Fast Rhythmic Bursting Can Be Induced in Layer 2/3 Cortical Neurons by Enhancing Persistent Na+ Conductance or by Blocking BK Channels
1 Departments of Physiology and Pharmacology and Neurology, State University of New York Health Science Center, Brooklyn, New York 11203; and 2 Division of Biomedical Sciences, The Worsley Building, University of Leeds, Leeds LS2 9NQ, United Kingdom Traub, Roger D., Eberhard H. Buhl, Tengis Glov...
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| Veröffentlicht in: | Journal of neurophysiology 2003-02, Vol.89 (2), p.909-921 |
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| creator | Traub, Roger D Buhl, Eberhard H Gloveli, Tengis Whittington, Miles A |
| description | 1 Departments of Physiology and Pharmacology
and Neurology, State University of New York Health Science Center,
Brooklyn, New York 11203; and 2 Division of
Biomedical Sciences, The Worsley Building, University of Leeds,
Leeds LS2 9NQ, United Kingdom
Traub, Roger D.,
Eberhard H. Buhl,
Tengis Gloveli, and
Miles A. Whittington.
Fast Rhythmic Bursting Can Be Induced in Layer 2/3 Cortical
Neurons by Enhancing Persistent Na + Conductance or by
Blocking BK Channels. J. Neurophysiol. 89: 909-921, 2003. Fast rhythmic bursting (or
"chattering") is a firing pattern exhibited by selected neocortical
neurons in cats in vivo and in slices of adult ferret and cat brain.
Fast rhythmic bursting (FRB) has been recorded in certain superficial
and deep principal neurons and in aspiny presumed local circuit
neurons; it can be evoked by depolarizing currents or by sensory
stimulation and has been proposed to depend on a persistent
g Na that causes spike depolarizing
afterpotentials. We constructed a multicompartment 11-conductance model
of a layer 2/3 pyramidal neuron, containing apical dendritic
calcium-mediated electrogenesis; the model can switch between rhythmic
spiking (RS) and FRB modes of firing, with various parameter changes.
FRB in this model is favored by enhancing persistent
g Na and also by measures that reduce
[Ca 2+ ] i or that reduce
the conductance of g K(C) (a fast
voltage- and Ca 2+ -dependent conductance). Axonal
excitability plays a critical role in generating fast bursts in the
model. In vitro experiments in rat layer 2/3 neurons confirmed (as
shown previously by others) that RS firing could be switched to fast
rhythmic bursting, either by buffering
[Ca 2+ ] i or by enhancing
persistent g Na . In addition, our
experiments confirmed the model prediction that reducing
g KC (with iberiotoxin) would favor
FRB. During the bursts, fast prepotentials (spikelets) could occur that
did not originate in apical dendrites and that appear to derive from
the axon. We suggest that modulator-induced regulation of
[Ca 2+ ] dynamics or of BK channel
conductance, for example via protein kinase A, could play a role in
determining the firing pattern of neocortical neurons; specifically,
such modulation could play a role in regulating whether neurons respond
to strong stimulation with fast rhythmic bursts. |
| doi_str_mv | 10.1152/jn.00573.2002 |
| format | Article |
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and Neurology, State University of New York Health Science Center,
Brooklyn, New York 11203; and 2 Division of
Biomedical Sciences, The Worsley Building, University of Leeds,
Leeds LS2 9NQ, United Kingdom
Traub, Roger D.,
Eberhard H. Buhl,
Tengis Gloveli, and
Miles A. Whittington.
Fast Rhythmic Bursting Can Be Induced in Layer 2/3 Cortical
Neurons by Enhancing Persistent Na + Conductance or by
Blocking BK Channels. J. Neurophysiol. 89: 909-921, 2003. Fast rhythmic bursting (or
"chattering") is a firing pattern exhibited by selected neocortical
neurons in cats in vivo and in slices of adult ferret and cat brain.
Fast rhythmic bursting (FRB) has been recorded in certain superficial
and deep principal neurons and in aspiny presumed local circuit
neurons; it can be evoked by depolarizing currents or by sensory
stimulation and has been proposed to depend on a persistent
g Na that causes spike depolarizing
afterpotentials. We constructed a multicompartment 11-conductance model
of a layer 2/3 pyramidal neuron, containing apical dendritic
calcium-mediated electrogenesis; the model can switch between rhythmic
spiking (RS) and FRB modes of firing, with various parameter changes.
FRB in this model is favored by enhancing persistent
g Na and also by measures that reduce
[Ca 2+ ] i or that reduce
the conductance of g K(C) (a fast
voltage- and Ca 2+ -dependent conductance). Axonal
excitability plays a critical role in generating fast bursts in the
model. In vitro experiments in rat layer 2/3 neurons confirmed (as
shown previously by others) that RS firing could be switched to fast
rhythmic bursting, either by buffering
[Ca 2+ ] i or by enhancing
persistent g Na . In addition, our
experiments confirmed the model prediction that reducing
g KC (with iberiotoxin) would favor
FRB. During the bursts, fast prepotentials (spikelets) could occur that
did not originate in apical dendrites and that appear to derive from
the axon. We suggest that modulator-induced regulation of
[Ca 2+ ] dynamics or of BK channel
conductance, for example via protein kinase A, could play a role in
determining the firing pattern of neocortical neurons; specifically,
such modulation could play a role in regulating whether neurons respond
to strong stimulation with fast rhythmic bursts.</description><identifier>ISSN: 0022-3077</identifier><identifier>EISSN: 1522-1598</identifier><identifier>DOI: 10.1152/jn.00573.2002</identifier><identifier>PMID: 12574468</identifier><language>eng</language><publisher>United States: Am Phys Soc</publisher><subject>Action Potentials - drug effects ; Action Potentials - physiology ; Animals ; Axons - physiology ; Calcium - metabolism ; Cerebral Cortex - cytology ; Cerebral Cortex - physiology ; Large-Conductance Calcium-Activated Potassium Channels ; Male ; Models, Neurological ; Nitric Oxide Donors - pharmacology ; Organ Culture Techniques ; Penicillamine - analogs & derivatives ; Penicillamine - pharmacology ; Periodicity ; Potassium Channels, Calcium-Activated - antagonists & inhibitors ; Pyramidal Cells - physiology ; Rats ; Rats, Wistar ; Sodium - metabolism ; Sodium Channels - physiology</subject><ispartof>Journal of neurophysiology, 2003-02, Vol.89 (2), p.909-921</ispartof><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c402t-15e3d14ef492c0656f32c37a1a50305e75996f25396990b9dab8e620a62d0403</citedby><cites>FETCH-LOGICAL-c402t-15e3d14ef492c0656f32c37a1a50305e75996f25396990b9dab8e620a62d0403</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,3039,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12574468$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Traub, Roger D</creatorcontrib><creatorcontrib>Buhl, Eberhard H</creatorcontrib><creatorcontrib>Gloveli, Tengis</creatorcontrib><creatorcontrib>Whittington, Miles A</creatorcontrib><title>Fast Rhythmic Bursting Can Be Induced in Layer 2/3 Cortical Neurons by Enhancing Persistent Na+ Conductance or by Blocking BK Channels</title><title>Journal of neurophysiology</title><addtitle>J Neurophysiol</addtitle><description> 1 Departments of Physiology and Pharmacology
and Neurology, State University of New York Health Science Center,
Brooklyn, New York 11203; and 2 Division of
Biomedical Sciences, The Worsley Building, University of Leeds,
Leeds LS2 9NQ, United Kingdom
Traub, Roger D.,
Eberhard H. Buhl,
Tengis Gloveli, and
Miles A. Whittington.
Fast Rhythmic Bursting Can Be Induced in Layer 2/3 Cortical
Neurons by Enhancing Persistent Na + Conductance or by
Blocking BK Channels. J. Neurophysiol. 89: 909-921, 2003. Fast rhythmic bursting (or
"chattering") is a firing pattern exhibited by selected neocortical
neurons in cats in vivo and in slices of adult ferret and cat brain.
Fast rhythmic bursting (FRB) has been recorded in certain superficial
and deep principal neurons and in aspiny presumed local circuit
neurons; it can be evoked by depolarizing currents or by sensory
stimulation and has been proposed to depend on a persistent
g Na that causes spike depolarizing
afterpotentials. We constructed a multicompartment 11-conductance model
of a layer 2/3 pyramidal neuron, containing apical dendritic
calcium-mediated electrogenesis; the model can switch between rhythmic
spiking (RS) and FRB modes of firing, with various parameter changes.
FRB in this model is favored by enhancing persistent
g Na and also by measures that reduce
[Ca 2+ ] i or that reduce
the conductance of g K(C) (a fast
voltage- and Ca 2+ -dependent conductance). Axonal
excitability plays a critical role in generating fast bursts in the
model. In vitro experiments in rat layer 2/3 neurons confirmed (as
shown previously by others) that RS firing could be switched to fast
rhythmic bursting, either by buffering
[Ca 2+ ] i or by enhancing
persistent g Na . In addition, our
experiments confirmed the model prediction that reducing
g KC (with iberiotoxin) would favor
FRB. During the bursts, fast prepotentials (spikelets) could occur that
did not originate in apical dendrites and that appear to derive from
the axon. We suggest that modulator-induced regulation of
[Ca 2+ ] dynamics or of BK channel
conductance, for example via protein kinase A, could play a role in
determining the firing pattern of neocortical neurons; specifically,
such modulation could play a role in regulating whether neurons respond
to strong stimulation with fast rhythmic bursts.</description><subject>Action Potentials - drug effects</subject><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>Axons - physiology</subject><subject>Calcium - metabolism</subject><subject>Cerebral Cortex - cytology</subject><subject>Cerebral Cortex - physiology</subject><subject>Large-Conductance Calcium-Activated Potassium Channels</subject><subject>Male</subject><subject>Models, Neurological</subject><subject>Nitric Oxide Donors - pharmacology</subject><subject>Organ Culture Techniques</subject><subject>Penicillamine - analogs & derivatives</subject><subject>Penicillamine - pharmacology</subject><subject>Periodicity</subject><subject>Potassium Channels, Calcium-Activated - antagonists & inhibitors</subject><subject>Pyramidal Cells - physiology</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>Sodium - metabolism</subject><subject>Sodium Channels - physiology</subject><issn>0022-3077</issn><issn>1522-1598</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNptkMGO0zAQhi0EYrsLR67IJy6o3YkdJ_WRRttlRbUg1LvlOpPGJXWK7WjJC_DcOLRoL5wsjb__18xHyLsMFlkm2O3BLQBEyRcMgL0gszRj80zI5UsySxM251CWV-Q6hAMAlALYa3KVMVHmebGckd9rHSL93o6xPVpDV4MP0bo9rbSjK6QPrh4M1tQ6utEjespuOa16H63RHX3Ewfcu0N1I71yrnZmS39AHGyK6SB_1xwRPFTF9Iu39hK663vyYyNUXWqWUwy68Ia8a3QV8e3lvyHZ9t60-zzdf7x-qT5u5yYHFdBfyOsuxySUzUIii4czwUmdaAAeBpZCyaJjgspASdrLWuyUWDHTBasiB35AP59qT738OGKI62mCw67TDfgiq5MkYiCyB8zNofB-Cx0advD1qP6oM1ORdHZz6611N3hP__lI87I5YP9MX0QlgZ6C1-_bJelSndgy27_r9qNZD123xV0ylS6mYkiDVqW6e1_1fKC3wD-Z_AOoEnEo</recordid><startdate>20030201</startdate><enddate>20030201</enddate><creator>Traub, Roger D</creator><creator>Buhl, Eberhard H</creator><creator>Gloveli, Tengis</creator><creator>Whittington, Miles A</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>7X8</scope></search><sort><creationdate>20030201</creationdate><title>Fast Rhythmic Bursting Can Be Induced in Layer 2/3 Cortical Neurons by Enhancing Persistent Na+ Conductance or by Blocking BK Channels</title><author>Traub, Roger D ; Buhl, Eberhard H ; Gloveli, Tengis ; Whittington, Miles A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c402t-15e3d14ef492c0656f32c37a1a50305e75996f25396990b9dab8e620a62d0403</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>Action Potentials - drug effects</topic><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>Axons - physiology</topic><topic>Calcium - metabolism</topic><topic>Cerebral Cortex - cytology</topic><topic>Cerebral Cortex - physiology</topic><topic>Large-Conductance Calcium-Activated Potassium Channels</topic><topic>Male</topic><topic>Models, Neurological</topic><topic>Nitric Oxide Donors - pharmacology</topic><topic>Organ Culture Techniques</topic><topic>Penicillamine - analogs & derivatives</topic><topic>Penicillamine - pharmacology</topic><topic>Periodicity</topic><topic>Potassium Channels, Calcium-Activated - antagonists & inhibitors</topic><topic>Pyramidal Cells - physiology</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>Sodium - metabolism</topic><topic>Sodium Channels - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Traub, Roger D</creatorcontrib><creatorcontrib>Buhl, Eberhard H</creatorcontrib><creatorcontrib>Gloveli, Tengis</creatorcontrib><creatorcontrib>Whittington, Miles A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of neurophysiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Traub, Roger D</au><au>Buhl, Eberhard H</au><au>Gloveli, Tengis</au><au>Whittington, Miles A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fast Rhythmic Bursting Can Be Induced in Layer 2/3 Cortical Neurons by Enhancing Persistent Na+ Conductance or by Blocking BK Channels</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>2003-02-01</date><risdate>2003</risdate><volume>89</volume><issue>2</issue><spage>909</spage><epage>921</epage><pages>909-921</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><abstract> 1 Departments of Physiology and Pharmacology
and Neurology, State University of New York Health Science Center,
Brooklyn, New York 11203; and 2 Division of
Biomedical Sciences, The Worsley Building, University of Leeds,
Leeds LS2 9NQ, United Kingdom
Traub, Roger D.,
Eberhard H. Buhl,
Tengis Gloveli, and
Miles A. Whittington.
Fast Rhythmic Bursting Can Be Induced in Layer 2/3 Cortical
Neurons by Enhancing Persistent Na + Conductance or by
Blocking BK Channels. J. Neurophysiol. 89: 909-921, 2003. Fast rhythmic bursting (or
"chattering") is a firing pattern exhibited by selected neocortical
neurons in cats in vivo and in slices of adult ferret and cat brain.
Fast rhythmic bursting (FRB) has been recorded in certain superficial
and deep principal neurons and in aspiny presumed local circuit
neurons; it can be evoked by depolarizing currents or by sensory
stimulation and has been proposed to depend on a persistent
g Na that causes spike depolarizing
afterpotentials. We constructed a multicompartment 11-conductance model
of a layer 2/3 pyramidal neuron, containing apical dendritic
calcium-mediated electrogenesis; the model can switch between rhythmic
spiking (RS) and FRB modes of firing, with various parameter changes.
FRB in this model is favored by enhancing persistent
g Na and also by measures that reduce
[Ca 2+ ] i or that reduce
the conductance of g K(C) (a fast
voltage- and Ca 2+ -dependent conductance). Axonal
excitability plays a critical role in generating fast bursts in the
model. In vitro experiments in rat layer 2/3 neurons confirmed (as
shown previously by others) that RS firing could be switched to fast
rhythmic bursting, either by buffering
[Ca 2+ ] i or by enhancing
persistent g Na . In addition, our
experiments confirmed the model prediction that reducing
g KC (with iberiotoxin) would favor
FRB. During the bursts, fast prepotentials (spikelets) could occur that
did not originate in apical dendrites and that appear to derive from
the axon. We suggest that modulator-induced regulation of
[Ca 2+ ] dynamics or of BK channel
conductance, for example via protein kinase A, could play a role in
determining the firing pattern of neocortical neurons; specifically,
such modulation could play a role in regulating whether neurons respond
to strong stimulation with fast rhythmic bursts.</abstract><cop>United States</cop><pub>Am Phys Soc</pub><pmid>12574468</pmid><doi>10.1152/jn.00573.2002</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Journal of neurophysiology, 2003-02, Vol.89 (2), p.909-921 |
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| source | MEDLINE; American Physiological Society Paid; EZB-FREE-00999 freely available EZB journals |
| subjects | Action Potentials - drug effects Action Potentials - physiology Animals Axons - physiology Calcium - metabolism Cerebral Cortex - cytology Cerebral Cortex - physiology Large-Conductance Calcium-Activated Potassium Channels Male Models, Neurological Nitric Oxide Donors - pharmacology Organ Culture Techniques Penicillamine - analogs & derivatives Penicillamine - pharmacology Periodicity Potassium Channels, Calcium-Activated - antagonists & inhibitors Pyramidal Cells - physiology Rats Rats, Wistar Sodium - metabolism Sodium Channels - physiology |
| title | Fast Rhythmic Bursting Can Be Induced in Layer 2/3 Cortical Neurons by Enhancing Persistent Na+ Conductance or by Blocking BK Channels |
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