Concurrent conditioned taste aversion: A learning mechanism based on rapid neural versus flexible humoral processing of visceral noxious substances

Mediavilla, Cristina; Molina, Filomena; Puerto, Amadeo

doi:10.1016/j.neubiorev.2005.06.002

Cited by 38 publications

(21 citation statements)

References 119 publications

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“…Our data support the proposal of two different mechanisms that explain the consequences of intragastrically administered nutrients (Agü ero et al 1993a,b;Mediavilla et al 2000Mediavilla et al , 2005. One is independent of the LPB, given that the lesioned animals and controls both show aversion to the intragastrically administered nutrients by rejecting the associated gustatory stimulus.…”

Section: Discussionsupporting

confidence: 90%

Lesions of the lateral parabrachial area block the aversive component and induced-flavor preference for the delayed intragastric administration of nutrients in rats: Effects on subsequent food and water intake

Zafra¹,

Simon²,

Molina³

et al. 2005

Nutritional Neuroscience

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The aim of this study was to examine the function of the lateral parabrachial area (LPB) in relation to the intragastric administration of nutrients. The consumption of flavors associated with intragastric nutrient administration and the subsequent food and water intake were measured in rats with lesions in the LPB. The results showed that bilateral LPB lesions prevented development of aversions and induced flavor preference when there was a delay between the presentation of a flavor and the intragastric administration of nutrients. However, these lesions did not disrupt development of the aversive process when there was no delay between the presentations. Likewise, the LPB lesions increased subsequent food intake when there was a delay but not when there was no delay between the presentations. In contrast, the water intake was reduced in both situations. These results are interpreted in terms of a dual visceral system for processing the intragastric effects of foods.

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Section: Discussionsupporting

confidence: 90%

Lesions of the lateral parabrachial area block the aversive component and induced-flavor preference for the delayed intragastric administration of nutrients in rats: Effects on subsequent food and water intake

Zafra¹,

Simon²,

Molina³

et al. 2005

Nutritional Neuroscience

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“…While both intraduodenal probe stimuli used here (DB and LiCl) are known to be aversive, they are also believed to engage different postingestive pathways. In particular, because LiCl acts primarily by a postabsorptive route to its targets in the central nervous system (e.g., area postrema) to produce aversive consequences (32,33) and was delivered so as to be difficult to discern on the basis of early sensory properties from safe NaCl (38), it was expected that rats would inhibit intake in the final minutes only of the LiCl probe sessions, reflecting the onset of the malaise. On the other hand, assuming DB activates bitter taste receptors in the GI tract, it was predicted that rats would rapidly curb intake in response to the arrival of the bitter stimulus in the intestine.…”

Section: Experiments 1: Rats Rapidly Suppress Ongoing Intake In Re-mentioning

confidence: 99%

Ongoing ingestive behavior is rapidly suppressed by a preabsorptive, intestinal “bitter taste” cue

Schier

Davidson

Powley

2011

American Journal of Physiology-Regulatory, Integrative and Comp

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Schier LA, Davidson TL, Powley TL. Ongoing ingestive behavior is rapidly suppressed by a preabsorptive, intestinal "bitter taste" cue. Am J Physiol Regul Integr Comp Physiol 301: R1557-R1568, 2011. First published August 24, 2011 doi:10.1152/ajpregu.00344.2011.-The discovery that cells in the gastrointestinal (GI) tract express the same molecular receptors and intracellular signaling components known to be involved in taste has generated great interest in potential functions of such post-oral "taste" receptors in the control of food intake. To determine whether taste cues in the GI tract are detected and can directly influence behavior, the present study used a microbehavioral analysis of intake, in which rats drank from lickometers that were programmed to simultaneously deliver a brief yoked infusion of a taste stimulus to the intestines. Specifically, in daily 30-min sessions, thirsty rats with indwelling intraduodenal catheters were trained to drink hypotonic (0.12 M) sodium chloride (NaCl) and simultaneously self-infuse a 0.12 M NaCl solution. Once trained, in a subsequent series of intestinal taste probe trials, rats reduced licking during a 6-min infusion period, when a bitter stimulus denatonium benzoate (DB; 10 mM) was added to the NaCl vehicle for infusion, apparently conditioning a mild taste aversion. Presentation of the DB in isomolar lithium chloride (LiCl) for intestinal infusions accelerated the development of the response across trials and strengthened the temporal resolution of the early licking suppression in response to the arrival of the DB in the intestine. In an experiment to evaluate whether CCK is involved as a paracrine signal in transducing the intestinal taste of DB, the CCK-1R antagonist devazepide partially blocked the response to intestinal DB. In contrast to their ability to detect and avoid the bitter taste in the intestine, rats did not modify their licking to saccharin intraduodenal probe infusions. The intestinal taste aversion paradigm developed here provides a sensitive and effective protocol for evaluating which tastants-and concentrations of tastants-in the lumen of the gut can control ingestion. chemoreceptor; gastrointestinal; denatonium benzoate; food learning; cholecystokinin CHEMORECEPTORS ARE INDISPENSABLE to the control of food intake. As taste receptors on the tongue and in the oral cavity, they supply signals critical for accepting and rejecting foods for consumption, promoting intake of palatable foods, and preparing the digestive system for the arrival of nutrients. Complementary to this early oral sensory processing, chemoreceptors in the stomach and intestines transduce signals from the lumen to adjust motility, secrete digestive enzymes, and initiate satiation (cf., 24). Accordingly, the gastrointestinal (GI) tract has been conventionally considered to have a more or less continuous sensory surface for tracking meals to engage and revise apposite and coordinated responses particular to the properties of the food and the body's physiological state. Despite th...

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“…To compensate for any natural flavor preferences of the subjects, pairing of the liquid diet was balanced. Thus, half of the animals received the liquid diet when they drank S and received physiological saline (PS) when they drank C, whereas the other half received the liquid diet paired with C, and PS paired with S. An illustration of this procedure was previously published (31). After 60 min, the animals were offered 10 g of food and, later in the evening (i.e., 15 h before the next session), any remaining food was removed.…”

Section: Experiments 1: Learned Concurrent Flavor Preferencesmentioning

confidence: 99%

“…However, this simultaneous administration does not appear to be necessary for sequential TAL (31). Information on nutrients in the gastrointestinal tract can reach the brain by both the neural and humoral pathway.…”

mentioning

confidence: 99%

Learned flavor preferences induced by intragastric administration of rewarding nutrients: role of capsaicin-sensitive vagal afferent fibers

Zafra

Molina²,

Puerto³

2007

American Journal of Physiology-Regulatory, Integrative and Comp

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Learned flavor preferences can be established after intragastric nutrient administration by two different behavioral procedures, concurrent and sequential. In a concurrent procedure, two flavored stimuli are offered separately but at the same time on a daily basis: one stimulus is paired with the simultaneous intragastric administration of partially digested food and the other with physiological saline. In sequential learning, the two stimuli are presented during alternate sessions. Neural mechanisms underlying these learning modalities have yet to be fully elucidated. The aim of this study was to examine the role of vagal afferent fibers in the visceral processing of rewarding nutrients during concurrent (experiment 1) and sequential (experiment 2) flavor preference learning in Wistar rats. For this purpose, capsaicin, a neurotoxin that destroys slightly myelinated or unmyelinated sensory axons, was applied to the subdiaphragmatic region of the esophagus to selectively damage most of the vagal afferent pathways that originate in the gastrointestinal system. Results showed that capsaicin [1 mg of capsaicin dissolved in 1 ml of vehicle (10% Tween 80 in oil)] blocked acquisition of concurrent but not sequential flavor preference learning. These results are interpreted in terms of a dual neurobiological system involved in processing the rewarding effects of intragastrically administered nutrients. The vagus nerve, specifically capsaicin-sensitive vagal afferent fibers, would only be essential in concurrent flavor preference learning, which requires rapid processing of visceral information.

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Concurrent conditioned taste aversion: A learning mechanism based on rapid neural versus flexible humoral processing of visceral noxious substances

Cited by 38 publications

References 119 publications

Lesions of the lateral parabrachial area block the aversive component and induced-flavor preference for the delayed intragastric administration of nutrients in rats: Effects on subsequent food and water intake

Lesions of the lateral parabrachial area block the aversive component and induced-flavor preference for the delayed intragastric administration of nutrients in rats: Effects on subsequent food and water intake

Ongoing ingestive behavior is rapidly suppressed by a preabsorptive, intestinal “bitter taste” cue

Learned flavor preferences induced by intragastric administration of rewarding nutrients: role of capsaicin-sensitive vagal afferent fibers

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