N-methyl-D-aspartate receptors at parallel fiber synapses in the dorsal cochlear nucleus
P. B. Manis and S. C. Molitor Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA. 1. N-methyl-D-aspartate (NMDA) binding and NMDA-receptors immunolocalization experiments have revealed an enhanced expression of these recept...
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| creator | Manis, P. B Molitor, S. C |
| description | P. B. Manis and S. C. Molitor
Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA.
1. N-methyl-D-aspartate (NMDA) binding and NMDA-receptors
immunolocalization experiments have revealed an enhanced expression of
these receptors in the outer two layers of the dorsal cochlear nucleus
(DCN). The distribution of the receptors is congruent with the distribution
of synapses produced by the granule cell-parallel fiber system. To
determine the functional distribution and contribution of NMDA receptors at
parallel fiber synapses, synaptic responses to parallel fiber stimulation
were studied in in vitro brain slice preparations of the guinea pig and rat
dorsal cochlear nucleus. 2. The field potential response to parallel fiber
stimulation in guinea pigs includes three postsynaptic components. The
short latency components (the P3(2) and N2(2)) are blocked by general
excitatory receptor antagonists, including the non-NMDA-receptor blockers
6,7-dinitroquinoxaline-2,3-dione (DNQX) and
6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), but are insensitive to
NMDA-receptor antagonists. 3. A slower component (P4(2)) is revealed when
the slices are washed with a low magnesium solution to eliminate the
magnesium block of currents through NMDA receptors. This slow component is
reduced by D- or DL-2-amino-5-phosphonovaleric acid (D-APV, DL-APV) and
3-[(+/-)-2-carboxypiperazine-4-yl] propyl-1-phosphonate, but is not blocked
by DNQX or CNQX. Eliminating the voltage dependence of the NMDA receptors
also results in a complex oscillatory response in some slices. This
response exhibits the same pharmacological sensitivity as the slow
potential. The pharmacologic sensitivity to NMDA-receptor antagonists
suggest that the slow component (P4(2)) and the associated oscillatory
response are mediated through activation of NMDA receptors. 4. Current
source-density analysis of the parallel fiber-evoked field potentials was
carried out to determine the relative spatial distributions of the fast and
slow synaptic currents. Both synaptic components were associated with a
superficial current sink and a deeper current source, localized within the
superficial 250 microM of the nucleus. The slow (APV-sensitive) current was
slightly shifted in depth relative to the fast (DNQX-sensitive) current in
three of five slices with the maximum current sink and source occurring
approximately 16 microns further from the surface of the DCN. T |
| doi_str_mv | 10.1152/jn.1996.76.3.1639 |
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Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA.
1. N-methyl-D-aspartate (NMDA) binding and NMDA-receptors
immunolocalization experiments have revealed an enhanced expression of
these receptors in the outer two layers of the dorsal cochlear nucleus
(DCN). The distribution of the receptors is congruent with the distribution
of synapses produced by the granule cell-parallel fiber system. To
determine the functional distribution and contribution of NMDA receptors at
parallel fiber synapses, synaptic responses to parallel fiber stimulation
were studied in in vitro brain slice preparations of the guinea pig and rat
dorsal cochlear nucleus. 2. The field potential response to parallel fiber
stimulation in guinea pigs includes three postsynaptic components. The
short latency components (the P3(2) and N2(2)) are blocked by general
excitatory receptor antagonists, including the non-NMDA-receptor blockers
6,7-dinitroquinoxaline-2,3-dione (DNQX) and
6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), but are insensitive to
NMDA-receptor antagonists. 3. A slower component (P4(2)) is revealed when
the slices are washed with a low magnesium solution to eliminate the
magnesium block of currents through NMDA receptors. This slow component is
reduced by D- or DL-2-amino-5-phosphonovaleric acid (D-APV, DL-APV) and
3-[(+/-)-2-carboxypiperazine-4-yl] propyl-1-phosphonate, but is not blocked
by DNQX or CNQX. Eliminating the voltage dependence of the NMDA receptors
also results in a complex oscillatory response in some slices. This
response exhibits the same pharmacological sensitivity as the slow
potential. The pharmacologic sensitivity to NMDA-receptor antagonists
suggest that the slow component (P4(2)) and the associated oscillatory
response are mediated through activation of NMDA receptors. 4. Current
source-density analysis of the parallel fiber-evoked field potentials was
carried out to determine the relative spatial distributions of the fast and
slow synaptic currents. Both synaptic components were associated with a
superficial current sink and a deeper current source, localized within the
superficial 250 microM of the nucleus. The slow (APV-sensitive) current was
slightly shifted in depth relative to the fast (DNQX-sensitive) current in
three of five slices with the maximum current sink and source occurring
approximately 16 microns further from the surface of the DCN. These data
suggest that either the NMDA receptors are not present at all of the
synapses that generate the fast non-NMDA currents or that postsynaptic
cells with different dendritic distributions have different densities of
NMDA receptors. 5. The types of cells in layers 1 and 2 exhibiting
NMDA-receptor-mediated synaptic potentials were investigated. Intracellular
recordings with sharp electrodes in guinea pig slices showed that
eliminating the voltage dependence of the NMDA receptors in low magnesium
revealed a slow excitatory postsynaptic potential (EPSP) in both simple and
complex spiking cells. The late phase of the EPSP could be reduced by APV
in both cell types. These results could be explained by NMDA receptors on
the postsynaptic cells or by NMDA receptors on excitatory interneurons.
Attempts to demonstrate an appropriate voltage dependence of the parallel
fiber synaptic response in normal magnesium medium under current clamp were
confounded by the intrinsic voltage-dependent conductances of the cells. 6.
To determine whether NMDA receptors were present on postsynaptic cells, the
direct sensitivity of DCN cells to NMDA application was examined during
intracellular recording. Both simple spiking and complex spiking cells
responded to NMDA with depolarization. The response to NMDA persisted when
non-NMDA receptors were blocked with CNQX or DNQX. However in all cells
tested, the response to NMDA was blocked by APV. These experiments further
support the postsynaptic localization of NMDA receptors on both simple and
complex spiking cells. (ABSTRACT TRUNCATED)</description><identifier>ISSN: 0022-3077</identifier><identifier>EISSN: 1522-1598</identifier><identifier>DOI: 10.1152/jn.1996.76.3.1639</identifier><identifier>PMID: 8890282</identifier><language>eng</language><publisher>United States: Am Phys Soc</publisher><subject>Animals ; Cochlear Nucleus - cytology ; Cochlear Nucleus - drug effects ; Cochlear Nucleus - physiology ; Dose-Response Relationship, Drug ; Electrophysiology ; Excitatory Amino Acid Antagonists - pharmacology ; Extracellular Space - physiology ; Guinea Pigs ; In Vitro Techniques ; Magnesium - pharmacology ; Membrane Potentials - drug effects ; Membrane Potentials - physiology ; Nerve Fibers - drug effects ; Nerve Fibers - physiology ; Patch-Clamp Techniques ; Rats ; Rats, Sprague-Dawley ; Receptors, N-Methyl-D-Aspartate - agonists ; Receptors, N-Methyl-D-Aspartate - antagonists & inhibitors ; Receptors, N-Methyl-D-Aspartate - physiology ; Rodentia ; Synapses - drug effects ; Synapses - physiology</subject><ispartof>Journal of neurophysiology, 1996-09, Vol.76 (3), p.1639-1656</ispartof><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c425t-d8c46185a4308f7f290e9bd8555da55ee8a696dc958f77f0d10623eb430b86d43</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/8890282$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Manis, P. B</creatorcontrib><creatorcontrib>Molitor, S. C</creatorcontrib><title>N-methyl-D-aspartate receptors at parallel fiber synapses in the dorsal cochlear nucleus</title><title>Journal of neurophysiology</title><addtitle>J Neurophysiol</addtitle><description>P. B. Manis and S. C. Molitor
Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA.
1. N-methyl-D-aspartate (NMDA) binding and NMDA-receptors
immunolocalization experiments have revealed an enhanced expression of
these receptors in the outer two layers of the dorsal cochlear nucleus
(DCN). The distribution of the receptors is congruent with the distribution
of synapses produced by the granule cell-parallel fiber system. To
determine the functional distribution and contribution of NMDA receptors at
parallel fiber synapses, synaptic responses to parallel fiber stimulation
were studied in in vitro brain slice preparations of the guinea pig and rat
dorsal cochlear nucleus. 2. The field potential response to parallel fiber
stimulation in guinea pigs includes three postsynaptic components. The
short latency components (the P3(2) and N2(2)) are blocked by general
excitatory receptor antagonists, including the non-NMDA-receptor blockers
6,7-dinitroquinoxaline-2,3-dione (DNQX) and
6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), but are insensitive to
NMDA-receptor antagonists. 3. A slower component (P4(2)) is revealed when
the slices are washed with a low magnesium solution to eliminate the
magnesium block of currents through NMDA receptors. This slow component is
reduced by D- or DL-2-amino-5-phosphonovaleric acid (D-APV, DL-APV) and
3-[(+/-)-2-carboxypiperazine-4-yl] propyl-1-phosphonate, but is not blocked
by DNQX or CNQX. Eliminating the voltage dependence of the NMDA receptors
also results in a complex oscillatory response in some slices. This
response exhibits the same pharmacological sensitivity as the slow
potential. The pharmacologic sensitivity to NMDA-receptor antagonists
suggest that the slow component (P4(2)) and the associated oscillatory
response are mediated through activation of NMDA receptors. 4. Current
source-density analysis of the parallel fiber-evoked field potentials was
carried out to determine the relative spatial distributions of the fast and
slow synaptic currents. Both synaptic components were associated with a
superficial current sink and a deeper current source, localized within the
superficial 250 microM of the nucleus. The slow (APV-sensitive) current was
slightly shifted in depth relative to the fast (DNQX-sensitive) current in
three of five slices with the maximum current sink and source occurring
approximately 16 microns further from the surface of the DCN. These data
suggest that either the NMDA receptors are not present at all of the
synapses that generate the fast non-NMDA currents or that postsynaptic
cells with different dendritic distributions have different densities of
NMDA receptors. 5. The types of cells in layers 1 and 2 exhibiting
NMDA-receptor-mediated synaptic potentials were investigated. Intracellular
recordings with sharp electrodes in guinea pig slices showed that
eliminating the voltage dependence of the NMDA receptors in low magnesium
revealed a slow excitatory postsynaptic potential (EPSP) in both simple and
complex spiking cells. The late phase of the EPSP could be reduced by APV
in both cell types. These results could be explained by NMDA receptors on
the postsynaptic cells or by NMDA receptors on excitatory interneurons.
Attempts to demonstrate an appropriate voltage dependence of the parallel
fiber synaptic response in normal magnesium medium under current clamp were
confounded by the intrinsic voltage-dependent conductances of the cells. 6.
To determine whether NMDA receptors were present on postsynaptic cells, the
direct sensitivity of DCN cells to NMDA application was examined during
intracellular recording. Both simple spiking and complex spiking cells
responded to NMDA with depolarization. The response to NMDA persisted when
non-NMDA receptors were blocked with CNQX or DNQX. However in all cells
tested, the response to NMDA was blocked by APV. These experiments further
support the postsynaptic localization of NMDA receptors on both simple and
complex spiking cells. (ABSTRACT TRUNCATED)</description><subject>Animals</subject><subject>Cochlear Nucleus - cytology</subject><subject>Cochlear Nucleus - drug effects</subject><subject>Cochlear Nucleus - physiology</subject><subject>Dose-Response Relationship, Drug</subject><subject>Electrophysiology</subject><subject>Excitatory Amino Acid Antagonists - pharmacology</subject><subject>Extracellular Space - physiology</subject><subject>Guinea Pigs</subject><subject>In Vitro Techniques</subject><subject>Magnesium - pharmacology</subject><subject>Membrane Potentials - drug effects</subject><subject>Membrane Potentials - physiology</subject><subject>Nerve Fibers - drug effects</subject><subject>Nerve Fibers - physiology</subject><subject>Patch-Clamp Techniques</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Receptors, N-Methyl-D-Aspartate - agonists</subject><subject>Receptors, N-Methyl-D-Aspartate - antagonists & inhibitors</subject><subject>Receptors, N-Methyl-D-Aspartate - physiology</subject><subject>Rodentia</subject><subject>Synapses - drug effects</subject><subject>Synapses - physiology</subject><issn>0022-3077</issn><issn>1522-1598</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1996</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkEtLxDAUhYMoOj5-gAshK121Jk2TJkvxDYNuFNyFNL21HTJtTVqk_94MM-jS1b2c852zOAidU5JSyrPrVZdSpURaiJSlVDC1hxZRzxLKldxHC0Liz0hRHKHjEFaEkIKT7BAdSqlIJrMF-nhJ1jA2s0vuEhMG40czAvZgYRh7H7AZcRSNc-Bw3ZbgcZg7MwQIuO3w2ACuImYctr1tHBiPu8k6mMIpOqiNC3C2uyfo_eH-7fYpWb4-Pt_eLBObZ3xMKmlzQSU3OSOyLupMEVBlJTnnleEcQBqhRGUVj25Rk4oSkTEoI15KUeXsBF1uewfff00QRr1ugwXnTAf9FHQhc8kIZ_-ClAuZ05xGkG5B6_sQPNR68O3a-FlTojez61WnN7PrQmimN7PHzMWufCrXUP0mdjtH_2rrN-1n89160EMzh7Z3_ee8qftr-gFwLIwN</recordid><startdate>19960901</startdate><enddate>19960901</enddate><creator>Manis, P. B</creator><creator>Molitor, S. C</creator><general>Am Phys Soc</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>7X8</scope></search><sort><creationdate>19960901</creationdate><title>N-methyl-D-aspartate receptors at parallel fiber synapses in the dorsal cochlear nucleus</title><author>Manis, P. B ; Molitor, S. C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c425t-d8c46185a4308f7f290e9bd8555da55ee8a696dc958f77f0d10623eb430b86d43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1996</creationdate><topic>Animals</topic><topic>Cochlear Nucleus - cytology</topic><topic>Cochlear Nucleus - drug effects</topic><topic>Cochlear Nucleus - physiology</topic><topic>Dose-Response Relationship, Drug</topic><topic>Electrophysiology</topic><topic>Excitatory Amino Acid Antagonists - pharmacology</topic><topic>Extracellular Space - physiology</topic><topic>Guinea Pigs</topic><topic>In Vitro Techniques</topic><topic>Magnesium - pharmacology</topic><topic>Membrane Potentials - drug effects</topic><topic>Membrane Potentials - physiology</topic><topic>Nerve Fibers - drug effects</topic><topic>Nerve Fibers - physiology</topic><topic>Patch-Clamp Techniques</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Receptors, N-Methyl-D-Aspartate - agonists</topic><topic>Receptors, N-Methyl-D-Aspartate - antagonists & inhibitors</topic><topic>Receptors, N-Methyl-D-Aspartate - physiology</topic><topic>Rodentia</topic><topic>Synapses - drug effects</topic><topic>Synapses - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Manis, P. B</creatorcontrib><creatorcontrib>Molitor, S. C</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>MEDLINE - Academic</collection><jtitle>Journal of neurophysiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Manis, P. B</au><au>Molitor, S. C</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>N-methyl-D-aspartate receptors at parallel fiber synapses in the dorsal cochlear nucleus</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>1996-09-01</date><risdate>1996</risdate><volume>76</volume><issue>3</issue><spage>1639</spage><epage>1656</epage><pages>1639-1656</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><abstract>P. B. Manis and S. C. Molitor
Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA.
1. N-methyl-D-aspartate (NMDA) binding and NMDA-receptors
immunolocalization experiments have revealed an enhanced expression of
these receptors in the outer two layers of the dorsal cochlear nucleus
(DCN). The distribution of the receptors is congruent with the distribution
of synapses produced by the granule cell-parallel fiber system. To
determine the functional distribution and contribution of NMDA receptors at
parallel fiber synapses, synaptic responses to parallel fiber stimulation
were studied in in vitro brain slice preparations of the guinea pig and rat
dorsal cochlear nucleus. 2. The field potential response to parallel fiber
stimulation in guinea pigs includes three postsynaptic components. The
short latency components (the P3(2) and N2(2)) are blocked by general
excitatory receptor antagonists, including the non-NMDA-receptor blockers
6,7-dinitroquinoxaline-2,3-dione (DNQX) and
6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), but are insensitive to
NMDA-receptor antagonists. 3. A slower component (P4(2)) is revealed when
the slices are washed with a low magnesium solution to eliminate the
magnesium block of currents through NMDA receptors. This slow component is
reduced by D- or DL-2-amino-5-phosphonovaleric acid (D-APV, DL-APV) and
3-[(+/-)-2-carboxypiperazine-4-yl] propyl-1-phosphonate, but is not blocked
by DNQX or CNQX. Eliminating the voltage dependence of the NMDA receptors
also results in a complex oscillatory response in some slices. This
response exhibits the same pharmacological sensitivity as the slow
potential. The pharmacologic sensitivity to NMDA-receptor antagonists
suggest that the slow component (P4(2)) and the associated oscillatory
response are mediated through activation of NMDA receptors. 4. Current
source-density analysis of the parallel fiber-evoked field potentials was
carried out to determine the relative spatial distributions of the fast and
slow synaptic currents. Both synaptic components were associated with a
superficial current sink and a deeper current source, localized within the
superficial 250 microM of the nucleus. The slow (APV-sensitive) current was
slightly shifted in depth relative to the fast (DNQX-sensitive) current in
three of five slices with the maximum current sink and source occurring
approximately 16 microns further from the surface of the DCN. These data
suggest that either the NMDA receptors are not present at all of the
synapses that generate the fast non-NMDA currents or that postsynaptic
cells with different dendritic distributions have different densities of
NMDA receptors. 5. The types of cells in layers 1 and 2 exhibiting
NMDA-receptor-mediated synaptic potentials were investigated. Intracellular
recordings with sharp electrodes in guinea pig slices showed that
eliminating the voltage dependence of the NMDA receptors in low magnesium
revealed a slow excitatory postsynaptic potential (EPSP) in both simple and
complex spiking cells. The late phase of the EPSP could be reduced by APV
in both cell types. These results could be explained by NMDA receptors on
the postsynaptic cells or by NMDA receptors on excitatory interneurons.
Attempts to demonstrate an appropriate voltage dependence of the parallel
fiber synaptic response in normal magnesium medium under current clamp were
confounded by the intrinsic voltage-dependent conductances of the cells. 6.
To determine whether NMDA receptors were present on postsynaptic cells, the
direct sensitivity of DCN cells to NMDA application was examined during
intracellular recording. Both simple spiking and complex spiking cells
responded to NMDA with depolarization. The response to NMDA persisted when
non-NMDA receptors were blocked with CNQX or DNQX. However in all cells
tested, the response to NMDA was blocked by APV. These experiments further
support the postsynaptic localization of NMDA receptors on both simple and
complex spiking cells. (ABSTRACT TRUNCATED)</abstract><cop>United States</cop><pub>Am Phys Soc</pub><pmid>8890282</pmid><doi>10.1152/jn.1996.76.3.1639</doi><tpages>18</tpages></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0022-3077 |
| ispartof | Journal of neurophysiology, 1996-09, Vol.76 (3), p.1639-1656 |
| issn | 0022-3077 1522-1598 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_78483053 |
| source | MEDLINE; Alma/SFX Local Collection |
| subjects | Animals Cochlear Nucleus - cytology Cochlear Nucleus - drug effects Cochlear Nucleus - physiology Dose-Response Relationship, Drug Electrophysiology Excitatory Amino Acid Antagonists - pharmacology Extracellular Space - physiology Guinea Pigs In Vitro Techniques Magnesium - pharmacology Membrane Potentials - drug effects Membrane Potentials - physiology Nerve Fibers - drug effects Nerve Fibers - physiology Patch-Clamp Techniques Rats Rats, Sprague-Dawley Receptors, N-Methyl-D-Aspartate - agonists Receptors, N-Methyl-D-Aspartate - antagonists & inhibitors Receptors, N-Methyl-D-Aspartate - physiology Rodentia Synapses - drug effects Synapses - physiology |
| title | N-methyl-D-aspartate receptors at parallel fiber synapses in the dorsal cochlear nucleus |
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