Topographically organized projection to posterior insular cortex from the posterior portion of the ventral medial nucleus in the long‐tailed macaque monkey

Abstract

Prior anterograde tracing work identified somatotopically organized lamina I trigemino- and spino-thalamic terminations in a cytoarchitectonically distinct portion of posterolateral thalamus of the macaque monkey, named the posterior part of the ventral medial nucleus (VMpo; Craig, 2004b). Microelectrode recordings from clusters of selectively thermoreceptive or nociceptive neurons were used to guide precise micro-injections of various tracers in VMpo. A prior report (Craig and Zhang, 2006) described retrograde tracing results, which confirmed the selective lamina I input to VMpo and the antero-posterior (head to foot) topography. The present report describes the results of micro-injections of anterograde tracers placed at different levels in VMpo, based on the antero-posterior topographic organization of selectively nociceptive units and clusters over nearly the entire extent of VMpo. Each injection produced dense, patchy terminal labeling in a single coherent field within a distinct granular cortical area centered in the fundus of the superior limiting sulcus. The terminations were distributed with a consistent antero-posterior topography over the posterior half of the superior limiting sulcus. These observations demonstrate a specific VMpo projection area in dorsal posterior insular cortex that provides the basis for a somatotopic representation of selectively nociceptive lamina I spinothalamic activity. These results also identify the VMpo terminal area as the posterior half of interoceptive cortex; the anterior half receives input from the vagal-responsive and gustatory neurons in the basal part of the ventral medial nucleus (VMb).

Neurophysiology of Skin Thermal Sensations

“…Hence, and similarly to what observed in the macaque thalamus, the posterior ventral medial nucleus (VMpo) of the human thalamus could represent the main rely site for pure cold sensations in the human thalamus (60,80). The fact that this thalamic region has been shown to convey thermo-sensory inputs to the insular cortex (a cortical region which has recently shown to be involved in temperature sensation in humans) (58,60,62,88), further support its role as a rely site for pure thermal sensibility within the central thermo-sensory pathway in humans.…”

“…Amongst these areas, the dorsal margin of the posterior insular cortex has been proposed as the specific area for the cortical processing of both the discriminative (157) and affective (62,251) components of thermal sensations in humans. The fact that this cortical region has been previously shown to receive projection from those third-order thermo-sensory neurons which are located in the posterior ventral medial nucleus (VMpo) of the primate and human thalamus, and which are part of that spino-thalamo temperature pathway representing the main ascending pathway for temperature sensation in both primates (58) and humans (88), has further strengthened the evidence in support of a specific thermo-sensory role for the human posterior insular cortex. Nevertheless, evidence arising from lesion studies observing retained thermosensory function in individuals presenting a disease-induce loss of insular cortices (72), has also questioned the hypothesis (57, 59) for which the human dorsal insula would be the exclusive cortical area for the processing of thermal sensibility (72) and of human feelings in general (73).…”

“…While the evidence presented above should be taken into consideration in the context of multimodal thermal processing, it is however important to stress the fact that within the context of pure thermal sensibility, the most recent evidence in primates point to the key role of the macaque's posterior ventral medial nucleus (VMpo) in thalamic thermo-sensory integration (58). The importance of such evidence is further highlighted by the observation that this area is a specific homologue of the posterior part of the human ventral medial thalamus (VMpo) (60), a thalamic region which has been proposed as the primary thalamic rely for cold sensation in humans (80).…”

The Insular Cortex and the Regulation of Cardiac Function

“…These areas were clearly demarcated from each other and it is speculated by the authors that they represent different connectivity relationships between each insular subzone and other brain areas subserving different functional activities. Their anterograde tracing studies investigating thalamoinsular connectivity to some extent have supported this conjecture (66).…”

Interoceptive contributions to healthy eating and obesity

“…This is surprising given that the nervous system’s wiring diagram reveals that many of the signals relevant to satiety and food intake travel via the vagus nerve from the stomach to the brain, terminating in a unique region of the cortex that subserves both monitoring the state of the body and the sense of taste [9,17,18]. Specifically, the primary interoceptive and gustatory cortices are co-located within a region of the dorsal posterior-to-mid insular cortex [19–22], which receives afferent projections from the vagus via the solitary nucleus, parabrachial nucleus, and the ventroposterior medial nucleus of the thalamus, the dedicated visceral and gustatory thalamic relay [23]. Activity in this region of the insula is observed in neuroimaging studies using gustatory stimulation [24], as well as various types of viscerosensation, including cardiovascular arousal [25,26], heartbeat-evoked response [27], gastric distension [28], bladder fullness [29], and vagal nerve stimulation [17].…”