The biphasic effect of morphine on odor conditioning in neonatal rats

Randall, Christopher K.; Kraemer, Philipp J.; Dose, John M.; Carbary, Timothy J.; Bardo, Michael T.

doi:10.1002/dev.420250506

Cited by 16 publications

(12 citation statements)

References 23 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Endogenous opioids have been shown to play a prominent role in the postnatal attachment process. Specifically in the rat neonate, opioids facilitate odor preference learning (Barr & Rossi, 1992;Kehoe & Blass, 1986a;Panksepp, Nelson, & Siviy, 1994;Randall, Kraemer, Dose, Carbary, & Bardo, 1992;Roth & Sullivan, 2001Shide & Blass, 1991), and nipple-milk conditioning (Petrov, Varlinskaya, Becker, & Smotherman, 1998, Petrov, Varlinskaya, & Smotherman, 2000Robinson, Arnold, Spear, & Smotherman, 1993;Robinson & Smotherman, 1997). Suggestive of their rewarding value in neonates, opioids are sufficient to alleviate separation distress (Carden, Barr, & Hofer, 1991;Goodwin, Molina, & Spear, 1994;Kehoe & Blass, 1986b;Panksepp, Herman, Conner, Bishop, & Scott, 1978).…”

Section: Discussionmentioning

confidence: 99%

Examining the role of endogenous opioids in learned odor–stroke associations in infant rats

Roth

Sullivan

2005

Developmental Psychobiology

View full text Add to dashboard Cite

Maternal touch profoundly regulates infant neural and behavioral development, and supports learned odor associations necessary for infant attachment. Endogenous opioids are well characterized to mediate the calming and analgesic properties of maternal touch; yet their role in learned odor-touch associations is unknown. We administered naltrexone, an opioid receptor antagonist, before or immediately following classical conditioning with peppermint odor and tactile stimulation (stroking) in rat neonates. Results indicate odor-stroke conditioning produces odor preferences facilitated by endogenous opioids during acquisition and memory consolidation. These results provide additional evidence for the modulatory role of opioids in neonate learning and memory. Disturbances to this system may alter the impact of touch on infant development, particularly in the realm of learning necessary for attachment. ß 2005 Wiley Periodicals, Inc. Dev Psychobiol 48: 71-78, 2006.

show abstract

Section: Discussionmentioning

confidence: 99%

Examining the role of endogenous opioids in learned odor–stroke associations in infant rats

Roth

Sullivan

2005

Developmental Psychobiology

View full text Add to dashboard Cite

show abstract

“…For example, odor paired with morphine or sucrose is sufficient to produce a conditioned odor preference in rat neonates, which is blocked with NTX (Kehoe and Blass 1986;Shide and Blass 1991;Barr and Rossi 1992;Randall et al 1992). Indicative of the role of opioids in the rewarding aspects of mother-infant interactions, opioid receptor antagonism prevents the learning of an odor preference for an odor paired directly with maternal care in older pups (Panksepp et al 1994).…”

Section: Opioids Modulate Learned Odor Behavior In Neonatesmentioning

confidence: 99%

Opioid modulation of Fos protein expression and olfactory circuitry plays a pivotal role in what neonates remember

Roth¹,

Moriceau²,

Sullivan³

2006

Learn. Mem.

View full text Add to dashboard Cite

Paradoxically, fear conditioning (odor-0.5 mA shock) yields a learned odor preference in the neonate, presumably due to a unique learning and memory circuit that does not include apparent amygdala participation. Post-training opioid antagonism with naltrexone (NTX) blocks consolidation of this odor preference and instead yields memory of a learned odor aversion. Here we characterize the neural circuitry underlying this switch during memory consolidation. Experiment 1 assessed post-training opioid modulation of Fos protein expression within olfactory circuitry (olfactory bulb, piriform cortex, amygdala). Odor-shock conditioning with no post-training treatment (odor preference) induced significant changes in Fos protein expression in the granule cell layer of the olfactory bulb and anterior piriform cortex. Post-training opioid receptor antagonism (odor aversion) prevented the learning-induced changes in the anterior piriform cortex and also induced significant changes in Fos protein expression in the central nucleus of the amygdala. Experiment 2 assessed intra-amygdala opioid modulation of neonate memory consolidation. Post-training infusion of NTX within the amygdala permitted consolidation of an odor aversion, while vehicle-infused pups continued to demonstrate an odor preference. Overall, results demonstrate that opioids modulate memory consolidation in the neonate via modulating Fos protein expression in olfactory circuitry. Furthermore, these results suggest that opioids are instrumental in suppressing neonate fear behavior via modulating the amygdala.Odor-shock conditioning, a learning paradigm that readily produces fear in adult animals, produces a paradoxical odor preference in rat pups <10 d old (Camp and Rudy 1988;Sullivan et al. 2000a;Roth and Sullivan 2001, 2003Moriceau and Sullivan 2004a). This paradoxical behavior is attributable to a relatively simplistic olfactory learning and memory circuit that incorporates the olfactory bulb, anterior piriform cortex, and an apparent lack of amygdala participation (Sullivan et al. 2000a,b; Moriceau and Sullivan 2004a,b;Roth and Sullivan 2005;Moriceau et al. 2006). Indeed, we have demonstrated that the emergence of learned fear coincides with significant amygdala participation (Sullivan et al. 2000a;Moriceau et al. 2006). We suggest this attenuated aversion learning and potentiated preference learning early in development ensures pups readily learn to approach the maternal odor regardless of the quality of care she provides. Indeed, a recent study from our laboratory has documented this paradoxical odor preference learning within a seminatural nest environment as an odor paired with rough handling from a stressed mother resulted in a preference for that odor (Roth and Sullivan 2005). A similar paradoxical attachment despite caregiver abuse has been demonstrated in other species: chick (Hess 1962), infant dogs (Rajecki et al. 1978), and nonhuman primates (Harlow and Harlow 1965;Maestripieri et al. 1997Maestripieri et al. , 1999.We have previously demonstrated a ...

show abstract

“…In postnatal Day 5 pups, pairings of low doses of morphine with odor produce odor preferences while high doses produce odor aversions (Randall, Kraemer, Dose, Carbary, & Bardo, 1992). Injections of morphine into the ventral tegmental area (an area associated with the adult reward pathway) paired with an odor in pups as young as postnatal Day 4 are suf®cient for an odor preference (Barr & Rossi, 1992).…”

mentioning

confidence: 99%

Endogenous opioids and their role in odor preference acquisition and consolidation following odor–shock conditioning in infant rats

Roth

Sullivan

2001

Developmental Psychobiology

View full text Add to dashboard Cite

We assessed the neurochemical basis of olfactory learning induced by presentations of odor and moderate shock in infant rats. Paradoxically, shock conditioning produces an odor preference in 8-day-olds, but an odor aversion in 12-day-olds. Studies have demonstrated the importance of opioids in early olfactory learning; their specific role remains undefined. In this study, postnatal Days 8 and 12 pups were systemically injected with naltrexone, a nonspecific opioid antagonist, or saline and received either paired or backward presentations of odor-moderate shock or odor-only presentations. Blocking the opioid system during conditioning disrupted acquisition of the Day 8 odor preference, but not the Day 12 odor aversion. Additional Day 8 pups were given naltrexone posttraining. Naltrexone not only blocked consolidation of an odor preference but also yielded an odor aversion. These results suggest that the opioid system has a critical role in both olfactory learning and consolidation of odor preferences during the sensitive period.

show abstract

The biphasic effect of morphine on odor conditioning in neonatal rats

Cited by 16 publications

References 23 publications

Examining the role of endogenous opioids in learned odor–stroke associations in infant rats

Examining the role of endogenous opioids in learned odor–stroke associations in infant rats

Opioid modulation of Fos protein expression and olfactory circuitry plays a pivotal role in what neonates remember

Endogenous opioids and their role in odor preference acquisition and consolidation following odor–shock conditioning in infant rats

Contact Info

Product

Resources

About