Elsevier

Behavioural Brain Research

Volume 153, Issue 2, 31 August 2004, Pages 357-365
Behavioural Brain Research

Research report
Insular cortex lesions alter conditioned taste avoidance in rats differentially when using two methods of sucrose delivery

https://doi.org/10.1016/j.bbr.2003.12.011Get rights and content

Abstract

The insular gustatory cortex may be essential for the evaluation of saliency and representation of the incentive values of tastes. Gustatory cortex lesions should interfere with conditioned taste avoidance according to these factors, which depend on the conditioned taste avoidance protocol used. The present study was aimed at investigating the effects of bilateral lesions of the gustatory cortex—focusing on electrolytic and excitotoxic lesions. Lesioned and sham-operated male Long–Evans rats were intoxicated using LiCl after drinking sucrose from a tube (SD) or having the same amount of sucrose fed directly into their mouths through a chronically implanted intra-oral (IO) cannula. Every aspect of the experiment was carefully counterbalanced between the experimental groups. In the control groups, the acquired avoidance towards sucrose was strongly preserved over eight extinction test days in SD rats but not in IO rats, in which a progressive decline was recorded. Electrolytic gustatory cortex lesions impaired but did not suppress conditioned taste avoidance in both protocols. Excitotoxic lesions tend to impair CTA also, but differentially according to the SD or IO protocols. Extinction of CTA was selectively impaired in the SD protocol by small lesions destroying the anterior insular cortex.

Introduction

A single association between a novel taste and a gastric malaise elicits disgust and long-term avoidance of the taste [5]. This phenomenon, evidenced by a diversity of conditioned taste avoidance (CTA) or taste aversion protocols, requires processing and association of gustatory and aversive visceral information. Lesions of the insular cortex were reported to alter CTA [2], [8], [16], [17], [18], [19], [20], [23], [33]. It still has to be ascertained what brain function is sufficiently altered by insular cortex lesions to hinder CTA or prevent its acquisition. The neocortex may be essential for attending to stimuli [27]. A kind of taste agnosia—or failure to recognize the behavioural significance of tastes—has been proposed to account for what happens after insular cortex lesions [16]. For lesioned rats, tastes were no longer salient as associative cues [19]. Electrophysiological observations indicated that insular cortex neurons were responsive to a wide range of non-gustatory stimuli that may help to enhance their saliency. Their responsiveness was enhanced when the animal was watchful and ready to produce a response to the taste [38]. Such increase of saliency when the taste is the outcome of an action may even contribute to its incentive property, which was proven to depend on the integrity of the insular cortex [1].

Studies have been performed in our laboratory for several years using a protocol comparing extinction of CTA according to whether rats were allowed to drink freely or a taste was fed directly into their mouth by perfusion. Rats allowed to drink freely consistently showed a delayed extinction of CTA [11]. Self-generated drinking action, as well as other active means of getting to the taste, strengthened the memory of CTA and this has been interpreted as a consequence of an enhanced saliency of the taste [38]. According to the hypothesis mentioned above about the contribution of the insular cortex to the saliency of taste stimuli, especially when they represent the outcome of an instrumental learning [38], its destruction should alter CTA extinction in our two protocols differentially. Lesions should be more deleterious to CTA retention when the rat has to drink during acquisition. A similar idea had already inspired a study by Cubero et al. [7], but they used oro-facial movements and rejection of the tasty fluid infused into the mouth of the rat as an index of CTA when this behaviour may merely reflect disgust, which is only one facet of CTA [19]. A discriminatory avoidance testing method, like the one used in our protocols, seemed a more appropriate way of investigating the processes impaired by insular cortex lesions during CTA.

As heterogeneous observations were reported and because the techniques used to destroy the insular cortex differed, we decided to proceed both to electrolytic and excitotoxic lesions.

Section snippets

Materials and methods

The experiments were conducted by researchers, all of whom were authorised to use live rats by the French Ministry of Agriculture in accordance with French animal welfare laws.

Subjects, apparatus, procedure, statistical analysis and histology

Subjects, apparatus, procedure and statistical analyses were as described in Section 2.

Surgery

One week after their arrival, 20 rats were assigned randomly to the lesioned group and a further 20 to the sham-operation group. All rats were anaesthetized and placed in a stereotaxic frame as in experiment 1. Two holes were drilled on each side of the skull, both 5.5 mm lateral to the midline, but one 0.3 mm caudal and the other 1.7 mm rostral to the bregma point. Two stainless steel guide cannulae (0.4 mm

General discussion

This study confirms that extended lesions of the insular cortex reduce conditioned taste avoidance (CTA), rather than suppressing it. The difference between experiments 1 and 2 gives us some cause to think that the fibres of passage exiting from the insular cortex might have been involved in the disruption of CTA acquisition. For both protocols used—i.e. when rats drank sucrose freely (SD) or had it imposed on them (IO)—lesions produced an upwards shift in the mean sucrose intake after

Acknowledgements

Dr. Nadine Fresquet was awarded a grant by the Elie Lilly pharmaceutical company. We would also like to thank Mr. Andrew Wright for his suggestions concerning the English language in the text.

References (38)

Cited by (27)

  • The role of dopamine D2 receptors in the nucleus accumbens during taste-aversive learning and memory extinction after long-term sugar consumption

    2017, Neuroscience
    Citation Excerpt :

    Nonetheless, under the two bottles choice protocol used in the experiments reported here, we did not observe a significant latent inhibition of CTA after 14 days of sugar consumption (Fig. 4B). Indeed, latent inhibition of CTA varies according to the protocol used and previous studies have examined the extent to which conditioning and testing methods influence the effects of lesions or pharmacological manipulations on CTA learning, suggesting different outcomes depending on the extent to which the delivery of the taste stimulus, in the conditioning protocol, incorporates a response requirement (Schafe et al., 1998; Cubero et al., 1999; Fresquet et al., 2004). Thus, in our study, rats were able to make a decision, choosing between water and sugar during taste-aversive memory retrieval and extinction trials.

  • Gustatory insular cortex, aversive taste memory and taste neophobia

    2015, Neurobiology of Learning and Memory
    Citation Excerpt :

    With regard to taste learning, most of the studies involving the GC are concerned with its role in CTA. Thus, lesions of the GC were reported to disrupt CTA acquisition (e.g., Bermudez-Rattoni and McGaugh, 1991; Braun, Slick, & Lorden, 1972; Cubero, Thiele, & Bernstein, 1999; Fresquet, Angst, & Sandner, 2004; Gallo, Roldan, & Bureš, 1992; Nerad, Ramı́rez-Amaya, Ormsby, & Bermúdez-Rattoni, 1996). However, as indicated by recent findings, these deficits seem not to be related to an impairment in associating the CS with the US.

  • Taste neophobia and c-Fos expression in the rat brain

    2012, Brain Research
    Citation Excerpt :

    Earlierwork using c-Fos to examine the neural substrates of neophobia (e.g., Houpt et al., 1994; Yamamoto et al., 1997) infusedthe taste stimuli directly into the mouth, an approach that may not be ideal for the assessment of a voluntary avoidancebehavior. Furthermore, CTA acquisition following intraorally infused CSs is known to engage a somewhat different neural substrate than CSs which are voluntarily consumed (Fresquet et al., 2004; Schafe et al., 1998; St. Andre and Reilly, 2007; for a review see Reilly, 2009) and, as shown by Wilkins and Bernstein (2006), each CS delivery method causes a different pattern of c-Fos expression. Accordingly, the present experiment investigated c-Fos expression in the BLA, BNST, CNA, GT, IC, MeA and mPBN in rats voluntarily drinking a novel taste or, after repeated exposures, the same taste when familiar.

  • Conditioned taste aversion and latent inhibition following extensive taste preexposure in rats with insular cortex lesions

    2009, Brain Research
    Citation Excerpt :

    A conditioned taste aversion (CTA) is manifested as a reduction in consumption of a taste (conditioned stimulus, CS) that has previously been followed by gastrointestinal illness (unconditioned stimulus, US). Considerable research has been conducted to identify the neurological substrates of this learning phenomenon (e.g., Reilly, 2009), and one brain structure that has been implicated in CTA acquisition is the insular cortex (IC; e.g., Bermúdez-Rattoni and McGaugh, 1991; Braun et al., 1972; Cubero et al., 1999; Fresquet et al., 2004; Gallo et al., 1992; Nerad et al., 1996). However, the inconsistent experimental procedures used in these studies have made it difficult to identify the exact nature of the IC lesion (ICX) deficit.

  • The hidden island of addiction: the insula

    2009, Trends in Neurosciences
    Citation Excerpt :

    Lesion studies in humans have shown effects on taste recognition after posterior insula lesions [33,34]. Lesion studies in rodents have demonstrated a role for the agranular insula in working memory for taste [35,36] and in conditioned taste aversion [37,38], in which the animal learns to avoid a previously palatable taste after it becomes associated with a stimulus that causes sickness or malaise. Dopaminergic function within this region has been found to play a particular part in this type of learning [39].

View all citing articles on Scopus
View full text