Kv4.2-Positive Domains on Dendrites in the Mouse Medial Geniculate Body Receive Ascending Excitatory and Inhibitory Inputs Preferentially From the Inferior Colliculus
The medial geniculate body (MGB) is the thalamic center of the auditory lemniscal pathway. The ventral division of MGB (MGV) receives excitatory and inhibitory inputs from the inferior colliculus (IC). MGV is involved in auditory attention by processing descending excitatory and inhibitory inputs fr...
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Frontiers Media S.A.
2021-09-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2021.740378/full |
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| author | Hisataka Fujimoto Hisataka Fujimoto Eiji Notsu Ryo Yamamoto Munenori Ono Hiroyuki Hioki Megumu Takahashi Megumu Takahashi Tetsufumi Ito Tetsufumi Ito Tetsufumi Ito |
| author_facet | Hisataka Fujimoto Hisataka Fujimoto Eiji Notsu Ryo Yamamoto Munenori Ono Hiroyuki Hioki Megumu Takahashi Megumu Takahashi Tetsufumi Ito Tetsufumi Ito Tetsufumi Ito |
| author_sort | Hisataka Fujimoto |
| collection | DOAJ |
| description | The medial geniculate body (MGB) is the thalamic center of the auditory lemniscal pathway. The ventral division of MGB (MGV) receives excitatory and inhibitory inputs from the inferior colliculus (IC). MGV is involved in auditory attention by processing descending excitatory and inhibitory inputs from the auditory cortex (AC) and reticular thalamic nucleus (RTN), respectively. However, detailed mechanisms of the integration of different inputs in a single MGV neuron remain unclear. Kv4.2 is one of the isoforms of the Shal-related subfamily of potassium voltage-gated channels that are expressed in MGB. Since potassium channel is important for shaping synaptic current and spike waveforms, subcellular distribution of Kv4.2 is likely important for integration of various inputs. Here, we aimed to examine the detailed distribution of Kv4.2, in MGV neurons to understand its specific role in auditory attention. We found that Kv4.2 mRNA was expressed in most MGV neurons. At the protein level, Kv4.2-immunopositive patches were sparsely distributed in both the dendrites and the soma of neurons. The postsynaptic distribution of Kv4.2 protein was confirmed using electron microscopy (EM). The frequency of contact with Kv4.2-immunopositive puncta was higher in vesicular glutamate transporter 2 (VGluT2)-positive excitatory axon terminals, which are supposed to be extending from the IC, than in VGluT1-immunopositive terminals, which are expected to be originating from the AC. VGluT2-immunopositive terminals were significantly larger than VGluT1-immunopositive terminals. Furthermore, EM showed that the terminals forming asymmetric synapses with Kv4.2-immunopositive MGV dendritic domains were significantly larger than those forming synapses with Kv4.2-negative MGV dendritic domains. In inhibitory axons either from the IC or from the RTN, the frequency of terminals that were in contact with Kv4.2-positive puncta was higher in IC than in RTN. In summary, our study demonstrated that the Kv4.2-immunopositive domains of the MGV dendrites received excitatory and inhibitory ascending auditory inputs preferentially from the IC, and not from the RTN or cortex. Our findings imply that time course of synaptic current and spike waveforms elicited by IC inputs is modified in the Kv4.2 domains. |
| first_indexed | 2024-12-21T16:13:58Z |
| format | Article |
| id | doaj.art-5a31a2e2d9f04dec801d3ec7762f76d5 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-12-21T16:13:58Z |
| publishDate | 2021-09-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Neuroscience |
| spelling | doaj.art-5a31a2e2d9f04dec801d3ec7762f76d52022-12-21T18:57:43ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2021-09-011510.3389/fnins.2021.740378740378Kv4.2-Positive Domains on Dendrites in the Mouse Medial Geniculate Body Receive Ascending Excitatory and Inhibitory Inputs Preferentially From the Inferior ColliculusHisataka Fujimoto0Hisataka Fujimoto1Eiji Notsu2Ryo Yamamoto3Munenori Ono4Hiroyuki Hioki5Megumu Takahashi6Megumu Takahashi7Tetsufumi Ito8Tetsufumi Ito9Tetsufumi Ito10Department of Anatomy, Kawasaki Medical School, Kurashiki, JapanDepartment of Ophthalmology, Kawasaki Medical School, Kurashiki, JapanDepartment of Anatomy, Kawasaki Medical School, Kurashiki, JapanDepartment of Physiology, Kanazawa Medical University, Uchinada, JapanDepartment of Physiology, Kanazawa Medical University, Uchinada, JapanDepartment of Neuroanatomy, Juntendo University Graduate School of Medicine, Tokyo, JapanDepartment of Neuroanatomy, Juntendo University Graduate School of Medicine, Tokyo, JapanDepartment of Neuroscience, Graduate School of Medicine, Kyoto University, Kyoto, JapanResearch and Education Program for Life Science, University of Fukui, Fukui, JapanDepartment of Anatomy, Kanazawa Medical University, Uchinada, JapanDepartment of Systems Function and Morphology, Graduate School of Innovative Life Science, University of Toyama, Toyama, JapanThe medial geniculate body (MGB) is the thalamic center of the auditory lemniscal pathway. The ventral division of MGB (MGV) receives excitatory and inhibitory inputs from the inferior colliculus (IC). MGV is involved in auditory attention by processing descending excitatory and inhibitory inputs from the auditory cortex (AC) and reticular thalamic nucleus (RTN), respectively. However, detailed mechanisms of the integration of different inputs in a single MGV neuron remain unclear. Kv4.2 is one of the isoforms of the Shal-related subfamily of potassium voltage-gated channels that are expressed in MGB. Since potassium channel is important for shaping synaptic current and spike waveforms, subcellular distribution of Kv4.2 is likely important for integration of various inputs. Here, we aimed to examine the detailed distribution of Kv4.2, in MGV neurons to understand its specific role in auditory attention. We found that Kv4.2 mRNA was expressed in most MGV neurons. At the protein level, Kv4.2-immunopositive patches were sparsely distributed in both the dendrites and the soma of neurons. The postsynaptic distribution of Kv4.2 protein was confirmed using electron microscopy (EM). The frequency of contact with Kv4.2-immunopositive puncta was higher in vesicular glutamate transporter 2 (VGluT2)-positive excitatory axon terminals, which are supposed to be extending from the IC, than in VGluT1-immunopositive terminals, which are expected to be originating from the AC. VGluT2-immunopositive terminals were significantly larger than VGluT1-immunopositive terminals. Furthermore, EM showed that the terminals forming asymmetric synapses with Kv4.2-immunopositive MGV dendritic domains were significantly larger than those forming synapses with Kv4.2-negative MGV dendritic domains. In inhibitory axons either from the IC or from the RTN, the frequency of terminals that were in contact with Kv4.2-positive puncta was higher in IC than in RTN. In summary, our study demonstrated that the Kv4.2-immunopositive domains of the MGV dendrites received excitatory and inhibitory ascending auditory inputs preferentially from the IC, and not from the RTN or cortex. Our findings imply that time course of synaptic current and spike waveforms elicited by IC inputs is modified in the Kv4.2 domains.https://www.frontiersin.org/articles/10.3389/fnins.2021.740378/fullauditory information processingventral division of medial geniculate bodyvoltage-dependent potassium 4 proteinsreticular thalamic nucleusinferior colliculus |
| spellingShingle | Hisataka Fujimoto Hisataka Fujimoto Eiji Notsu Ryo Yamamoto Munenori Ono Hiroyuki Hioki Megumu Takahashi Megumu Takahashi Tetsufumi Ito Tetsufumi Ito Tetsufumi Ito Kv4.2-Positive Domains on Dendrites in the Mouse Medial Geniculate Body Receive Ascending Excitatory and Inhibitory Inputs Preferentially From the Inferior Colliculus Frontiers in Neuroscience auditory information processing ventral division of medial geniculate body voltage-dependent potassium 4 proteins reticular thalamic nucleus inferior colliculus |
| title | Kv4.2-Positive Domains on Dendrites in the Mouse Medial Geniculate Body Receive Ascending Excitatory and Inhibitory Inputs Preferentially From the Inferior Colliculus |
| title_full | Kv4.2-Positive Domains on Dendrites in the Mouse Medial Geniculate Body Receive Ascending Excitatory and Inhibitory Inputs Preferentially From the Inferior Colliculus |
| title_fullStr | Kv4.2-Positive Domains on Dendrites in the Mouse Medial Geniculate Body Receive Ascending Excitatory and Inhibitory Inputs Preferentially From the Inferior Colliculus |
| title_full_unstemmed | Kv4.2-Positive Domains on Dendrites in the Mouse Medial Geniculate Body Receive Ascending Excitatory and Inhibitory Inputs Preferentially From the Inferior Colliculus |
| title_short | Kv4.2-Positive Domains on Dendrites in the Mouse Medial Geniculate Body Receive Ascending Excitatory and Inhibitory Inputs Preferentially From the Inferior Colliculus |
| title_sort | kv4 2 positive domains on dendrites in the mouse medial geniculate body receive ascending excitatory and inhibitory inputs preferentially from the inferior colliculus |
| topic | auditory information processing ventral division of medial geniculate body voltage-dependent potassium 4 proteins reticular thalamic nucleus inferior colliculus |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2021.740378/full |
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