Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat

Abstract

The functional organization of the insular cortex was studied by recording neuronal responses to visceral sensory stimuli. Horseradish peroxidase (HRP) was then iontophoresed at the recording sites to identify afferents from the ventrobasal thalamus to specific visceroceptive sites in the insular cortex. The relationship of the ventrobasal thalamus to the insular cortex and to brainstem relay nuclei for the ascending visceral projections was then examined by using the axonal transport of HRP, wheat germ agglutinin conjugated to HRP (WGA-HRP), and fluorescent dyes. Of a total of 55 neurons that were tested for responses to visceral sensory stimuli, 33 units responded to at least one visceral sensory modality: 6 received gastric mechanoreceptor input, 8 responded to taste inputs, 13 were activated by arterial chemoreceptors and/or showed respiratory related activity, and 6 responded to cardiovascular baroreceptor stimulation. On the basis of its cytoarchitecture and connections with the thalamus, the insular cortex was divided into a dorsal granular area, an intermediate dysgranular region, and a ventral agranular strip. Taste-responsive neurons were located anteriorly, primarily in the dysgranular region, whereas unit responses to general visceral modalities were distributed dorsally and posteriorly in the granular insular cortex. Gastric mechanoreceptor-responsive units were situated more dorsally and anteriorly in the granular insular cortex, while cardiopulmonary inputs were located more ventrally and posteriorly. Injections of HRP into the gustatory insular cortex resulted in retrograde labeling of neurons in the parvicellular part of the ventroposterior medial thalamic nucleus (VPMpc). Injections into the general visceral insular cortex retrogradely labeled neurons lateral to VPMpc in the ventroposterior lateral parvicellular thalamic nucleus (VPLpc). Injections of HRP, WGA-HRP, and fluorescent dyes into VPMpc and VPLpc verified that their projection to the insular cortex is topographically organized. In the same experiments, retrogradely labeled neurons in the parabrachial nucleus identified the likely subnuclei within this nucleus for relay of visceral sensory information to the thalamus. Injections of WGA-HRP into the parabrachial nucleus demonstrated that its projection to the ventrobasal thalamus is also topographically organized. These results demonstrate the relationship of general visceral and special visceral (taste) representations in the insular cortex. The ascending pathway for visceral sensory information appears to be viscerotopically organized at all levels of the neuraxis, including the insular cortex.

The Insular Cortex and the Amygdala: Shared Functions and Interactions

“…Although a clear map of the viscerosensory area of the IC is still missing, areas within both the dysgranular and granular cortices have been identified as viscerosensory responsive [3,10,19,[92][93][94]. In Cechetto and Saper (1987) [3], a viscerosensory area within the Insular cortex was reported while exploring from 2.0 mm anterior to 0.5 mm posterior to the crossing of the anterior commissure (around the bregma) in rats. They found the majority of the baroreceptor-responsive units between +1.00 and -0.5 mm.…”

“…The most accepted subdivisions of the IC are the three regions described by Cecheto and Saper (1987) [3], based on the cytoarchitecture of its layers within the ventrodorsal plane. These include (1) the agranular insular cortex (AI) which surrounds the rhinal fissure and lacks a granular layer, (2) the dysgranular insular cortex (DI) which is located just dorsal to the rhinal fissure and contains a diffuse granular layer, and (3) the granular insular cortex (GI), situated just ventral to the secondary somatosensory cortex with a clear granular layer [3].…”

“…These include (1) the agranular insular cortex (AI) which surrounds the rhinal fissure and lacks a granular layer, (2) the dysgranular insular cortex (DI) which is located just dorsal to the rhinal fissure and contains a diffuse granular layer, and (3) the granular insular cortex (GI), situated just ventral to the secondary somatosensory cortex with a clear granular layer [3]. Each subdivision is believed to process particular sensory information.…”

“…Each subdivision is believed to process particular sensory information. For example, the AI is believed to participate in nociceptive [4][5][6] and autonomic processing [3], the DI plays a role in gustatory processing [7,8] and the GI has an important role in modulating visceral function [3].…”

“…Such studies include anatomical, electrophysiological, lesion, pharmacological and imaging studies, as well as operatory stimulation techniques which have yielded plausible roles for the IC in dozens of different functions. Several studies indicate that the IC is involved in taste processing [7,8,28,41], viscerosensory information processing [3,20,26,38,42,43], temperature and pain perception [44,45], olfaction [46] auditory processing [47][48][49], somatosensory perception [49,50], drug craving [51], motor tasks [52] and post-stroke motor-recovery functions [53].…”