Satb2 neurons in the parabrachial nucleus mediate taste perception

Jarvie, Brooke C.; Chen, Jane; King, Hunter O.; Palmiter, Richard D.

doi:10.1038/s41467-020-20100-8

Cited by 41 publications

(44 citation statements)

References 57 publications

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“…TRPV1-lineage positive gustatory neurons frequented the lateral PB nucleus including its external subregion (Figure 1H). Other studies have described gustatory activity in lateral PB areas including the external capsule (Yamamoto et al, 1994;Geran and Travers, 2009;Tokita et al, 2014;Tokita and Boughter, 2016;Jarvie et al, 2021), with the present and our prior work (Li and Lemon, 2019) identifying trigeminal projections reach taste cells in this PB region.…”

Section: Chr2 Expression In the Trigeminal Tract Was Regulated By Cre In Trpv1-lineage Fiberssupporting

confidence: 72%

TRPV1-lineage somatosensory fibers communicate with taste neurons in the mouse parabrachial nucleus

Ali

Lemon

2021

Preprint

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Trigeminal neurons supply somatosensation to craniofacial tissues. In mouse brain, ascending projections from medullary trigeminal neurons arrive at taste neurons in the autonomic parabrachial nucleus, suggesting taste neurons participate in somatosensory processing. However, the genetic cell types that support this convergence were undefined. Using Cre-directed optogenetics and in vivo neurophysiology in anesthetized mice of both sexes, here we studied whether TRPV1-lineage nociceptive and thermosensory fibers are primary neurons that drive trigeminal circuits reaching parabrachial taste cells. We monitored spiking activity in individual parabrachial neurons during photoexcitation of the terminals of TRPV1-lineage fibers that arrived at the dorsal spinal trigeminal nucleus pars caudalis, which relays orofacial somatosensory messages to the parabrachial area. Parabrachial neural responses to oral delivery of taste, chemesthetic, and thermal stimuli were also recorded. We found that optical excitation of TRPV1-lineage fibers frequently stimulated traditionally defined taste neurons in lateral parabrachial nuclei. The tuning of neurons across diverse tastes associated with their sensitivity to excitation of TRPV1-lineage fibers, which only sparingly engaged neurons oriented to preferred tastes like sucrose. Moreover, neurons that responded to photostimulation of TRPV1-lineage afferents showed strong responses to temperature including noxious heat, which predominantly excited parabrachial bitter taste cells. Multivariate analyses revealed the parabrachial confluence of TRPV1-lineage signals with taste captured sensory valence information shared across aversive gustatory, nociceptive, and thermal stimuli. Our results reveal that trigeminal fibers with defined roles in thermosensation and pain communicate with parabrachial taste neurons. This multisensory convergence supports dependencies between gustatory and somatosensory hedonic representations in the brain.

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Section: Chr2 Expression In the Trigeminal Tract Was Regulated By Cre In Trpv1-lineage Fiberssupporting

confidence: 72%

TRPV1-lineage somatosensory fibers communicate with taste neurons in the mouse parabrachial nucleus

Ali

Lemon

2021

Preprint

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“…First, the transcription factor Satb2 marks PB neurons that relay gustatory information to the thalamus (Fu et al., 2019; Huang et al., 2013; Jarvie et al., 2021; Maeda et al., 2009). We confirmed that both Satb2 mRNA (not shown) and Satb2 immunofluorescence (Figure 18a) identify a restricted distribution of PB neurons, primarily at caudal levels.…”

Section: Resultsmentioning

confidence: 99%

“…Most injection sites and implants were larger than most PB subpopulations, which intermingle extensively, so these approaches simultaneously targeted subsets of PB neurons with distinct connections and functions. Now, genetic methods allow investigators to target more specific subpopulations, including an overlapping potpourri of neurons that express Satb2, Calca , Pdyn, Cck , Oxtr1 , Htr2c , Oprm1 , or Tacr1 (Barik et al., 2021; Chiang et al., 2020; Fu et al., 2019; Garfield et al., 2014; Jarvie et al., 2021; Kaur et al., 2017; Liu et al., 2021; Norris et al., 2021; Palmiter, 2018; Park et al., 2020; Ryan et al., 2017; Yang et al., 2020). Limiting the immense potential of this approach were the lack of a framework for understanding ontological relationships between subpopulations and a lack of markers for remaining PB neurons.…”

Section: Discussionmentioning

confidence: 99%

Molecular ontology of the parabrachial nucleus

Karthik

Huang

Delgado

et al. 2022

J of Comparative Neurology

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Diverse neurons in the parabrachial nucleus (PB) communicate with widespread brain regions. Despite evidence linking them to a variety of homeostatic functions, it remains difficult to determine which PB neurons influence which functions because their subpopulations intermingle extensively. An improved framework for identifying these intermingled subpopulations would help advance our understanding of neural circuit functions linked to this region. Here, we present the foundation of a developmental‐genetic ontology that classifies PB neurons based on their intrinsic, molecular features. By combining transcription factor labeling with Cre fate‐mapping, we find that the PB is a blend of two, developmentally distinct macropopulations of glutamatergic neurons. Neurons in the first macropopulation express Lmx1b (and, to a lesser extent, Lmx1a) and are mutually exclusive with those in a second macropopulation, which derive from precursors expressing Atoh1. This second, Atoh1‐derived macropopulation includes many Foxp2‐expressing neurons, but Foxp2 also identifies a subset of Lmx1b‐expressing neurons in the Kölliker–Fuse nucleus (KF) and a population of GABAergic neurons ventrolateral to the PB (“caudal KF”). Immediately ventral to the PB, Phox2b‐expressing glutamatergic neurons (some coexpressing Lmx1b) occupy the KF, supratrigeminal nucleus, and reticular formation. We show that this molecular framework organizes subsidiary patterns of adult gene expression (including Satb2, Calca, Grp, and Pdyn) and predicts output projections to the amygdala (Lmx1b), hypothalamus (Atoh1), and hindbrain (Phox2b/Lmx1b). Using this molecular ontology to organize, interpret, and communicate PB‐related information could accelerate the translation of experimental findings from animal models to human patients.

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“…Miniscope imaging also revealed that bidirectional modulation within genetically defined cell types is responsible for the varied permutations of consumptive decision-making, as glutamatergic neurons in the median preoptic area (MPOA) bidirectionally respond to water intake [ 42 ] and clusters of glutamatergic neurons in the anterior peri-locus coeruleus are activated or inhibited by food and water intake [ 43 ]. Single-cell recordings of parabrachial neurons expressing transcription factor Satb2 have also shown that the same neurons can be excited or inhibited by different taste stimuli [ 44 ]. Importantly, some miniscope results have challenged earlier findings on hunger and thirst that originated from studies lacking single-cell resolution.…”

Section: Scientific Applications In Rodent Modelsmentioning

confidence: 99%

Miniature microscopes for manipulating and recording in vivo brain activity

et al. 2021

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Here we describe the development and application of miniature integrated microscopes (miniscopes) paired with microendoscopes that allow for the visualization and manipulation of neural circuits in superficial and subcortical brain regions in freely behaving animals. Over the past decade the miniscope platform has expanded to include simultaneous optogenetic capabilities, electrically-tunable lenses that enable multi-plane imaging, color-corrected optics, and an integrated data acquisition platform that streamlines multimodal experiments. Miniscopes have given researchers an unprecedented ability to monitor hundreds to thousands of genetically-defined neurons from weeks to months in both healthy and diseased animal brains. Sophisticated algorithms that take advantage of constrained matrix factorization allow for background estimation and reliable cell identification, greatly improving the reliability and scalability of source extraction for large imaging datasets. Data generated from miniscopes have empowered researchers to investigate the neural circuit underpinnings of a wide array of behaviors that cannot be studied under head-fixed conditions, such as sleep, reward seeking, learning and memory, social behaviors, and feeding. Importantly, the miniscope has broadened our understanding of how neural circuits can go awry in animal models of progressive neurological disorders, such as Parkinson’s disease. Continued miniscope development, including the ability to record from multiple populations of cells simultaneously, along with continued multimodal integration of techniques such as electrophysiology, will allow for deeper understanding into the neural circuits that underlie complex and naturalistic behavior.

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Satb2 neurons in the parabrachial nucleus mediate taste perception

Cited by 41 publications

References 57 publications

TRPV1-lineage somatosensory fibers communicate with taste neurons in the mouse parabrachial nucleus

TRPV1-lineage somatosensory fibers communicate with taste neurons in the mouse parabrachial nucleus

Molecular ontology of the parabrachial nucleus

Miniature microscopes for manipulating and recording in vivo brain activity

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