Early experience alters limbic forebrain Fos responses to a stressful interoceptive stimulus in young adult rats

Koehnle, Thomas J.; Rinaman, Linda

doi:10.1016/j.physbeh.2010.02.006

Cited by 15 publications

(7 citation statements)

References 47 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Our findings that juvenile rats with a developmental history of MS15 displayed less stress-induced Fos activation within the caudal PVN and dBNST concur with previous reports of attenuated Fos activation of hypothalamic and limbic forebrain regions in adult MS15 rats after stress (Abraham and Kovacs, 2000, Koehnle and Rinaman, 2010). Interestingly, the PVN region in which juvenile MS15 rats displayed a decrease in restraint-induced Fos is the same region in which juvenile MS15 rats display enhanced retrograde transynaptic viral transport from the stomach wall (Banihashemi and Rinaman, 2010).…”

Section: Discussionsupporting

confidence: 92%

Central neural responses to restraint stress are altered in rats with an early life history of repeated brief maternal separation

2011

View full text Add to dashboard Cite

Repeated brief maternal separation (i.e., 15 minutes daily, MS15) of rat pups during the first one to two postnatal weeks enhances active maternal care received by the pups and attenuates their later behavioral and neuroendocrine responses to stress. In previous work, we found that MS15 also alters the developmental assembly and later structure of central neural circuits that control autonomic outflow to the viscera, suggesting that MS15 may alter central visceral circuit responses to stress. To examine this, juvenile rats with a developmental history of either MS15 or no separation (NS) received microinjection of retrograde neural tracer, FluoroGold (FG), into the hindbrain dorsal vagal complex (DVC). After one week, FG-injected rats and surgically intact littermates were exposed to either a 15-minute restraint stress or an unrestrained control condition, and then perfused one hour later. Brain tissue sections from surgically-intact littermates were processed for Fos alone or in combination with phenotypic markers to examine stress-induced activation of neurons within the paraventricular nucleus of the hypothalamus (PVN), bed nucleus of the stria terminalis (BNST), and hindbrain DVC. Compared to NS controls, MS15 rats displayed less restraint-induced Fos activation within the dorsolateral BNST (dBNST), the caudal PVN, and noradrenergic neurons within the caudal DVC. To examine whether these differences corresponded with altered neural inputs to the DVC, sections from tracer-injected rats were double-labeled for FG and Fos to quantify retrogradely-labeled neurons within hypothalamic and limbic forebrain regions of interest, and the proportion of these neurons activated after restraint. Only the dBNST displayed a significant effect of postnatal experience on restraint-induced Fos activation of DVC-projecting neurons. The distinct regional effects of MS15 on stress-induced recruitment of neurons within hypothalamic, limbic forebrain, and hindbrain regions has interesting implications for understanding how early life experience shapes the functional organization of stress-responsive circuits.

show abstract

Section: Discussionsupporting

confidence: 92%

Central neural responses to restraint stress are altered in rats with an early life history of repeated brief maternal separation

2011

View full text Add to dashboard Cite

show abstract

“…We previously had demonstrated that central neural Fos responses to systemic LiCl matured during postnatal development [126], suggesting that the circuits underlying these responses might be susceptible to alteration by manipulating pups’ early life experience during that period of maturation. Similar to previous reports in adult rats, adolescent rats (P35-45) with a developmental history of MS15 displayed less anxiety-like behavior on the elevated plus maze compared to control and MS180 rats [179]. MS15 rats tended to display fewer LiCl-activated neurons in most brain regions compared with rats in the other two rearing groups.…”

Section: 0 Early Experience Modifies Visceral Circuit Assemblysupporting

confidence: 85%

“…To test this idea, we examined whether MS15 and/or MS180 might alter the later ability of an interoceptive challenge to recruit central neural circuits that receive visceral sensory signals and generate stress responses [179]. We previously had demonstrated that central neural Fos responses to systemic LiCl matured during postnatal development [126], suggesting that the circuits underlying these responses might be susceptible to alteration by manipulating pups’ early life experience during that period of maturation.…”

Section: 0 Early Experience Modifies Visceral Circuit Assemblymentioning

confidence: 99%

Early life experience shapes the functional organization of stress-responsive visceral circuits

Rinaman

Banihashemi

Koehnle

2011

Physiology & Behavior

Self Cite

View full text Add to dashboard Cite

Emotions are closely tied to changes in autonomic (i.e., visceral motor) function, and interoceptive sensory feedback from body to brain exerts powerful modulatory control over motivation, affect, and stress responsiveness. This manuscript reviews evidence that early life experience can shape the structure and function of central visceral circuits that underlie behavioral and physiological responses to emotive and stressful events. The review begins with a general discussion of descending autonomic and ascending visceral sensory pathways within the brain, and then summarizes what is known about the postnatal development of these central visceral circuits in rats. Evidence is then presented to support the view that early life experience, particularly maternal care, can modify the developmental assembly and structure of these circuits in a way that impacts later stress responsiveness and emotional behavior. The review concludes by presenting a working hypothesis that endogenous cholecystokinin signaling and subsequent recruitment of gastric vagal sensory inputs to the caudal brainstem may be an important mechanism by which maternal care influences visceral circuit development in rat pups. Early life experience may contribute to meaningful individual differences in emotionality and stress responsiveness by shaping the postnatal developmental trajectory of central visceral circuits.

show abstract

“…What are the specific effects of microbial signals on plasticity of gene expression by vagal sensory neurons within the nodose ganglia, and on neurons within the REVIEW PHYSIOLOGY • Volume 33 • March 2018 • www.physiologyonline.org cNTS that carry gut-derived signals to higher brain regions? Furthermore, given the powerful impact of early life events on the developmental assembly and life-long function of central visceral sensory and motor circuits, stress responsiveness, and emotionality (15,88,129,130,206,208,255,262), it is critical to determine how pre-and postnatal stress exposure, maternal diet during pregnancy and lactation, offspring diet from infancy through adolescence, and other environmental factors affect gene expression and signal transmission in vagal sensory pathways from gut to brain.…”

Section: Discussionmentioning

confidence: 99%

Vagal Interoceptive Modulation of Motivated Behavior

Maniscalco

Rinaman

2018

Physiology

View full text Add to dashboard Cite

In addition to regulating the ingestion and digestion of food, sensory feedback from gut to brain modifies emotional state and motivated behavior by subconsciously shaping cognitive and affective responses to events that bias behavioral choice. This focused review highlights evidence that gut-derived signals impact motivated behavior by engaging vagal afferents and central neural circuits that generally serve to limit or terminate goal-directed approach behaviors, and to initiate or maintain behavioral avoidance.

show abstract

Early experience alters limbic forebrain Fos responses to a stressful interoceptive stimulus in young adult rats

Cited by 15 publications

References 47 publications

Central neural responses to restraint stress are altered in rats with an early life history of repeated brief maternal separation

Central neural responses to restraint stress are altered in rats with an early life history of repeated brief maternal separation

Early life experience shapes the functional organization of stress-responsive visceral circuits

Vagal Interoceptive Modulation of Motivated Behavior

Contact Info

Product

Resources

About