DOI: 10.1152/jn.2001.86.6.2986. Dopamine D2 Receptor–Mediated Presynaptic Inhibition of Olfactory Nerve Terminals

Dopamine D2 Receptor–Mediated Presynaptic Inhibition of Olfactory Nerve Terminals

10.1152/jn.2001.86.6.2986

Crossref journal-article

American Physiological Society

Journal of Neurophysiology (24)

Abstract

Olfactory receptor neurons of the nasal epithelium project via the olfactory nerve (ON) to the glomeruli of the main olfactory bulb, where they form glutamatergic synapses with the apical dendrites of mitral and tufted cells, the output cells of the olfactory bulb, and with juxtaglomerular interneurons. The glomerular layer contains one of the largest population of dopamine (DA) neurons in the brain, and DA in the olfactory bulb is found exclusively in juxtaglomerular neurons. D2 receptors, the predominant DA receptor subtype in the olfactory bulb, are found in the ON and glomerular layers, and are present on ON terminals. In the present study, field potential and single-unit recordings, as well as whole cell patch-clamp techniques, were used to investigate the role of DA and D2 receptors in glomerular synaptic processing in rat and mouse olfactory bulb slices. DA and D2 receptor agonists reduced ON-evoked synaptic responses in mitral/tufted and juxtaglomerular cells. Spontaneous and ON-evoked spiking of mitral cells was also reduced by DA and D2 agonists, and enhanced by D2 antagonists. DA did not produce measurable postsynaptic changes in juxtaglomerular cells, nor did it alter their responses to mitral/tufted cell inputs. DA also reduced 1) paired-pulse depression of ON-evoked synaptic responses in mitral/tufted and juxtaglomerular cells and 2) the amplitude and frequency of spontaneous, but not miniature, excitatory postsynaptic currents in juxtaglomerular cells. Taken together, these findings are consistent with the hypothesis that activation of D2 receptors presynaptically inhibits ON terminals. DA and D2 agonists had no effect in D2 receptor knockout mice, suggesting that D2 receptors are the only type of DA receptors that affect signal transmission from the ON to the rodent olfactory bulb.

Bibliography

Ennis, M., Zhou, F.-M., Ciombor, K. J., Aroniadou-Anderjaska, V., Hayar, A., Borrelli, E., Zimmer, L. A., Margolis, F., & Shipley, M. T. (2001). Dopamine D2 ReceptorâMediated Presynaptic Inhibition of Olfactory Nerve Terminals. Journal of Neurophysiology, 86(6), 2986â2997.

Authors 9

Matthew Ennis (first)
Fu-Ming Zhou (additional)
Kelly J. Ciombor (additional)
Vassiliki Aroniadou-Anderjaska (additional)
Abdallah Hayar (additional)
Emiliana Borrelli (additional)
Lee A. Zimmer (additional)
Frank Margolis (additional)
Michael T. Shipley (additional)

References 59 Referenced 192

10.1152/jn.1999.81.1.15
10.1152/jn.2000.84.3.1194
10.1016/S0306-4522(96)00706-3
10.1038/377424a0
10.1016/0306-4522(90)90018-Y
10.1016/0306-4522(84)90047-2
10.1523/JNEUROSCI.03-01-00069.1983
10.1097/00001756-199607290-00033
10.1523/JNEUROSCI.21-06-02113.2001
10.1016/S0006-8993(99)02342-2
10.1152/jn.1994.71.6.2557
10.1016/S0304-3940(99)00697-7
10.1016/0165-3806(85)90063-X
10.1016/S0306-4522(98)00437-0
10.1016/S0891-0618(97)00215-9
10.1002/cne.902140407
10.1113/jphysiol.1996.sp021204
10.1097/00001756-199604100-00007
10.1111/j.1469-7793.1998.395bn.x
10.1016/S0896-6273(00)80314-1
10.1002/cne.902660302
10.1073/pnas.90.8.3329
10.1007/BF01257970
10.1152/jn.1999.82.2.1082
10.1002/(SICI)1096-9861(19961223)376:4<557::AID-CNE5>3.0.CO;2-0
10.1002/(SICI)1096-9861(19980420)393:4<457::AID-CNE5>3.0.CO;2-#
10.1523/JNEUROSCI.18-07-02602.1998
10.1111/j.1469-7793.2000.t01-2-00163.x
10.1037/h0028709
10.1007/BF00230117
10.1016/S0306-4522(96)00308-9
10.1016/0006-8993(85)91172-2
10.1002/(SICI)1096-9861(19990906)411:4<666::AID-CNE10>3.0.CO;2-S
10.1113/jphysiol.1988.sp017171
10.1016/S0896-6273(00)80066-5
10.1038/346565a0
10.1016/0896-6273(92)90273-G
10.1152/jn.1993.70.4.1451
10.1038/341237a0
10.1523/JNEUROSCI.10-08-02587.1990
10.1002/(SICI)1096-9861(19990315)405:3<299::AID-CNE2>3.0.CO;2-6
10.1523/JNEUROSCI.08-10-03658.1988
10.1126/science.286.5440.707
10.1126/science.286.5440.711
10.1097/00001756-199101000-00002
{'key': 'B47', 'first-page': '158', 'volume': '17', 'author': 'Niznik HB', 'year': '1992', 'journal-title': 'J Psychiatry Neurosci'} / J Psychiatry Neurosci by Niznik HB (1992)
10.1038/307462a0
10.1242/jcs.9.2.347 / J Cell Sci by Pinching AJ (1971)
10.1016/0006-8993(77)90211-6
10.1523/JNEUROSCI.18-17-06790.1998
10.1016/0896-6273(94)90245-3
10.1002/(SICI)1097-4695(199605)30:1<123::AID-NEU11>3.0.CO;2-N
10.1016/0165-6147(92)90025-2
10.1016/0166-2236(93)90160-N
10.1523/JNEUROSCI.19-20-08808.1999
10.1163/156853964X00030
10.1523/JNEUROSCI.10-03-00757.1990
10.1016/S0166-2236(96)01015-6
10.1152/jn.1997.77.5.2416

Dates

Type	When
Created	7 years, 8 months ago (Dec. 21, 2017, 1:06 a.m.)
Deposited	3 years ago (Aug. 10, 2022, 3:50 p.m.)
Indexed	1 month, 1 week ago (July 25, 2025, 6:51 a.m.)
Issued	23 years, 9 months ago (Dec. 1, 2001)
Published	23 years, 9 months ago (Dec. 1, 2001)
Published Print	23 years, 9 months ago (Dec. 1, 2001)

Funders 0

None

BibTeX

@article{Ennis_2001, title={Dopamine D2 Receptor–Mediated Presynaptic Inhibition of Olfactory Nerve Terminals}, volume={86}, ISSN={1522-1598}, url={http://dx.doi.org/10.1152/jn.2001.86.6.2986}, DOI={10.1152/jn.2001.86.6.2986}, number={6}, journal={Journal of Neurophysiology}, publisher={American Physiological Society}, author={Ennis, Matthew and Zhou, Fu-Ming and Ciombor, Kelly J. and Aroniadou-Anderjaska, Vassiliki and Hayar, Abdallah and Borrelli, Emiliana and Zimmer, Lee A. and Margolis, Frank and Shipley, Michael T.}, year={2001}, month=dec, pages={2986–2997} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        25
      ]
    ],
    "date-time": "2025-07-25T10:51:53Z",
    "timestamp": 1753440713829
  },
  "reference-count": 59,
  "publisher": "American Physiological Society",
  "issue": "6",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2001,
        12,
        1
      ]
    ]
  },
  "abstract": "<jats:p>Olfactory receptor neurons of the nasal epithelium project via the olfactory nerve (ON) to the glomeruli of the main olfactory bulb, where they form glutamatergic synapses with the apical dendrites of mitral and tufted cells, the output cells of the olfactory bulb, and with juxtaglomerular interneurons. The glomerular layer contains one of the largest population of dopamine (DA) neurons in the brain, and DA in the olfactory bulb is found exclusively in juxtaglomerular neurons. D2 receptors, the predominant DA receptor subtype in the olfactory bulb, are found in the ON and glomerular layers, and are present on ON terminals. In the present study, field potential and single-unit recordings, as well as whole cell patch-clamp techniques, were used to investigate the role of DA and D2 receptors in glomerular synaptic processing in rat and mouse olfactory bulb slices. DA and D2 receptor agonists reduced ON-evoked synaptic responses in mitral/tufted and juxtaglomerular cells. Spontaneous and ON-evoked spiking of mitral cells was also reduced by DA and D2 agonists, and enhanced by D2 antagonists. DA did not produce measurable postsynaptic changes in juxtaglomerular cells, nor did it alter their responses to mitral/tufted cell inputs. DA also reduced 1) paired-pulse depression of ON-evoked synaptic responses in mitral/tufted and juxtaglomerular cells and 2) the amplitude and frequency of spontaneous, but not miniature, excitatory postsynaptic currents in juxtaglomerular cells. Taken together, these findings are consistent with the hypothesis that activation of D2 receptors presynaptically inhibits ON terminals. DA and D2 agonists had no effect in D2 receptor knockout mice, suggesting that D2 receptors are the only type of DA receptors that affect signal transmission from the ON to the rodent olfactory bulb.</jats:p>",
  "DOI": "10.1152/jn.2001.86.6.2986",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2017,
        12,
        21
      ]
    ],
    "date-time": "2017-12-21T06:06:05Z",
    "timestamp": 1513836365000
  },
  "page": "2986-2997",
  "source": "Crossref",
  "is-referenced-by-count": 192,
  "title": "Dopamine D2 Receptor\u2013Mediated Presynaptic Inhibition of Olfactory Nerve Terminals",
  "prefix": "10.1152",
  "volume": "86",
  "author": [
    {
      "given": "Matthew",
      "family": "Ennis",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Anatomy and Neurobiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201; and"
        }
      ]
    },
    {
      "given": "Fu-Ming",
      "family": "Zhou",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy and Neurobiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201; and"
        }
      ]
    },
    {
      "given": "Kelly J.",
      "family": "Ciombor",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy and Neurobiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201; and"
        }
      ]
    },
    {
      "given": "Vassiliki",
      "family": "Aroniadou-Anderjaska",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy and Neurobiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201; and"
        }
      ]
    },
    {
      "given": "Abdallah",
      "family": "Hayar",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy and Neurobiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201; and"
        }
      ]
    },
    {
      "given": "Emiliana",
      "family": "Borrelli",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Institut de G\u00e9n\u00e9tique et de Biologie Mol\u00e9culaire et Cellulaire, Centre National de la Recherche Scientifique/Institut National de la Sant\u00e9 et de la Recherche M\u00e9dicale/Universit\u00e9 Louis Pasteur, BP163, 67404 Illkirch Cedex, Strasbourg, France"
        }
      ]
    },
    {
      "given": "Lee A.",
      "family": "Zimmer",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy and Neurobiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201; and"
        }
      ]
    },
    {
      "given": "Frank",
      "family": "Margolis",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy and Neurobiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201; and"
        }
      ]
    },
    {
      "given": "Michael T.",
      "family": "Shipley",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy and Neurobiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201; and"
        }
      ]
    }
  ],
  "member": "24",
  "reference": [
    {
      "doi-asserted-by": "publisher",
      "key": "B1",
      "DOI": "10.1152/jn.1999.81.1.15"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B2",
      "DOI": "10.1152/jn.2000.84.3.1194"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B3",
      "DOI": "10.1016/S0306-4522(96)00706-3"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B4",
      "DOI": "10.1038/377424a0"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B5",
      "DOI": "10.1016/0306-4522(90)90018-Y"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B6",
      "DOI": "10.1016/0306-4522(84)90047-2"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B7",
      "DOI": "10.1523/JNEUROSCI.03-01-00069.1983"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B8",
      "DOI": "10.1097/00001756-199607290-00033"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B9",
      "DOI": "10.1523/JNEUROSCI.21-06-02113.2001"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B10",
      "DOI": "10.1016/S0006-8993(99)02342-2"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B11",
      "DOI": "10.1152/jn.1994.71.6.2557"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B13",
      "DOI": "10.1016/S0304-3940(99)00697-7"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B14",
      "DOI": "10.1016/0165-3806(85)90063-X"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B15",
      "DOI": "10.1016/S0306-4522(98)00437-0"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B16",
      "DOI": "10.1016/S0891-0618(97)00215-9"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B17",
      "DOI": "10.1002/cne.902140407"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B18",
      "DOI": "10.1113/jphysiol.1996.sp021204"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B19",
      "DOI": "10.1097/00001756-199604100-00007"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B20",
      "DOI": "10.1111/j.1469-7793.1998.395bn.x"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B21",
      "DOI": "10.1016/S0896-6273(00)80314-1"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B22",
      "DOI": "10.1002/cne.902660302"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B23",
      "DOI": "10.1073/pnas.90.8.3329"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B24",
      "DOI": "10.1007/BF01257970"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B25",
      "DOI": "10.1152/jn.1999.82.2.1082"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B26",
      "DOI": "10.1002/(SICI)1096-9861(19961223)376:4<557::AID-CNE5>3.0.CO;2-0"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B27",
      "DOI": "10.1002/(SICI)1096-9861(19980420)393:4<457::AID-CNE5>3.0.CO;2-#"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B28",
      "DOI": "10.1523/JNEUROSCI.18-07-02602.1998"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B29",
      "DOI": "10.1111/j.1469-7793.2000.t01-2-00163.x"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B30",
      "DOI": "10.1037/h0028709"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B31",
      "DOI": "10.1007/BF00230117"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B32",
      "DOI": "10.1016/S0306-4522(96)00308-9"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B33",
      "DOI": "10.1016/0006-8993(85)91172-2"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B34",
      "DOI": "10.1002/(SICI)1096-9861(19990906)411:4<666::AID-CNE10>3.0.CO;2-S"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B35",
      "DOI": "10.1113/jphysiol.1988.sp017171"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B36",
      "DOI": "10.1016/S0896-6273(00)80066-5"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B37",
      "DOI": "10.1038/346565a0"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B38",
      "DOI": "10.1016/0896-6273(92)90273-G"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B39",
      "DOI": "10.1152/jn.1993.70.4.1451"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B40",
      "DOI": "10.1038/341237a0"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B41",
      "DOI": "10.1523/JNEUROSCI.10-08-02587.1990"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B42",
      "DOI": "10.1002/(SICI)1096-9861(19990315)405:3<299::AID-CNE2>3.0.CO;2-6"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B43",
      "DOI": "10.1523/JNEUROSCI.08-10-03658.1988"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B44",
      "DOI": "10.1126/science.286.5440.707"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B45",
      "DOI": "10.1126/science.286.5440.711"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B46",
      "DOI": "10.1097/00001756-199101000-00002"
    },
    {
      "key": "B47",
      "first-page": "158",
      "volume": "17",
      "author": "Niznik HB",
      "year": "1992",
      "journal-title": "J Psychiatry Neurosci"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B48",
      "DOI": "10.1038/307462a0"
    },
    {
      "key": "B49",
      "doi-asserted-by": "crossref",
      "first-page": "347",
      "DOI": "10.1242/jcs.9.2.347",
      "volume": "9",
      "author": "Pinching AJ",
      "year": "1971",
      "journal-title": "J Cell Sci"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B50",
      "DOI": "10.1016/0006-8993(77)90211-6"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B51",
      "DOI": "10.1523/JNEUROSCI.18-17-06790.1998"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B52",
      "DOI": "10.1016/0896-6273(94)90245-3"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B53",
      "DOI": "10.1002/(SICI)1097-4695(199605)30:1<123::AID-NEU11>3.0.CO;2-N"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B54",
      "DOI": "10.1016/0165-6147(92)90025-2"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B55",
      "DOI": "10.1016/0166-2236(93)90160-N"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B56",
      "DOI": "10.1523/JNEUROSCI.19-20-08808.1999"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B57",
      "DOI": "10.1163/156853964X00030"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B58",
      "DOI": "10.1523/JNEUROSCI.10-03-00757.1990"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B59",
      "DOI": "10.1016/S0166-2236(96)01015-6"
    },
    {
      "doi-asserted-by": "publisher",
      "key": "B60",
      "DOI": "10.1152/jn.1997.77.5.2416"
    }
  ],
  "container-title": "Journal of Neurophysiology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.physiology.org/doi/pdf/10.1152/jn.2001.86.6.2986",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        8,
        10
      ]
    ],
    "date-time": "2022-08-10T19:50:36Z",
    "timestamp": 1660161036000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.physiology.org/doi/10.1152/jn.2001.86.6.2986"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2001,
        12,
        1
      ]
    ]
  },
  "references-count": 59,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          2001,
          12,
          1
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1152/jn.2001.86.6.2986"
  ],
  "URL": "http://dx.doi.org/10.1152/jn.2001.86.6.2986",
  "relation": {},
  "ISSN": [
    "0022-3077",
    "1522-1598"
  ],
  "subject": [],
  "container-title-short": "Journal of Neurophysiology",
  "published": {
    "date-parts": [
      [
        2001,
        12,
        1
      ]
    ]
  }
}