Modulation of Neural Microcircuits That Control Complex Dynamics in Olfactory Networks
Neuromodulation influences neuronal processing, conferring neuronal circuits the flexibility to integrate sensory inputs with behavioral states and the ability to adapt to a continuously changing environment. In this original research report, we broadly discuss the basis of neuromodulation that is k...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-06-01
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| Series: | Frontiers in Cellular Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncel.2021.662184/full |
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| author | Zhenbo Huang Roberta Tatti Ashley M. Loeven Daniel R. Landi Conde Debra Ann Fadool Debra Ann Fadool Debra Ann Fadool |
| author_facet | Zhenbo Huang Roberta Tatti Ashley M. Loeven Daniel R. Landi Conde Debra Ann Fadool Debra Ann Fadool Debra Ann Fadool |
| author_sort | Zhenbo Huang |
| collection | DOAJ |
| description | Neuromodulation influences neuronal processing, conferring neuronal circuits the flexibility to integrate sensory inputs with behavioral states and the ability to adapt to a continuously changing environment. In this original research report, we broadly discuss the basis of neuromodulation that is known to regulate intrinsic firing activity, synaptic communication, and voltage-dependent channels in the olfactory bulb. Because the olfactory system is positioned to integrate sensory inputs with information regarding the internal chemical and behavioral state of an animal, how olfactory information is modulated provides flexibility in coding and behavioral output. Herein we discuss how neuronal microcircuits control complex dynamics of the olfactory networks by homing in on a special class of local interneurons as an example. While receptors for neuromodulation and metabolic peptides are widely expressed in the olfactory circuitry, centrifugal serotonergic and cholinergic inputs modulate glomerular activity and are involved in odor investigation and odor-dependent learning. Little is known about how metabolic peptides and neuromodulators control specific neuronal subpopulations. There is a microcircuit between mitral cells and interneurons that is comprised of deep-short-axon cells in the granule cell layer. These local interneurons express pre-pro-glucagon (PPG) and regulate mitral cell activity, but it is unknown what initiates this type of regulation. Our study investigates the means by which PPG neurons could be recruited by classical neuromodulators and hormonal peptides. We found that two gut hormones, leptin and cholecystokinin, differentially modulate PPG neurons. Cholecystokinin reduces or increases spike frequency, suggesting a heterogeneous signaling pathway in different PPG neurons, while leptin does not affect PPG neuronal firing. Acetylcholine modulates PPG neurons by increasing the spike frequency and eliciting bursts of action potentials, while serotonin does not affect PPG neuron excitability. The mechanisms behind this diverse modulation are not known, however, these results clearly indicate a complex interplay of metabolic signaling molecules and neuromodulators that may fine-tune neuronal microcircuits. |
| first_indexed | 2024-12-14T18:21:43Z |
| format | Article |
| id | doaj.art-63c376ec162242fb92faa174b0576af1 |
| institution | Directory Open Access Journal |
| issn | 1662-5102 |
| language | English |
| last_indexed | 2024-12-14T18:21:43Z |
| publishDate | 2021-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular Neuroscience |
| spelling | doaj.art-63c376ec162242fb92faa174b0576af12022-12-21T22:52:03ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022021-06-011510.3389/fncel.2021.662184662184Modulation of Neural Microcircuits That Control Complex Dynamics in Olfactory NetworksZhenbo Huang0Roberta Tatti1Ashley M. Loeven2Daniel R. Landi Conde3Debra Ann Fadool4Debra Ann Fadool5Debra Ann Fadool6Program in Neuroscience, Florida State University, Tallahassee, FL, United StatesProgram in Neuroscience, Florida State University, Tallahassee, FL, United StatesCell and Molecular Biology Program, Department of Biological Science, Florida State University, Tallahassee, FL, United StatesProgram in Neuroscience, Florida State University, Tallahassee, FL, United StatesProgram in Neuroscience, Florida State University, Tallahassee, FL, United StatesCell and Molecular Biology Program, Department of Biological Science, Florida State University, Tallahassee, FL, United StatesInstitute of Molecular Biophysics, Florida State University, Tallahassee, FL, United StatesNeuromodulation influences neuronal processing, conferring neuronal circuits the flexibility to integrate sensory inputs with behavioral states and the ability to adapt to a continuously changing environment. In this original research report, we broadly discuss the basis of neuromodulation that is known to regulate intrinsic firing activity, synaptic communication, and voltage-dependent channels in the olfactory bulb. Because the olfactory system is positioned to integrate sensory inputs with information regarding the internal chemical and behavioral state of an animal, how olfactory information is modulated provides flexibility in coding and behavioral output. Herein we discuss how neuronal microcircuits control complex dynamics of the olfactory networks by homing in on a special class of local interneurons as an example. While receptors for neuromodulation and metabolic peptides are widely expressed in the olfactory circuitry, centrifugal serotonergic and cholinergic inputs modulate glomerular activity and are involved in odor investigation and odor-dependent learning. Little is known about how metabolic peptides and neuromodulators control specific neuronal subpopulations. There is a microcircuit between mitral cells and interneurons that is comprised of deep-short-axon cells in the granule cell layer. These local interneurons express pre-pro-glucagon (PPG) and regulate mitral cell activity, but it is unknown what initiates this type of regulation. Our study investigates the means by which PPG neurons could be recruited by classical neuromodulators and hormonal peptides. We found that two gut hormones, leptin and cholecystokinin, differentially modulate PPG neurons. Cholecystokinin reduces or increases spike frequency, suggesting a heterogeneous signaling pathway in different PPG neurons, while leptin does not affect PPG neuronal firing. Acetylcholine modulates PPG neurons by increasing the spike frequency and eliciting bursts of action potentials, while serotonin does not affect PPG neuron excitability. The mechanisms behind this diverse modulation are not known, however, these results clearly indicate a complex interplay of metabolic signaling molecules and neuromodulators that may fine-tune neuronal microcircuits.https://www.frontiersin.org/articles/10.3389/fncel.2021.662184/fullolfactory bulbcholecystokininleptinglucagon-like peptide 1GLP-1acetylcholine |
| spellingShingle | Zhenbo Huang Roberta Tatti Ashley M. Loeven Daniel R. Landi Conde Debra Ann Fadool Debra Ann Fadool Debra Ann Fadool Modulation of Neural Microcircuits That Control Complex Dynamics in Olfactory Networks Frontiers in Cellular Neuroscience olfactory bulb cholecystokinin leptin glucagon-like peptide 1 GLP-1 acetylcholine |
| title | Modulation of Neural Microcircuits That Control Complex Dynamics in Olfactory Networks |
| title_full | Modulation of Neural Microcircuits That Control Complex Dynamics in Olfactory Networks |
| title_fullStr | Modulation of Neural Microcircuits That Control Complex Dynamics in Olfactory Networks |
| title_full_unstemmed | Modulation of Neural Microcircuits That Control Complex Dynamics in Olfactory Networks |
| title_short | Modulation of Neural Microcircuits That Control Complex Dynamics in Olfactory Networks |
| title_sort | modulation of neural microcircuits that control complex dynamics in olfactory networks |
| topic | olfactory bulb cholecystokinin leptin glucagon-like peptide 1 GLP-1 acetylcholine |
| url | https://www.frontiersin.org/articles/10.3389/fncel.2021.662184/full |
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