Kainate receptors mediate signaling in both transient and sustained OFF bipolar cell pathways in mouse retina
A fundamental question in sensory neuroscience is how parallel processing is implemented at the level of molecular and circuit mechanisms. In the retina, it has been proposed that distinct OFF cone bipolar cell types generate fast/transient and slow/sustained pathways by the differential expression...
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| Veröffentlicht in: | The Journal of neuroscience 2014-04, Vol.34 (18), p.6128-6139 |
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| container_end_page | 6139 |
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| container_issue | 18 |
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| container_title | The Journal of neuroscience |
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| creator | Borghuis, Bart G Looger, Loren L Tomita, Susumu Demb, Jonathan B |
| description | A fundamental question in sensory neuroscience is how parallel processing is implemented at the level of molecular and circuit mechanisms. In the retina, it has been proposed that distinct OFF cone bipolar cell types generate fast/transient and slow/sustained pathways by the differential expression of AMPA- and kainate-type glutamate receptors, respectively. However, the functional significance of these receptors in the intact circuit during light stimulation remains unclear. Here, we measured glutamate release from mouse bipolar cells by two-photon imaging of a glutamate sensor (iGluSnFR) expressed on postsynaptic amacrine and ganglion cell dendrites. In both transient and sustained OFF layers, cone-driven glutamate release from bipolar cells was blocked by antagonists to kainate receptors but not AMPA receptors. Electrophysiological recordings from bipolar and ganglion cells confirmed the essential role of kainate receptors for signaling in both transient and sustained OFF pathways. Kainate receptors mediated responses to contrast modulation up to 20 Hz. Light-evoked responses in all mouse OFF bipolar pathways depend on kainate, not AMPA, receptors. |
| doi_str_mv | 10.1523/JNEUROSCI.4941-13.2014 |
| format | Article |
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In the retina, it has been proposed that distinct OFF cone bipolar cell types generate fast/transient and slow/sustained pathways by the differential expression of AMPA- and kainate-type glutamate receptors, respectively. However, the functional significance of these receptors in the intact circuit during light stimulation remains unclear. Here, we measured glutamate release from mouse bipolar cells by two-photon imaging of a glutamate sensor (iGluSnFR) expressed on postsynaptic amacrine and ganglion cell dendrites. In both transient and sustained OFF layers, cone-driven glutamate release from bipolar cells was blocked by antagonists to kainate receptors but not AMPA receptors. Electrophysiological recordings from bipolar and ganglion cells confirmed the essential role of kainate receptors for signaling in both transient and sustained OFF pathways. Kainate receptors mediated responses to contrast modulation up to 20 Hz. Light-evoked responses in all mouse OFF bipolar pathways depend on kainate, not AMPA, receptors.</description><subject>Action Potentials - drug effects</subject><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>Drug Interactions</subject><subject>Excitatory Amino Acid Antagonists - pharmacology</subject><subject>Female</subject><subject>Glutamic Acid - metabolism</subject><subject>Hexamethonium - pharmacology</subject><subject>In Vitro Techniques</subject><subject>Light</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Nicotinic Antagonists - pharmacology</subject><subject>Patch-Clamp Techniques</subject><subject>Photic Stimulation</subject><subject>Propionates - pharmacology</subject><subject>Receptors, Kainic Acid - agonists</subject><subject>Receptors, Kainic Acid - antagonists & inhibitors</subject><subject>Receptors, Kainic Acid - physiology</subject><subject>Retina - cytology</subject><subject>Retinal Bipolar Cells - drug effects</subject><subject>Retinal Bipolar Cells - physiology</subject><subject>Signal Transduction - drug effects</subject><subject>Signal Transduction - physiology</subject><subject>Visual Pathways - drug effects</subject><subject>Visual Pathways - physiology</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkU9v1DAQxS1URJfCV6h87CXL-M8m8QWpWnVLoWIloGdrEju7RomT2t5W--1x1LKCkzWeeW_m6UfIJYMlW3Hx6ev3m4cf25_ru6VUkhVMLDkw-YYsclcVXAI7IwvgFRSlrOQ5eR_jbwCogFXvyDmXlQJWiwUZvqHzmCwNtrVTGkOkgzVu_olu57F3fkedp82Y9jQF9NFZnyh6Q-Mhpiy2hm43G9q4aewx0Nb2PZ0w7Z_xGGflMB7ibJ_yng_kbYd9tB9f3wvysLn5tf5S3G9v79bX90W7AkiFUNBIoxBlKWzX8sZ0VSl5ubJC1dgYFMJytapFK3KJxnZgoOVCCFlZZjpxQT6_-E6HJsdp88kBez0FN2A46hGd_r_j3V7vxictAWQNIhtcvRqE8fFgY9KDi3M09Dbn0azmVV2XSqo8Wr6MtmGMMdjutIaBnlnpEys9s9JM6JlVFl7-e-RJ9heO-APYupRj</recordid><startdate>20140430</startdate><enddate>20140430</enddate><creator>Borghuis, Bart G</creator><creator>Looger, Loren L</creator><creator>Tomita, Susumu</creator><creator>Demb, Jonathan B</creator><general>Society for Neuroscience</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>5PM</scope></search><sort><creationdate>20140430</creationdate><title>Kainate receptors mediate signaling in both transient and sustained OFF bipolar cell pathways in mouse retina</title><author>Borghuis, Bart G ; Looger, Loren L ; Tomita, Susumu ; Demb, Jonathan B</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c500t-390b4d9aa463efc2bdf764265e398abda33e29583c38abadef0d0c233347e1df3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Action Potentials - drug effects</topic><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>Drug Interactions</topic><topic>Excitatory Amino Acid Antagonists - pharmacology</topic><topic>Female</topic><topic>Glutamic Acid - metabolism</topic><topic>Hexamethonium - pharmacology</topic><topic>In Vitro Techniques</topic><topic>Light</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Nicotinic Antagonists - pharmacology</topic><topic>Patch-Clamp Techniques</topic><topic>Photic Stimulation</topic><topic>Propionates - pharmacology</topic><topic>Receptors, Kainic Acid - agonists</topic><topic>Receptors, Kainic Acid - antagonists & inhibitors</topic><topic>Receptors, Kainic Acid - physiology</topic><topic>Retina - cytology</topic><topic>Retinal Bipolar Cells - drug effects</topic><topic>Retinal Bipolar Cells - physiology</topic><topic>Signal Transduction - drug effects</topic><topic>Signal Transduction - physiology</topic><topic>Visual Pathways - drug effects</topic><topic>Visual Pathways - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Borghuis, Bart G</creatorcontrib><creatorcontrib>Looger, Loren L</creatorcontrib><creatorcontrib>Tomita, Susumu</creatorcontrib><creatorcontrib>Demb, Jonathan B</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Borghuis, Bart G</au><au>Looger, Loren L</au><au>Tomita, Susumu</au><au>Demb, Jonathan B</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Kainate receptors mediate signaling in both transient and sustained OFF bipolar cell pathways in mouse retina</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2014-04-30</date><risdate>2014</risdate><volume>34</volume><issue>18</issue><spage>6128</spage><epage>6139</epage><pages>6128-6139</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>A fundamental question in sensory neuroscience is how parallel processing is implemented at the level of molecular and circuit mechanisms. In the retina, it has been proposed that distinct OFF cone bipolar cell types generate fast/transient and slow/sustained pathways by the differential expression of AMPA- and kainate-type glutamate receptors, respectively. However, the functional significance of these receptors in the intact circuit during light stimulation remains unclear. Here, we measured glutamate release from mouse bipolar cells by two-photon imaging of a glutamate sensor (iGluSnFR) expressed on postsynaptic amacrine and ganglion cell dendrites. In both transient and sustained OFF layers, cone-driven glutamate release from bipolar cells was blocked by antagonists to kainate receptors but not AMPA receptors. Electrophysiological recordings from bipolar and ganglion cells confirmed the essential role of kainate receptors for signaling in both transient and sustained OFF pathways. Kainate receptors mediated responses to contrast modulation up to 20 Hz. 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| subjects | Action Potentials - drug effects Action Potentials - physiology Animals Drug Interactions Excitatory Amino Acid Antagonists - pharmacology Female Glutamic Acid - metabolism Hexamethonium - pharmacology In Vitro Techniques Light Male Mice Mice, Inbred C57BL Nicotinic Antagonists - pharmacology Patch-Clamp Techniques Photic Stimulation Propionates - pharmacology Receptors, Kainic Acid - agonists Receptors, Kainic Acid - antagonists & inhibitors Receptors, Kainic Acid - physiology Retina - cytology Retinal Bipolar Cells - drug effects Retinal Bipolar Cells - physiology Signal Transduction - drug effects Signal Transduction - physiology Visual Pathways - drug effects Visual Pathways - physiology |
| title | Kainate receptors mediate signaling in both transient and sustained OFF bipolar cell pathways in mouse retina |
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