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Abstract:
The posterior dorsal granular fundus of the insular cortex (IDFP) is the terminus of a phylogenetically recent spino-thalamo-cortical pathway, representing various interoceptive modalities, including thermoception. Prior tract-tracing and electrophysiological recordings in the anesthetized macaque, and neuroimaging in humans, indicated that thermoception is encoded along a posterior-to-anterior sacral-to-trigeminal somatotopy, with the face being represented in the most anterior portion of IDFP. Yet, direct evidence for the occurrence of a thermoceptive representation of trigeminal afferent in the awake macaque monkey is still needed. Here, we used an infrared Nd:YAP laser adapted for MR-compatibility to deliver 20 ms pulses of radiant heat over 0.9 mm diameter targets, along the maxillary division of the face, during contrast-agent enhanced, whole-brain, high-resolution fMRI (0.6 mm isotropic voxels at 3T) in an awake rhesus monkey implanted with 8-channel receiver coils. Low and high laser intensities were set to activate trigeminal C-/Aδ primary afferent fibers with temperatures reaching ~43°C and ~49°C, respectively (mean interstimulus interval = 21 sec). A GLM contrasting high intensity vs. null revealed activation predominantly in the anterior portion of IDFP, as well as in cortical areas 3a and 24, the posterior portion of the ventromedial thalamic nucleus, the periaqueductal gray, and the principal trigeminal nucleus, contralateral to the side of stimulation (voxel-wise, p<0.001). Additional activation occurred in the anterior insula, medial prefrontal area 32, lateral orbitofrontal area 11, and visual areas (V6), bilaterally. Split-half conjunction analysis of the high vs. null contrast further highlighted contralateral IDFP and bilateral anterior insula. Similar activations occurred in IDFP at more liberal thresholds when contrasting low intensity vs. null, consistent with prior evidence that the insula encodes stimulus intensity. Finally, epoched pupil diameter time-courses differentiated the conditions (cluster permutation, p<0.05). These results support the preponderance of a trigemino-thalamo-insular pathway for thermoception (including thermonociception) in primates with a localization of a face representation in anterior IDFP. Future analyses will test whether arousal (pupil dilation and heart rate variations) correlates with the thermosensory activation in bilateral anterior insula and extrastriate visual area V6, which may elucidate the contributions of salience and attention, respectively, in the processing of thermoception in primates.
