Habituation of the forelimb-withdrawal response in neonatal rats.

Stehouwer, Donald J.; Campbell, Byron A.

doi:10.1037/0097-7403.4.2.104

Cited by 53 publications

(43 citation statements)

References 22 publications

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“…Additional species exhibiting a similar phenomenon include nonhuman primates (Harlow and Harlow, 1965), dogs [Fisher (1955), cited in Rajecki et al (1978)], and humans (Helfer et al, 1997). Our imprinting model in rat pups uses a fearconditioning paradigm in which odor paired with 0.5 mA shock paradoxically causes an odor preference during a temporally defined sensitive period (Sullivan et al, 1986a(Sullivan et al, ,b, 2000aCamp and Rudy, 1988;Moriceau and Sullivan, 2004b;Roth and Sullivan, 2005), although pups clearly show pain-related responses during shock (Stehouwer and Campbell, 1978;Emerich et al, 1985;Barr, 1995;Sullivan et al, 2000a). Our data suggest the amygdala does not participate in the sensitive-period odor-shock conditioning that may underlie the pups' attenuated aversion learning (Sullivan et al, 2000a;Moriceau and Sullivan, 2004b;Roth and Sullivan 2005).…”

Section: Introductionmentioning

confidence: 99%

Dual Circuitry for Odor-Shock Conditioning during Infancy: Corticosterone Switches between Fear and Attraction via Amygdala

Moriceau

Wilson

Levine

et al. 2006

Journal of Neuroscience

208

231

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Rat pups must learn maternal odor to support attachment behaviors, including nursing and orientation toward the mother. Neonates have a sensitive period for rapid, robust odor learning characterized by increased ability to learn odor preferences and decreased ability to learn odor aversions. Specifically, odor-0.5 mA shock association paradoxically causes an odor preference and coincident failure of amygdala activation in pups until postnatal day 10 (P10). Because sensitive-period termination coincides with a declining "stress hyporesponsive period" when corticosterone release is attenuated, we explored the role of corticosterone in sensitive-period termination. Odor was paired with 0.5 mA shock in either sensitive-period (P8) or postsensitive-period (P12) pups while manipulating corticosterone. We then assessed preference/aversion learning and the olfactory neural circuitry underlying its acquisition. Although sensitive-period control paired odor-shock pups learned an odor preference without amygdala participation, systemic (3 mg/kg, i.p.; 24 h and 30 min before training) or intra-amygdala corticosterone (50 or 100 ng; during training) permitted precocious odor-aversion learning and evoked amygdala neural activity similar to that expressed by older pups. In postsensitive-period (P12) pups, control paired odor-shock pups showed an odor aversion and amygdala activation, whereas corticosterone-depleted (adrenalectomized) paired odor-shock pups showed odor-preference learning and activation of an odor learning circuit characteristic of the sensitive period. Intra-amygdala corticosterone receptor antagonist (0.3 ng; during training) infused into postsensitive-period (P12) paired odor-shock pups also showed odor-preference learning. These results suggest corticosterone is important in sensitive-period termination and developmental emergence of olfactory fear conditioning, acting via the amygdala as a switch between fear and attraction. Because maternal stimulation of pups modulates the pups' endogenous corticosterone, this suggests maternal care quality may alter sensitive-period duration.

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Section: Introductionmentioning

confidence: 99%

Dual Circuitry for Odor-Shock Conditioning during Infancy: Corticosterone Switches between Fear and Attraction via Amygdala

Moriceau

Wilson

Levine

et al. 2006

Journal of Neuroscience

208

231

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“…Before this age, odor-shock associations paradoxically induce an odor preference (Stehouwer and Campbell 1978;Haroutunian and Campbell 1979;Camp and Rudy 1988;Sullivan et al 2000) despite pups feeling pain from shock (Collier and Bolles 1980;Barr 1995;Fitzgerald 2005). The neural network sustaining this paradoxical preference involves OB and anterior piriform cortex (aPCx) whereas the amygdala does not appear to participate in the circuit (Sullivan and Wilson 1995;Roth and Sullivan 2005;Moriceau et al 2006).…”

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confidence: 99%

Neonatal odor-shock conditioning alters the neural network involved in odor fear learning at adulthood

Sevelinges¹,

Sullivan²,

Messaoudi³

et al. 2008

Learn. Mem.

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Adult learning and memory functions are strongly dependent on neonatal experiences. We recently showed that neonatal odor-shock learning attenuates later life odor fear conditioning and amygdala activity. In the present work we investigated whether changes observed in adults can also be observed in other structures normally involved, namely olfactory cortical areas. For this, pups were trained daily from postnatal (PN) 8 to 12 in an odor-shock paradigm, and retrained at adulthood in the same task. 14 C 2-DG autoradiographic brain mapping was used to measure training-related activation in amygdala cortical nucleus (CoA), anterior (aPCx), and posterior (pPCx) piriform cortex. In addition, field potentials induced in the three sites in response to paired-pulse stimulation of the olfactory bulb were recorded in order to assess short-term inhibition and facilitation in these structures. Attenuated adult fear learning was accompanied by a deficit in 2-DG activation in CoA and pPCx. Moreover, electrophysiological recordings revealed that, in these sites, the level of inhibition was lower than in control animals. These data indicate that early life odor-shock learning produces changes throughout structures of the adult learning circuit that are independent, at least in part, from those involved in infant learning. Moreover, these enduring effects were influenced by the contingency of the infant experience since paired odor-shock produced greater disruption of adult learning and its supporting neural pathway than unpaired presentations. These results suggest that some enduring effects of early life experience are potentiated by contingency and extend beyond brain areas involved in infant learning.

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“…Haroutunian and Campbell (1979) demonstrated that moderately painful shock could not support aversion learning in neonatal rat pups unless it was delivered intraperitoneally, although higher shock (>1.0 mA) readily produced an odor aversion in very young pups (Kucharski and Spear 1984;Miller et al 1990a;Sullivan and Wilson 1995). While lower shock levels are painful to pups (Stehouwer and Campbell 1978;Collier and Bolles 1980;Emerich et al 1985;Sullivan et al 2000a), they paradoxically produce an odor preference in pups younger than PN10-12 (Sullivan et al 1986;Camp and Rudy 1988), apparently due to the amygdala's failure to participate during the conditioning (Sullivan et al 2000a).These data suggest that pups have access to at least two neural pathways for odor-aversion learning, although each has a different developmental time course. To test this, we made a direct neurobehavioral comparison of LiCl-induced odor aversion, 1.2-mA shock-induced odor aversion, and the 0.5-mA shock that produces a preference in young pups but an aversion in older pups.…”

mentioning

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

Learn. Mem.

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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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Habituation of the forelimb-withdrawal response in neonatal rats.

Cited by 53 publications

References 22 publications

Dual Circuitry for Odor-Shock Conditioning during Infancy: Corticosterone Switches between Fear and Attraction via Amygdala

Dual Circuitry for Odor-Shock Conditioning during Infancy: Corticosterone Switches between Fear and Attraction via Amygdala

Neonatal odor-shock conditioning alters the neural network involved in odor fear learning at adulthood

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

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