Differential Effects of Anterior and Posterior Insular Cortex Lesions on the Acquisition of Conditioned Taste Aversion and Spatial Learning

Nerad, Ludı̀k; Ramírez‐Amaya, Víctor; Ormsby, Christopher E.; Bermúdez‐Rattoni, Federico

doi:10.1006/nlme.1996.0042

Cited by 83 publications

(46 citation statements)

References 4 publications

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supporting

confidence: 90%

“…These findings provide compelling evidence that the IC is not engaged uniquely in the (associative) learning and recognition of taste, but that it plays a more general role in recognition memory. Such findings fit well with recent findings of two brain imaging studies suggesting an involvement of the IC in human face and tactile recognition (Paller et al 2003;Reed et al 2004), as well as with evidence that reversible or permanent lesions of the IC produce strong impairments in the consolidation of inhibitory avoidance and watermaze spatial learning Nerad et al 1996).It is well established that a network of temporal structures including the perirhinal, parahippocampal, and entorhinal cortices and the hippocampus participates in recognition memory. Our results suggest that the IC is part of this network, as it is highly involved in processing the consolidation of newly presented tastes and, as the present findings indicate, of objects.…”

supporting

confidence: 90%

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Insular cortex is involved in consolidation of object recognition memory

Bermúdez-Rattoni¹,

Okuda²,

Roozendaal³

et al. 2005

Learn. Mem.

107

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Previous findings indicate that the insular cortex (IC) is involved in conditioned taste aversion and taste recognition. Here we report evidence that the IC is not uniquely dedicated to taste learning but plays a more general role in consolidating recognition memories. Immediate post-training infusions of the muscarinic cholinergic receptor antagonist scopolamine administered into the IC produced locus-specific and time-dependent impairment of object recognition memory.Extensive evidence indicates that the IC, also termed gustatory cortex, is critically involved in conditioned taste aversion and taste recognition memory (Bermudez-Rattoni 2004). Although most studies of the involvement of the IC in memory have investigated taste, there is some evidence that the IC is involved in memory that is not based on taste Paller et al. 2003;Reed et al. 2004). Converging evidence from animal and human studies suggests that a network of temporal cortical regions participates in recognition memory (Tang et al. 1997;Aggleton and Brown 1999;Malkova and Mishkin 2003;Reed et al. 2004). However, there is little information on the role of the IC in visual recognition memory. Therefore, the present study examined the involvement of the IC in the consolidation of object recognition memory, a task based on the tendency of rodents to explore a novel object more than a familiar one (Ennaceur and Delacour 1988). As microdialysis studies have shown that the release of acetylcholine in the IC in response to a novel, but not a familiar, taste stimulus (Miranda et al. 2000) and cortical cholinergic activity is involved in the acquisition of object recognition memory (Tang et al. 1997;Warburton et al. 2003), the present study examined whether the muscarinic cholinergic receptor antagonist scopolamine infused into the IC immediately after training impairs the consolidation of object recognition memory. To control for site specificity, other rats received posttraining infusions of scopolamine into the frontoparietal cortex (FPC), dorsomedial but adjacent to the IC. All experimental procedures were in compliance with NIH guidelines and approved by the UC Irvine's Institutional Animal Care and Use Committee.Adult male Sprague-Dawley rats (280-320 g at time of surgery) from Charles River Laboratories were implanted under sodium pentobarbital anesthesia (50 mg/kg, ip) with bilateral guide cannulae (23-ga.) aimed either at the IC [coordinates of the infusion sites from bregma (Paxinos and Watson 1986): anteroposterior (AP), +1.2 mm; mediolateral (ML), ‫5.5ע‬ mm; dorsoventral (DV), ‫5.6מ‬ mm] or the FPC (AP, +1.2 mm; ML, ‫0.4ע‬ mm; DV, ‫0.3מ‬ mm). Histological examination revealed that the injection needle tips were placed in the granular and agranular divisions of the IC, from ‫3.0מ‬ to +1.7 mm from bregma (Fig. 1A). Needles aimed at the FPC were found in the dorsal FPC from ‫8.0מ‬ to +1.7 mm from bregma (Fig. 1B). Three animals with cannulae misplacements were excluded from analyses, leaving 8-11 animals per group.After recovery, the rats were trai...

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supporting

confidence: 90%

supporting

confidence: 90%

Insular cortex is involved in consolidation of object recognition memory

Bermúdez-Rattoni¹,

Okuda²,

Roozendaal³

et al. 2005

Learn. Mem.

107

View full text Add to dashboard Cite

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“…2,18,21,22,25,27,30,36,37). This, coupled with the fact that previous studies (24,38) showed that neither damage to AI just caudal to GC nor to an area even more posterior in insular cortex than the hot spot identified here affected CTA, highlights the strong possibility that discrepancies across studies critically hinge upon the involvement of a specific area (or areas) of this cortical region. Especially considering that the lesion's impact on CTA expression was partial in the present study, it remains crucial to determine whether this relates more to the function of insular cortex in CTA (e.g., modulatory) and/ or if the region identified here collaborates with some or all of nearby GC and/or brain sites outside of insular cortex that remained unscathed.…”

Section: Discussionsupporting

confidence: 55%

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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“…Electrophysiological recordings in the GC showed that some neurons vary their response pattern before and after CTA (19,32). Cortical lesions studies demonstrated that the insular cortex (that contains the GC) is important for CTA acquisition (11,33), although some particular insular lesions only partially disrupt CTA (34). However, the consensus is that GC is necessary for an effective acquisition of CTA (12).…”

Section: Discussionmentioning

confidence: 99%

Internal body state influences topographical plasticity of sensory representations in the rat gustatory cortex

Accolla

Carleton²

2008

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

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Primary sensory cortices are remarkably organized in spatial maps according to specific sensory features of the stimuli. These cortical maps can undergo plastic rearrangements after changes in afferent (''bottom-up'') sensory inputs such as peripheral lesions or passive sensory experience. However, much less is known about the influence of ''top-down'' factors on cortical plasticity. Here, we studied the effect of a visceral malaise on taste representations in the gustatory cortex (GC). Using in vivo optical imaging, we showed that inducing conditioned taste aversion (CTA) to a sweet and pleasant stimulus induced plastic rearrangement of its cortical representation, becoming more similar to a bitter and unpleasant taste representation. Using a behavior task, we showed that changes in hedonic perception are directly related to the maps plasticity in the GC. Indeed imaging the animals after CTA extinction indicated that sweet and bitter representations were dissimilar. In conclusion, we showed that an internal state of malaise induces plastic reshaping in the GC associated to behavioral shift of the stimulus hedonic value. We propose that the GC not only encodes taste modality, intensity, and memory but extends its integrative properties to process also the stimulus hedonic value.chemical senses ͉ map plasticity ͉ taste coding

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Differential Effects of Anterior and Posterior Insular Cortex Lesions on the Acquisition of Conditioned Taste Aversion and Spatial Learning

Cited by 83 publications

References 4 publications

Insular cortex is involved in consolidation of object recognition memory

Insular cortex is involved in consolidation of object recognition memory

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

Internal body state influences topographical plasticity of sensory representations in the rat gustatory cortex

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