Abstract
The origin of spontaneous preference for dietary lipids in humans and rodents is debated, though recent compelling evidence has shown the existence of fat taste that might be considered a sixth taste quality. We investigated the implication of gustatory and reward brain circuits, triggered by linoleic acid (LA), a long-chain fatty acid. The LA was applied onto the circumvallate papillae for 30 min in conscious C57BL/6J mice, and neuronal activation was assessed using c-Fos immunohistochemistry. By using real-time reverse transcription polymerase chain reaction (RT-qPCR), we also studied the expression of mRNA encoding brain-derived neurotrophic factor (BDNF), Zif-268, and Glut-1 in some brain areas of these animals. LA induced a significant increase in c-Fos expression in the nucleus of solitary tract (NST), parabrachial nucleus (PBN), and ventroposterior medialis parvocellularis (VPMPC) of the thalamus, which are the regions known to be activated by gustatory signals. LA also triggered c-Fos expression in the central amygdala and ventral tegmental area (VTA), involved in food reward, in conjunction with emotional traits. Interestingly, we noticed a high expression of BDNF, Zif-268, and Glut-1 mRNA in the arcuate nucleus (Arc) and hippocampus (Hipp), where neuronal activation leads to memory formation. Our study demonstrates that oral lipid taste perception might trigger the activation of canonical gustatory and reward pathways.
Highlights
Taste modality serves as an important factor for food choice and for appreciating its hedonic value [1]
The abovementioned studies show that different brain areas might be activated by dietary fat; there is a dearth of information on the identification of sequential activation of cerebral areas/pathways that are activated in response to taste bud stimulation by dietary fat prior to ingestion of the bolus
Quantitative analysis of the immunohistochemical data revealed that oral linoleic acid (LA) application produced a robust increase in c-Fos expression in most brain revealed that oral LA application produced a robust increase in c-Fos expression in most brain regions explored along the putative pathway for gustatory lipid perception (Figures 1A,B and 2)
Summary
Taste modality serves as an important factor for food choice and for appreciating its hedonic value [1]. The abovementioned studies show that different brain areas might be activated by dietary fat; there is a dearth of information on the identification of sequential activation of cerebral areas/pathways that are activated in response to taste bud stimulation by dietary fat prior to ingestion of the bolus Information on this subject would be crucial to better understand the fundamental mechanisms of fat intake and its related addiction, and to modulate fat-eating behavior that is altered in obese subjects [17]. Keeping this argument in view, we designed the present study wherein we added linoleic acid (LA), a long-chain fatty acid, on the circumvallate papillae, which are rich in fat taste receptors, of conscious mice and assessed the neural activity using immunocytochemical localization of c-Fos protein in different brain areas. We analyzed the mRNA expression of brain-derived neurotrophic factor (BDNF), involved in synaptic plasticity and memory processes, Zif-268, an immediate-early gene, and Glut-1, another marker of neuronal activation during enhanced glucose demand in three brain areas of these animals [18]
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