Molecular and spatial profiling of the paraventricular nucleus of the thalamus

  1. Claire Gao  Is a corresponding author
  2. Chiraag A Gohel
  3. Yan Leng
  4. Jun Ma
  5. David Goldman
  6. Ariel J Levine
  7. Mario A Penzo  Is a corresponding author
  1. National Institute of Mental Health, United States
  2. National Institute on Alcohol Abuse and Alcoholism, United States
  3. National Institute of Child Health and Human Development, United States

Abstract

The paraventricular nucleus of the thalamus (PVT) is known to regulate various cognitive and behavioral processes. However, while functional diversity among PVT circuits has often been linked to cellular differences, the molecular identity and spatial distribution of PVT cell types remains unclear. To address this gap, here we used single nucleus RNA sequencing (snRNA-seq) and identified five molecularly distinct PVT neuronal subtypes in the mouse brain. Additionally, multiplex fluorescent in situ hybridization of top marker genes revealed that PVT subtypes are organized by a combination of previously unidentified molecular gradients. Lastly, comparing our dataset with a recently published single-cell sequencing atlas of thalamus yielded novel insight into the PVT's connectivity with cortex, including unexpected innervation of auditory and visual areas. This comparison also revealed that our data contains a largely non-overlapping transcriptomic map of multiple midline thalamic nuclei. Collectively, our findings uncover previously unknown features of the molecular diversity and anatomical organization of the PVT and provide a valuable resource for future investigations.

Data availability

All RNA-seq data generated in our study have been deposited into the Gene Expression Omnibus repository (GSE208707). Raw images of RNAscope experiments are publicly available at: https://figshare.com/s/e2918829cabfdd0392fb.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Claire Gao

    National Institute of Mental Health, Bethesda, United States
    For correspondence
    claire.gao@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
  2. Chiraag A Gohel

    National Institute on Alcohol Abuse and Alcoholism, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Yan Leng

    National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jun Ma

    National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. David Goldman

    National Institute on Alcohol Abuse and Alcoholism, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Ariel J Levine

    National Institute of Child Health and Human Development, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0335-0730
  7. Mario A Penzo

    National Institute of Mental Health, Bethesda, United States
    For correspondence
    mario.penzo@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5368-1802

Funding

National Institute of Mental Health (1ZIAMH002950)

  • Mario A Penzo

National Institute of Neurological Disorders and Stroke (ZIANS003153)

  • Ariel J Levine

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures were performed in accordance with the Guide for the Care and Use of Laboratory Animals and were approved by the National Institute of Mental Health Animal Care and Use Committee. (See Methods - Mice)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Metrics

  • 4,312
    views
  • 642
    downloads
  • 23
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Claire Gao
  2. Chiraag A Gohel
  3. Yan Leng
  4. Jun Ma
  5. David Goldman
  6. Ariel J Levine
  7. Mario A Penzo
(2023)
Molecular and spatial profiling of the paraventricular nucleus of the thalamus
eLife 12:e81818.
https://doi.org/10.7554/eLife.81818

Share this article

https://doi.org/10.7554/eLife.81818

Further reading

    1. Neuroscience
    Samuel Noorman, Timo Stein ... Simon van Gaal
    Research Article

    This study investigates failures in conscious access resulting from either weak sensory input (perceptual impairments) or unattended input (attentional impairments). Participants viewed a Kanizsa stimulus with or without an illusory triangle within a rapid serial visual presentation of distractor stimuli. We designed a novel Kanizsa stimulus that contained additional ancillary features of different complexity (local contrast and collinearity) that were independently manipulated. Perceptual performance on the Kanizsa stimulus (presence vs. absence of an illusion) was equated between the perceptual (masking) and attentional (attentional blink) manipulation to circumvent common confounds related to conditional differences in task performance. We trained and tested classifiers on electroencephalogram (EEG) data to reflect the processing of specific stimulus features, with increasing levels of complexity. We show that late stages of processing (~200–250 ms), reflecting the integration of complex stimulus features (collinearity, illusory triangle), were impaired by masking but spared by the attentional blink. In contrast, decoding of local contrast (the spatial arrangement of stimulus features) was observed early in time (~80 ms) and was left largely unaffected by either manipulation. These results replicate previous work showing that feedforward processing is largely preserved under both perceptual and attentional impairments. Crucially, however, under matched levels of performance, only attentional impairments left the processing of more complex visual features relatively intact, likely related to spared lateral and local feedback processes during inattention. These findings reveal distinct neural mechanisms associated with perceptual and attentional impairments and thus contribute to a comprehensive understanding of distinct neural stages leading to conscious access.

    1. Evolutionary Biology
    2. Neuroscience
    Anastasia A Makarova, Nicholas J Chua ... Alexey A Polilov
    Research Article

    The structure of compound eyes in arthropods has been the subject of many studies, revealing important biological principles. Until recently, these studies were constrained by the two-dimensional nature of available ultrastructural data. By taking advantage of the novel three-dimensional ultrastructural dataset obtained using volume electron microscopy, we present the first cellular-level reconstruction of the whole compound eye of an insect, the miniaturized parasitoid wasp Megaphragma viggianii. The compound eye of the female M. viggianii consists of 29 ommatidia and contains 478 cells. Despite the almost anucleate brain, all cells of the compound eye contain nuclei. As in larger insects, the dorsal rim area of the eye in M. viggianii contains ommatidia that are believed to be specialized in polarized light detection as reflected in their corneal and retinal morphology. We report the presence of three ‘ectopic’ photoreceptors. Our results offer new insights into the miniaturization of compound eyes and scaling of sensory organs in general.