Uncrossed disynaptic inhibition of second-order vestibular neurons and its interaction with monosynaptic excitation from vestibular nerve afferent fibers in the frog
H. Straka and N. Dieringer Physiologisches Institut, Munich, Germany. 1. Eighth nerve evoked responses in central vestibular neurons (n = 146) were studied in the isolated brain stem of frogs. Ninety percent of these neurons responded with a monosynaptic excitatory postsynaptic potential (EPSP) afte...
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| Veröffentlicht in: | Journal of neurophysiology 1996-11, Vol.76 (5), p.3087-3101 |
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| description | H. Straka and N. Dieringer
Physiologisches Institut, Munich, Germany.
1. Eighth nerve evoked responses in central vestibular neurons (n = 146)
were studied in the isolated brain stem of frogs. Ninety percent of these
neurons responded with a monosynaptic excitatory postsynaptic potential
(EPSP) after electrical stimulation of the ipsilateral VIIIth nerve. In 5%
of these neurons, the EPSP was truncated by a disynaptic inhibitory
postsynaptic potential (IPSP), and in 5% of these neurons a pure disynaptic
IPSP was evoked. 2. Disynaptic IPSPs superimposed upon apparently pure
EPSPs were revealed by bath application of the glycine receptor antagonist
strychnine (0.5-5 microM) or of the gamma-aminobutyric acid-A (GABAA)
receptor antagonist bicuculline (0.5-2 microM). The evoked EPSP increased
in most central vestibular neurons (strychnine: 15 out of 16 neurons;
bicuculline 26 out of 29 neurons). At higher stimulus intensities, the
evoked spike discharge increased from 2 to 3 spikes before up to 8-10
spikes per electrical pulse during the application of blocking agents. The
unmasked disynaptic inhibitory component increased with stimulus intensity
to a different extent in different neurons. 3. Lesion studies demonstrated
that these inhibitory components were generated ipsilaterally with respect
to the recording side. The disynaptic strychnine-sensitive inhibition was
mediated by neurons located either in the ventral vestibular nuclear
complex (VNC) or in the adjacent reticular formation. The spatial
distribution of the disynaptic inhibition was investigated by simultaneous
recordings of VIIIth nerve-evoked field potentials at different
rostrocaudal locations of the VNC. A significant strychnine-sensitive
component was detected in the middle and caudal parts but not in the
rostral part of the VNC. A bicuculline-sensitive component was detected in
the rostral and in the caudal parts but not in the middle part of the VNC.
In view of a similar rostrocaudal distribution of glycineor
GABA-immunoreactive neurons in the VNC of frogs, our results suggest that
part of the disynaptic inhibition is mediated by local interneurons with a
spatially restricted projection area. 4. The monosynaptic EPSP of
second-order vestibular neurons was mediated in part by
N-methyl-D-aspartate (NMDA) and in part by non-NMDA receptors. The relative
contribution of the NMDA receptor-mediated component of the EPSP decreased
with stronger stimuli. This negative correlation could have resulted fro |
| doi_str_mv | 10.1152/jn.1996.76.5.3087 |
| format | Article |
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Physiologisches Institut, Munich, Germany.
1. Eighth nerve evoked responses in central vestibular neurons (n = 146)
were studied in the isolated brain stem of frogs. Ninety percent of these
neurons responded with a monosynaptic excitatory postsynaptic potential
(EPSP) after electrical stimulation of the ipsilateral VIIIth nerve. In 5%
of these neurons, the EPSP was truncated by a disynaptic inhibitory
postsynaptic potential (IPSP), and in 5% of these neurons a pure disynaptic
IPSP was evoked. 2. Disynaptic IPSPs superimposed upon apparently pure
EPSPs were revealed by bath application of the glycine receptor antagonist
strychnine (0.5-5 microM) or of the gamma-aminobutyric acid-A (GABAA)
receptor antagonist bicuculline (0.5-2 microM). The evoked EPSP increased
in most central vestibular neurons (strychnine: 15 out of 16 neurons;
bicuculline 26 out of 29 neurons). At higher stimulus intensities, the
evoked spike discharge increased from 2 to 3 spikes before up to 8-10
spikes per electrical pulse during the application of blocking agents. The
unmasked disynaptic inhibitory component increased with stimulus intensity
to a different extent in different neurons. 3. Lesion studies demonstrated
that these inhibitory components were generated ipsilaterally with respect
to the recording side. The disynaptic strychnine-sensitive inhibition was
mediated by neurons located either in the ventral vestibular nuclear
complex (VNC) or in the adjacent reticular formation. The spatial
distribution of the disynaptic inhibition was investigated by simultaneous
recordings of VIIIth nerve-evoked field potentials at different
rostrocaudal locations of the VNC. A significant strychnine-sensitive
component was detected in the middle and caudal parts but not in the
rostral part of the VNC. A bicuculline-sensitive component was detected in
the rostral and in the caudal parts but not in the middle part of the VNC.
In view of a similar rostrocaudal distribution of glycineor
GABA-immunoreactive neurons in the VNC of frogs, our results suggest that
part of the disynaptic inhibition is mediated by local interneurons with a
spatially restricted projection area. 4. The monosynaptic EPSP of
second-order vestibular neurons was mediated in part by
N-methyl-D-aspartate (NMDA) and in part by non-NMDA receptors. The relative
contribution of the NMDA receptor-mediated component of the EPSP decreased
with stronger stimuli. This negative correlation could have resulted from a
preferential activation of NMDA receptors via thick vestibular nerve
afferent fibers. Alternatively, the activation of NMDA receptors became
disfacilitated at higher stimulus intensities due to the recruitment of
disynaptic inhibitory inputs. Comparison of data obtained in the presence
and in the absence of these glycine and GABAA receptor blockers indicates a
preferential activation of NMDA receptors via larger-diameter vestibular
nerve afferent fibers. 5. The kinetics of NMDA receptors (delay, rise time)
activated by afferent nerve inputs were relatively fast. These fast
kinetics were independent of superimposed IPSPs. The association of these
receptors with large-diameter vestibular nerve afferent fibers suggests
that fast NMDA receptor kinetics might be matched to the more phasic
response dynamics of the large diameter vestibular afferent neurons to
natural head accelerations.</description><identifier>ISSN: 0022-3077</identifier><identifier>EISSN: 1522-1598</identifier><identifier>DOI: 10.1152/jn.1996.76.5.3087</identifier><identifier>PMID: 8930257</identifier><language>eng</language><publisher>United States: Am Phys Soc</publisher><subject>Afferent Pathways - physiology ; Animals ; Brain Stem - physiology ; Electric Stimulation ; Rana esculenta ; Strychnine - pharmacology ; Synaptic Transmission - drug effects ; Synaptic Transmission - physiology ; Vestibular Nerve - physiology</subject><ispartof>Journal of neurophysiology, 1996-11, Vol.76 (5), p.3087-3101</ispartof><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c359t-612f668053e47108295f47e3cfed3e93b9da76f5794fb92a7301973d978c957f3</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/8930257$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Straka, H</creatorcontrib><creatorcontrib>Dieringer, N</creatorcontrib><title>Uncrossed disynaptic inhibition of second-order vestibular neurons and its interaction with monosynaptic excitation from vestibular nerve afferent fibers in the frog</title><title>Journal of neurophysiology</title><addtitle>J Neurophysiol</addtitle><description>H. Straka and N. Dieringer
Physiologisches Institut, Munich, Germany.
1. Eighth nerve evoked responses in central vestibular neurons (n = 146)
were studied in the isolated brain stem of frogs. Ninety percent of these
neurons responded with a monosynaptic excitatory postsynaptic potential
(EPSP) after electrical stimulation of the ipsilateral VIIIth nerve. In 5%
of these neurons, the EPSP was truncated by a disynaptic inhibitory
postsynaptic potential (IPSP), and in 5% of these neurons a pure disynaptic
IPSP was evoked. 2. Disynaptic IPSPs superimposed upon apparently pure
EPSPs were revealed by bath application of the glycine receptor antagonist
strychnine (0.5-5 microM) or of the gamma-aminobutyric acid-A (GABAA)
receptor antagonist bicuculline (0.5-2 microM). The evoked EPSP increased
in most central vestibular neurons (strychnine: 15 out of 16 neurons;
bicuculline 26 out of 29 neurons). At higher stimulus intensities, the
evoked spike discharge increased from 2 to 3 spikes before up to 8-10
spikes per electrical pulse during the application of blocking agents. The
unmasked disynaptic inhibitory component increased with stimulus intensity
to a different extent in different neurons. 3. Lesion studies demonstrated
that these inhibitory components were generated ipsilaterally with respect
to the recording side. The disynaptic strychnine-sensitive inhibition was
mediated by neurons located either in the ventral vestibular nuclear
complex (VNC) or in the adjacent reticular formation. The spatial
distribution of the disynaptic inhibition was investigated by simultaneous
recordings of VIIIth nerve-evoked field potentials at different
rostrocaudal locations of the VNC. A significant strychnine-sensitive
component was detected in the middle and caudal parts but not in the
rostral part of the VNC. A bicuculline-sensitive component was detected in
the rostral and in the caudal parts but not in the middle part of the VNC.
In view of a similar rostrocaudal distribution of glycineor
GABA-immunoreactive neurons in the VNC of frogs, our results suggest that
part of the disynaptic inhibition is mediated by local interneurons with a
spatially restricted projection area. 4. The monosynaptic EPSP of
second-order vestibular neurons was mediated in part by
N-methyl-D-aspartate (NMDA) and in part by non-NMDA receptors. The relative
contribution of the NMDA receptor-mediated component of the EPSP decreased
with stronger stimuli. This negative correlation could have resulted from a
preferential activation of NMDA receptors via thick vestibular nerve
afferent fibers. Alternatively, the activation of NMDA receptors became
disfacilitated at higher stimulus intensities due to the recruitment of
disynaptic inhibitory inputs. Comparison of data obtained in the presence
and in the absence of these glycine and GABAA receptor blockers indicates a
preferential activation of NMDA receptors via larger-diameter vestibular
nerve afferent fibers. 5. The kinetics of NMDA receptors (delay, rise time)
activated by afferent nerve inputs were relatively fast. These fast
kinetics were independent of superimposed IPSPs. The association of these
receptors with large-diameter vestibular nerve afferent fibers suggests
that fast NMDA receptor kinetics might be matched to the more phasic
response dynamics of the large diameter vestibular afferent neurons to
natural head accelerations.</description><subject>Afferent Pathways - physiology</subject><subject>Animals</subject><subject>Brain Stem - physiology</subject><subject>Electric Stimulation</subject><subject>Rana esculenta</subject><subject>Strychnine - pharmacology</subject><subject>Synaptic Transmission - drug effects</subject><subject>Synaptic Transmission - physiology</subject><subject>Vestibular Nerve - 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>eNpVkcFu1DAURS0EKtPCB7BA8gpWCXY8juMlqoAiVWJD15ZjP088SuzBdlrmg_hPkplREatnvXvv0ZMvQu8oqSnlzad9qKmUbS3amteMdOIF2iz7pqJcdi_RhpDlzYgQr9F1zntCiOCkuUJXnWSk4WKD_jwEk2LOYLH1-Rj0oXiDfRh874uPAUeHM5gYbBWThYQfIRffz6NOOMCcYshYB4t9yUuqQNLmFHvyZcBTDPGZCb-NL_okuhSn_0HpEbB2DhKEgp3vIa04XAZYzbs36JXTY4a3l3mDHr5--Xl7V93_-Pb99vN9ZRiXpWpp49q2I5zBVlDSNZK7rQBmHFgGkvXSatE6LuTW9bLRghEqBbNSdEZy4dgN-nDmHlL8NS8HqslnA-OoA8Q5K8pFR2TDFyM9G0-fl8CpQ_KTTkdFiVqrUfug1mqUaBVXazVL5v0FPvcT2OfEpYtF_3jWB78bnnwCdRiO2ccx7o4r7h_pLyh0nOw</recordid><startdate>19961101</startdate><enddate>19961101</enddate><creator>Straka, H</creator><creator>Dieringer, N</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></search><sort><creationdate>19961101</creationdate><title>Uncrossed disynaptic inhibition of second-order vestibular neurons and its interaction with monosynaptic excitation from vestibular nerve afferent fibers in the frog</title><author>Straka, H ; Dieringer, N</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c359t-612f668053e47108295f47e3cfed3e93b9da76f5794fb92a7301973d978c957f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1996</creationdate><topic>Afferent Pathways - physiology</topic><topic>Animals</topic><topic>Brain Stem - physiology</topic><topic>Electric Stimulation</topic><topic>Rana esculenta</topic><topic>Strychnine - pharmacology</topic><topic>Synaptic Transmission - drug effects</topic><topic>Synaptic Transmission - physiology</topic><topic>Vestibular Nerve - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Straka, H</creatorcontrib><creatorcontrib>Dieringer, N</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><jtitle>Journal of neurophysiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Straka, H</au><au>Dieringer, N</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Uncrossed disynaptic inhibition of second-order vestibular neurons and its interaction with monosynaptic excitation from vestibular nerve afferent fibers in the frog</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>1996-11-01</date><risdate>1996</risdate><volume>76</volume><issue>5</issue><spage>3087</spage><epage>3101</epage><pages>3087-3101</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><abstract>H. Straka and N. Dieringer
Physiologisches Institut, Munich, Germany.
1. Eighth nerve evoked responses in central vestibular neurons (n = 146)
were studied in the isolated brain stem of frogs. Ninety percent of these
neurons responded with a monosynaptic excitatory postsynaptic potential
(EPSP) after electrical stimulation of the ipsilateral VIIIth nerve. In 5%
of these neurons, the EPSP was truncated by a disynaptic inhibitory
postsynaptic potential (IPSP), and in 5% of these neurons a pure disynaptic
IPSP was evoked. 2. Disynaptic IPSPs superimposed upon apparently pure
EPSPs were revealed by bath application of the glycine receptor antagonist
strychnine (0.5-5 microM) or of the gamma-aminobutyric acid-A (GABAA)
receptor antagonist bicuculline (0.5-2 microM). The evoked EPSP increased
in most central vestibular neurons (strychnine: 15 out of 16 neurons;
bicuculline 26 out of 29 neurons). At higher stimulus intensities, the
evoked spike discharge increased from 2 to 3 spikes before up to 8-10
spikes per electrical pulse during the application of blocking agents. The
unmasked disynaptic inhibitory component increased with stimulus intensity
to a different extent in different neurons. 3. Lesion studies demonstrated
that these inhibitory components were generated ipsilaterally with respect
to the recording side. The disynaptic strychnine-sensitive inhibition was
mediated by neurons located either in the ventral vestibular nuclear
complex (VNC) or in the adjacent reticular formation. The spatial
distribution of the disynaptic inhibition was investigated by simultaneous
recordings of VIIIth nerve-evoked field potentials at different
rostrocaudal locations of the VNC. A significant strychnine-sensitive
component was detected in the middle and caudal parts but not in the
rostral part of the VNC. A bicuculline-sensitive component was detected in
the rostral and in the caudal parts but not in the middle part of the VNC.
In view of a similar rostrocaudal distribution of glycineor
GABA-immunoreactive neurons in the VNC of frogs, our results suggest that
part of the disynaptic inhibition is mediated by local interneurons with a
spatially restricted projection area. 4. The monosynaptic EPSP of
second-order vestibular neurons was mediated in part by
N-methyl-D-aspartate (NMDA) and in part by non-NMDA receptors. The relative
contribution of the NMDA receptor-mediated component of the EPSP decreased
with stronger stimuli. This negative correlation could have resulted from a
preferential activation of NMDA receptors via thick vestibular nerve
afferent fibers. Alternatively, the activation of NMDA receptors became
disfacilitated at higher stimulus intensities due to the recruitment of
disynaptic inhibitory inputs. Comparison of data obtained in the presence
and in the absence of these glycine and GABAA receptor blockers indicates a
preferential activation of NMDA receptors via larger-diameter vestibular
nerve afferent fibers. 5. The kinetics of NMDA receptors (delay, rise time)
activated by afferent nerve inputs were relatively fast. These fast
kinetics were independent of superimposed IPSPs. The association of these
receptors with large-diameter vestibular nerve afferent fibers suggests
that fast NMDA receptor kinetics might be matched to the more phasic
response dynamics of the large diameter vestibular afferent neurons to
natural head accelerations.</abstract><cop>United States</cop><pub>Am Phys Soc</pub><pmid>8930257</pmid><doi>10.1152/jn.1996.76.5.3087</doi><tpages>15</tpages></addata></record> |
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| ispartof | Journal of neurophysiology, 1996-11, Vol.76 (5), p.3087-3101 |
| issn | 0022-3077 1522-1598 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_15780925 |
| source | MEDLINE; Alma/SFX Local Collection |
| subjects | Afferent Pathways - physiology Animals Brain Stem - physiology Electric Stimulation Rana esculenta Strychnine - pharmacology Synaptic Transmission - drug effects Synaptic Transmission - physiology Vestibular Nerve - physiology |
| title | Uncrossed disynaptic inhibition of second-order vestibular neurons and its interaction with monosynaptic excitation from vestibular nerve afferent fibers in the frog |
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