Enkephalin Surges in Dorsal Neostriatum as a Signal to Eat

Abstract

Summary Compulsive over-consumption of rewards characterizes disorders ranging from binge eating to drug addiction. Here, we provide evidence that enkephalin surges in an anteromedial quadrant of dorsal neostriatum contribute to generating intense consumption of palatable food. In ventral striatum, mu opioid circuitry contributes an important component of motivation to consume rewards [1–4]. In dorsal neostriatum, mu opioid receptors are concentrated within striosomes that receive inputs from limbic regions of prefrontal cortex [5–13]. We employed advanced opioid microdialysis techniques that allow detection of extracellular enkephalin levels. Endogenous >150% enkephalin surges in anterior dorsomedial neostriatum were triggered as rats began to consume palatable chocolates. By contrast, dynorphin levels remained unchanged. Further, a causal role for mu opioid stimulation in over-consumption was demonstrated by observations that microinjection in the same anterior dorsomedial quadrant of a mu receptor agonist (DAMGO) generated intense >250% increases in intake of palatable sweet food (without altering hedonic impact of sweet tastes). Mapping by “Fos plume” methods confirmed the hyperphagic effect to be anatomically localized to the anterior medial quadrant of the dorsal neostriatum, whereas other quadrants were relatively ineffective. These findings reveal that opioid signals in anteromedial dorsal neostriatum are able to code and cause motivation to consume sensory rewards.

Orexin in Rostral Hotspot of Nucleus Accumbens Enhances Sucrose ‘Liking’ and Intake but Scopolamine in Caudal Shell Shifts ‘Liking’ Toward ‘Disgust’ and ‘Fear’

“…By contrast, the motivation to eat, expressed as higher food consumption, was increased by orexin at all sites throughout the entire medial shell. Widespread anatomical NAc stimulation of intake is also similar to mu-opioid stimulation, which increases eating at all sites throughout shell and core, as well as in dorsal and ventrolateral regions of neostriatum, in central nucleus of amygdala, and in medial prefrontal cortex (Castro and Berridge, 2014;DiFeliceantonio et al, 2012;Mahler and Berridge, 2009;Mena et al, 2011;Pecina and Berridge, 2005;Ragnauth et al, 2000;Richard et al, 2013;Thorpe and Kotz, 2005;Zhang and Kelley, 2000).…”

Breaking Bread: the Functions of Social Eating

“…We also know that activities such as laughter, singing and dancing all lead to an enhanced sense of bonding towards those with whom one does these activities Pearce et al 2015;Tarr et al 2015Tarr et al , 2016Manninen et al, submitted), mainly because they trigger the endorphin system in the brain that underpins primate social bonding (Panksepp et al 1997;Curley and Keverne 2005;Dunbar 2010;Machin and Dunbar 2011). Since endorphins are involved in the control of feeding (Bakshi and Kelley 1993;Zhang and Kelley 2000;DiFeliceantonio et al 2012), the very fact of eating might itself trigger the endorphin system and promote bonding, and doing so socially may lead to the same kind of enhanced endorphin effects from behavioural synchrony that have been noted in physical exercise (Cohen et al 2010). Hence, people who eat often with others might be expected to have larger social networks and be happier and more satisfied with their lives, as well as being more engaged with their communities.…”

Upregulation of Gene Expression in Reward-Modulatory Striatal Opioid Systems by Sleep Loss

“…Striatal ENK is modulated by motivational contingencies such as the expectation of scheduled feeding or contextual stimuli associated with palatable food, but not by food restriction (Schlitz et al, 2007;Will et al, 2007), and stimulation of striatal m-opioid receptors (the cognate receptors for ENK) strongly enhances palatable feeding and hedonic taste reactivity (Baldo and Kelley, 2007;Pecina and Berridge, 2005;Woolley et al, 2006;Zhang et al, 1998;Zhang and Kelley, 2002). A recent study showed that surges of endogenously released striatal ENK act as signals to overeat palatable foods (Difeliceantonio et al, 2012). Accordingly, with regard to food motivation, fluctuations in striatal ENK expression have been hypothesized to track short-term motivational contingencies associated with feeding (Kelley et al, 2005;Will et al, 2007).…”

“…Stimulation of receptors for ENK within striatal subregions (particularly the nucleus accumbens (Acb)) augments the 'liking' of sweet tastes (Pecina and Berridge, 2005) and enhances the intake of sweet, and/or fat-rich foodstuffs (Woolley et al, 2006;Zhang et al, 1998)-the same types of food whose intake is augmented in sleep loss. Furthermore, endogenous ENK release in rat striatum accompanies the 'binge-like' intake of palatable food (Difeliceantonio et al, 2012), and striatal ENK gene expression is upregulated by palatable food-conditioned cues (Schiltz et al, 2007). ENK and related systems could therefore have an important role in the palatable or high-fat food snacking seen with sleep loss in humans, which appears to be a crucial factor promoting weight gain (Markwald et al, 2013;StOnge et al, 2011).…”