Diverging neural pathways assemble a behavioural state from separable features in anxiety
Open accessAbstract
Behavioural states in mammals, such as the anxious state, are characterized by several features that are coordinately regulated by diverse nervous system outputs, ranging from behavioural choice patterns to changes in physiology (in anxiety, exemplified respectively by risk-avoidance and respiratory rate alterations). Here we investigate if and how defined neural projections arising from a single coordinating brain region in mice could mediate diverse features of anxiety. Integrating behavioural assays, in vivo and in vitro electrophysiology, respiratory physiology and optogenetics, we identify a surprising new role for the bed nucleus of the stria terminalis (BNST) in the coordinated modulation of diverse anxiety features. First, two BNST subregions were unexpectedly found to exert opposite effects on the anxious state: oval BNST activity promoted several independent anxious state features, whereas anterodorsal BNST-associated activity exerted anxiolytic influence for the same features. Notably, we found that three distinct anterodorsal BNST efferent projections-to the lateral hypothalamus, parabrachial nucleus and ventral tegmental area-each implemented an independent feature of anxiolysis: reduced risk-avoidance, reduced respiratory rate, and increased positive valence, respectively. Furthermore, selective inhibition of corresponding circuit elements in freely moving mice showed opposing behavioural effects compared with excitation, and in vivo recordings during free behaviour showed native spiking patterns in anterodorsal BNST neurons that differentiated safe and anxiogenic environments. These results demonstrate that distinct BNST subregions exert opposite effects in modulating anxiety, establish separable anxiolytic roles for different anterodorsal BNST projections, and illustrate circuit mechanisms underlying selection of features for the assembly of the anxious state.
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Optogenetic studies show projection-specific effects of BNST neurons on behavior.
“This is supported by optogenetic studies showing the projection-specific effects of BNST neurons on behavior (87–90).”
From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [88]
The BNST and the CeA have been implicated in diverse behavioral functions.
“The BNST and the CeA have been implicated in diverse behavioral functions (Davis et al., 2010, Janak and Tye, 2015, Kim et al., 2013)”
From Dorsal raphe dopamine neurons represent the experience of social isolation (2016) · cites this paper as Kim et al., 2013
The neural systems implicated in anxiety by rodent studies are consistent with those identified in human patients.
“This contrast notwithstanding, the neural systems implicated in anxiety by rodent studies are consistent with those identified in human patients26-34, underscoring the utility and translatability of these rodent studies.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [31]
Individual subregions of the BNST differentially regulate separable features of the anxiety phenotype.
“Moreover, individual subregions of the BNST have been shown to differentially regulate separable features of the anxiety phenotype31,85 (Fig. 3).”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [31]
BLA inputs to the anterodorsal BNST promote behavioral and physiological anxiolysis; local inhibition of anterodorsal BNST by the oval nucleus of the BNST is anxiogenic.
“BLA inputs to the anterodorsal BNST promote behavioral and physiological anxiolysis; local inhibition of anterodorsal BNST by the oval nucleus of the BNST is anxiogenic31.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [31]
Changes in heart rate, respiration and glucocorticoid levels require the activation of distinct pathways from those that drive anxiety-like behaviors.
“Moreover, a thorough understanding of the neural circuits underlying anxiety must include a consideration of its somatic symptoms, as changes in heart rate, respiration and glucocorticoid levels require the activation of distinct pathways from those that drive anxiety-like behaviors31,52.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [31]
In fear- or anxiety-provoking circumstances, projections from the BLA targeting the central amygdala and the BNST are activated.
“in fear- or anxiety-provoking circumstances, projections from the BLA targeting the central amygdala (CeA, containing the lateral (CeL) and medial (CeM) subdivisions)53,64 and the BNST31,65 are activated.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [31]
Effects on the innate anxiety state are mediated via projections from the anterodorsal BNST to the VTA, lateral hypothalamus and parabrachial nucleus, which independently regulate subjective preference, risk avoidance in the EPM and OFT, and respiration rate, respectively.
“These effects on the innate anxiety state are mediated via projections from the anterodorsal BNST to the ventral tegmental area (VTA), lateral hypothalamus and parabrachial nucleus, which independently regulate subjective preference, risk avoidance in the EPM and OFT, and respiration rate, respectively31.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [31]
The BNST contains distinct anxiogenic and anxiolytic GABAergic neuronal subsets with unique patterns of long-range connections.
“It has recently been shown that the BNST contains distinct anxiogenic and anxiolytic GABAergic neuronal subsets with unique patterns of long-range connections (Jennings et al., 2013; Kim et al., 2013).”
From Control of Stress-Induced Persistent Anxiety by an Extra-Amygdala Septohypothalamic Circuit (2014) · cites this paper as Kim et al., 2013
Our results provide further evidence of the importance of long-range GABAergic projection neurons in the control of anxiety.
“Our results provide further evidence of the importance of long-range GABAergic projection neurons in the control of anxiety (Jennings et al., 2013; Kim et al., 2013).”
From Control of Stress-Induced Persistent Anxiety by an Extra-Amygdala Septohypothalamic Circuit (2014) · cites this paper as Kim et al., 2013
Optogenetic stimulation of Drd1a+ neurons in the oval nucleus of the BNST acutely but reversibly elevated anxiety.
“Similarly, optogenetic stimulation of Drd1a+ neurons in the oval nucleus of BNST acutely but reversibly elevated anxiety (Kim et al., 2013).”
From Control of Stress-Induced Persistent Anxiety by an Extra-Amygdala Septohypothalamic Circuit (2014) · cites this paper as Kim et al., 2013
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- Authors
- Kim, S.-Y., Adhikari, A., Lee, S. Y., Marshel, J. H., Kim, C. K., Mallory, C. S., Lo, M., Pak, S., Mattis, J., Lim, B. K., Malenka, R. C., Warden, M. R., Neve, R., Tye, K. M., & Deisseroth, K.
- Affiliations
- Stanford University (US)
- Massachusetts Institute of Technology (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Deisseroth, Karl
- ORCID
- Venue
- Nature
- Published
- 2013-03-20
- Volume
- 496
- Issue
- 7444
- Pages
- 219-223
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC6690364
- OpenAlex
- W1971994650
- Cited by
- 666
- References
- 30
- Citations by year
- 2026: 40 · 2025: 46 · 2024: 40 · 2023: 52 · 2022: 41 · 2021: 60 · 2020: 68 · 2019: 44 · 2018: 49 · 2017: 49 · 2016: 57 · 2015: 51 · 2014: 40 · 2013: 28
- FWCI
- 32.05
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Mental Health (F32MH088010)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- bed nucleus of the stria terminalis, anxiety, ventral tegmental area, lateral hypothalamus, parabrachial nucleus, risk avoidance, respiratory rate, neural circuits, optogenetics, in vivo electrophysiology
- MeSH terms
- Action Potentials, Animals, Anxiety, Electrophysiology, Neural Pathways, Septal Nuclei, Mice, Optogenetics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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