Identification of an Amygdala–Thalamic Circuit That Acts as a Central Gain Mechanism in Taste Perceptions

Abstract

Peripheral sources of individual variation in taste intensity perception have been well described. The existence of a central source has been proposed but remains unexplored. Here we used functional magnetic resonance imaging in healthy human participants (20 women, 8 men) to evaluate the hypothesis that the amygdala exerts an inhibitory influence that affects the "gain" of the gustatory system during tasting. Consistent with the existence of a central gain mechanism (CGM), we found that central amygdala response was correlated with mean intensity ratings across multiple tastants. In addition, psychophysiological and dynamic causal modeling analyses revealed that the connection strength between inhibitory outputs from amygdala to medial dorsal and ventral posterior medial thalamus predicted individual differences in responsiveness to taste stimulation. These results imply that inhibitory inputs from the amygdala to the thalamus act as a CGM that influences taste intensity perception.

The Function of Paraventricular Thalamic Circuitry in Adaptive Control of Feeding Behavior

“…A recent study by Veldhuizen, Small and colleagues ( Veldhuizen et al, 2020 ) showed that the CEA responses in humans were correlated with intensity ratings across multiple tastants and that these individual differences were also reflected in activation patterns in the thalamus. Their psychophysiological and dynamic causal modeling analyses suggested that inhibitory inputs from the amygdala to the thalamus act as a central gain mechanism that influences taste intensity perception.…”

“…Thus, it is possible that the PVT contributed to the observed thalamic activity in that study, but was not specifically detected due to its size and limits of fMRI resolution. The PVT is interconnected with the CEA and insular cortex, and could be a missing link in the observed functional circuitry from the CEA to the insular cortex and to the ventral posterior medial thalamus, where the CEA impacted activity without direct connections ( Veldhuizen et al, 2020 ).…”

Inhibitory Central Amygdala Outputs to Thalamus Control the Gain of Taste Perception

“…This is an important issue because knowing whether central mechanisms play a significant role in interindividual variability in taste perception could help us understand not only individual differences in food preferences and diet, but also how gustatory circuit dysfunction may contribute to obesity. Veldhuizen et al (2020) hypothesized that inhibitory output from the central amygdala to gustatory brain regions act as a central gain mechanism that influences taste intensity perception. This idea is supported by three previous findings: (1) patients who had undergone surgical resection of the anterior medial temporal lobe, particularly those involving the amygdala, had increased taste sensitivity and stronger ratings of perceived taste (Small et al, 1997(Small et al, , 2001, which hinted at an inhibitory influence from the amygdala; (2) in directed attention tasks, amygdala circuits regulate gain by assigning greater weights to salient sensory sti-muli (Vuilleumier et al, 2004); and (3) Within the amygdala, the central nucleus is sensitive to changes in taste intensity perception, and this structure has reciprocal connectivity with all major gustatory regions (NST, VPM, IC; Small et al, 2003).…”

“…This idea is supported by three previous findings: (1) patients who had undergone surgical resection of the anterior medial temporal lobe, particularly those involving the amygdala, had increased taste sensitivity and stronger ratings of perceived taste (Small et al, 1997(Small et al, , 2001, which hinted at an inhibitory influence from the amygdala; (2) in directed attention tasks, amygdala circuits regulate gain by assigning greater weights to salient sensory sti-muli (Vuilleumier et al, 2004); and (3) Within the amygdala, the central nucleus is sensitive to changes in taste intensity perception, and this structure has reciprocal connectivity with all major gustatory regions (NST, VPM, IC; Small et al, 2003). To test their hypothesis, Veldhuizen et al (2020) assessed blood oxygenation level-dependent (BOLD) responses to sweet, sour, salty, and bitter tastants in 28 healthy participants using psychophysiological measurements, regression, and dynamic causal modeling.…”

“…The first question Veldhuizen et al (2020) addressed was whether amygdala responses to the different tastants covaried with the mean intensity rating across tastants. Using taste psychophysics, they found that intensity ratings of sweet, sour, and salty positively correlated with each other.…”