Abstract
Environmental enrichment (EE) has a beneficial effect on rodent behaviour, neuronal plasticity and brain function. Although it may also improve stress coping, it is not known whether EE influences the brain response to an external (psychological) stressor such as water avoidance stress (WAS) or an internal (systemic) stressor such as gastrointestinal inflammation. This study hence explored whether EE modifies WAS-induced activation of the mouse corticolimbic system and whether this stress response is altered by gastritis or colitis. Male C67BL/6N mice were housed under standard or enriched environment for 9 weeks, after which they were subjected to a 1-week treatment with oral iodoacetamide to induce gastritis or oral dextran sulfate sodium to induce colitis. Following exposure to WAS the expression of c-Fos, a marker of neuronal activation, was measured by immunocytochemistry. EE aggravated experimentally induced colitis, but not gastritis, as shown by an increase in the disease activity score and the colonic myeloperoxidase content. In the brain, EE enhanced the WAS-induced activation of the dentate gyrus and unmasked an inhibitory effect of gastritis and colitis on WAS-evoked c-Fos expression within this part of the hippocampus. Conversely, EE inhibited the WAS-evoked activation of the central amygdala and prevented the inhibitory effect of gastritis and colitis on WAS-evoked c-Fos expression in this region. EE, in addition, blunted the WAS-induced activation of the infralimbic cortex and attenuated the inhibitory effect of gastritis and colitis on WAS-evoked c-Fos expression in this area. These data reveal that EE has a region-specific effect on stress-induced c-Fos expression in the corticolimbic system, which is likely to improve stress resilience. The response of the prefrontal cortex – amygdala – hippocampus circuitry to psychological stress is also modified by the systemic stress of gut inflammation, and this interaction between external and internal stressors is modulated by the housing environment.
Highlights
Environmental enrichment (EE) has several beneficial effects on rodent behaviour and brain neurochemistry [1]
Trunk blood was collected for measurement of corticosterone, the stomach and colon were excised for determination of the myeloperoxidase (MPO) content, and the brain was collected for immunocytochemical visualization of c-Fos expression in selected brain regions
Twoway repeated-measures analysis of variance (ANOVA) showed that the latency to find the hidden platform differed with housing condition (F(1, 118) = 11.804, P = 0.001) and trial day (F(1.551, 182.959) = 63.996, P,0.001), without a significant interaction between these factors
Summary
Environmental enrichment (EE) has several beneficial effects on rodent behaviour and brain neurochemistry [1]. Given that EE enhances neuronal plasticity, it has been argued that EE improves the welfare of captive animals as it enables them to express a much greater variety of species-specific behaviours than animals maintained under standard laboratory housing conditions [1]. Some studies indicate that EE can lower the response of rodents to psychological stress [4,6,17,18] and improve their recovery from this adverse condition [19]. These implications have been revealed by measuring key components of the hypothalamic-pituitaryadrenal (HPA) axis. EE is able to blunt the rise of adrenocorticotropic hormone (ACTH) and corticosterone plasma levels in response to individual housing stress [17], exposure to cat odour [4] or restraint stress [18,20]
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