The Role of the Amygdala and Olfaction in Unconditioned Fear in Developing Rats

Chen, Sean W. C.; Shemyakin, Alexei; Wiedenmayer, Christoph P.

doi:10.1523/jneurosci.2890-05.2006

Cited by 28 publications

(26 citation statements)

References 69 publications

(70 reference statements)

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“…Injection cannulas for all ages were constructed so that they extended 0.5 mm beyond the tip of the guide cannula. Previous radiolabeling results (Chen et al 2006) found that this volume of muscimol spreads to a maximum radius of 0.5 mm from the cannula tip, restricting the pharmacological inactivation effect to the mPFC subdivisions. Cannula placements were verified in later histology procedures (see below).…”

Section: Methodsmentioning

confidence: 85%

The Role of the Medial Prefrontal Cortex in Innate Fear Regulation in Infants, Juveniles, and Adolescents

Chan¹,

Kyere²,

Davis³

et al. 2011

J. Neurosci.

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In adult animals, the medial prefrontal cortex (mPFC) plays a significant role in regulating emotions and projects to the amygdala and periaqueductal gray (PAG) to modulate emotional responses. However, little is known about the development of this neural circuit and its relevance to unlearned fear in pre-adulthood. To address these issues, we examined the mPFC of 14 (infants), 26 (juveniles), and 38–42 (adolescents) day old rats, to represent different developmental and social milestones. The expression patterns of the neuronal marker FOS were used to assess neurological activity. Muscimol, a GABA agonist, was used to inactivate the prelimbic and infralimbic mPFC subdivisions (400 ng in 200 nl). Animals were exposed to either a threatening or non-threatening stimulus that was ecologically relevant and age-specific. Freezing was measured as an indicator of innate fear behavior. The data indicated that the mPFC is neither active nor responsive to innate fear in infant rats. In juveniles, the prelimbic mPFC became responsive in processing aversive sensory stimulation, but did not regulate freezing behavior. Finally, during adolescence, inactivation of the prelimbic mPFC significantly attenuated freezing, and decreased FOS expression in the ventral PAG. Surprisingly, across all ages, there were no significant differences in FOS levels in the medial and basolateral/lateral amygdala when either mPFC subdivision was inactivated. Taken together, unlearned fear has a unique developmental course with different brain areas involved in unlearned fear in the immature animal than the adult. In particular, the mPFC neural circuitry is different in young animals and progressively develops more capacities as the animal matures.

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Section: Methodsmentioning

confidence: 85%

The Role of the Medial Prefrontal Cortex in Innate Fear Regulation in Infants, Juveniles, and Adolescents

Chan¹,

Kyere²,

Davis³

et al. 2011

J. Neurosci.

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show abstract

“…In contrast, at P23-24, the basolateral complex is activated under all three conditions (Raineki et al, 2009;Shionoya et al, 2006). Similarly, at P14, exposure to a male rat induces c-fos expression in the medial nucleus of the amygdala, but not in the lateral nucleus, whereas, at P18, c-fos expression is observed in both the medial and the lateral nuclei (Chen et al, 2006;but see Wiedenmayer and Barr, 2001a). This suggests that there are several neural pathways for threat-induced fear responses, which exhibit different developmental time courses, and that the lateral, basal, and accessory basal nuclei of the amygdala do not become involved in these pathways until sometime during the second postnatal week.…”

Section: Functional Considerationsmentioning

confidence: 95%

“…Individual components of the fear response are thought to incorporate sequentially as animals mature, eventually giving rise to what are identified as mature fear behaviors (Wiedenmayer, 2009). Indeed, several studies have revealed that distinct fear behaviors emerge at different times during early postnatal life and continue to mature during late postnatal development (Blozovski and Cudennec, 1980;Bronstein and Hirsch, 1976;Chen et al, 2006;Collier et al, 1979;Foster and Burman, 2010;Hefner and Holmes, 2007;Hubbard et al, 2004;Ito et al, 2009;Kim and Richardson, 2007;Moriceau et al, 2004;Raineki et al, 2010;Rudy, 1993;Takahashi, 1992;Wiedenmayer andBarr, 1998, 2001a,b).…”

Section: Introductionmentioning

confidence: 99%

Postnatal development of the amygdala: A stereological study in rats

Chareyron

Lavenex

2012

J of Comparative Neurology

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The amygdala is the central component of a functional brain system regulating fear and emotional behaviors. Studies of the ontogeny of fear behaviors reveal the emergence of distinct fear responses at different postnatal ages. Here, we performed a stereological analysis of the rat amygdala to characterize the cellular changes underlying its normal structural development. Distinct amygdala nuclei exhibited different patterns of postnatal development, which were largely similar to those we have previously shown in monkeys. The combined volume of the lateral, basal, and accessory basal nuclei increased by 113% from 1 to 3 weeks of age and by an additional 33% by 7 months of age. The volume of the central nucleus increased only 37% from 1 to 2 weeks of age and 38% from 2 weeks to 7 months. At 1 week of age, the medial nucleus was 77% of the 7-monthold's volume and exhibited a constant, marginal increase until 7 months. Neuron number did not differ in the amygdala from 1 week to 7 months of age. In contrast, astrocyte number decreased from 3 weeks to 2 months of age in the whole amygdala. Oligodendrocyte number increased in all amygdala nuclei from 3 weeks to 7 months of age. Our findings revealed that distinct amygdala nuclei exhibit different developmental profiles and that the rat amygdala is not fully mature for an extended period postnatally. We identified different periods of postnatal development of distinct amygdala nuclei and cellular components, which are concomitant with the ontogeny of different fear and emotional behaviors.

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“…At PN14 and PN23, decreased activity was found in the aPCX, suggesting a fundamental difference in the processing of male odor after this switch of hedonic value (Nacher et al, 2004;Roth and Sullivan, 2005;. Furthermore, the pPCX, which has been implicated in aversive odor hedonic tagging within the context of threat conditioning, showed decreased activation at PN14, but not PN23, suggesting that this area may be important for aversive odor hedonics of innately threatening stimuli in infancy only (Chan et al, 2011;Li, 2014). The decrease in MeA activity is consistent with lesion data showing reduced freezing to predator odor in infancy (Chen et al, 2006) and adulthood (Blanchard et al, 2005) after MeA lesions.…”

Section: Response Plasticitymentioning

confidence: 99%

Development of Odor Hedonics: Experience-Dependent Ontogeny of Circuits Supporting Maternal and Predator Odor Responses in Rats

et al. 2016

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A major component of perception is hedonic valence: perceiving stimuli as pleasant or unpleasant. Here, we used early olfactory experiences that shape odor preferences and aversions to explore developmental plasticity in circuits mediating odor hedonics. We used 2-deoxyglucose autoradiographic mapping of neural activity to identify circuits differentially activated by biologically relevant preferred and avoided odors across rat development. We then further probed this system by increasing or decreasing hedonic value. Using both region of interest and functional connectivity analyses, we identified regions within primary olfactory, amygdala/hippocampal, and prefrontal cortical networks that were activated differentially by maternal and male odors. Although some activated regions remained stable across development (postnatal days 7-23), there was a developmental emergence of others that resulted in an age-dependent elaboration of hedonic-response-specific circuitry despite stable behavioral responses (approach/avoidance) to the odors across age. Hedonic responses to these biologically important odors were modified through diet suppression of the maternal odor and co-rearing with a male. This allowed assessment of hedonic circuits in isolation of the specific odor quality and/or intensity. Early experience significantly modified odor-evoked circuitry in an age-dependent manner. For example, co-rearing with a male, which induced pup attraction to male odor, reduced activity in amygdala regions normally activated by the unfamiliar avoided male odor, making this region more consistent with maternal odor. Understanding the development of odor hedonics, particularly within the context of altered early life experience, provides insight into the development of sensory processes, food preferences, and the formation of social affiliations, among other behaviors.

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The Role of the Amygdala and Olfaction in Unconditioned Fear in Developing Rats

Cited by 28 publications

References 69 publications

The Role of the Medial Prefrontal Cortex in Innate Fear Regulation in Infants, Juveniles, and Adolescents

The Role of the Medial Prefrontal Cortex in Innate Fear Regulation in Infants, Juveniles, and Adolescents

Postnatal development of the amygdala: A stereological study in rats

Development of Odor Hedonics: Experience-Dependent Ontogeny of Circuits Supporting Maternal and Predator Odor Responses in Rats

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