Neural processing of gustatory information in insular circuits

Maffei, Arianna; Haley, Melissa S.; Fontanini, Alfredo

doi:10.1016/j.conb.2012.04.001

Cited by 118 publications

(97 citation statements)

References 66 publications

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“…The IC received abundant projections from the basolateral amygdala, lateral hypothalamic area, and infralimbic cortex (Allen et al, 1991). Among these limbic structures, the basolateral amygdala has been well established as a critical region for CTA (Escobar et al, 2002;Escobar and Bermudez-Rattoni, 2000;Fontanini et al, 2009) and palatability (Fontanini et al, 2009;Maffei et al, 2012). Stimulation of the basolateral amygdala induces EPSPs, followed by profound IPSCs that are mediated by GABA B receptors in the IC pyramidal cells (Stone et al, 2011).…”

Section: Functional Implicationsmentioning

confidence: 99%

Anatomical and electrophysiological mechanisms for asymmetrical excitatory propagation in the rat insular cortex: In vivo optical imaging and whole‐cell patch‐clamp studies

Adachi

Fujita

Yoshida

et al. 2013

J of Comparative Neurology

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The insular cortex (IC) integrates limbic information from the amygdala and hypothalamic nucleus to multimodal sensory inputs, including visceral, gustatory, and somatosensory information. However, the functional framework of excitation in the IC is still unknown. We performed optical imaging and single pyramidal neuronal staining using a whole-cell patch-clamp technique in urethane-anesthetized rats to elucidate the precise anatomical and physiological features of IC pyramidal neurons, which regulate cortical information processing via their horizontal connections. Optical imaging revealed that electrical stimulation of the granular (GI) or dysgranular (DI) IC elicited characteristic excitatory propagations along the rostrocaudal axis parallel to the rhinal fissure, with a preference toward the rostral direction. Spatial patterns of the dendrites and axons of layer II/III pyramidal cells in the DI/GI support these functional features of excitation; for example, rostrocaudal axonal arbors tend to extend with a rostral directional preference. The mean length of the axons from the soma to the farthest site rostrally was ∼50% longer than that of the caudal length. Pyramidal cells in the DI/GI exhibited spontaneous membrane oscillation in the UP and DOWN states. Similarly to the evoked signals obtained by optical imaging, repetitive electrical stimulation of the caudal IC ∼1 mm away from the recorded cells (five pulses at 50 Hz) induced the summation of evoked excitatory postsynaptic potentials during the DOWN state and profound inhibitory postsynaptic potentials during the UP state. Clarification of the excitation feature with its cellular basis provides new clues about the functional mechanisms of the asymmetric propagation of neural activities in the IC.

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Section: Functional Implicationsmentioning

confidence: 99%

Anatomical and electrophysiological mechanisms for asymmetrical excitatory propagation in the rat insular cortex: In vivo optical imaging and whole‐cell patch‐clamp studies

Adachi

Fujita

Yoshida

et al. 2013

J of Comparative Neurology

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“…Taste is represented in the insula in both humans (Small, 2010) and rodents (Sewards and Sewards, 2001). Indeed, the insular cortex is the primary cortical region involved in taste and smell (Maffei et al, 2012), which may be part of a visceral response circuit that regulates food cravings and aversions (de Araujo and Simon, 2009). Interestingly, lesions of the insula are known to affect olfaction in humans (Mak et al, 2005; Stevenson et al, 2013), as well as diminished taste recognition and intensity deficits (Pritchard et al, 1999).…”

Section: The Functional Insula In Migrainementioning

confidence: 99%

The Insula

et al. 2016

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The insula, a ‘cortical hub’ buried within the lateral sulcus, is involved in a number of processes including goal-directed cognition, conscious awareness, autonomic regulation, interoception and somatosensation. While some of these processes are well known in the clinical presentation of migraine (i.e., autonomic and somatosensory alterations), other more complex behaviors in migraine, such as conscious awareness and error detection, are less well described. Since the insula processes and relays afferent inputs from brain areas involved in these functions to areas involved in higher cortical function such as frontal, temporal and parietal regions, it may be implicated as a brain region that translates the signals of altered internal milieu in migraine, along with other chronic pain conditions, through the insula into complex behaviors. Here we review how the insula function and structure is altered in migraine. As a brain region of a number of brain functions, it may serve as a model to study new potential clinical perspectives for migraine treatment.

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“…Additionally, viscerosensory signals are received in the adjoining region of granular insular cortex (GI) just dorsal and posterior to GC (5,6,11,14). Extensive and reciprocating projections are found both within the subdivisions of GC proper and among GC and its neighboring sensory fields in insular cortex, making it an ideal candidate region for multimodal sensory integration and associative processing of taste stimuli (15)(16)(17).…”

mentioning

confidence: 99%

High-resolution lesion-mapping strategy links a hot spot in rat insular cortex with impaired expression of taste aversion learning

Schier

Hashimoto

Bales

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Gustatory cortex (GC), an assemblage of taste-responsive neurons in insular cortex, is widely regarded as integral to conditioned taste aversion (CTA) retention, a link that has been primarily established using lesion approaches in rats. In contrast to this prevailing view, we found that even the most complete bilateral damage to GC produced by ibotenic acid was insufficient to disrupt postsurgical expression of a presurgical CTA; nor were such lesions sufficient to disrupt postsurgical acquisition and initial expression of a second CTA. However, some rats with lesions were significantly impaired on these tests. Further examination of all conditioned rats with lesions, regardless of the lesion topography, revealed a significant positive association between damage in the posterior portion of GC and especially within adjacent posterior regions of insular cortex. Accordingly, we developed a high-resolution lesion-mapping program that permitted the overlay of the individual lesion maps from rats with CTA impairments to produce a groupwise aggregate lesion map. Comparison of this map with one derived from the unimpaired counterparts indicated a specific lesion "hot spot" associated with CTA deficits that included the most posterior end of GC and overlying granular layer and encompassed an area provisionally referred to in the literature as visceral cortex. Thus, the detailed mapping of the lesion in behaviorally defined subgroups of rats allowed us to exploit the variability in performance to uncloak an important potential component of the functional topography of insular cortex; such an approach could have general applicability to other brain structure-function endeavors as well. W ith its primary receptors situated at the front end of the alimentary tract, the gustatory system is integrally involved in guiding food selection, promoting and discouraging intake, and evoking preparatory physiological reflexes (1). To best serve these functions, taste signals must confer with both the contemporary physiological milieu (e.g., satiety, malaise) and neurally stored representations of the associated effects of that particular taste stimulus [e.g., associative history with visceral malaise, as in conditioned taste aversion (CTA)]. However, the neural circuits underlying these critical integrative processes remain to be fully elucidated. In this regard, gustatory cortex (GC), an assemblage of taste-responsive neurons in the anterior dysgranular and agranular layers of insular cortex, is of particular interest (2-7). Receiving convergent input from both the thalamic and limbic taste pathways, GC consists of neurons that may potentially respond to various features of the taste stimulus, including chemosensory and hedonic alike, situated in close proximity to one another (5,(8)(9)(10)(11)(12)(13). Additionally, viscerosensory signals are received in the adjoining region of granular insular cortex (GI) just dorsal and posterior to GC (5,6,11,14). Extensive and reciprocating projections are found both within the subdivisions of G...

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Neural processing of gustatory information in insular circuits

Cited by 118 publications

References 66 publications

Anatomical and electrophysiological mechanisms for asymmetrical excitatory propagation in the rat insular cortex: In vivo optical imaging and whole‐cell patch‐clamp studies

Anatomical and electrophysiological mechanisms for asymmetrical excitatory propagation in the rat insular cortex: In vivo optical imaging and whole‐cell patch‐clamp studies

The Insula

High-resolution lesion-mapping strategy links a hot spot in rat insular cortex with impaired expression of taste aversion learning

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