond to auditory stimuli even in non-behaviorally relevant contexts and change our understanding of this brain region, suggesting that processing basic auditory stimuli is an important integrative function of insular cortex.Significance Statement The insula is postulated to integrate interoceptive and exteroceptive signals. However, response properties of insula neurons to simple auditory stimuli have not previously been examined. Here, we record single neurons from the anterior and posterior insula in humans, as well as from adjacent auditory cortex. We characterize response properties and show that all three regions respond to basic sounds in the absence of any behavioral context. These data are of fundamental importance for understanding how the insula contributes to our perception of the external world.