The ontogenesis of defensive reactions to shock in preweanling rats

Collier, Alexis C.; Bolles, Robert C.

doi:10.1002/dev.420130206

Cited by 60 publications

(42 citation statements)

References 13 publications

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“…Falcon et al [77] found that the nadir for thermal pain thresholds in infant rats occurred at P6 and similar age-related patterns were noted in thresholds for the cutaneous withdrawal reflex [73] and foot-shock responses [122]. When rat pups of different age groups (P4, P7, P14) were tested with graded painful stimuli in our laboratory, the number of ultrasonic cries at P7 were significantly increased (ANOVA, F = 57.94, p !…”

Section: Critical Periods Of Vulnerabilitymentioning

confidence: 99%

Can Adverse Neonatal Experiences Alter Brain Development and Subsequent Behavior?

Anand

Scalzo²

2000

Neonatology

538

316

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Self-destructive behavior in current society promotes a search for psychobiological factors underlying this epidemic. Perinatal brain plasticity increases the vulnerability to early adverse experiences, thus leading to abnormal development and behavior. Although several epidemiological investigations have correlated perinatal and neonatal complications with abnormal adult behavior, our understanding of the underlying mechanisms remains rudimentary. Models of early experience, such as repetitive pain, sepsis, or maternal separation in rodents and other species have noted multiple alterations in the adult brain, correlated with specific behavioral phenotypes depending on the timing and nature of the insult. The mechanisms mediating such changes in the neonatal brain have remained largely unexplored. We propose that lack of N-methyl-D-aspartate (NMDA) receptor activity from maternal separation and sensory isolation leads to increased apoptosis in multiple areas of the immature brain. On the other hand, exposure to repetitive pain may cause excessive NMDA/excitatory amino acid activation resulting in excitotoxic damage to developing neurons. These changes promote two distinct behavioral phenotypes characterized by increased anxiety, altered pain sensitivity, stress disorders, hyperactivity/attention deficit disorder, leading to impaired social skills and patterns of self-destructive behavior. The clinical important of these mechanisms lies in the prevention of early insults, effective treatment of neonatal pain and stress, and perhaps the discovery of novel therapeutic approaches that limit neuronal excitotoxicity or apoptosis.

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Section: Critical Periods Of Vulnerabilitymentioning

confidence: 99%

Can Adverse Neonatal Experiences Alter Brain Development and Subsequent Behavior?

Anand

Scalzo²

2000

Neonatology

538

316

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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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“…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).…”

mentioning

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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The ontogenesis of defensive reactions to shock in preweanling rats

Cited by 60 publications

References 13 publications

Can Adverse Neonatal Experiences Alter Brain Development and Subsequent Behavior?

Can Adverse Neonatal Experiences Alter Brain Development and Subsequent Behavior?

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

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

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