Abstract
Although adverse early experiences prime individuals to be at increased risk for chronic pain, little research has examined the trauma–pain relationship in early life or the underlying mechanisms that drive pathology over time. Given that early experiences can potentiate the nociceptive response, this study aimed to examine the effects of a high-fat, high-sugar (HFHS) diet and early life stress (maternal separation [MS]) on pain outcomes in male and female adolescent rats. Half of the rats also underwent a plantar-incision surgery to investigate how the pain system responded to a mildly painful stimuli in adolescence. Compared with controls, animals that were on the HFHS diet, experienced MS, or had exposure to both, exhibited increased anxiety-like behavior and altered thermal and mechanical nociception at baseline and following the surgery. Advanced magnetic resonance imaging demonstrated that the HFHS diet and MS altered the maturation of the brain, leading to changes in brain volume and diffusivity within the anterior cingulate, amygdala, corpus callosum, nucleus accumbens, and thalamus, while also modifying the integrity of the corticospinal tracts. The effects of MS and HFHS diet were often cumulative, producing exacerbated pain sensitivity and increased neurobiological change. As early experiences are modifiable, understanding their role in pain may provide targets for early intervention/prevention.
Highlights
Chronic pain is one of the most prevalent and expensive health conditions affecting adolescents (King et al 2011)
Advanced magnetic resonance imaging demonstrated that the HFHS diet and maternal separation (MS) altered the maturation of the brain, leading to changes in brain volume and diffusivity within the anterior cingulate, amygdala, corpus callosum, nucleus accumbens, and thalamus, while modifying the integrity of the corticospinal tracts
Body weight at euthanasia was consistent with the HFHS diet phenotype, whereby animals that consumed the HFHS diet and animals fed the standard diet were significantly different (P < 0.01); weight was unaltered by the MS exposure early in life or by the plantar incision surgery (Ps > 0.05)
Summary
Chronic pain is one of the most prevalent and expensive health conditions affecting adolescents (King et al 2011). Adolescence is a critical developmental period that results in maturational changes in both the body and brain (Spear 2013) These include changes in hormone levels, the development of secondary sex characteristics, as well as increased myelination and synaptic pruning that remodel the neurocircuitry of the brain (Giedd 2008; Steinberg et al 2008; Blakemore et al 2010). Given the significant development that occurs during this period, environmental factors have the potential to substantially modify long-term trajectories. This can occur via programming mechanisms where, during critical periods of plasticity, organisms are primed to adapt to their environment in an effort to increase their propensity for survival (Welberg and Seckl 2001). If circumstances early in life do not match with those in their later environment, these adaptations can be maladaptive and prime systems to inappropriately respond to stimuli (Welberg and Seckl 2001)
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