A specialization of taste aversion learning during suckling and its weaning‐associated transformation

Gubernick, David J.; Alberts, Jeffrey R.

doi:10.1002/dev.420170605

Cited by 25 publications

(22 citation statements)

References 26 publications

(49 reference statements)

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“…1), and these results replicate previous work on odor-malaise learning in pups Haroutunian and Campbell 1979;Smotherman 1982;Stickrod et al 1982b;Rudy and Cheatle 1983;Robinson 1985, 1990;Alleva and Calamandrei 1986;Molina et al 1986;Miller et al 1990;Abate et al 2001;Richardson and McNally 2003). Similar to previous work, nursing modifies odor-LiCl-induced aversion at all ages tested and produces an odor preference in pups 7-8-and 12-13-d old, but blocks the aversion learning in PN23-PN24 pups (Martin and Alberts 1979;Gubernick and Alberts 1984;Melcer et al 1985). Figure 1 depicts performance in the Y-maze test and indicates that Paired odor-LiCl pups without the presence of a mother learned an odor aversion at all ages, and nursing pups learned an odor preference at the two youngest ages.…”

Section: Behaviorsupporting

confidence: 88%

“…1) (Gubernick and Alberts 1984;Melcer et al 1985). The mechanism for this is unclear, although its presumed significance is to transmit food odors/tastes from the mother's diet to pups to enhance later food selection and consumption of presumably safe foods (Bilko et al 1994;Galef Jr.1997;Mennella et al 2001).…”

Section: Unique Infant Constraints On Malaise Learningmentioning

confidence: 99%

“…Taste/odor aversion acquisition shows some specific differences between pups and adults. First, nursing during acquisition disturbs taste-aversion learning, although this diminishes as pups approach weanling (Martin and Alberts 1979;Gubernick and Alberts 1984;Melcer et al 1985;Kehoe and Blass 1986). Second, in contrast to the long temporal parameters permitted between the odor/taste (conditioned stimulus, CS) and illness (unconditioned stimulus, US) in adult taste aversion, the temporal constraints between the CS and the malaise producing US for pup learning are very limited (Rudy and Cheatle 1983;Kraemer et al 1988Kraemer et al , 1989Hoffmann et al 1990Hoffmann et al , 1991.…”

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Development switch in neural circuitry underlying odor-malaise learning

Shionoya¹,

Moriceau²,

Lunday³

et al. 2006

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Fetal and infant rats can learn to avoid odors paired with illness before development of brain areas supporting this learning in adults, suggesting an alternate learning circuit. Here we begin to document the transition from the infant to adult neural circuit underlying odor-malaise avoidance learning using LiCl (0.3 M; 1% of body weight, ip) and a 30-min peppermint-odor exposure. Conditioning groups included: Paired odor-LiCl, Paired odor-LiCl-Nursing, LiCl, and odor-saline. Results showed that Paired LiCl-odor conditioning induced a learned odor aversion in postnatal day (PN) 7, 12, and 23 pups. Odor-LiCl Paired Nursing induced a learned odor preference in PN7 and PN12 pups but blocked learning in PN23 pups. 14C 2-deoxyglucose (2-DG) autoradiography indicated enhanced olfactory bulb activity in PN7 and PN12 pups with odor preference and avoidance learning. The odor aversion in weanling aged (PN23) pups resulted in enhanced amygdala activity in Paired odor-LiCl pups, but not if they were nursing. Thus, the neural circuit supporting malaise-induced aversions changes over development, indicating that similar infant and adult-learned behaviors may have distinct neural circuits.Animals rapidly learn to avoid tastes, smells, and textures of foods associated with malaise, and this learning process produces conditioned taste and odor aversions (Garcia et al. 1966(Garcia et al. , 1974 Best 1992, 1993). This learning has been demonstrated early in development, including both the embryonic day (ED) 18 rat and mouse fetuses, with retention time lasting weeks Haroutunian and Campbell 1979;Smotherman 1982;Stickrod et al. 1982b;Rudy and Cheatle 1983; Robinson 1985, 1990;Alleva and Calamandrei 1986;Molina et al. 1986;Hoffmann et al. 1987Hoffmann et al. , 1990Miller et al. 1990;Hunt et al. 1991Hunt et al. , 1993Abate et al. 2001;Richardson and McNally 2003;Gruest et al. 2004a). Taste/odor aversion acquisition shows some specific differences between pups and adults. First, nursing during acquisition disturbs taste-aversion learning, although this diminishes as pups approach weanling (Martin and Alberts 1979;Gubernick and Alberts 1984;Melcer et al. 1985;Kehoe and Blass 1986). Second, in contrast to the long temporal parameters permitted between the odor/taste (conditioned stimulus, CS) and illness (unconditioned stimulus, US) in adult taste aversion, the temporal constraints between the CS and the malaise producing US for pup learning are very limited (Rudy and Cheatle 1983;Kraemer et al. 1988Kraemer et al. , 1989Hoffmann et al. 1990Hoffmann et al. , 1991.There is evidence that the neural basis of odor/taste aversion learning may change over development. In adults, the amygdala is thought to support taste-aversion learning, though there are discrepancies in the literature (Nachman and Ashe 1974;Burt and Smotherman 1980;Dunn and Everitt 1988;Yamamoto and Fujimoto 1991;Kesner et al. 1992;Yamamoto et al. 1994;Bures et al. 1998;Schafe et al. 1998;Sakai and Yamamoto 1999;Wilkins and Bernstein 2006). When the taste and smell component...

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Section: Behaviorsupporting

confidence: 88%

Section: Unique Infant Constraints On Malaise Learningmentioning

confidence: 99%

mentioning

confidence: 99%

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Development switch in neural circuitry underlying odor-malaise learning

Shionoya¹,

Moriceau²,

Lunday³

et al. 2006

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“…For example, it has been found that nursing-related taste aversions are affected by the young animal's experience with solid food. Specifically, taste aversions conditioned while nursing are more readily expressed in animals that have had experience with solid food, either before or after conditioning (Gubernick & Alberts, 1986). In the present case, weanlings tested after 21 days would have had much more exposure to solid food, and this experience could have affected expression of a previously established taste aversion.…”

Section: Discussionmentioning

confidence: 72%

Increase in retention of a taste aversion by weanling rats after a long interval

Kraemer

Lariviere

Spear

1988

Animal Learning & Behavior

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Weanling rats were tested for retention of an aversion to a novel flavor (chocolate milk) that had been conditioned as a single-element conditioned stimulus (CS) or in compound with a novel ambient odor (banana). The presence of the ambient odor during conditioning had no effect on flavor aversion shortly thereafter, confirming previous results. The flavor aversion observed 21 days after conditioning, however, was significantly stronger for pups conditioned with the singleelement CS than for those given the flavor-odor compound as the CS. This retention effect was due to a surprising increasein the conditioned aversion observed 21 days after conditioning with the single-element CS. A second experiment confirmed this paradoxical increase in retention of the aversion to chocolate milk. This experiment also verified that no such increase occurred in retention of the conditioned aversion to a different flavor (saccharin), whether the initial aversion was strong or weak. The results may be explained in terms of generalized latent inhibition from consumption of mother's milk.

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“…A similar learning constraint exists with odor-LiCl and taste-LiCl learning. Specifically, if pups nurse during odor-LiCl conditioning, they develop a preference for the odor (Shionoya et al 2006), while taste-LiCl avoidance learning is blocked (Martin and Alberts 1979;Gubernick and Alberts 1984;Melcer et al 1985;Kehoe and Blass 1986).…”

Section: Ecological Significancementioning

confidence: 99%

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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A specialization of taste aversion learning during suckling and its weaning‐associated transformation

Cited by 25 publications

References 26 publications

Development switch in neural circuitry underlying odor-malaise learning

Development switch in neural circuitry underlying odor-malaise learning

Increase in retention of a taste aversion by weanling rats after a long interval

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

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