DOI: 10.1126/science.8085161. Inhibitory CA1-CA3-Hilar Region Feedback in the Hippocampus

Inhibitory CA1-CA3-Hilar Region Feedback in the Hippocampus

10.1126/science.8085161

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

The organization of the hippocampus is generally thought of as a series of cell groups that form a unidirectionally excited chain, regulated by localized inhibitory circuits. With the use of in vivo intracellular labeling, histochemical, and extracellular tracing methods, a longitudinally widespread, inhibitory feedback in rat brain from the CA1 area to the CA3 and hilar regions was observed. This long-range, cross-regional inhibition may allow precise synchronization of population activity by timing the occurrence of action potentials in the principal cells and may contribute to the coordinated induction of synaptic plasticity in distributed networks.

Bibliography

Sik, A., Ylinen, A., Penttonen, M., & BuzsÃ¡ki, G. (1994). Inhibitory CA1-CA3-Hilar Region Feedback in the Hippocampus. Science, 265(5179), 1722â1724.

Authors 4

Attila Sik (first)
Aarne Ylinen (additional)
Markku Penttonen (additional)
György Buzsáki (additional)

References 42 Referenced 174

10.1016/0306-4522(89)90424-7
ANDERSEN, P, LAMELLAR ORGANIZATION OF HIPPOCAMPAL EXCITATORY PATHWAYS, EXPERIMENTAL BRAIN RESEARCH 13: 222 (1971). / EXPERIMENTAL BRAIN RESEARCH (1971)
10.1016/0896-6273(92)90104-L
BUCKMASTER, P.S., MOSSY CELL AXONAL PROJECTIONS TO THE DENTATE GYRUS MOLECULAR LAYER IN THE RAT HIPPOCAMPAL SLICE, HIPPOCAMPUS 2: 349 (1992). (10.1002/hipo.450020403) / HIPPOCAMPUS (1992)
BUHL, E.H., DIVERSE SOURCES OF HIPPOCAMPAL UNITARY INHIBITORY POSTSYNAPTIC POTENTIALS AND THE NUMBER OF SYNAPTIC RELEASE SITES, NATURE 368: 823 (1994). (10.1038/368823a0) / NATURE (1994)
BULLOCK, T.H., COHERENCE OF COMPOUND FIELD POTENTIALS REVEALS DISCONTINUITIES IN THE CA1-SUBICULUM OF THE HIPPOCAMPUS IN FREELY-MOVING RATS, NEUROSCIENCE 38: 609 (1990). (10.1016/0306-4522(90)90055-9) / NEUROSCIENCE (1990)
BUZSAKI, G, RESTORATION OF RHYTHMIC SLOW ACTIVITY (THETA) IN THE SUBCORTICALLY DENERVATED HIPPOCAMPUS BY FETAL CNS TRANSPLANTS, BRAIN RESEARCH 400: 334 (1987). (10.1016/0006-8993(87)90632-9) / BRAIN RESEARCH (1987)
BUZSAKI, G, HIPPOCAMPUS 1: 163 (1991). (10.1002/hipo.450010205) / HIPPOCAMPUS (1991)
10.1016/0306-4522(89)90423-5
10.1126/science.1589772
DASILVA, FHL, ANATOMIC ORGANIZATION AND PHYSIOLOGY OF THE LIMBIC CORTEX, PHYSIOLOGICAL REVIEWS 70: 453 (1990). (10.1152/physrev.1990.70.2.453) / PHYSIOLOGICAL REVIEWS (1990)
Douglas, R. J., Neural Computation 2: 283 (1990). (10.1162/neco.1990.2.3.283) / Neural Computation (1990)
ENGEL, J, PRESURGICAL EVALUATION FOR PARTIAL EPILEPSY - RELATIVE CONTRIBUTIONS OF CHRONIC DEPTH-ELECTRODE RECORDINGS VERSUS FDG-PET AND SCALP-SPHENOIDAL ICTAL EEG, NEUROLOGY 40: 1670 (1990). (10.1212/WNL.40.11.1670) / NEUROLOGY (1990)
GULYAS, A.I., PRECISION AND VARIABILITY IN POSTSYNAPTIC TARGET SELECTION OF INHIBITORY CELLS IN THE HIPPOCAMPAL CA3 REGION, EUROPEAN JOURNAL OF NEUROSCIENCE 5: 1729 (1993). (10.1111/j.1460-9568.1993.tb00240.x) / EUROPEAN JOURNAL OF NEUROSCIENCE (1993)
10.1038/366683a0
HALASY, K, SUBDIVISIONS IN THE MULTIPLE GABAERGIC INNERVATION OF GRANULE CELLS IN THE DENTATE GYRUS OF THE RAT HIPPOCAMPUS, EUROPEAN JOURNAL OF NEUROSCIENCE 5: 411 (1993). (10.1111/j.1460-9568.1993.tb00508.x) / EUROPEAN JOURNAL OF NEUROSCIENCE (1993)
HAN, Z.S., A HIGH-DEGREE OF SPATIAL SELECTIVITY IN THE AXONAL AND DENDRITIC DOMAINS OF PHYSIOLOGICALLY IDENTIFIED LOCAL-CIRCUIT NEURONS IN THE DENTATE GYRUS OF THE RAT HIPPOCAMPUS, EUROPEAN JOURNAL OF NEUROSCIENCE 5: 395 (1993). (10.1111/j.1460-9568.1993.tb00507.x) / EUROPEAN JOURNAL OF NEUROSCIENCE (1993)
HOLSHEIMER, J, PROPAGATION VELOCITY OF EPILEPTIFORM ACTIVITY IN THE HIPPOCAMPUS, EXPERIMENTAL BRAIN RESEARCH 77: 69 (1989). (10.1007/BF00250568) / EXPERIMENTAL BRAIN RESEARCH (1989)
HORIKAWA, K, A VERSATILE MEANS OF INTRACELLULAR LABELING - INJECTION OF BIOCYTIN AND ITS DETECTION WITH AVIDIN CONJUGATES, JOURNAL OF NEUROSCIENCE METHODS 25: 1 (1988). / JOURNAL OF NEUROSCIENCE METHODS (1988)
10.1002/ana.410200406
KAWAGUCHI, Y, FAST SPIKING CELLS IN RAT HIPPOCAMPUS (CA1 REGION) CONTAIN THE CALCIUM-BINDING PROTEIN PARVALBUMIN, BRAIN RESEARCH 416: 369 (1987). (10.1016/0006-8993(87)90921-8) / BRAIN RESEARCH (1987)
KUNKEL, D.D., ULTRASTRUCTURE OF STRATUM LACUNOSUM-MOLECULARE INTERNEURONS OF HIPPOCAMPAL CA1 REGION, SYNAPSE 2: 382 (1988). (10.1002/syn.890020405) / SYNAPSE (1988)
LACAILLE, J.C., LOCAL CIRCUIT INTERACTIONS BETWEEN ORIENS-ALVEUS INTERNEURONS AND CA1 PYRAMIDAL CELLS IN HIPPOCAMPAL SLICES - ELECTROPHYSIOLOGY AND MORPHOLOGY, JOURNAL OF NEUROSCIENCE 7: 1979 (1987). (10.1523/JNEUROSCI.07-07-01979.1987) / JOURNAL OF NEUROSCIENCE (1987)
LI, X.G., AXONAL AND DENDRITIC ARBORIZATION OF AN INTRACELLULARLY LABELED CHANDELIER CELL IN THE CA1 REGION OF RAT HIPPOCAMPUS, EXPERIMENTAL BRAIN RESEARCH 90: 519 (1992). / EXPERIMENTAL BRAIN RESEARCH (1992)
LI, X.G., THE HIPPOCAMPAL CA3 NETWORK - AN IN-VIVO INTRACELLULAR LABELING STUDY, JOURNAL OF COMPARATIVE NEUROLOGY 339: 181 (1994). (10.1002/cne.903390204) / JOURNAL OF COMPARATIVE NEUROLOGY (1994)
LYTTON, W.W., SIMULATIONS OF CORTICAL PYRAMIDAL NEURONS SYNCHRONIZED BY INHIBITORY INTERNEURONS, JOURNAL OF NEUROPHYSIOLOGY 66: 1059 (1991). (10.1152/jn.1991.66.3.1059) / JOURNAL OF NEUROPHYSIOLOGY (1991)
NICOLL, R.A., FUNCTIONAL COMPARISON OF NEUROTRANSMITTER RECEPTOR SUBTYPES IN MAMMALIAN CENTRAL-NERVOUS-SYSTEM, PHYSIOLOGICAL REVIEWS 70: 513 (1990). (10.1152/physrev.1990.70.2.513) / PHYSIOLOGICAL REVIEWS (1990)
10.1073/pnas.88.24.11285
PULSINELLI, W.A., NEW MODEL OF BILATERAL HEMISPHERIC ISCHEMIA IN THE UNANESTHETIZED RAT, STROKE 10: 267 (1979). (10.1161/01.STR.10.3.267) / STROKE (1979)
10.1126/science.1720572
10.1126/science.8290963
SIK, A, COMPLETE AXON ARBORIZATION OF A SINGLE CA3 PYRAMIDAL CELL IN THE RAT HIPPOCAMPUS, AND ITS RELATIONSHIP WITH POSTSYNAPTIC PARVALBUMIN-CONTAINING INTERNEURONS, EUROPEAN JOURNAL OF NEUROSCIENCE 5: 1719 (1993). (10.1111/j.1460-9568.1993.tb00239.x) / EUROPEAN JOURNAL OF NEUROSCIENCE (1993)
SLOVITER, R.S., IMMUNOCYTOCHEMICAL LOCALIZATION OF GABA-, CHOLECYSTOKININ-LIKE, VASOACTIVE INTESTINAL POLYPEPTIDE-LIKE, AND SOMATOSTATIN-LIKE IMMUNOREACTIVITY IN THE AREA DENTATA AND HIPPOCAMPUS OF THE RAT, JOURNAL OF COMPARATIVE NEUROLOGY 256: 42 (1987). (10.1002/cne.902560105) / JOURNAL OF COMPARATIVE NEUROLOGY (1987)
10.1037/0033-295X.99.2.195
TAMAMAKI, N, 3-DIMENSIONAL ANALYSIS OF THE WHOLE AXONAL ARBORS ORIGINATING FROM SINGLE CA2 PYRAMIDAL NEURONS IN THE RAT HIPPOCAMPUS WITH THE AID OF A COMPUTER GRAPHIC TECHNIQUE, BRAIN RESEARCH 452: 255 (1988). (10.1016/0006-8993(88)90030-3) / BRAIN RESEARCH (1988)
TAMAMAKI, N, DISPOSITION OF THE SLAB-LIKE MODULES FORMED BY AXON BRANCHES ORIGINATING FROM SINGLE CA1 PYRAMIDAL NEURONS IN THE RAT HIPPOCAMPUS, JOURNAL OF COMPARATIVE NEUROLOGY 291: 509 (1990). (10.1002/cne.902910403) / JOURNAL OF COMPARATIVE NEUROLOGY (1990)
TAMAMAKI, N, CROSSING FIBER ARRAYS IN THE RAT HIPPOCAMPUS AS DEMONSTRATED BY 3-DIMENSIONAL RECONSTRUCTION, JOURNAL OF COMPARATIVE NEUROLOGY 303: 435 (1991). (10.1002/cne.903030309) / JOURNAL OF COMPARATIVE NEUROLOGY (1991)
VALTSCHANOFF, J.G., NEURONS IN RAT HIPPOCAMPUS THAT SYNTHESIZE NITRIC-OXIDE, JOURNAL OF COMPARATIVE NEUROLOGY 331: 111 (1993). (10.1002/cne.903310107) / JOURNAL OF COMPARATIVE NEUROLOGY (1993)
10.1016/0306-4522(92)90184-4
Ylinen, A., Journal of Neuroscience 15: 30 (1995). (10.1523/JNEUROSCI.15-01-00030.1995) / Journal of Neuroscience (1995)
YOUNG, H.M., COLOCALIZATION OF NITRIC-OXIDE SYNTHASE IMMUNOREACTIVITY AND NADPH DIAPHORASE STAINING IN NEURONS OF THE GUINEA-PIG INTESTINE, HISTOCHEMISTRY 97: 375 (1992). (10.1007/BF00270041) / HISTOCHEMISTRY (1992)
10.1126/science.8100368

Dates

Type	When
Created	18 years, 11 months ago (Oct. 5, 2006, 8:01 p.m.)
Deposited	1 year, 7 months ago (Jan. 14, 2024, 10:53 p.m.)
Indexed	1 day, 22 hours ago (Sept. 4, 2025, 9:59 a.m.)
Issued	30 years, 11 months ago (Sept. 16, 1994)
Published	30 years, 11 months ago (Sept. 16, 1994)
Published Print	30 years, 11 months ago (Sept. 16, 1994)

Funders 0

None

BibTeX

@article{Sik_1994, title={Inhibitory CA1-CA3-Hilar Region Feedback in the Hippocampus}, volume={265}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.8085161}, DOI={10.1126/science.8085161}, number={5179}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Sik, Attila and Ylinen, Aarne and Penttonen, Markku and Buzsáki, György}, year={1994}, month=sep, pages={1722–1724} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        9,
        4
      ]
    ],
    "date-time": "2025-09-04T13:59:43Z",
    "timestamp": 1756994383405
  },
  "reference-count": 42,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "5179",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1994,
        9,
        16
      ]
    ]
  },
  "abstract": "<jats:p>The organization of the hippocampus is generally thought of as a series of cell groups that form a unidirectionally excited chain, regulated by localized inhibitory circuits. With the use of in vivo intracellular labeling, histochemical, and extracellular tracing methods, a longitudinally widespread, inhibitory feedback in rat brain from the CA1 area to the CA3 and hilar regions was observed. This long-range, cross-regional inhibition may allow precise synchronization of population activity by timing the occurrence of action potentials in the principal cells and may contribute to the coordinated induction of synaptic plasticity in distributed networks.</jats:p>",
  "DOI": "10.1126/science.8085161",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        6
      ]
    ],
    "date-time": "2006-10-06T00:01:25Z",
    "timestamp": 1160092885000
  },
  "page": "1722-1724",
  "source": "Crossref",
  "is-referenced-by-count": 174,
  "title": "Inhibitory CA1-CA3-Hilar Region Feedback in the Hippocampus",
  "prefix": "10.1126",
  "volume": "265",
  "author": [
    {
      "given": "Attila",
      "family": "Sik",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark, NJ 07102."
        }
      ]
    },
    {
      "given": "Aarne",
      "family": "Ylinen",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark, NJ 07102."
        }
      ]
    },
    {
      "given": "Markku",
      "family": "Penttonen",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark, NJ 07102."
        }
      ]
    },
    {
      "given": "Gy\u00f6rgy",
      "family": "Buzs\u00e1ki",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark, NJ 07102."
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_2_1_1_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(89)90424-7"
    },
    {
      "key": "e_1_2_1_2_1",
      "first-page": "222",
      "volume": "13",
      "year": "1971",
      "unstructured": "ANDERSEN, P, LAMELLAR ORGANIZATION OF HIPPOCAMPAL EXCITATORY PATHWAYS, EXPERIMENTAL BRAIN RESEARCH 13: 222 (1971).",
      "journal-title": "EXPERIMENTAL BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_3_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0896-6273(92)90104-L"
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "crossref",
      "first-page": "349",
      "DOI": "10.1002/hipo.450020403",
      "volume": "2",
      "year": "1992",
      "unstructured": "BUCKMASTER, P.S., MOSSY CELL AXONAL PROJECTIONS TO THE DENTATE GYRUS MOLECULAR LAYER IN THE RAT HIPPOCAMPAL SLICE, HIPPOCAMPUS 2: 349 (1992).",
      "journal-title": "HIPPOCAMPUS"
    },
    {
      "key": "e_1_2_1_5_1",
      "doi-asserted-by": "crossref",
      "first-page": "823",
      "DOI": "10.1038/368823a0",
      "volume": "368",
      "year": "1994",
      "unstructured": "BUHL, E.H., DIVERSE SOURCES OF HIPPOCAMPAL UNITARY INHIBITORY POSTSYNAPTIC POTENTIALS AND THE NUMBER OF SYNAPTIC RELEASE SITES, NATURE 368: 823 (1994).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "crossref",
      "first-page": "609",
      "DOI": "10.1016/0306-4522(90)90055-9",
      "volume": "38",
      "year": "1990",
      "unstructured": "BULLOCK, T.H., COHERENCE OF COMPOUND FIELD POTENTIALS REVEALS DISCONTINUITIES IN THE CA1-SUBICULUM OF THE HIPPOCAMPUS IN FREELY-MOVING RATS, NEUROSCIENCE 38: 609 (1990).",
      "journal-title": "NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "crossref",
      "first-page": "334",
      "DOI": "10.1016/0006-8993(87)90632-9",
      "volume": "400",
      "year": "1987",
      "unstructured": "BUZSAKI, G, RESTORATION OF RHYTHMIC SLOW ACTIVITY (THETA) IN THE SUBCORTICALLY DENERVATED HIPPOCAMPUS BY FETAL CNS TRANSPLANTS, BRAIN RESEARCH 400: 334 (1987).",
      "journal-title": "BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_8_1",
      "doi-asserted-by": "crossref",
      "first-page": "163",
      "DOI": "10.1002/hipo.450010205",
      "volume": "1",
      "year": "1991",
      "unstructured": "BUZSAKI, G, HIPPOCAMPUS 1: 163 (1991).",
      "journal-title": "HIPPOCAMPUS"
    },
    {
      "key": "e_1_2_1_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(89)90423-5"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1589772"
    },
    {
      "key": "e_1_2_1_11_1",
      "doi-asserted-by": "crossref",
      "first-page": "453",
      "DOI": "10.1152/physrev.1990.70.2.453",
      "volume": "70",
      "year": "1990",
      "unstructured": "DASILVA, FHL, ANATOMIC ORGANIZATION AND PHYSIOLOGY OF THE LIMBIC CORTEX, PHYSIOLOGICAL REVIEWS 70: 453 (1990).",
      "journal-title": "PHYSIOLOGICAL REVIEWS"
    },
    {
      "key": "e_1_2_1_12_1",
      "doi-asserted-by": "crossref",
      "first-page": "283",
      "DOI": "10.1162/neco.1990.2.3.283",
      "volume": "2",
      "year": "1990",
      "unstructured": "Douglas, R. J., Neural Computation 2: 283 (1990).",
      "journal-title": "Neural Computation"
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "crossref",
      "first-page": "1670",
      "DOI": "10.1212/WNL.40.11.1670",
      "volume": "40",
      "year": "1990",
      "unstructured": "ENGEL, J, PRESURGICAL EVALUATION FOR PARTIAL EPILEPSY - RELATIVE CONTRIBUTIONS OF CHRONIC DEPTH-ELECTRODE RECORDINGS VERSUS FDG-PET AND SCALP-SPHENOIDAL ICTAL EEG, NEUROLOGY 40: 1670 (1990).",
      "journal-title": "NEUROLOGY"
    },
    {
      "key": "e_1_2_1_14_1",
      "doi-asserted-by": "crossref",
      "first-page": "1729",
      "DOI": "10.1111/j.1460-9568.1993.tb00240.x",
      "volume": "5",
      "year": "1993",
      "unstructured": "GULYAS, A.I., PRECISION AND VARIABILITY IN POSTSYNAPTIC TARGET SELECTION OF INHIBITORY CELLS IN THE HIPPOCAMPAL CA3 REGION, EUROPEAN JOURNAL OF NEUROSCIENCE 5: 1729 (1993).",
      "journal-title": "EUROPEAN JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_15_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/366683a0"
    },
    {
      "key": "e_1_2_1_16_1",
      "doi-asserted-by": "crossref",
      "first-page": "411",
      "DOI": "10.1111/j.1460-9568.1993.tb00508.x",
      "volume": "5",
      "year": "1993",
      "unstructured": "HALASY, K, SUBDIVISIONS IN THE MULTIPLE GABAERGIC INNERVATION OF GRANULE CELLS IN THE DENTATE GYRUS OF THE RAT HIPPOCAMPUS, EUROPEAN JOURNAL OF NEUROSCIENCE 5: 411 (1993).",
      "journal-title": "EUROPEAN JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_17_1",
      "doi-asserted-by": "crossref",
      "first-page": "395",
      "DOI": "10.1111/j.1460-9568.1993.tb00507.x",
      "volume": "5",
      "year": "1993",
      "unstructured": "HAN, Z.S., A HIGH-DEGREE OF SPATIAL SELECTIVITY IN THE AXONAL AND DENDRITIC DOMAINS OF PHYSIOLOGICALLY IDENTIFIED LOCAL-CIRCUIT NEURONS IN THE DENTATE GYRUS OF THE RAT HIPPOCAMPUS, EUROPEAN JOURNAL OF NEUROSCIENCE 5: 395 (1993).",
      "journal-title": "EUROPEAN JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_18_1",
      "doi-asserted-by": "crossref",
      "first-page": "69",
      "DOI": "10.1007/BF00250568",
      "volume": "77",
      "year": "1989",
      "unstructured": "HOLSHEIMER, J, PROPAGATION VELOCITY OF EPILEPTIFORM ACTIVITY IN THE HIPPOCAMPUS, EXPERIMENTAL BRAIN RESEARCH 77: 69 (1989).",
      "journal-title": "EXPERIMENTAL BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_19_1",
      "first-page": "1",
      "volume": "25",
      "year": "1988",
      "unstructured": "HORIKAWA, K, A VERSATILE MEANS OF INTRACELLULAR LABELING - INJECTION OF BIOCYTIN AND ITS DETECTION WITH AVIDIN CONJUGATES, JOURNAL OF NEUROSCIENCE METHODS 25: 1 (1988).",
      "journal-title": "JOURNAL OF NEUROSCIENCE METHODS"
    },
    {
      "key": "e_1_2_1_20_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ana.410200406"
    },
    {
      "key": "e_1_2_1_21_1",
      "doi-asserted-by": "crossref",
      "first-page": "369",
      "DOI": "10.1016/0006-8993(87)90921-8",
      "volume": "416",
      "year": "1987",
      "unstructured": "KAWAGUCHI, Y, FAST SPIKING CELLS IN RAT HIPPOCAMPUS (CA1 REGION) CONTAIN THE CALCIUM-BINDING PROTEIN PARVALBUMIN, BRAIN RESEARCH 416: 369 (1987).",
      "journal-title": "BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_22_1",
      "doi-asserted-by": "crossref",
      "first-page": "382",
      "DOI": "10.1002/syn.890020405",
      "volume": "2",
      "year": "1988",
      "unstructured": "KUNKEL, D.D., ULTRASTRUCTURE OF STRATUM LACUNOSUM-MOLECULARE INTERNEURONS OF HIPPOCAMPAL CA1 REGION, SYNAPSE 2: 382 (1988).",
      "journal-title": "SYNAPSE"
    },
    {
      "key": "e_1_2_1_23_1",
      "doi-asserted-by": "crossref",
      "first-page": "1979",
      "DOI": "10.1523/JNEUROSCI.07-07-01979.1987",
      "volume": "7",
      "year": "1987",
      "unstructured": "LACAILLE, J.C., LOCAL CIRCUIT INTERACTIONS BETWEEN ORIENS-ALVEUS INTERNEURONS AND CA1 PYRAMIDAL CELLS IN HIPPOCAMPAL SLICES - ELECTROPHYSIOLOGY AND MORPHOLOGY, JOURNAL OF NEUROSCIENCE 7: 1979 (1987).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_24_1",
      "first-page": "519",
      "volume": "90",
      "year": "1992",
      "unstructured": "LI, X.G., AXONAL AND DENDRITIC ARBORIZATION OF AN INTRACELLULARLY LABELED CHANDELIER CELL IN THE CA1 REGION OF RAT HIPPOCAMPUS, EXPERIMENTAL BRAIN RESEARCH 90: 519 (1992).",
      "journal-title": "EXPERIMENTAL BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_25_1",
      "doi-asserted-by": "crossref",
      "first-page": "181",
      "DOI": "10.1002/cne.903390204",
      "volume": "339",
      "year": "1994",
      "unstructured": "LI, X.G., THE HIPPOCAMPAL CA3 NETWORK - AN IN-VIVO INTRACELLULAR LABELING STUDY, JOURNAL OF COMPARATIVE NEUROLOGY 339: 181 (1994).",
      "journal-title": "JOURNAL OF COMPARATIVE NEUROLOGY"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "crossref",
      "first-page": "1059",
      "DOI": "10.1152/jn.1991.66.3.1059",
      "volume": "66",
      "year": "1991",
      "unstructured": "LYTTON, W.W., SIMULATIONS OF CORTICAL PYRAMIDAL NEURONS SYNCHRONIZED BY INHIBITORY INTERNEURONS, JOURNAL OF NEUROPHYSIOLOGY 66: 1059 (1991).",
      "journal-title": "JOURNAL OF NEUROPHYSIOLOGY"
    },
    {
      "key": "e_1_2_1_27_1",
      "doi-asserted-by": "crossref",
      "first-page": "513",
      "DOI": "10.1152/physrev.1990.70.2.513",
      "volume": "70",
      "year": "1990",
      "unstructured": "NICOLL, R.A., FUNCTIONAL COMPARISON OF NEUROTRANSMITTER RECEPTOR SUBTYPES IN MAMMALIAN CENTRAL-NERVOUS-SYSTEM, PHYSIOLOGICAL REVIEWS 70: 513 (1990).",
      "journal-title": "PHYSIOLOGICAL REVIEWS"
    },
    {
      "key": "e_1_2_1_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.88.24.11285"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "crossref",
      "first-page": "267",
      "DOI": "10.1161/01.STR.10.3.267",
      "volume": "10",
      "year": "1979",
      "unstructured": "PULSINELLI, W.A., NEW MODEL OF BILATERAL HEMISPHERIC ISCHEMIA IN THE UNANESTHETIZED RAT, STROKE 10: 267 (1979).",
      "journal-title": "STROKE"
    },
    {
      "key": "e_1_2_1_30_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1720572"
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8290963"
    },
    {
      "key": "e_1_2_1_32_1",
      "doi-asserted-by": "crossref",
      "first-page": "1719",
      "DOI": "10.1111/j.1460-9568.1993.tb00239.x",
      "volume": "5",
      "year": "1993",
      "unstructured": "SIK, A, COMPLETE AXON ARBORIZATION OF A SINGLE CA3 PYRAMIDAL CELL IN THE RAT HIPPOCAMPUS, AND ITS RELATIONSHIP WITH POSTSYNAPTIC PARVALBUMIN-CONTAINING INTERNEURONS, EUROPEAN JOURNAL OF NEUROSCIENCE 5: 1719 (1993).",
      "journal-title": "EUROPEAN JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_33_1",
      "doi-asserted-by": "crossref",
      "first-page": "42",
      "DOI": "10.1002/cne.902560105",
      "volume": "256",
      "year": "1987",
      "unstructured": "SLOVITER, R.S., IMMUNOCYTOCHEMICAL LOCALIZATION OF GABA-, CHOLECYSTOKININ-LIKE, VASOACTIVE INTESTINAL POLYPEPTIDE-LIKE, AND SOMATOSTATIN-LIKE IMMUNOREACTIVITY IN THE AREA DENTATA AND HIPPOCAMPUS OF THE RAT, JOURNAL OF COMPARATIVE NEUROLOGY 256: 42 (1987).",
      "journal-title": "JOURNAL OF COMPARATIVE NEUROLOGY"
    },
    {
      "key": "e_1_2_1_34_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1037/0033-295X.99.2.195"
    },
    {
      "key": "e_1_2_1_35_1",
      "doi-asserted-by": "crossref",
      "first-page": "255",
      "DOI": "10.1016/0006-8993(88)90030-3",
      "volume": "452",
      "year": "1988",
      "unstructured": "TAMAMAKI, N, 3-DIMENSIONAL ANALYSIS OF THE WHOLE AXONAL ARBORS ORIGINATING FROM SINGLE CA2 PYRAMIDAL NEURONS IN THE RAT HIPPOCAMPUS WITH THE AID OF A COMPUTER GRAPHIC TECHNIQUE, BRAIN RESEARCH 452: 255 (1988).",
      "journal-title": "BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_36_1",
      "doi-asserted-by": "crossref",
      "first-page": "509",
      "DOI": "10.1002/cne.902910403",
      "volume": "291",
      "year": "1990",
      "unstructured": "TAMAMAKI, N, DISPOSITION OF THE SLAB-LIKE MODULES FORMED BY AXON BRANCHES ORIGINATING FROM SINGLE CA1 PYRAMIDAL NEURONS IN THE RAT HIPPOCAMPUS, JOURNAL OF COMPARATIVE NEUROLOGY 291: 509 (1990).",
      "journal-title": "JOURNAL OF COMPARATIVE NEUROLOGY"
    },
    {
      "key": "e_1_2_1_37_1",
      "doi-asserted-by": "crossref",
      "first-page": "435",
      "DOI": "10.1002/cne.903030309",
      "volume": "303",
      "year": "1991",
      "unstructured": "TAMAMAKI, N, CROSSING FIBER ARRAYS IN THE RAT HIPPOCAMPUS AS DEMONSTRATED BY 3-DIMENSIONAL RECONSTRUCTION, JOURNAL OF COMPARATIVE NEUROLOGY 303: 435 (1991).",
      "journal-title": "JOURNAL OF COMPARATIVE NEUROLOGY"
    },
    {
      "key": "e_1_2_1_38_1",
      "doi-asserted-by": "crossref",
      "first-page": "111",
      "DOI": "10.1002/cne.903310107",
      "volume": "331",
      "year": "1993",
      "unstructured": "VALTSCHANOFF, J.G., NEURONS IN RAT HIPPOCAMPUS THAT SYNTHESIZE NITRIC-OXIDE, JOURNAL OF COMPARATIVE NEUROLOGY 331: 111 (1993).",
      "journal-title": "JOURNAL OF COMPARATIVE NEUROLOGY"
    },
    {
      "key": "e_1_2_1_39_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(92)90184-4"
    },
    {
      "key": "e_1_2_1_40_1",
      "doi-asserted-by": "crossref",
      "first-page": "30",
      "DOI": "10.1523/JNEUROSCI.15-01-00030.1995",
      "volume": "15",
      "year": "1995",
      "unstructured": "Ylinen, A., Journal of Neuroscience 15: 30 (1995).",
      "journal-title": "Journal of Neuroscience"
    },
    {
      "key": "e_1_2_1_41_1",
      "doi-asserted-by": "crossref",
      "first-page": "375",
      "DOI": "10.1007/BF00270041",
      "volume": "97",
      "year": "1992",
      "unstructured": "YOUNG, H.M., COLOCALIZATION OF NITRIC-OXIDE SYNTHASE IMMUNOREACTIVITY AND NADPH DIAPHORASE STAINING IN NEURONS OF THE GUINEA-PIG INTESTINE, HISTOCHEMISTRY 97: 375 (1992).",
      "journal-title": "HISTOCHEMISTRY"
    },
    {
      "key": "e_1_2_1_42_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8100368"
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.8085161",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        15
      ]
    ],
    "date-time": "2024-01-15T03:53:51Z",
    "timestamp": 1705290831000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.8085161"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1994,
        9,
        16
      ]
    ]
  },
  "references-count": 42,
  "journal-issue": {
    "issue": "5179",
    "published-print": {
      "date-parts": [
        [
          1994,
          9,
          16
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.8085161"
  ],
  "URL": "http://dx.doi.org/10.1126/science.8085161",
  "relation": {},
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        1994,
        9,
        16
      ]
    ]
  }
}