Unique Neural Circuitry for Neonatal Olfactory Learning

Moriceau, Stéphanie; Sullivan, Regina M.

doi:10.1523/jneurosci.4578-03.2004

Cited by 129 publications

(116 citation statements)

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“…For example, corticosterone (CORT) modulates GABAergic inhibition and principal cell excitability in the adult amygdala (Duvarci and Pare, 2007) and other limbic regions (Verkuyl et al, 2005). Elevating CORT levels within the amygdala of sensitive period pups allows precocial emergence of fear conditioning (Moriceau and Sullivan, 2004a), while reducing CORT levels in post-sensitive period pups either by adrenalectomy or maternal presence (Wiedenmayer et al, 2003) reinstates the sensitive period blockade on fear conditioning Sullivan, 2004b, Moriceau andSullivan, 2006).…”

Section: Discussionmentioning

confidence: 99%

“…Importantly however, while GABA synthetic enzymes (e.g., GAD (Stork et al, 2000)) and receptor subunits (Zhang et al, 1991) are present at birth in the amygdala, they do not attain adult levels there until several weeks later, suggesting a potential late emergence for the mature expression of amygdala synaptic plasticity (Gilbert and Cain, 1981). In fact, odor-foot shock association that induces amygdala activation (e.g., c-fos labeling) and learned fear in PN12 rat pups, induces neither amygdala activation nor fear in PN10 pups (Sullivan et al, 2000, Moriceau and Sullivan, 2004b, Roth and Sullivan, 2005. It should be noted that pain threshold to footshock is very similar across this age range of pups (Emerich et al, 1985, Barr, 1995, Sullivan et al, 2000, Fitzgerald and Beggs, 2001).…”

Section: Introductionmentioning

confidence: 99%

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Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity

2008

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Mother-infant attachment is facilitated in altricial rodents through unique neural mechanisms that include impaired neonatal fear conditioning until the time that pups first begin to leave the nest (sensitive period). Here, we confirmed the developmental emergence of odor fear conditioning in neonatal rat pups, and examined synaptic plasticity of inputs to the basolateral amygdala in vitro. Coronal slices through the amygdala were obtained from sensitive (< 10 days) and post-sensitive (> 10, < 19 days) period pups. Field potentials were recorded in the basolateral amygdala in response to stimulation of either the external capsule (neocortical inputs) or fibers from the cortical nucleus of the amygdala (olfactory inputs). The effects of tetanic stimulation were examined in each pathway. In both pathways, tetanic stimulation induce significant long-term synaptic plasticity in post-sensitive period pups, but no significant plasticity in sensitive period pups incapable of learning odor aversions. GABA A receptor blockade in post-sensitive period slices reverts synaptic plasticity to sensitive period characteristics. The results suggest that sensitive period deficits in fear conditioning may be related to impaired amygdala synaptic plasticity and the immature state of GABAergic inhibition and/or it modulation in the neonatal amygdala.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity

2008

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“…Enhanced brain activation along with growth may facilitate memory processes and so shorten the time for memory stabilization. That could result from maturation of modulatory systems such as cholinergic and noradrenergic systems (Harley 2004;Moriceau and Sullivan 2004;Field et al 2007;Mellott et al 2007), which are both involved in arousal and memory. It could be noted that a release of catecholamines with AN (Canal et al 2007), given developmental differences in sensitivity to these modulators, may also explain why AN affects pups of different ages differently.…”

Section: Discussionmentioning

confidence: 99%

The temporal dynamics of consolidation and reconsolidation decrease during postnatal development

Languille¹,

Gruest²,

Richer³

et al. 2008

Learn. Mem.

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The temporal dynamics of consolidation and reconsolidation of taste/odor aversion memory are evaluated during rat pup growth at postnatal days 3, 10, and 18. This is assessed through the temporal gradients of efficacy of a protein synthesis inhibitor (anisomycin) in inducing amnesia after either acquisition (consolidation) or reactivation (reconsolidation). The results show a progressive reduction with age of the delay during which the inhibitor is able to induce amnesia. Control experiments rule out a reduction of anisomycin efficacy due to blood brain barrier growth or decrease in protein synthesis inhibition. Thus, these results present the first evidence that the protein synthesis-dependent phase of memory stabilization requires less time with age. This decrease occurs in parallel for consolidation and reconsolidation. Such changes in the dynamics of memory processing could contribute to the cognitive improvement associated with development.Neurobiological changes occurring during development have been extensively explored, but the functional consequences of these changes for cognition are still not well understood. Research on cognitive development has demonstrated very early learning capacities in vertebrates; different kinds of associative learning may be acquired by neonates and even by the fetus (Smotherman et al. 1982;Kehoe and Blass 1986;Cheslock et al. 2000;Sullivan 2001;Smotherman 2002;Gruest et al. 2004a;Shionoya et al. 2006). Some of these early acquisitions have been shown to be retained in the long term, but the characteristics of long-term memory in the course of development are still poorly known, particularly concerning its stabilization.In the adult, it is well known that memory stabilization is not instantaneous but requires time for the biological processes involved. To be stored in the long term, the memory trace must be consolidated (McGaugh 1966(McGaugh , 2000 and this consolidation requires new protein synthesis (Davis and Squire 1984). Thus, protein synthesis inhibitors given at the time of acquisition, or just afterward, cause amnesia by blocking consolidation. Recently, numerous experiments have enriched this notion by showing that retrieval of a previously consolidated memory induces a new period of lability and that stabilization of the memory in the long term requires a new wave of protein synthesis (for reviews, see Despite the theoretical importance of consolidation and reconsolidation, little is known about the emergence of these characteristics of memory during development. We have recently shown that consolidation and reconsolidation can be detected in the neonate and so may be considered as innate properties of memory processing (Gruest et al. 2004b). However, that does not rule out any possibilities of ontogenetic modifications of these memory characteristics. An indication of this possibility is that retrograde amnesia may be induced in the pup one hour after conditioned aversion training, a delay which has never been observed in the adult in the same kind of learning. Th...

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“…We hypothesize that biparental rearing causes an alteration in the pups' USV response to the male, which is mediated by neural mechanisms similar to that described for the induction of an odor preference [71,[99][100][101]. That is, stimulation of the pups in the presence of the adult male activates the locus coeruleus and norepinephrine secretion to enhance the development of an odor preference and a social bond.…”

Section: Hypothesized Mechanism For Acquisition Of Paternal Potentiationmentioning

confidence: 91%

“…Sullivan, Wilson and colleagues have mapped many of the neurobiological mechanisms underlying olfactory learning in the infant rat [102][103][104]112]. Important roles have been found for alterations in the olfactory bulb, norepinephrine secretion from the locus coeruleus into the bulb, and modulating We hypothesize that biparental rearing causes an alteration in the pups' USV response to the male, which is mediated by neural mechanisms similar to that described for the induction of an odor preference [71,[99][100][101]. That is, stimulation of the pups in the presence of the adult male activates the locus coeruleus and norepinephrine secretion to enhance the development of an odor preference and a social bond.…”

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confidence: 90%

Acquisition and expression of a socially mediated separation response

Shair¹

2007

Behavioural Brain Research

108

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INTRODUCTIONSocial bonds are made up of numerous subsystems mediating the overall social relationships that develop between infants and caretakers. The effects of an infant's formation of early life relationships and its social interactions with caretakers are known to last well in to adulthood with both beneficial and harmful effects [28,35,70]. In our laboratory, we study the development of social relationships between infant rats and their dams, sires, and littermates using an isolation, reunion, and re-isolation test paradigm.Infant rats emit ultrasonic vocalizations (USV) in a variety of situations, including as a response to isolation, physical manipulation, and thermal and olfactory challenge [1][2][3]6,19,25,46,79,80,82,97]. Many researchers have used the presence and absence of these sounds to make inferences about the internal state of the rodents, e.g., isolation-induced USV's have often been called "distress vocalizations" [29,76,78].The isolation-induced vocalization of a rat pup is modulated both by current social interactions and by the pup's rearing experience. This modulation of USV by social interactions provides a paradigm for investigating the neurobehavioral mechanisms underlying acquisition and expression of infant attachment. What is maternal potentiation of isolation-induced vocalizations of infant rats?Maternal potentiation of ultrasonic vocalization occurs when, after a brief contact with the dam, isolated infant rats produce USV at a rate significantly higher than they would during an isolation not preceded by dam contact. Although the definition may seem of narrow interest, there is a growing belief that the potentiation phenomenon has broad applicability for the study of early life social relationships in many species. But before going further, the reader needs to understand the usual test paradigm in our laboratory.Developmental Psychobiology, Unit 40, New York State Psychiatric Institute, 1051 Riverside Dr. NY, NY 100032, Tele 212-543-5695, Fax 212-543-5467, hns1@columbia.edu Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. NIH Public Access NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptTest procedure-On the day of testing, the dam is removed from the home cage and anesthetized. The litter is allowed to adapt to her removal for ~15-20min in the home cage on a thermoregulated heating pad. Then, each pup is tested in turn. The pup is picked up and placed alone in a clean polycarbonate rectangular box (18 × 21 × 20 cm) at room temperature. The test consists of three periods, which can range from 1-5min in length (3mi...

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Unique Neural Circuitry for Neonatal Olfactory Learning

Cited by 129 publications

References 108 publications

Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity

Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity

The temporal dynamics of consolidation and reconsolidation decrease during postnatal development

Acquisition and expression of a socially mediated separation response

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