Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization
Animals vocalize only in certain behavioral contexts, but the circuits and synapses through which forebrain neurons trigger or suppress vocalization remain unknown. Here, we used transsynaptic tracing to identify two populations of inhibitory neurons that lie upstream of neurons in the periaqueducta...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2020-12-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/63493 |
| _version_ | 1818019931354038272 |
|---|---|
| author | Valerie Michael Jack Goffinet John Pearson Fan Wang Katherine Tschida Richard Mooney |
| author_facet | Valerie Michael Jack Goffinet John Pearson Fan Wang Katherine Tschida Richard Mooney |
| author_sort | Valerie Michael |
| collection | DOAJ |
| description | Animals vocalize only in certain behavioral contexts, but the circuits and synapses through which forebrain neurons trigger or suppress vocalization remain unknown. Here, we used transsynaptic tracing to identify two populations of inhibitory neurons that lie upstream of neurons in the periaqueductal gray (PAG) that gate the production of ultrasonic vocalizations (USVs) in mice (i.e. PAG-USV neurons). Activating PAG-projecting neurons in the preoptic area of the hypothalamus (POAPAG neurons) elicited USV production in the absence of social cues. In contrast, activating PAG-projecting neurons in the central-medial boundary zone of the amygdala (AmgC/M-PAG neurons) transiently suppressed USV production without disrupting non-vocal social behavior. Optogenetics-assisted circuit mapping in brain slices revealed that POAPAG neurons directly inhibit PAG interneurons, which in turn inhibit PAG-USV neurons, whereas AmgC/M-PAG neurons directly inhibit PAG-USV neurons. These experiments identify two major forebrain inputs to the PAG that trigger and suppress vocalization, respectively, while also establishing the synaptic mechanisms through which these neurons exert opposing behavioral effects. |
| first_indexed | 2024-04-14T07:58:17Z |
| format | Article |
| id | doaj.art-505e060038ed4e0d950aa10f3f5395eb |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-14T07:58:17Z |
| publishDate | 2020-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-505e060038ed4e0d950aa10f3f5395eb2022-12-22T02:04:58ZengeLife Sciences Publications LtdeLife2050-084X2020-12-01910.7554/eLife.63493Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalizationValerie Michael0https://orcid.org/0000-0003-3288-9409Jack Goffinet1https://orcid.org/0000-0001-6729-0848John Pearson2https://orcid.org/0000-0002-9876-7837Fan Wang3Katherine Tschida4https://orcid.org/0000-0002-8171-1722Richard Mooney5https://orcid.org/0000-0002-3308-1367Department of Neurobiology, Duke University Medical Center, Durham, United StatesDepartment of Neurobiology, Duke University Medical Center, Durham, United StatesDepartment of Neurobiology, Duke University Medical Center, Durham, United States; Department of Biostatistics & Bioinformatics, Duke University Medical Center, Durham, United StatesDepartment of Neurobiology, Duke University Medical Center, Durham, United StatesDepartment of Psychology, Cornell University, Ithaca, United StatesDepartment of Neurobiology, Duke University Medical Center, Durham, United StatesAnimals vocalize only in certain behavioral contexts, but the circuits and synapses through which forebrain neurons trigger or suppress vocalization remain unknown. Here, we used transsynaptic tracing to identify two populations of inhibitory neurons that lie upstream of neurons in the periaqueductal gray (PAG) that gate the production of ultrasonic vocalizations (USVs) in mice (i.e. PAG-USV neurons). Activating PAG-projecting neurons in the preoptic area of the hypothalamus (POAPAG neurons) elicited USV production in the absence of social cues. In contrast, activating PAG-projecting neurons in the central-medial boundary zone of the amygdala (AmgC/M-PAG neurons) transiently suppressed USV production without disrupting non-vocal social behavior. Optogenetics-assisted circuit mapping in brain slices revealed that POAPAG neurons directly inhibit PAG interneurons, which in turn inhibit PAG-USV neurons, whereas AmgC/M-PAG neurons directly inhibit PAG-USV neurons. These experiments identify two major forebrain inputs to the PAG that trigger and suppress vocalization, respectively, while also establishing the synaptic mechanisms through which these neurons exert opposing behavioral effects.https://elifesciences.org/articles/63493vocalizationsultrasonicpreoptichypothalamusamygdalaperiaqueductal gray |
| spellingShingle | Valerie Michael Jack Goffinet John Pearson Fan Wang Katherine Tschida Richard Mooney Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization eLife vocalizations ultrasonic preoptic hypothalamus amygdala periaqueductal gray |
| title | Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization |
| title_full | Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization |
| title_fullStr | Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization |
| title_full_unstemmed | Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization |
| title_short | Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization |
| title_sort | circuit and synaptic organization of forebrain to midbrain pathways that promote and suppress vocalization |
| topic | vocalizations ultrasonic preoptic hypothalamus amygdala periaqueductal gray |
| url | https://elifesciences.org/articles/63493 |
| work_keys_str_mv | AT valeriemichael circuitandsynapticorganizationofforebraintomidbrainpathwaysthatpromoteandsuppressvocalization AT jackgoffinet circuitandsynapticorganizationofforebraintomidbrainpathwaysthatpromoteandsuppressvocalization AT johnpearson circuitandsynapticorganizationofforebraintomidbrainpathwaysthatpromoteandsuppressvocalization AT fanwang circuitandsynapticorganizationofforebraintomidbrainpathwaysthatpromoteandsuppressvocalization AT katherinetschida circuitandsynapticorganizationofforebraintomidbrainpathwaysthatpromoteandsuppressvocalization AT richardmooney circuitandsynapticorganizationofforebraintomidbrainpathwaysthatpromoteandsuppressvocalization |