Rethinking Food Reward de Araujo, Ivan E; Schatzker, Mark; Small, Dana M
Annual review of psychology,
01/2020, Letnik:
71, Številka:
1
Journal Article
Recenzirano
Odprti dostop
The conscious perception of the hedonic sensory properties of caloric foods is commonly believed to guide our dietary choices. Current and traditional models implicate the consciously perceived ...hedonic qualities of food as driving overeating, whereas subliminal signals arising from the gut would curb our uncontrolled desire for calories. Here we review recent animal and human studies that support a markedly different model for food reward. These findings reveal in particular the existence of subcortical body-to-brain neural pathways linking gastrointestinal nutrient sensors to the brain's reward regions. Unexpectedly, consciously perceptible hedonic qualities appear to play a less relevant, and mostly transient, role in food reinforcement. In this model, gut-brain reward pathways bypass cranial taste and aroma sensory receptors and the cortical networks that give rise to flavor perception. They instead reinforce behaviors independently of the cognitive processes that support overt insights into the nature of our dietary decisions.
Glucagon-like peptide-1 (GLP-1) is a signal peptide released from enteroendocrine cells of the lower intestine. GLP-1 exerts anorectic and antimotility actions that protect the body against nutrient ...malabsorption. However, little is known about how intestinal GLP-1 affects distant organs despite rapid enzymatic inactivation. We show that intestinal GLP-1 inhibits gastric emptying and eating via intestinofugal neurons, a subclass of myenteric neurons that project to abdominal sympathetic ganglia. Remarkably, cell-specific ablation of intestinofugal neurons eliminated intestinal GLP-1 effects, and their chemical activation functioned as a GLP-1 mimetic. GLP-1 sensing by intestinofugal neurons then engaged a sympatho-gastro-spinal-reticular-hypothalamic pathway that links abnormal stomach distension to craniofacial programs for food rejection. Within this pathway, cell-specific activation of discrete neuronal populations caused systemic GLP-1-like effects. These molecularly identified, delimited enteric circuits may be targeted to ameliorate the abdominal bloating and loss of appetite typical of gastric motility disorders.
Area postrema in brainstem has long been known to trigger emesis by detecting blood-borne toxins and pathogens. In this issue, Zhang and colleagues provide a single-cell molecular atlas of this ...region, opening new possibilities for harnessing its neurons in vivo.
Area postrema in brainstem has long been known to trigger emesis by detecting blood-borne toxins and pathogens. In this issue, Zhang and colleagues provide a single-cell molecular atlas of this region, opening new possibilities for harnessing its neurons in vivo.
The gut is now recognized as a major regulator of motivational and emotional states. However, the relevant gut-brain neuronal circuitry remains unknown. We show that optical activation of ...gut-innervating vagal sensory neurons recapitulates the hallmark effects of stimulating brain reward neurons. Specifically, right, but not left, vagal sensory ganglion activation sustained self-stimulation behavior, conditioned both flavor and place preferences, and induced dopamine release from Substantia nigra. Cell-specific transneuronal tracing revealed asymmetric ascending pathways of vagal origin throughout the CNS. In particular, transneuronal labeling identified the glutamatergic neurons of the dorsolateral parabrachial region as the obligatory relay linking the right vagal sensory ganglion to dopamine cells in Substantia nigra. Consistently, optical activation of parabrachio-nigral projections replicated the rewarding effects of right vagus excitation. Our findings establish the vagal gut-to-brain axis as an integral component of the neuronal reward pathway. They also suggest novel vagal stimulation approaches to affective disorders.
Display omitted
•Critical role for the vagal gut-to-brain axis in motivation and reward•Optogenetic stimulation of the vagal gut-to-brain axis produces reward behaviors•Asymmetric brain pathways of vagal origin mediate motivation and dopamine activity•Gut-innervating vagal sensory neurons are major components of the reward circuitry
A gut-to-brain neural circuit establishes vagal neurons as an essential component of the reward neuronal pathway, linking sensory neurons in the upper gut to striatal dopamine release.
Superior predatory skills led to the evolutionary triumph of jawed vertebrates. However, the mechanisms by which the vertebrate brain controls predation remain largely unknown. Here, we reveal a ...critical role for the central nucleus of the amygdala in predatory hunting. Both optogenetic and chemogenetic stimulation of central amygdala of mice elicited predatory-like attacks upon both insect and artificial prey. Coordinated control of cervical and mandibular musculatures, which is necessary for accurately positioning lethal bites on prey, was mediated by a central amygdala projection to the reticular formation in the brainstem. In contrast, prey pursuit was mediated by projections to the midbrain periaqueductal gray matter. Targeted lesions to these two pathways separately disrupted biting attacks upon prey versus the initiation of prey pursuit. Our findings delineate a neural network that integrates distinct behavioral modules and suggest that central amygdala neurons instruct predatory hunting across jawed vertebrates.
Display omitted
•Stimulation of central amygdala (CeA) elicited hunting of live and artificial prey•CeA projections to the reticular formation (PCRt) control biting attacks•CeA projections to periaqueductal gray (PAG) control locomotion during pursuit•CeA integrates craniofacial and locomotor modules during goal-directed behavior
Two neuronal pathways originating in the central amygdala coordinate distinct behaviors necessary for efficient predatory hunting: the ability to pursue a prey and deliver fatal bites upon capture.
Identification of energy sources depends upon the ability to form associations between food cues and nutritional value. As such, cues previously paired with calories elicit neuronal activation in the ...nucleus accumbens (NAcc), which reflects the reinforcing value of food 1–4. The identity of the physiological signals regulating this response remains elusive. Using fMRI, we examined brain response to noncaloric versions of flavors that had been consumed in previous days with either 0 or 112.5 calories from undetected maltodextrin. We report a small but perceptually meaningful increase in liking for the flavor that had been paired with calories and find that change in liking was associated with changes in insular responses to this beverage. In contrast, NAcc and hypothalamic response to the calorie-paired flavor was unrelated to liking but was strongly associated with the changes in plasma glucose levels produced by ingestion of the beverage when consumed previously with calories. Importantly, because each participant ingested the same caloric dose, the change in plasma glucose depended upon individual differences in glucose metabolism. We conclude that glucose metabolism is a critical signal regulating NAcc and hypothalamic response to food cues, and that this process operates independently from the ability of calories to condition liking.
Display omitted
•Postoral signals from carbohydrate ingestion can increase flavor liking•This hedonic conditioning is reflected in insular response to flavor•Glucose metabolism regulates accumbal/hypothalamic (NAcc/Hyp) response to flavor•Hedonic conditioning is not associated with glucose metabolism or NAcc/Hyp response
The neuroanatomical circuitry of jaw muscles has been mostly explored in non‐human animals. A recent rodent study revealed a novel circuit from the central amygdala (CeA) to the trigeminal motor ...nucleus (5M), which controls biting attacks. This circuit has yet to be delineated in humans. Ultra‐high diffusion‐weighted imaging data from the Human Connectome Project (HCP) allow in vivo delineation of circuits identified in other species—for example, the CeA–5M pathway—in humans. We hypothesized that the CeA–5M circuit could be resolved in humans at both 7 and 3 T. We performed probabilistic tractography between the CeA and 5M in 30 healthy young adults from the HCP database. As a negative control, we performed tractography between the basolateral amygdala (BLAT) and 5M, as CeA is the only amygdalar nucleus with extensive projections to the brainstem. Connectivity strength was operationalized as the number of streamlines between each region of interest. Connectivity strength between CeA–5M and BLAT–5M within each hemisphere was compared, and CeA–5M circuit had significantly stronger connectivity than the BLAT–5M circuit, bilaterally at both 7 T (all p < .001) and 3 T (all p < .001). This study is the first to delineate the CeA–5M circuit in humans.
The neuroanatomical circuitry of jaw muscles has been mostly explored in nonhuman animals. A recent rodent study revealed a novel circuit from the central amygdala (CeA) to the trigeminal motor nucleus (5M), which controls biting attacks. Here, we use an open‐source ultra‐high field (7 T) MRI database, the Human Connectome Project, to delinate the CeA–5M circuit in vivo in humans for the first time. As a negative control, we also performed tractography between the basolateral amygdala and 5M, as CeA is the only amygdalar nucleus with extensive projections to the brainstem. We further replicate this study at 3 T, to show that this circuit can also be resolved at this more widely available MRI field strength.
Abstract Sugar's potent reinforcing properties arise from the complex interplay between gustatory and nutritive signals. This commentary addresses a unique organizational aspect of the neuronal ...circuitry that mediates sugar reinforcement in both Drosophila and rodents. Specifically, current evidence supports a general circuit model where separate populations of dopaminergic neurons encode the gustatory and nutritive values of sugar. This arrangement allows animals to prioritize energy seeking over taste quality, and implies that specialized subpopulations of dopamine-containing neurons form a class of evolutionary conserved chemo- and nutrient-sensors.
Excessive intake of dietary fats leads to diminished brain dopaminergic function. It has been proposed that dopamine deficiency exacerbates obesity by provoking compensatory overfeeding as one way to ...restore reward sensitivity. However, the physiological mechanisms linking prolonged high-fat intake to dopamine deficiency remain elusive. We show that administering oleoylethanolamine, a gastrointestinal lipid messenger whose synthesis is suppressed after prolonged high-fat exposure, is sufficient to restore gut-stimulated dopamine release in high-fat—fed mice. Administering oleoylethanolamine to high-fat—fed mice also eliminated motivation deficits during flavorless intragastric feeding and increased oral intake of low-fat emulsions. Our findings suggest that high-fat—induced gastrointestinal dysfunctions play a key role in dopamine deficiency and that restoring gut-generated lipid signaling may increase the reward value of less palatable, yet healthier, foods.
Reductions in calorie intake contribute significantly to the positive outcome of bariatric surgeries. However, the physiological mechanisms linking the rerouting of the gastrointestinal tract to ...reductions in sugar cravings remain uncertain. We show that a duodenal-jejunal bypass (DJB) intervention inhibits maladaptive sweet appetite by acting on dopamine-responsive striatal circuitries. DJB disrupted the ability of recurrent sugar exposure to promote sweet appetite in sated animals, thereby revealing a link between recurrent duodenal sugar influx and maladaptive sweet intake. Unlike ingestion of a low-calorie sweetener, ingestion of sugar was associated with significant dopamine effluxes in the dorsal striatum, with glucose infusions into the duodenum inducing greater striatal dopamine release than equivalent jejunal infusions. Consistently, optogenetic activation of dopamine-excitable cells of the dorsal striatum was sufficient to restore maladaptive sweet appetite in sated DJB mice. Our findings point to a causal link between striatal dopamine signaling and the outcomes of bariatric interventions.
Display omitted
•Nigrostriatal dopamine pathways are specifically sensitive to duodenal sugar sensing•Bypassing duodenum inhibits maladaptive sweetness seeking and nigrostriatal activity•Optogenetic activation of striatal pathways annuls the effects of bypassing duodenum•The striatal system contains a representation of different intestinal segments
Han et al. show that duodenal-jejunal bypass surgery curbs sugar cravings by eliminating sugar-induced dopamine release specifically in the dorsal striatum, revealing how dorsal and ventral striatal regions reflect sugar sensing in different intestinal segments. Dopamine-like optical stimulation of the dorsal striatum restores maladaptive sweet seeking in DJB mice.
PDF
