Flavor-illness aversions: The role of the amygdala in the acquisition of taste-potentiated odor aversions

Bermúdez‐Rattoni, Federico; Grijalva, Carlos V.; Kiefer, Stephen W.; García, John

doi:10.1016/0031-9384(86)90417-8

Cited by 66 publications

(45 citation statements)

References 25 publications

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“…Ontogeny of amygdala-dependent odor aversion www.learnmem.org the adult, which requires the amygdala (Bermudez-Rattoni et al 1986;Ferry and Di Scala 1997;Touzani and Sclafani 2005).…”

Section: Development Of Licl Learningmentioning

confidence: 99%

“…Several lines of evidence indicate that in adult rats, the amygdala plays a crucial role in both fear conditioning and odor-LiCl conditioning (Bermudez-Rattoni et al 1986;Ferry and Di Scala 1997;LeDoux 2000;Gale et al 2004;Touzani and Sclafani 2005). It should be noted that the basolateral complex of the amygdala is essential for odormalaise learning, although results are inconsistent for tastemalaise learning (Nachman and Ashe 1974;Burt and Smotherman 1980;Bermudez-Rattoni et al 1986;Dunn and Everitt 1988;Yamamoto and Fujimoto 1991;Kesner et al 1992;Sakai and Yamamoto 1999;Bahar et al 2004;Touzani and Sclafani 2005;Wilkins and Bernstein 2006).…”

Section: Amygdala Basolateral Complexmentioning

confidence: 99%

“…We used rats ranging from an age of complete dependence on the mother through an age of independence at weaning. We focused on the amygdala basolateral complex, which is implicated in adult fear conditioning and odor-malaise learning (Bermudez-Rattoni et al 1986;LeDoux 2000;Batsell and Blankenship 2002;Gale et al 2004;Holland and Gallagher 2004), and the anterior and posterior piriform cortex, olfactory pathway areas that have previously been implicated in infant odor-aversion and odor-preference learning Roth and Sullivan 2005;Roth et al 2006) as well as adult odor learning (Ferry and Di Scala 1997;Litaudon et al 1997;Barkai and Saar 2001;Mouly et al 2001;Mouly and Gervais 2002;Tronel and Sara 2002;Sevelinges et al 2004;Wilson et al 2004;Touzani and Sclafani 2005).…”

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Ontogeny of odor-LiCl vs. odor-shock learning: Similar behaviors but divergent ages of functional amygdala emergence

Raineki¹,

Shionoya²,

Sander³

et al. 2009

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Both odor-preference and odor-aversion learning occur in perinatal pups before the maturation of brain structures that support this learning in adults. To characterize the development of odor learning, we compared three learning paradigms: (1) odor-LiCl (0.3M; 1% body weight, ip) and (2) odor-1.2-mA shock (hindlimb, 1sec)-both of which consistently produce odor-aversion learning throughout life and (3) odor-0.5-mA shock, which produces an odor preference in early life but an odor avoidance as pups mature. Pups were trained at postnatal day (PN) 7-8, 12-13, or 23-24, using odor-LiCl and two odor-shock conditioning paradigms of odor-0.5-mA shock and odor-1.2-mA shock. Here we show that in the youngest pups (PN7-8), odor-preference learning was associated with activity in the anterior piriform (olfactory) cortex, while odor-aversion learning was associated with activity in the posterior piriform cortex. At PN12-13, when all conditioning paradigms produced an odor aversion, the odor-0.5-mA shock, odor-1.2-mA shock, and odor-LiCl all continued producing learning-associated changes in the posterior piriform cortex. However, only odor-0.5-mA shock induced learning-associated changes within the basolateral amygdala. At weaning (PN23-24), all learning paradigms produced learning-associated changes in the posterior piriform cortex and basolateral amygdala complex. These results suggest at least two basic principles of the development of the neurobiology of learning: (1) Learning that appears similar throughout development can be supported by neural systems showing very robust developmental changes, and (2) the emergence of amygdala function depends on the learning protocol and reinforcement condition being assessed.Even in utero, infant rats rapidly learn to avoid odors paired with malaise (LiCl) as expressed by learning an odor aversion (Garcia et al. 1966(Garcia et al. , 1974Hennessey et al. 1976;Haroutunian and Campbell 1979;Smotherman 1982;Stickrod et al. 1982;Rudy and Cheatle 1983;Kucharski and Spear 1984;Smotherman and Robinson 1985, 1990;Alleva and Calamandrei 1986;Miller et al. 1990b; Best 1992, 1993;Richardson and McNally 2003;Gruest et al. 2004;Shionoya et al. 2006). In contrast to adult odor-LiCl learning, which relies on the amygdala (Touzani and Sclafani 2005), this early-life, odoraversion learning relies on the olfactory bulb until the pup approaches weaning age, when the amygdala is incorporated into the learning circuitry (Shionoya et al. 2006). In contrast, if infant rats receive an odor paired with a moderately painful stimulus (0.5-mA foot or tail shock, or tail pinch) the amygdala appears to be incorporated into this learning circuitry around postnatal day Here we expand assessment of the developing pups' odoraversion learning circuit by including the anterior and posterior piriform cortex, which have previously been demonstrated to be important for both pup and adult odor learning (Litaudon et al. 1997;Barkai and Saar 2001;Mouly et al. 2001;Mouly and Gervais 2002;Tronel and Sara 2002;Moriceau and Su...

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“…Ontogeny of amygdala-dependent odor aversion www.learnmem.org the adult, which requires the amygdala (Bermudez-Rattoni et al 1986;Ferry and Di Scala 1997;Touzani and Sclafani 2005).…”

Section: Development Of Licl Learningmentioning

confidence: 99%

Section: Amygdala Basolateral Complexmentioning

confidence: 99%

mentioning

confidence: 99%

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Ontogeny of odor-LiCl vs. odor-shock learning: Similar behaviors but divergent ages of functional amygdala emergence

Raineki¹,

Shionoya²,

Sander³

et al. 2009

Learn. Mem.

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“…The amygdala, and especially its basolateral nucleus, plays a prominent role in the processes of acquisition, consolidation, and retrieval of the COA (Bermú dez- Rattoni et al, 1986;Ferry and Di Scala, 1997;Miranda et al, 2003;Desgranges et al, 2008;Sevelinges et al, 2009). This study to our knowledge is the first report that COA training strongly changes BLA response to odors.…”

Section: An Effective Cs-us Association Duringmentioning

confidence: 99%

The Way an Odor Is Experienced during Aversive Conditioning Determines the Extent of the Network Recruited during Retrieval: A Multisite Electrophysiological Study in Rats

Chapuis¹,

Garcia²,

Messaoudi³

et al. 2009

J. Neurosci.

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Recent findings have revealed the importance of orthonasal and retronasal olfaction in food memory, especially in conditioned odor aversion (COA); however, little is known about the dynamics of the cerebral circuit involved in the recognition of an odor as a toxic food signal and whether the activated network depends on the way (orthonasal vs retronasal) the odor was first experienced. In this study, we mapped the modulations of odor-induced oscillatory activities through COA learning using multisite recordings of local field potentials in behaving rats. During conditioning, orthonasal odor alone or associated with ingested odor was paired with immediate illness. For all animals, COA retrieval was assessed by orthonasal smelling only. Both types of conditioning induced similarly strong COA. Results pointed out (1) a predictive correlation between the emergence of powerful beta (15-40 Hz) activity and the behavioral expression of COA and (2) a differential network distribution of this beta activity according to the way the animals were exposed to the odor during conditioning. Indeed, for both types of conditioning, the aversive behavior was predicted by the emergence of a strong beta oscillatory activity in response to the odor in the olfactory bulb, piriform cortex, orbitofrontal cortex, and basolateral amygdala. This network was selectively extended to the infralimbic and insular cortices when the odor was ingested during acquisition. These differential networks could participate in different food odor memory; these results are discussed in line with recent behavioral results that indicate that COA can be formed over long odor-illness delays only if the odor is ingested.

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“…Among the structures involved in the initial phases of taste memory formation are the gustatory neocortex and amygdala (8). Thus, damage to either the gustatory insular cortex (IC) or amygdala in adult rats leads to impaired acquisition of CTA (6,7,[9][10][11][12][13][14][15][16][17]. However, the functional roles of IC and amygdala seem to be different during the phases of taste memory formation.…”

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confidence: 99%

Glutamatergic activity in the amygdala signals visceral input during taste memory formation

Miranda

Ferreira

Ramı́rez-Lugo

et al. 2002

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

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Conditioned taste aversion (CTA) is a learning paradigm in which an animal avoids a taste (conditioned stimulus) previously associated with visceral toxic effects [or unconditioned stimulus (US)]. Although many studies have implicated glutamate-mediated neurotransmission in memory consolidation of different types of learning tasks, including CTA, the exact role of this neurotransmitter system in memory formation is not known. Thus, we set out to determine whether glutamate mediates signaling of the US in CTA. We present evidence obtained by in vivo microdialysis that the US (i.p. injection of lithium chloride) induced a dramatic increase in glutamate release in the amygdala and a modest but significant release in the insular cortex. Moreover, CTA can be elicited by intra-amygdalar microinjections of glutamate; consequently, when glutamate is administered just before the presentation of a weak US, a clear CTA is induced. In contrast, the injection of glutamate alone or glutamate 2 h after the suboptimal US did not have any effect on the acquisition of CTA. These results indicate that glutamate activation of the amygdala can partially substitute the US in CTA, thus providing a clear indication that the amygdala conveys visceral information for this kind of memory.A number of studies (1-5) have implicated glutamatemediated transmission in consolidation of memory for different types of training, such as inhibitory avoidance, Morris water maze, and conditioned taste aversion (CTA). CTA is a learning paradigm in which the novel taste of food or drink (conditioned stimulus, CS) is paired with visceral signals of poisoning (unconditioned stimulus, US). Consequently, the animals avoid consuming the food or drink previously associated with toxic effects. CTA has unique properties; it is established after a single trial, permits long delays between stimuli presentation, and lasts for very long periods of time, even weeks. This feature makes it possible to separate the acquisition process into phases-CS presentation and US presentation-which can be studied independently under different experimental treatments (6).CTA is established by the interaction of brainstem, limbic, and neocortical structures underlying different phases of the acquisition storage and retrieval of gustatory memory (7). Among the structures involved in the initial phases of taste memory formation are the gustatory neocortex and amygdala (8). Thus, damage to either the gustatory insular cortex (IC) or amygdala in adult rats leads to impaired acquisition of CTA (6,7,[9][10][11][12][13][14][15][16][17]. However, the functional roles of IC and amygdala seem to be different during the phases of taste memory formation. Functional blockade of IC before taste presentation, but not between taste presentation and lithium chloride (LiCl) injection, blocks CTA (16, 18), suggesting that the gustatory cortex is involved in taste processing and͞or memory but is not necessary for processing the visceral signals of poisoning. Conversely, amygdala functional inactivation...

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Flavor-illness aversions: The role of the amygdala in the acquisition of taste-potentiated odor aversions

Cited by 66 publications

References 25 publications

Ontogeny of odor-LiCl vs. odor-shock learning: Similar behaviors but divergent ages of functional amygdala emergence

Ontogeny of odor-LiCl vs. odor-shock learning: Similar behaviors but divergent ages of functional amygdala emergence

The Way an Odor Is Experienced during Aversive Conditioning Determines the Extent of the Network Recruited during Retrieval: A Multisite Electrophysiological Study in Rats

Glutamatergic activity in the amygdala signals visceral input during taste memory formation

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