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Yeon, J.

Publications and source records attributed to Yeon, J..

9 recordsLinked to original sources

An enteric neuron-expressed variant ionotropic receptor detects ingested salts to regulate salt stress resistance

The detection of internal chemicals by interoceptive chemosensory pathways is critical for regulating metabolism and physiology. The molecular identities of interoceptors, and the functional consequences of chemosensation by specific interoceptive neurons remain to be fully described. The C. elegans pharyngeal neuronal network is anatomically and functionally homologous to the mammalian enteric nervous system. Here, we show that the I3 pharyngeal enteric neuron responds to cations via an I3-specific variant ionotropic receptor (IR) to regulate salt stress tolerance. The GLR-9 IR, located at the gut lumen-exposed sensory end of I3, is necessary and sufficient for salt sensation, establishing a chemosensory function for IRs beyond insects. Salt detection by I3 protects specifically against high salt stress, as glr-9 mutants show reduced tolerance of hypertonic salt but not sugar solutions, with or without prior acclimation. While cholinergic signaling from I3 promotes tolerance to acute high salt stress, peptidergic signaling from I3 during acclimation is essential for resistance to a subsequent high salt challenge. Transcriptomic analyses show that I3 regulates salt tolerance in part via regulating the expression of osmotic stress response genes in distal tissues. Our results describe the mechanisms by which chemosensation mediated by a defined enteric neuron regulates physiological homeostasis in response to a specific abiotic stress.

neuroscience↗

PIEZO acts in an intestinal valve to regulate swallowing in C. elegans

Sensations of the internal state of the body play crucial roles in regulating the physiological processes and maintaining homeostasis of an organism. However, our understanding of how internal signals are sensed, processed, and integrated to generate appropriate biological responses remains limited. Here, we show that the C. elegans PIEZO channel, encoded by pezo-1, regulates food movement in the intestine by detecting food accumulation in the anterior part of the intestinal lumen, thereby triggering rhythmical movement of the pharynx, referred to as the pharyngeal plunge. pezo-1 deletion mutants exhibit defects in the pharyngeal plunge, which is rescued by PEZO-1 or mouse PIEZO1 expression, but not by PIEZO2, in a single isolated non-neuronal tissue of the digestive tract, the pharyngeal-intestinal valve. Genetic ablation or optogenetic activation of this valve inhibits or induces the pharyngeal plunge, respectively. Moreover, pressure built in the anterior lumen of the intestine results in a pezo-1-dependent pharyngeal plunge, which is driven by head muscle contraction. These findings illustrate how interoceptive processes in a digestive organ regulate swallowing through the PIEZO channel, providing insights into how interoception coordinates ingestive processes in higher animals, including humans.

neuroscience↗

Behavior can be decoded across the cortex when individual differences are considered

Group-level analyses have typically linked behavioral signatures to a constrained set of brain areas. Here we show that two behavioral metrics - reaction time (RT) and confidence - can be decoded across the cortex when each individual is considered separately. Subjects (N=50) completed a perceptual decision-making task with confidence. We built models decoding trial-level RT and confidence separately for each subject using the activation patterns in one brain area at a time after splitting the entire cortex into 200 regions of interest (ROIs). First, we developed a simple test to determine the robustness of decoding performance, which showed that several hundred trials per subject are required for robust decoding. We then examined the decoding performance at the group and subject levels. At the group level, we replicated previous results by showing that both RT and confidence could be decoded from a small number of ROIs (12.0% and 3.5%, respectively). Critically, at the subject level, both RT and confidence could be decoded from most brain regions even after Bonferroni correction (90.0% and 72.5%, respectively). Surprisingly, we observed that many brain regions exhibited opposite brain-behavior relationships across individuals, such that, for example, higher activations predicted fast RTs in some subjects but slow RTs in others. All results were replicated in a second dataset. These findings show that behavioral signatures can be decoded from a much broader range of cortical areas than previously recognized and suggest the need to study the brain-behavior relationship at both the group and subject levels.

neuroscience↗

Multiple brain activation patterns for the same task

Meaningful variation in internal states that impacts cognition and behavior remains challenging to discover and characterize. Here we leveraged trial-to-trial fluctuations in the brain-wide signal recorded using functional MRI to test if distinct sets of brain regions are activated on different trials when accomplishing the same task. Across three different perceptual decision-making experiments, we estimated the brain activations for each trial. We then clustered the trials based on their similarity using modularity-maximization, a data-driven classification method. In each experiment, we found multiple distinct but stable subtypes of trials, suggesting that the same task can be accomplished in the presence of widely varying brain activation patterns. Surprisingly, in all experiments, one of the subtypes exhibited strong activation in the default mode network, which is typically thought to decrease in activity during tasks that require externally focused attention. The remaining subtypes were characterized by activations in different task-positive areas. The default mode network subtype was characterized by behavioral signatures that were similar to the other subtypes exhibiting activation with task-positive regions. These findings demonstrate that the same perceptual decision-making task is accomplished through multiple brain activation patterns.

neuroscience↗

Task learning is subserved by a domain-general brain network

One of the most important human faculties is the ability to acquire not just new memories but the capacity to perform entirely new tasks. However, little is known about the brain mechanisms underlying the learning of novel tasks. Specifically, it is unclear to what extent learning of different tasks depends on domain-general and/or domain-specific brain mechanisms. Here human subjects (N=45) learned to perform six new tasks while undergoing functional MRI. The different tasks required the engagement of perceptual, motor, and various cognitive processes (attention, expectation, speed-accuracy tradeoff, and metacognition). We found that a bilateral frontoparietal network was more active during the initial compared to the later stages of task learning, and that this effect was stronger for task variants requiring more new learning. Critically, the same frontoparietal network was engaged by all six tasks, demonstrating its domain generality. Finally, although task learning decreased the overall activity in the frontoparietal network, it increased the connectivity strength between the different nodes of that network. These results demonstrate the existence of a domain-general brain network whose activity and connectivity reflect learning for a wide variety of new tasks, and thus may underlie the human capacity for acquiring new abilities.

neuroscience↗

Idiosyncratic relation between human brain activity and behavior

Research in neuroscience often assumes universal neural mechanisms, but increasing evidence points towards sizeable individual differences in brain activations. What remains unclear is the extent of the idiosyncrasy and whether different types of analyses are associated with different levels of idiosyncrasy. Here we develop a new method for addressing these questions. The method consists of computing the within-subject reliability and subject-to-group similarity of brain activations and submitting these values to a computational model that quantifies the relative strength of group- and subject-level factors. We apply this method to a perceptual decision-making task (N=50) and find that activations related to task, reaction time (RT), and confidence are influenced equally strongly by group- and subject-level factors. Both group- and subject-level factors are dwarfed by a noise factor, though higher levels of smoothing increases their contributions relative to noise. Overall, our method allows for the quantification of group- and subject-level factors of brain activations and thus provides a more detailed understanding of the idiosyncrasy levels in brain activations.

neuroscience↗

Feeding state functionally reconfigures a sensory circuit to drive thermosensory behavioral plasticity

Internal state alters sensory behaviors to optimize survival strategies. The neuronal mechanisms underlying hunger-dependent behavioral plasticity are not fully characterized. Here we show that feeding state regulates C. elegans negative thermotaxis behavior by engaging a modulatory circuit whose activity gates the output of the core thermotaxis network. Feeding state does not alter the activity of the core thermotaxis circuit comprised of AFD thermosensory and AIY interneurons. Instead, prolonged food deprivation potentiates temperature responses in the AWC sensory neurons, which inhibit the postsynaptic AIA interneurons to override and disrupt AFD-driven thermotaxis behavior. Acute inhibition and activation of AWC and AIA, respectively, restores negative thermotaxis in starved animals. We find that state-dependent modulation of AWC-AIA temperature responses requires INS-1 insulin-like peptide signaling from the gut and DAF-16 FOXO function in AWC. Our results describe a mechanism by which functional reconfiguration of a sensory network via gut-brain signaling drives state-dependent behavioral flexibility.

neuroscience↗

The nature of the perceptual representation for decision making

It is becoming widely appreciated that human perceptual decision making is suboptimal but the nature and origins of this suboptimality remain poorly understood. Most past research has employed tasks with two stimulus categories, but such designs cannot fully capture the limitations inherent in naturalistic perceptual decisions where choices are rarely between only two alternatives. We conducted four experiments with tasks involving multiple alternatives and used computational modeling to determine the decision-level representation on which the perceptual decisions were based. The results from all four experiments pointed to the existence of robust suboptimality such that most of the information in the sensory representation was lost during the transformation to a decision-level representation. These results reveal severe limits in the quality of decision-level representations for multiple alternatives and have strong implications about perceptual decision making in naturalistic settings.

neuroscience↗

Overlapping and unique neural circuits support perceptual decision making and confidence

The period of making a perceptual decision is often followed by a period of confidence generation where one rates the likely accuracy of the initial decision. However, it remains unclear whether the same or different neural circuits are engaged during periods of perceptual decision making and confidence generation. To address this question, we conducted two functional MRI experiments in which we dissociated the periods related to perceptual decision making and confidence report by either separating their respective regressors or asking for confidence ratings only in the second half of the experiment. We found that perceptual decision making and confidence reports gave rise to activations in large and mostly overlapping brain circuits including frontal, parietal, posterior, and cingulate regions with the results being remarkably consistent across the two experiments. Further, the confidence report period activated a number of unique regions, whereas there was no evidence for the decision period activating unique regions not involved in the confidence period. We discuss the possible reasons for this overlap and explore their implications about theories of perceptual decision making and confidence generation.

neuroscience↗