Postsynaptic activity of inhibitory neurons evokes hemodynamic fMRI responses
Functional MRI responses are localized to the synaptic sites of evoked inhibitory neurons, but it is unknown whether, or by what mechanisms, these neurons initiate functional hyperemia. Here, the neuronal origins of these hemodynamic responses were investigated by fMRI or local field potential and b...
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| Format: | Article |
| Language: | English |
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Elsevier
2021-01-01
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| Series: | NeuroImage |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811920309423 |
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| author | Alexander John Poplawsky Bistra Iordanova Alberto L. Vazquez Seong-Gi Kim Mitsuhiro Fukuda |
| author_facet | Alexander John Poplawsky Bistra Iordanova Alberto L. Vazquez Seong-Gi Kim Mitsuhiro Fukuda |
| author_sort | Alexander John Poplawsky |
| collection | DOAJ |
| description | Functional MRI responses are localized to the synaptic sites of evoked inhibitory neurons, but it is unknown whether, or by what mechanisms, these neurons initiate functional hyperemia. Here, the neuronal origins of these hemodynamic responses were investigated by fMRI or local field potential and blood flow measurements during topical application of pharmacological agents when GABAergic granule cells in the rat olfactory bulb were synaptically targeted. First, to examine if postsynaptic activation of these inhibitory neurons was required for neurovascular coupling, we applied an NMDA receptor antagonist during cerebral blood volume-weighted fMRI acquisition and found that responses below the drug application site (up to ~1.5 mm) significantly decreased within ~30 min. Similarly, large decreases in granule cell postsynaptic activities and blood flow responses were observed when AMPA or NMDA receptor antagonists were applied. Second, inhibition of nitric oxide synthase preferentially decreased the initial, fast component of the blood flow response, while inhibitors of astrocyte-specific glutamate transporters and vasoactive intestinal peptide receptors did not decrease blood flow responses. Third, inhibition of GABA release with a presynaptic GABAB receptor agonist caused less reduction of neuronal and blood flow responses compared to the postsynaptic glutamate receptor antagonists. In conclusion, local hyperemia by synaptically-evoked inhibitory neurons was primarily driven by their postsynaptic activities, possibly through NMDA receptor-dependent calcium signaling that was not wholly dependent on nitric oxide. |
| first_indexed | 2024-12-19T05:18:39Z |
| format | Article |
| id | doaj.art-610f4eb7808c4cb59392b715391abc8f |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-12-19T05:18:39Z |
| publishDate | 2021-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-610f4eb7808c4cb59392b715391abc8f2022-12-21T20:34:33ZengElsevierNeuroImage1095-95722021-01-01225117457Postsynaptic activity of inhibitory neurons evokes hemodynamic fMRI responsesAlexander John Poplawsky0Bistra Iordanova1Alberto L. Vazquez2Seong-Gi Kim3Mitsuhiro Fukuda4Department of Radiology, University of Pittsburgh, Pittsburgh, PA 15203, United StatesDepartment of Bioengineering, University of Pittsburgh, Pittsburgh, PA 15203, United StatesDepartment of Radiology, University of Pittsburgh, Pittsburgh, PA 15203, United States; Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA 15203, United StatesCenter for Neuroscience Imaging Research, Institute for Basic Science, Suwon 440-330, Korea; Department of Biomedical Engineering, Sungkyunkwan University, Suwon, 440-330, KoreaDepartment of Radiology, University of Pittsburgh, Pittsburgh, PA 15203, United States; Corresponding author.Functional MRI responses are localized to the synaptic sites of evoked inhibitory neurons, but it is unknown whether, or by what mechanisms, these neurons initiate functional hyperemia. Here, the neuronal origins of these hemodynamic responses were investigated by fMRI or local field potential and blood flow measurements during topical application of pharmacological agents when GABAergic granule cells in the rat olfactory bulb were synaptically targeted. First, to examine if postsynaptic activation of these inhibitory neurons was required for neurovascular coupling, we applied an NMDA receptor antagonist during cerebral blood volume-weighted fMRI acquisition and found that responses below the drug application site (up to ~1.5 mm) significantly decreased within ~30 min. Similarly, large decreases in granule cell postsynaptic activities and blood flow responses were observed when AMPA or NMDA receptor antagonists were applied. Second, inhibition of nitric oxide synthase preferentially decreased the initial, fast component of the blood flow response, while inhibitors of astrocyte-specific glutamate transporters and vasoactive intestinal peptide receptors did not decrease blood flow responses. Third, inhibition of GABA release with a presynaptic GABAB receptor agonist caused less reduction of neuronal and blood flow responses compared to the postsynaptic glutamate receptor antagonists. In conclusion, local hyperemia by synaptically-evoked inhibitory neurons was primarily driven by their postsynaptic activities, possibly through NMDA receptor-dependent calcium signaling that was not wholly dependent on nitric oxide.http://www.sciencedirect.com/science/article/pii/S1053811920309423BOLDCBFCBVGABAergic neuronsNeurovascular coupling |
| spellingShingle | Alexander John Poplawsky Bistra Iordanova Alberto L. Vazquez Seong-Gi Kim Mitsuhiro Fukuda Postsynaptic activity of inhibitory neurons evokes hemodynamic fMRI responses NeuroImage BOLD CBF CBV GABAergic neurons Neurovascular coupling |
| title | Postsynaptic activity of inhibitory neurons evokes hemodynamic fMRI responses |
| title_full | Postsynaptic activity of inhibitory neurons evokes hemodynamic fMRI responses |
| title_fullStr | Postsynaptic activity of inhibitory neurons evokes hemodynamic fMRI responses |
| title_full_unstemmed | Postsynaptic activity of inhibitory neurons evokes hemodynamic fMRI responses |
| title_short | Postsynaptic activity of inhibitory neurons evokes hemodynamic fMRI responses |
| title_sort | postsynaptic activity of inhibitory neurons evokes hemodynamic fmri responses |
| topic | BOLD CBF CBV GABAergic neurons Neurovascular coupling |
| url | http://www.sciencedirect.com/science/article/pii/S1053811920309423 |
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