DOI: 10.1523/jneurosci.4341-06.2007. Roles of Subthreshold Calcium Current and Sodium Current in Spontaneous Firing of Mouse Midbrain Dopamine Neurons

Roles of Subthreshold Calcium Current and Sodium Current in Spontaneous Firing of Mouse Midbrain Dopamine Neurons

10.1523/jneurosci.4341-06.2007

Crossref journal-article

Society for Neuroscience

The Journal of Neuroscience (393)

Abstract

We used a preparation of acutely dissociated neurons to quantify the ionic currents driving the spontaneous firing of substantia nigra pars compacta neurons, isolated from transgenic mice in which the tyrosine hydroxylase promoter drives expression of human placental alkaline phosphatase (PLAP) on the outer surface of the cell membrane. Dissociated neurons identified by fluorescent antibodies to PLAP showed firing properties similar to those of dopaminergic neurons in brain slice, including rhythmic spontaneous firing of broad action potentials and, in some cells, rhythmic oscillatory activity in the presence of tetrodotoxin (TTX). Spontaneous activity in TTX had broader, smaller spikes than normal pacemaking and was stopped by removal of external calcium. Normal pacemaking was also consistently silenced by replacement of external calcium by cobalt and was slowed by more specific calcium channel blockers. Nimodipine produced a slowing of pacemaking frequency. Pacemaking was also slowed by the P/Q-channel blocker ω-Aga-IVA, but the N-type channel blocker ω-conotoxin GVIA had no effect. In voltage-clamp experiments, using records of pacemaking as command voltage, cobalt-sensitive current and TTX-sensitive current were both sizeable at subthreshold voltages between spikes. Cobalt-sensitive current was consistently larger than TTX-sensitive current at interspike voltages from −70 to −50 mV, with TTX-sensitive current larger at voltages positive to −45 mV. These results support previous evidence for a major role of voltage-dependent calcium channels in driving pacemaking of midbrain dopamine neurons and suggest that multiple calcium channel types contribute to this function. The results also show a significant contribution of subthreshold TTX-sensitive sodium current.

Bibliography

Puopolo, M., Raviola, E., & Bean, B. P. (2007). Roles of Subthreshold Calcium Current and Sodium Current in Spontaneous Firing of Mouse Midbrain Dopamine Neurons. The Journal of Neuroscience, 27(3), 645â656.

Authors 3

Michelino Puopolo (first)
Elio Raviola (additional)
Bruce P. Bean (additional)

References 68 Referenced 261

10.1523/JNEUROSCI.4907-05.2006
10.1523/JNEUROSCI.1475-05.2005
10.1523/JNEUROSCI.12-11-04460.1992 / J Neurosci / 5′ flanking sequences of the rat tyrosine hydroxylase gene target accurate tissue-specific, developmental, and transsynaptic expression in transgenic mice by Banerjee (1992)
10.1523/JNEUROSCI.20-22-08493.2000 / J Neurosci / Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons by Bennett (2000)
10.1152/jn.2000.83.4.1951 / J Neurophysiol / Slowly inactivating sodium current (I(NaP)) underlies single-spike activity in rat subthalamic neurons by Beurrier (2000)
10.1523/JNEUROSCI.19-17-07617.1999 / J Neurosci / Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons by Bevan (1999)
10.1523/JNEUROSCI.22-23-10277.2002 / J Neurosci / Roles of tetrodotoxin (TTX)-sensitive Na+ current, TTX-resistant Na+ current, and Ca2+ current in the action potentials of nociceptive sensory neurons by Blair (2002)
10.1152/jn.1995.74.3.1137 / J Neurophysiol / Voltage-dependent calcium channels in rat midbrain dopamine neurons: modulation by dopamine and GABAB receptors by Cardozo (1995)
10.1523/JNEUROSCI.23-05-01593.2003 / J Neurosci / Afterhyperpolarization regulates firing rate in neurons of the suprachiasmatic nucleus by Cloues (2003)
10.1016/S0896-6273(03)00568-3
10.1093/clinchem/29.1.115 / Clin Chem / Use of monoclonal antibodies to detect human placental alkaline phosphatase by De Groote (1983)
10.1016/S0896-6273(03)00360-X
10.1152/jn.01015.2003
10.1523/JNEUROSCI.23-05-01557.2003 / J Neurosci / The wake-promoting hypocretin-orexin neurons are in an intrinsic state of membrane depolarization by Eggermann (2003)
10.1523/JNEUROSCI.18-17-06776.1998 / J Neurosci / Spontaneous activity of solitary dopaminergic cells of the retina by Feigenspan (1998)
Fujimura K Matsuda Y (1989) Autogenous oscillatory potentials in neurons of the guinea pig substantia nigra pars compacta in vitro. Neurosci Lett, 10453–57. (10.1016/0304-3940(89)90328-5)
10.1523/JNEUROSCI.04-11-02866.1984 / J Neurosci / The control of firing pattern in nigral dopamine neurons: single spike firing by Grace (1984)
10.1523/JNEUROSCI.09-10-03463.1989 / J Neurosci / Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro by Grace (1989)
10.1016/S0896-6273(00)80313-X
10.1016/0306-4522(91)90419-O
10.1523/JNEUROSCI.23-20-07525.2003 / J Neurosci / Apamin-sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons in vitro by Hallworth (2004)
10.1016/0306-4522(89)90379-5
10.1016/0896-6273(95)90152-3
10.1523/JNEUROSCI.2146-04.2004
10.1016/0168-0102(93)90056-V
10.1016/0168-0102(93)90055-U
10.1523/JNEUROSCI.3664-05.2006
10.1016/S0896-6273(00)80557-7
10.1074/jbc.M101469200
10.1152/jn.00691.2004
10.1016/S0896-6273(00)00111-2
10.1152/jn.1992.68.4.1307 / J Neurophysiol / Electrophysiology of the mammillary complex in vitro. I. Tuberomammillary and lateral mammillary neurons by Llinás (1992)
10.1073/pnas.79.7.2415
10.1038/nn962
10.1523/JNEUROSCI.18-19-07613.1998 / J Neurosci / Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons by Magee (1998)
10.1016/S0166-2236(96)40004-2
10.1016/S0006-3495(98)74007-X / Biophys J / Modalities of distortion of physiological voltage signals by patch-clamp amplifiers: a modeling study by Magistretti (1998)
10.1023/A:1024422802673
10.1111/j.1476-5381.1994.tb17068.x
10.1111/j.1460-9568.1995.tb00342.x
10.1016/0896-6273(92)90223-Z / Neuron / P-type calcium channels in central and peripheral neurons by Mintz (1992)
10.1016/0306-4522(92)90502-S
{'key': '2023041303225831000_27.3.645.43'}
10.1016/0076-6879(92)07008-C
10.1523/JNEUROSCI.22-04-01290.2002 / J Neurosci / I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain by Neuhoff (2002)
10.1016/S0301-0082(02)00011-4
10.1152/jn.1997.78.4.1811 / J Neurophysiol / Cellular mechanisms underlying spontaneous firing in rat suprachiasmatic nucleus: involvement of a slowly inactivating component of sodium current by Pennartz (1997)
10.1113/jphysiol.2005.084632
10.1097/00001756-199602290-00031 / NeuroReport / Apamin-sensitive Ca2+-activated K+ channels regulate pacemaker activity in nigral dopamine neurons by Ping (1996)
10.1152/jn.00225.2005
10.1523/JNEUROSCI.19-05-01663.1999 / J Neurosci / Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons by Raman (1999)
10.1523/JNEUROSCI.20-24-09004.2000 / J Neurosci / Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei by Raman (2000)
10.1113/jphysiol.2005.100305
10.1210/me.15.7.1211
10.1016/S0896-6273(02)00967-4
10.1097/00001756-200102120-00015
10.1016/S0006-3495(03)74642-6 / Biophys J / Spontaneous activity of dopaminergic retinal neurons by Steffen (2003)
10.1016/S0896-6273(02)00574-3
10.1046/j.1460-9568.2001.01435.x
10.1016/S0306-4522(96)00540-4
10.1038/nn1648
10.1152/jn.2000.83.5.3177 / J Neurophysiol / Site independence of EPSP time course is mediated by dendritic Ih in neocortical pyramidal neurons by Williams (2000)
{'key': '2023041303225831000_27.3.645.63'}
10.1038/nrn1406
10.1523/JNEUROSCI.21-10-03443.2001 / J Neurosci / Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons by Wolfart (2001)
10.1523/JNEUROSCI.21-16-05944.2001 / J Neurosci / Neuronal CaV1.3α1 L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines by Xu (2001)
10.1113/jphysiol.1991.sp018571 / J Physiol (Lond) / Electrophysiology of dopaminergic and non-dopaminergic neurones of the guinea-pig substantia nigra pars compacta in vitro by Yung (1991)
10.1111/j.1469-7793.1997.677ba.x

Dates

Type	When
Created	18 years, 7 months ago (Jan. 17, 2007, 6:33 p.m.)
Deposited	2 years, 4 months ago (April 13, 2023, 1:50 p.m.)
Indexed	3 weeks, 4 days ago (Aug. 7, 2025, 4:55 a.m.)
Issued	18 years, 7 months ago (Jan. 17, 2007)
Published	18 years, 7 months ago (Jan. 17, 2007)
Published Online	18 years, 7 months ago (Jan. 17, 2007)
Published Print	18 years, 7 months ago (Jan. 17, 2007)

Funders 0

None

BibTeX

@article{Puopolo_2007, title={Roles of Subthreshold Calcium Current and Sodium Current in Spontaneous Firing of Mouse Midbrain Dopamine Neurons}, volume={27}, ISSN={1529-2401}, url={http://dx.doi.org/10.1523/jneurosci.4341-06.2007}, DOI={10.1523/jneurosci.4341-06.2007}, number={3}, journal={The Journal of Neuroscience}, publisher={Society for Neuroscience}, author={Puopolo, Michelino and Raviola, Elio and Bean, Bruce P.}, year={2007}, month=jan, pages={645–656} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        7
      ]
    ],
    "date-time": "2025-08-07T08:55:49Z",
    "timestamp": 1754556949086
  },
  "reference-count": 68,
  "publisher": "Society for Neuroscience",
  "issue": "3",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2007,
            7,
            17
          ]
        ],
        "date-time": "2007-07-17T00:00:00Z",
        "timestamp": 1184630400000
      },
      "content-version": "vor",
      "delay-in-days": 181,
      "URL": "https://creativecommons.org/licenses/by-nc-sa/4.0/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2007,
        1,
        17
      ]
    ]
  },
  "abstract": "<jats:p>We used a preparation of acutely dissociated neurons to quantify the ionic currents driving the spontaneous firing of substantia nigra pars compacta neurons, isolated from transgenic mice in which the tyrosine hydroxylase promoter drives expression of human placental alkaline phosphatase (PLAP) on the outer surface of the cell membrane. Dissociated neurons identified by fluorescent antibodies to PLAP showed firing properties similar to those of dopaminergic neurons in brain slice, including rhythmic spontaneous firing of broad action potentials and, in some cells, rhythmic oscillatory activity in the presence of tetrodotoxin (TTX). Spontaneous activity in TTX had broader, smaller spikes than normal pacemaking and was stopped by removal of external calcium. Normal pacemaking was also consistently silenced by replacement of external calcium by cobalt and was slowed by more specific calcium channel blockers. Nimodipine produced a slowing of pacemaking frequency. Pacemaking was also slowed by the P/Q-channel blocker \u03c9-Aga-IVA, but the N-type channel blocker \u03c9-conotoxin GVIA had no effect. In voltage-clamp experiments, using records of pacemaking as command voltage, cobalt-sensitive current and TTX-sensitive current were both sizeable at subthreshold voltages between spikes. Cobalt-sensitive current was consistently larger than TTX-sensitive current at interspike voltages from \u221270 to \u221250 mV, with TTX-sensitive current larger at voltages positive to \u221245 mV. These results support previous evidence for a major role of voltage-dependent calcium channels in driving pacemaking of midbrain dopamine neurons and suggest that multiple calcium channel types contribute to this function. The results also show a significant contribution of subthreshold TTX-sensitive sodium current.</jats:p>",
  "DOI": "10.1523/jneurosci.4341-06.2007",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2007,
        1,
        17
      ]
    ],
    "date-time": "2007-01-17T23:33:28Z",
    "timestamp": 1169076808000
  },
  "page": "645-656",
  "source": "Crossref",
  "is-referenced-by-count": 261,
  "title": "Roles of Subthreshold Calcium Current and Sodium Current in Spontaneous Firing of Mouse Midbrain Dopamine Neurons",
  "prefix": "10.1523",
  "volume": "27",
  "author": [
    {
      "given": "Michelino",
      "family": "Puopolo",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Elio",
      "family": "Raviola",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Bruce P.",
      "family": "Bean",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "393",
  "published-online": {
    "date-parts": [
      [
        2007,
        1,
        17
      ]
    ]
  },
  "reference": [
    {
      "key": "2023041303225831000_27.3.645.1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.4907-05.2006"
    },
    {
      "key": "2023041303225831000_27.3.645.2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.1475-05.2005"
    },
    {
      "key": "2023041303225831000_27.3.645.3",
      "doi-asserted-by": "crossref",
      "first-page": "4460",
      "DOI": "10.1523/JNEUROSCI.12-11-04460.1992",
      "article-title": "5\u2032 flanking sequences of the rat tyrosine hydroxylase gene target accurate tissue-specific, developmental, and transsynaptic expression in transgenic mice",
      "volume": "12",
      "author": "Banerjee",
      "year": "1992",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.4",
      "doi-asserted-by": "crossref",
      "first-page": "8493",
      "DOI": "10.1523/JNEUROSCI.20-22-08493.2000",
      "article-title": "Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons",
      "volume": "20",
      "author": "Bennett",
      "year": "2000",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.5",
      "doi-asserted-by": "crossref",
      "first-page": "1951",
      "DOI": "10.1152/jn.2000.83.4.1951",
      "article-title": "Slowly inactivating sodium current (I(NaP)) underlies single-spike activity in rat subthalamic neurons",
      "volume": "83",
      "author": "Beurrier",
      "year": "2000",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "2023041303225831000_27.3.645.6",
      "doi-asserted-by": "crossref",
      "first-page": "7617",
      "DOI": "10.1523/JNEUROSCI.19-17-07617.1999",
      "article-title": "Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons",
      "volume": "19",
      "author": "Bevan",
      "year": "1999",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.7",
      "doi-asserted-by": "crossref",
      "first-page": "10277",
      "DOI": "10.1523/JNEUROSCI.22-23-10277.2002",
      "article-title": "Roles of tetrodotoxin (TTX)-sensitive Na+ current, TTX-resistant Na+ current, and Ca2+ current in the action potentials of nociceptive sensory neurons",
      "volume": "22",
      "author": "Blair",
      "year": "2002",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.8",
      "doi-asserted-by": "crossref",
      "first-page": "1137",
      "DOI": "10.1152/jn.1995.74.3.1137",
      "article-title": "Voltage-dependent calcium channels in rat midbrain dopamine neurons: modulation by dopamine and GABAB receptors",
      "volume": "74",
      "author": "Cardozo",
      "year": "1995",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "2023041303225831000_27.3.645.9",
      "doi-asserted-by": "crossref",
      "first-page": "1593",
      "DOI": "10.1523/JNEUROSCI.23-05-01593.2003",
      "article-title": "Afterhyperpolarization regulates firing rate in neurons of the suprachiasmatic nucleus",
      "volume": "23",
      "author": "Cloues",
      "year": "2003",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.10",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0896-6273(03)00568-3"
    },
    {
      "key": "2023041303225831000_27.3.645.11",
      "doi-asserted-by": "crossref",
      "first-page": "115",
      "DOI": "10.1093/clinchem/29.1.115",
      "article-title": "Use of monoclonal antibodies to detect human placental alkaline phosphatase",
      "volume": "29",
      "author": "De Groote",
      "year": "1983",
      "journal-title": "Clin Chem"
    },
    {
      "key": "2023041303225831000_27.3.645.12",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0896-6273(03)00360-X"
    },
    {
      "key": "2023041303225831000_27.3.645.13",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.01015.2003"
    },
    {
      "key": "2023041303225831000_27.3.645.14",
      "doi-asserted-by": "crossref",
      "first-page": "1557",
      "DOI": "10.1523/JNEUROSCI.23-05-01557.2003",
      "article-title": "The wake-promoting hypocretin-orexin neurons are in an intrinsic state of membrane depolarization",
      "volume": "23",
      "author": "Eggermann",
      "year": "2003",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.15",
      "doi-asserted-by": "crossref",
      "first-page": "6776",
      "DOI": "10.1523/JNEUROSCI.18-17-06776.1998",
      "article-title": "Spontaneous activity of solitary dopaminergic cells of the retina",
      "volume": "18",
      "author": "Feigenspan",
      "year": "1998",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.16",
      "doi-asserted-by": "crossref",
      "unstructured": "Fujimura K Matsuda Y (1989) Autogenous oscillatory potentials in neurons of the guinea pig substantia nigra pars compacta in vitro. Neurosci Lett, 10453\u201357.",
      "DOI": "10.1016/0304-3940(89)90328-5"
    },
    {
      "key": "2023041303225831000_27.3.645.17",
      "doi-asserted-by": "crossref",
      "first-page": "2866",
      "DOI": "10.1523/JNEUROSCI.04-11-02866.1984",
      "article-title": "The control of firing pattern in nigral dopamine neurons: single spike firing",
      "volume": "4",
      "author": "Grace",
      "year": "1984",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.18",
      "doi-asserted-by": "crossref",
      "first-page": "3463",
      "DOI": "10.1523/JNEUROSCI.09-10-03463.1989",
      "article-title": "Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro",
      "volume": "9",
      "author": "Grace",
      "year": "1989",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0896-6273(00)80313-X"
    },
    {
      "key": "2023041303225831000_27.3.645.20",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(91)90419-O"
    },
    {
      "key": "2023041303225831000_27.3.645.21",
      "doi-asserted-by": "crossref",
      "first-page": "7525",
      "DOI": "10.1523/JNEUROSCI.23-20-07525.2003",
      "article-title": "Apamin-sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons in vitro",
      "volume": "23",
      "author": "Hallworth",
      "year": "2004",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.22",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(89)90379-5"
    },
    {
      "key": "2023041303225831000_27.3.645.23",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0896-6273(95)90152-3"
    },
    {
      "key": "2023041303225831000_27.3.645.24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.2146-04.2004"
    },
    {
      "key": "2023041303225831000_27.3.645.25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0168-0102(93)90056-V"
    },
    {
      "key": "2023041303225831000_27.3.645.26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0168-0102(93)90055-U"
    },
    {
      "key": "2023041303225831000_27.3.645.27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.3664-05.2006"
    },
    {
      "key": "2023041303225831000_27.3.645.28",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0896-6273(00)80557-7"
    },
    {
      "key": "2023041303225831000_27.3.645.29",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M101469200"
    },
    {
      "key": "2023041303225831000_27.3.645.30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.00691.2004"
    },
    {
      "key": "2023041303225831000_27.3.645.31",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0896-6273(00)00111-2"
    },
    {
      "key": "2023041303225831000_27.3.645.32",
      "doi-asserted-by": "crossref",
      "first-page": "1307",
      "DOI": "10.1152/jn.1992.68.4.1307",
      "article-title": "Electrophysiology of the mammillary complex in vitro. I. Tuberomammillary and lateral mammillary neurons",
      "volume": "68",
      "author": "Llin\u00e1s",
      "year": "1992",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "2023041303225831000_27.3.645.33",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.79.7.2415"
    },
    {
      "key": "2023041303225831000_27.3.645.34",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nn962"
    },
    {
      "key": "2023041303225831000_27.3.645.35",
      "doi-asserted-by": "crossref",
      "first-page": "7613",
      "DOI": "10.1523/JNEUROSCI.18-19-07613.1998",
      "article-title": "Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons",
      "volume": "18",
      "author": "Magee",
      "year": "1998",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.36",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0166-2236(96)40004-2"
    },
    {
      "key": "2023041303225831000_27.3.645.37",
      "doi-asserted-by": "crossref",
      "first-page": "831",
      "DOI": "10.1016/S0006-3495(98)74007-X",
      "article-title": "Modalities of distortion of physiological voltage signals by patch-clamp amplifiers: a modeling study",
      "volume": "74",
      "author": "Magistretti",
      "year": "1998",
      "journal-title": "Biophys J"
    },
    {
      "key": "2023041303225831000_27.3.645.38",
      "doi-asserted-by": "publisher",
      "DOI": "10.1023/A:1024422802673"
    },
    {
      "key": "2023041303225831000_27.3.645.39",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1476-5381.1994.tb17068.x"
    },
    {
      "key": "2023041303225831000_27.3.645.40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1460-9568.1995.tb00342.x"
    },
    {
      "key": "2023041303225831000_27.3.645.41",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/0896-6273(92)90223-Z",
      "article-title": "P-type calcium channels in central and peripheral neurons",
      "volume": "9",
      "author": "Mintz",
      "year": "1992",
      "journal-title": "Neuron"
    },
    {
      "key": "2023041303225831000_27.3.645.42",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(92)90502-S"
    },
    {
      "key": "2023041303225831000_27.3.645.43"
    },
    {
      "key": "2023041303225831000_27.3.645.44",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0076-6879(92)07008-C"
    },
    {
      "key": "2023041303225831000_27.3.645.45",
      "doi-asserted-by": "crossref",
      "first-page": "1290",
      "DOI": "10.1523/JNEUROSCI.22-04-01290.2002",
      "article-title": "I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain",
      "volume": "22",
      "author": "Neuhoff",
      "year": "2002",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.46",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0301-0082(02)00011-4"
    },
    {
      "key": "2023041303225831000_27.3.645.47",
      "doi-asserted-by": "crossref",
      "first-page": "1811",
      "DOI": "10.1152/jn.1997.78.4.1811",
      "article-title": "Cellular mechanisms underlying spontaneous firing in rat suprachiasmatic nucleus: involvement of a slowly inactivating component of sodium current",
      "volume": "78",
      "author": "Pennartz",
      "year": "1997",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "2023041303225831000_27.3.645.48",
      "doi-asserted-by": "publisher",
      "DOI": "10.1113/jphysiol.2005.084632"
    },
    {
      "key": "2023041303225831000_27.3.645.49",
      "doi-asserted-by": "crossref",
      "first-page": "809",
      "DOI": "10.1097/00001756-199602290-00031",
      "article-title": "Apamin-sensitive Ca2+-activated K+ channels regulate pacemaker activity in nigral dopamine neurons",
      "volume": "7",
      "author": "Ping",
      "year": "1996",
      "journal-title": "NeuroReport"
    },
    {
      "key": "2023041303225831000_27.3.645.50",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.00225.2005"
    },
    {
      "key": "2023041303225831000_27.3.645.51",
      "doi-asserted-by": "crossref",
      "first-page": "1663",
      "DOI": "10.1523/JNEUROSCI.19-05-01663.1999",
      "article-title": "Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons",
      "volume": "19",
      "author": "Raman",
      "year": "1999",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.52",
      "doi-asserted-by": "crossref",
      "first-page": "9004",
      "DOI": "10.1523/JNEUROSCI.20-24-09004.2000",
      "article-title": "Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei",
      "volume": "20",
      "author": "Raman",
      "year": "2000",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.53",
      "doi-asserted-by": "publisher",
      "DOI": "10.1113/jphysiol.2005.100305"
    },
    {
      "key": "2023041303225831000_27.3.645.54",
      "doi-asserted-by": "publisher",
      "DOI": "10.1210/me.15.7.1211"
    },
    {
      "key": "2023041303225831000_27.3.645.55",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0896-6273(02)00967-4"
    },
    {
      "key": "2023041303225831000_27.3.645.56",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00001756-200102120-00015"
    },
    {
      "key": "2023041303225831000_27.3.645.57",
      "doi-asserted-by": "crossref",
      "first-page": "2158",
      "DOI": "10.1016/S0006-3495(03)74642-6",
      "article-title": "Spontaneous activity of dopaminergic retinal neurons",
      "volume": "85",
      "author": "Steffen",
      "year": "2003",
      "journal-title": "Biophys J"
    },
    {
      "key": "2023041303225831000_27.3.645.58",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0896-6273(02)00574-3"
    },
    {
      "key": "2023041303225831000_27.3.645.59",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1460-9568.2001.01435.x"
    },
    {
      "key": "2023041303225831000_27.3.645.60",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0306-4522(96)00540-4"
    },
    {
      "key": "2023041303225831000_27.3.645.61",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nn1648"
    },
    {
      "key": "2023041303225831000_27.3.645.62",
      "doi-asserted-by": "crossref",
      "first-page": "3177",
      "DOI": "10.1152/jn.2000.83.5.3177",
      "article-title": "Site independence of EPSP time course is mediated by dendritic Ih in neocortical pyramidal neurons",
      "volume": "83",
      "author": "Williams",
      "year": "2000",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "2023041303225831000_27.3.645.63"
    },
    {
      "key": "2023041303225831000_27.3.645.64",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nrn1406"
    },
    {
      "key": "2023041303225831000_27.3.645.65",
      "doi-asserted-by": "crossref",
      "first-page": "3443",
      "DOI": "10.1523/JNEUROSCI.21-10-03443.2001",
      "article-title": "Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons",
      "volume": "21",
      "author": "Wolfart",
      "year": "2001",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.66",
      "doi-asserted-by": "crossref",
      "first-page": "5944",
      "DOI": "10.1523/JNEUROSCI.21-16-05944.2001",
      "article-title": "Neuronal CaV1.3\u03b11 L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines",
      "volume": "21",
      "author": "Xu",
      "year": "2001",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303225831000_27.3.645.67",
      "doi-asserted-by": "crossref",
      "first-page": "643",
      "DOI": "10.1113/jphysiol.1991.sp018571",
      "article-title": "Electrophysiology of dopaminergic and non-dopaminergic neurones of the guinea-pig substantia nigra pars compacta in vitro",
      "volume": "436",
      "author": "Yung",
      "year": "1991",
      "journal-title": "J Physiol (Lond)"
    },
    {
      "key": "2023041303225831000_27.3.645.68",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1469-7793.1997.677ba.x"
    }
  ],
  "container-title": "The Journal of Neuroscience",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://syndication.highwire.org/content/doi/10.1523/JNEUROSCI.4341-06.2007",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        4,
        13
      ]
    ],
    "date-time": "2023-04-13T17:50:19Z",
    "timestamp": 1681408219000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.jneurosci.org/lookup/doi/10.1523/JNEUROSCI.4341-06.2007"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2007,
        1,
        17
      ]
    ]
  },
  "references-count": 68,
  "journal-issue": {
    "issue": "3",
    "published-online": {
      "date-parts": [
        [
          2007,
          1,
          17
        ]
      ]
    },
    "published-print": {
      "date-parts": [
        [
          2007,
          1,
          17
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1523/JNEUROSCI.4341-06.2007"
  ],
  "URL": "http://dx.doi.org/10.1523/JNEUROSCI.4341-06.2007",
  "relation": {},
  "ISSN": [
    "0270-6474",
    "1529-2401"
  ],
  "subject": [],
  "container-title-short": "J. Neurosci.",
  "published": {
    "date-parts": [
      [
        2007,
        1,
        17
      ]
    ]
  }
}