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

Rinaman, Linda; Banihashemi, Layla; Koehnle, Thomas J.

doi:10.1016/j.physbeh.2011.04.008

Cited by 28 publications

(28 citation statements)

References 195 publications

(192 reference statements)

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“…Environmental events during early postnatal life can influence the formation of neural circuits that provide limbic and cortical control over autonomic emotional motor output since a differential timing of hypothalamic and limbic forebrain synaptic inputs to autonomic neurons has been observed during the first 1-2 weeks postnatal (Rinaman, et al 2011). This provides a potential structural correlate for early experience-dependent effects on later responsiveness to emotionally evocative stimuli and an enhanced risk for the development of psychopathologies such as mood and aggressive disorders.…”

Section: Amygdala and Early Stressmentioning

confidence: 99%

The Irritable Bowel Syndrome: How Stress Can Affect the Amygdala Activity and the Brain-Gut Axis

Bonaz¹,

Pellissier²,

Sinniger³

et al. 2012

The Amygdala - A Discrete Multitasking Manager

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Section: Amygdala and Early Stressmentioning

confidence: 99%

The Irritable Bowel Syndrome: How Stress Can Affect the Amygdala Activity and the Brain-Gut Axis

Bonaz¹,

Pellissier²,

Sinniger³

et al. 2012

The Amygdala - A Discrete Multitasking Manager

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“…Several studies have demonstrated the dramatic consequences that environmental and maternal stress during this period can exert upon the development and patterning of neural circuits controlling GI functions (Banihashemi & Rinaman, ; Rinaman et al . ).…”

Section: Introductionmentioning

confidence: 97%

“…The perinatal period therefore provides a critical opportunity during which autonomic neurocircuits may be re-wired permanently. Several studies have demonstrated the dramatic consequences that environmental and maternal stress during this period can exert upon the development and patterning of neural circuits controlling GI functions (Banihashemi & Rinaman, 2010;Rinaman et al 2011).…”

Section: Introductionmentioning

confidence: 99%

Exposure to a high fat diet during the perinatal period alters vagal motoneurone excitability, even in the absence of obesity

Bhagat

Fortna

Browning

2014

The Journal of Physiology

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Key pointsr Obesity is recognized as being multifactorial in origin, involving both genetic and environmental factors. The perinatal period is known to be critically important in the development of neural circuits responsible for energy homeostasis and the integration of autonomic reflexes.r Diet-induced obesity alters the biophysical, pharmacological and morphological properties of vagal neurocircuits regulating upper gastrointestinal tract functions, including satiety. Less information is available, however, regarding the effects of a high fat diet (HFD) itself on the properties of vagal neurocircuits.r The present study was designed to test the hypothesis that exposure to a HFD during the perinatal period alters the electrophysiological, pharmacological and morphological properties of vagal efferent motoneurones innervating the stomach.r Our data indicate that perinatal HFD decreases the excitability of gastric-projecting dorsal motor nucleus neurones and dysregulates neurotransmitter release from synaptic inputs and that these alterations occur prior to the development of obesity. These findings represent the first direct evidence that exposure to a HFD modulates the processing of central vagal neurocircuits even in the absence of obesity.Abstract The perinatal period is critically important to the development of autonomic neural circuits responsible for energy homeostasis. Vagal neurocircuits are vital to the regulation of upper gastrointestinal functions, including satiety. Diet-induced obesity modulates the excitability and responsiveness of both peripheral vagal afferents and central vagal efferents but less information is available regarding the effects of diet per se on vagal neurocircuit functions. The aims of this study were to investigate whether perinatal exposure to a high fat diet (HFD) dysregulated dorsal motor nucleus of the vagus (DMV) neurones, prior to the development of obesity. Whole cell patch clamp recordings were made from gastric-projecting DMV neurones in thin brainstem slices from rats that were exposed to either a control diet or HFD from pregnancy day 13. Our data demonstrate that following perinatal HFD: (i) DMV neurones had decreased excitability and input resistance with a reduced ability to fire action potentials; (ii) the proportion of DMV neurones excited by cholecystokinin (CCK) was unaltered but the proportion of neurones in which CCK increased excitatory glutamatergic synaptic inputs was reduced; (iii) the tonic activation of presynaptic group II metabotropic glutamate receptors on inhibitory nerve terminals was attenuated, allowing modulation of GABAergic synaptic transmission; and (iv) the size and dendritic arborization of gastric-projecting DMV neurones was increased. These results suggest that perinatal HFD exposure compromises the excitability and responsiveness of gastric-projecting DMV neurones, even in the absence of obesity, suggesting that attenuation of vago-vagal reflex signalling may precede the development of obesity.

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“…Other environmental conditions also contribute to adult stress reactivity, and early life is a particularly sensitive period that can shape the health, coping style and physiological responses across the lifespan (de Kloet et al 2005, Cottrell and Seckl 2009, Lupien et al 2009, Rinaman et al 2011, Entringer et al 2015). To this end, we designed a study to assess whether early life stress would alter adult stress responses and behaviors within the VBS.…”

Section: Introductionmentioning

confidence: 99%

Susceptibility or resilience? Prenatal stress predisposes male rats to social subordination, but facilitates adaptation to subordinate status

Scott

Kloet

Smeltzer

et al. 2017

Physiology & Behavior

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Mood disorders such as major depressive disorder (MDD) affect a significant proportion of the population. Although progress has been made in the development of therapeutics, a large number of individuals do not attain full remission of symptoms and adverse side effects affect treatment compliance for some. In order to develop new therapies, there is a push for new models that better reflect the multiple risk factors that likely contribute to the development of depressive illness. We hypothesized that early life stress would exacerbate the depressive-like phenotype that we have previously observed in socially subordinate (SUB), adult male rats in the visible burrow system (VBS), a semi-natural, ethologically relevant environment in which males in a colony form a dominance hierarchy. Dams were exposed to chronic variable stress (CVS) during the last week of gestation, resulting in a robust and non-habituating glucocorticoid response that did not alter maternal food intake, body weight or litter size and weight. As adults, one prenatal CVS (PCVS) and one non-stressed (NS) male were housed in the VBS with adult females. Although there were no overt differences between PCVS and NS male offspring prior to VBS housing, a greater percentage of PCVS males became SUB. However, the depressive-like phenotype of SUB males was not exacerbated in PCVS males; rather, they appeared to better cope with SUB status than NS SUB males. They had lower basal plasma corticosterone than NS SUB males at the end of VBS housing. In situ hybridization for CRH in the PVN and CeA did not reveal any prenatal treatment or status effects, while NPY expression was higher within the MeA of dominant and subordinate males exposed to the VBS in comparison with controls, but with no effect of prenatal treatment. These data suggest that prenatal chronic variable stress may confer resilience to offspring when exposed to social stress in adulthood.

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

Cited by 28 publications

References 195 publications

The Irritable Bowel Syndrome: How Stress Can Affect the Amygdala Activity and the Brain-Gut Axis

The Irritable Bowel Syndrome: How Stress Can Affect the Amygdala Activity and the Brain-Gut Axis

Exposure to a high fat diet during the perinatal period alters vagal motoneurone excitability, even in the absence of obesity

Susceptibility or resilience? Prenatal stress predisposes male rats to social subordination, but facilitates adaptation to subordinate status

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