Functional and Comparative Organization of the Insular Cortex and Interoceptive Pathways in Primates

COEX 

The brain evolved around the fundamental homeostatic needs of our organism. Therefore unsurprisingly, sensory afferents representing the physiological condition of the body (or interoception) profoundly influence even our most sophisticated brain functions. Likewise, interoceptive pathologies concur with various neuropsychiatric disorders. Our laboratory examines the interoceptive and autonomic circuits regulating bodily and brain states. In primates, interoceptive afferents form a phylogenetically novel ascending pathway terminating predominantly in the insular cortex. In this talk, I will present architectonics, tract-tracing, electrophysiological and neuroimaging evidence suggesting the existence of (1) a topographic representation of bodily afferents in the dorsal posterior insula or "primary interoceptive cortex", (2) a fine subdivision of the middle insula into distinct architectonic and hodological horizontal "stripes" putatively integrating interoception with poly-sensory inputs, and (3) an ultimate re-representation of contextualized homeostatic states in the ventral anterior insula. I will also show that the morphologically unique, spindle-shaped, von Economo neuron of the ventral anterior insula occupies one specific architectonic area and projects directly back to the primary central relays of interoception as well as to premotor and to pre-ganglionic autonomic centers in the brainstem. Using resting state functional connectivity in neurotypical and coma human subjects, we showed in collaboration that some of these projections may be crucial to associate cortical ‘awareness’ centers with subcortical ‘arousal’ centers, motivating a new series of studies aiming at better appreciating the role of interoception and the insula in brain states. FMRI with concurrent recording or microstimulation in the unique 'von Economo neuron area' confirmed the subcortical projections and unraveled prominent functional relations with high-order cortical areas. These observations support the idea that the ventral anterior insula serves as hub for the simultaneous interoceptive shaping of poly-sensory perceptual experience in an egocentric (‘sentient self’) perspective and the high-order affective regulation of homeostatic bodily states. My talk will illustrate also the advantage of combining fine neuroanatomical methods (architectonics and tract-tracing) with brainwide low spatial resolution fMRI and local high spatial resolution electrophysiology to investigate complex neural systems. It will also conclude on the importance of refined neuroanatomical examination for the comparison of cortical parcellation across species, suggesting the emergence of a higher structural complexity in the human anterior insula, compared to other primate species.