DOI: 10.1002/cne.901860203. Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers

Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers

10.1002/cne.901860203

Crossref journal-article

Wiley

Journal of Comparative Neurology (311)

Abstract

AbstractSingle primary afferent myelinated fibers from cutaneous receptors of cat and monkey were functionally identified by recording from the spinal cord with micropipettes filled with horseradish peroxidase (HRP). Relatively slowly conducting fibers (< 40 m/sec) from high threshold mechanoreceptors (mechanical nociceptors) and two types of low threshold mechanoreceptor (D‐hair and field) were selected for staining. Iontophoresis of the HRP and subsequent histochemical reaction stained the axons recorded from and their collaterals, including terminations, for several millimeters. The termination patterns in the two species proved essentially identical. Ipsilaterally, the mechanical nociceptor fibers terminated principally in the dorsal horn's marginal zone and in the ventral parts of the nucleus proprius (lamina V in the cat). Some of these nociceptors also had terminals in the midline just dorsal to the central canal, contralaterally in the marginal zone, and at the base of the opposite nucleus proprius. In contrast, the D‐hair primary afferent axons terminated in the dorsal part of the nucleus proprius overlapping into the innermost portion of the substantia gelatinosa. The field receptor fibers terminated predominantly in the middle part of the nucleus proprius. These results suggest that there is a highly specialized central projection of primary afferent endings which is related to sensory function and not to fiber diameter. The marginal zone and most dorsal parts of the substantia gelatinosa receive direct projections from cutaneous nociceptors but do not have direct input from cutaneous receptors transmitting activity initiated by innocuous stimulation.

Bibliography

Light, A. R., & Perl, E. R. (1979). Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. Journal of Comparative Neurology, 186(2), 133â150. Portico.

Authors 2

A. R. Light (first)
E. R. Perl (additional)

References 60 Referenced 646

10.1016/0304-3940(75)90048-8
10.1016/0006-8993(74)90238-8
10.1002/cne.901680106
10.1152/jn.1977.40.2.199 / J. Neurophysiol. / Spinal cord potentials evoked by cutaneous afferents in the monkey by Beall J. E. (1977)
10.1152/jn.1969.32.6.1025
10.1113/jphysiol.1978.sp012137
10.1113/jphysiol.1967.sp008390
10.1113/jphysiol.1977.sp012073
10.1113/jphysiol.1978.sp012257 / J. Physiol. (London) / Morphology and organization of axon collaterals from afferent fibres of slowly adapting Type I units in cat spinal cord by Brown A. G. (1978)
10.1113/jphysiol.1967.sp008227
{'key': 'e_1_2_1_12_1', 'first-page': '29', 'volume-title': 'Handbook of Sensory Physiology. Vol. 2, Somatosensory System', 'author': 'Burgess P. R.', 'year': '1973'} / Handbook of Sensory Physiology. Vol. 2, Somatosensory System by Burgess P. R. (1973)
10.1152/jn.1968.31.6.833
10.1109/C-M.1978.217983 / Computer / The neuroscience display processor by Capowski J. J. (1978)
10.1002/cne.901820111
10.1016/0304-3959(76)90042-7
10.1152/jn.1970.33.2.293
10.1016/0304-3940(76)90165-8
10.1016/0006-8993(77)90427-9
10.1002/cne.901810102
10.1007/BF01003075
10.1016/0006-8993(76)90603-X
10.1007/BF01740343 / Mitteilung. Pfluegers Arch. / Zur Kenntnis der Schmerzleitung im Rückenmark. II by Karplus I. P. (1925)
10.1002/cne.901000304
10.1016/0006-8993(76)90039-1
10.1016/B978-0-08-021208-1.50011-4 / Sensory Functions of the Skin in Primates by Kumazawa T. (1976)
{'key': 'e_1_2_1_27_1', 'first-page': '287', 'article-title': 'Primate cutaneous receptors with unmyelinated (C) fibres and their projection to the substantia gelatinosa', 'volume': '73', 'author': 'Kumazawa T.', 'year': '1977', 'journal-title': 'J. Physiol. (Paris)'} / J. Physiol. (Paris) / Primate cutaneous receptors with unmyelinated (C) fibres and their projection to the substantia gelatinosa by Kumazawa T. (1977)
10.1152/jn.1977.40.6.1325
10.1002/cne.901770305
10.1002/cne.901620102
10.1002/cne.901720308
10.1016/0014-4886(76)90159-X
{'key': 'e_1_2_1_33_1', 'first-page': '486', 'article-title': 'Central termination of identified cutaneous afferent units with fine myelinated fibers', 'volume': '3', 'author': 'Light A. R.', 'year': '1977', 'journal-title': 'Soc. Neurosci. Abstracts'} / Soc. Neurosci. Abstracts / Central termination of identified cutaneous afferent units with fine myelinated fibers by Light A. R. (1977)
10.1002/cne.901860202
10.1002/cne.901860204
10.1152/jn.1943.6.4.317
10.1152/jn.1950.13.1.39
Merzenich M. M.1968Some Observations on the Encoding of Somesthetic Stimuli by Receptor Populations in the Hairy Skin of Primates. Ph.D. dissertation Johns Hopkins University.
10.1016/0006-8993(78)90056-2
10.1001/archneurpsyc.1952.02320220092011 / Arch. Neurol. Psychiatr. / Role of gelatinous substance of spinal cord in the conduction of pain by Pearson A. A. (1952)
10.1113/jphysiol.1968.sp008576
{'key': 'e_1_2_1_42_1', 'first-page': '582', 'article-title': 'Nociception and the functional organization of dorsal marginal zone and substantia gelatinosa of the spinal cord', 'volume': '12', 'author': 'Perl E. R.', 'year': '1977', 'journal-title': 'Proc. Int. Union. Physiol. Sci.'} / Proc. Int. Union. Physiol. Sci. / Nociception and the functional organization of dorsal marginal zone and substantia gelatinosa of the spinal cord by Perl E. R. (1977)
10.1007/BF02138738
10.1016/0006-8993(74)90425-9
10.1002/cne.901840403
10.1002/cne.901840404
10.5962/bhl.title.48637 / Histologie du Système Nerveux de l'Homme et des Vertébrés by Ramón y Cajal S. (1909)
10.1002/cne.901720307
{'key': 'e_1_2_1_49_1', 'first-page': '269', 'article-title': 'The terminal arborization pattern of primary afferent fibers in the substantia gelatinosa of the spinal cord in the cat', 'volume': '73', 'author': 'Réthelyi M.', 'year': '1977', 'journal-title': 'J. Physiol. (Paris)'} / J. Physiol. (Paris) / The terminal arborization pattern of primary afferent fibers in the substantia gelatinosa of the spinal cord in the cat by Réthelyi M. (1977)
10.1007/BF00239033
10.1002/cne.901850403
10.1002/cne.900960303
10.1016/0006-8993(68)90256-4
10.1016/0006-8993(69)90258-3
10.1126/science.54936
10.1016/0006-8993(67)90144-8
10.1002/cne.901220207
10.1016/0006-8993(75)90518-1
10.1152/jn.1973.36.4.750 / J. Neurophysiol. / Location of cells of origin of spinothalamic tract in lumbar enlargement of the monkey by Trevino D. L. (1973)
{'key': 'e_1_2_1_60_1', 'volume-title': 'Pain: Its Mechanisms and Neurosurgical Control', 'author': 'White J. C.', 'year': '1955'} / Pain: Its Mechanisms and Neurosurgical Control by White J. C. (1955)
10.1152/jn.1974.37.2.358 / J. Neurophysiol. / Responses of primate spinothalamic tract nuerons to natural stimulation of hindlimb by Willis W. D. (1974)

Dates

Type	When
Created	20 years, 7 months ago (Jan. 1, 2005, 6:09 p.m.)
Deposited	1 year, 9 months ago (Nov. 12, 2023, 6 p.m.)
Indexed	1 month ago (July 19, 2025, 11:53 p.m.)
Issued	46 years, 1 month ago (July 15, 1979)
Published	46 years, 1 month ago (July 15, 1979)
Published Online	20 years, 10 months ago (Oct. 9, 2004)
Published Print	46 years, 1 month ago (July 15, 1979)

Funders 0

None

BibTeX

@article{Light_1979, title={Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers}, volume={186}, ISSN={1096-9861}, url={http://dx.doi.org/10.1002/cne.901860203}, DOI={10.1002/cne.901860203}, number={2}, journal={Journal of Comparative Neurology}, publisher={Wiley}, author={Light, A. R. and Perl, E. R.}, year={1979}, month=jul, pages={133–150} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        20
      ]
    ],
    "date-time": "2025-07-20T03:53:22Z",
    "timestamp": 1752983602922
  },
  "reference-count": 60,
  "publisher": "Wiley",
  "issue": "2",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2004,
            10,
            9
          ]
        ],
        "date-time": "2004-10-09T00:00:00Z",
        "timestamp": 1097280000000
      },
      "content-version": "vor",
      "delay-in-days": 9218,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1979,
        7,
        15
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>Single primary afferent myelinated fibers from cutaneous receptors of cat and monkey were functionally identified by recording from the spinal cord with micropipettes filled with horseradish peroxidase (HRP). Relatively slowly conducting fibers (&lt; 40 m/sec) from high threshold mechanoreceptors (mechanical nociceptors) and two types of low threshold mechanoreceptor (D\u2010hair and field) were selected for staining. Iontophoresis of the HRP and subsequent histochemical reaction stained the axons recorded from and their collaterals, including terminations, for several millimeters. The termination patterns in the two species proved essentially identical. Ipsilaterally, the mechanical nociceptor fibers terminated principally in the dorsal horn's marginal zone and in the ventral parts of the nucleus proprius (lamina V in the cat). Some of these nociceptors also had terminals in the midline just dorsal to the central canal, contralaterally in the marginal zone, and at the base of the opposite nucleus proprius. In contrast, the D\u2010hair primary afferent axons terminated in the dorsal part of the nucleus proprius overlapping into the innermost portion of the substantia gelatinosa. The field receptor fibers terminated predominantly in the middle part of the nucleus proprius. These results suggest that there is a highly specialized central projection of primary afferent endings which is related to sensory function and not to fiber diameter. The marginal zone and most dorsal parts of the substantia gelatinosa receive direct projections from cutaneous nociceptors but do not have direct input from cutaneous receptors transmitting activity initiated by innocuous stimulation.</jats:p>",
  "DOI": "10.1002/cne.901860203",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2005,
        1,
        1
      ]
    ],
    "date-time": "2005-01-01T23:09:25Z",
    "timestamp": 1104620965000
  },
  "page": "133-150",
  "source": "Crossref",
  "is-referenced-by-count": 646,
  "title": "Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers",
  "prefix": "10.1002",
  "volume": "186",
  "author": [
    {
      "given": "A. R.",
      "family": "Light",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "E. R.",
      "family": "Perl",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2004,
        10,
        9
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_1_2_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(75)90048-8"
    },
    {
      "key": "e_1_2_1_3_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(74)90238-8"
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901680106"
    },
    {
      "key": "e_1_2_1_5_1",
      "doi-asserted-by": "crossref",
      "first-page": "199",
      "DOI": "10.1152/jn.1977.40.2.199",
      "article-title": "Spinal cord potentials evoked by cutaneous afferents in the monkey",
      "volume": "40",
      "author": "Beall J. E.",
      "year": "1977",
      "journal-title": "J. Neurophysiol."
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.1969.32.6.1025"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1113/jphysiol.1978.sp012137"
    },
    {
      "key": "e_1_2_1_8_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1113/jphysiol.1967.sp008390"
    },
    {
      "key": "e_1_2_1_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1113/jphysiol.1977.sp012073"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "crossref",
      "first-page": "15",
      "DOI": "10.1113/jphysiol.1978.sp012257",
      "article-title": "Morphology and organization of axon collaterals from afferent fibres of slowly adapting Type I units in cat spinal cord",
      "volume": "277",
      "author": "Brown A. G.",
      "year": "1978",
      "journal-title": "J. Physiol. (London)"
    },
    {
      "key": "e_1_2_1_11_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1113/jphysiol.1967.sp008227"
    },
    {
      "key": "e_1_2_1_12_1",
      "first-page": "29",
      "volume-title": "Handbook of Sensory Physiology. Vol. 2, Somatosensory System",
      "author": "Burgess P. R.",
      "year": "1973"
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.1968.31.6.833"
    },
    {
      "key": "e_1_2_1_14_1",
      "doi-asserted-by": "crossref",
      "first-page": "45",
      "DOI": "10.1109/C-M.1978.217983",
      "article-title": "The neuroscience display processor",
      "volume": "11",
      "author": "Capowski J. J.",
      "year": "1978",
      "journal-title": "Computer"
    },
    {
      "key": "e_1_2_1_15_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901820111"
    },
    {
      "key": "e_1_2_1_16_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3959(76)90042-7"
    },
    {
      "key": "e_1_2_1_17_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.1970.33.2.293"
    },
    {
      "key": "e_1_2_1_18_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(76)90165-8"
    },
    {
      "key": "e_1_2_1_19_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(77)90427-9"
    },
    {
      "key": "e_1_2_1_20_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901810102"
    },
    {
      "key": "e_1_2_1_21_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF01003075"
    },
    {
      "key": "e_1_2_1_22_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(76)90603-X"
    },
    {
      "key": "e_1_2_1_23_1",
      "doi-asserted-by": "crossref",
      "first-page": "134",
      "DOI": "10.1007/BF01740343",
      "article-title": "Zur Kenntnis der Schmerzleitung im R\u00fcckenmark. II",
      "volume": "207",
      "author": "Karplus I. P.",
      "year": "1925",
      "journal-title": "Mitteilung. Pfluegers Arch."
    },
    {
      "key": "e_1_2_1_24_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901000304"
    },
    {
      "key": "e_1_2_1_25_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(76)90039-1"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "crossref",
      "first-page": "67",
      "DOI": "10.1016/B978-0-08-021208-1.50011-4",
      "volume-title": "Sensory Functions of the Skin in Primates",
      "author": "Kumazawa T.",
      "year": "1976"
    },
    {
      "key": "e_1_2_1_27_1",
      "first-page": "287",
      "article-title": "Primate cutaneous receptors with unmyelinated (C) fibres and their projection to the substantia gelatinosa",
      "volume": "73",
      "author": "Kumazawa T.",
      "year": "1977",
      "journal-title": "J. Physiol. (Paris)"
    },
    {
      "key": "e_1_2_1_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.1977.40.6.1325"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901770305"
    },
    {
      "key": "e_1_2_1_30_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901620102"
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901720308"
    },
    {
      "key": "e_1_2_1_32_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-4886(76)90159-X"
    },
    {
      "key": "e_1_2_1_33_1",
      "first-page": "486",
      "article-title": "Central termination of identified cutaneous afferent units with fine myelinated fibers",
      "volume": "3",
      "author": "Light A. R.",
      "year": "1977",
      "journal-title": "Soc. Neurosci. Abstracts"
    },
    {
      "key": "e_1_2_1_34_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901860202"
    },
    {
      "key": "e_1_2_1_35_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901860204"
    },
    {
      "key": "e_1_2_1_36_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.1943.6.4.317"
    },
    {
      "key": "e_1_2_1_37_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.1950.13.1.39"
    },
    {
      "key": "e_1_2_1_38_1",
      "unstructured": "Merzenich M. M.1968Some Observations on the Encoding of Somesthetic Stimuli by Receptor Populations in the Hairy Skin of Primates. Ph.D. dissertation Johns Hopkins University."
    },
    {
      "key": "e_1_2_1_39_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(78)90056-2"
    },
    {
      "key": "e_1_2_1_40_1",
      "doi-asserted-by": "crossref",
      "first-page": "515",
      "DOI": "10.1001/archneurpsyc.1952.02320220092011",
      "article-title": "Role of gelatinous substance of spinal cord in the conduction of pain",
      "volume": "68",
      "author": "Pearson A. A.",
      "year": "1952",
      "journal-title": "Arch. Neurol. Psychiatr."
    },
    {
      "key": "e_1_2_1_41_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1113/jphysiol.1968.sp008576"
    },
    {
      "key": "e_1_2_1_42_1",
      "first-page": "582",
      "article-title": "Nociception and the functional organization of dorsal marginal zone and substantia gelatinosa of the spinal cord",
      "volume": "12",
      "author": "Perl E. R.",
      "year": "1977",
      "journal-title": "Proc. Int. Union. Physiol. Sci."
    },
    {
      "key": "e_1_2_1_43_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF02138738"
    },
    {
      "key": "e_1_2_1_44_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(74)90425-9"
    },
    {
      "key": "e_1_2_1_45_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901840403"
    },
    {
      "key": "e_1_2_1_46_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901840404"
    },
    {
      "key": "e_1_2_1_47_1",
      "doi-asserted-by": "crossref",
      "DOI": "10.5962/bhl.title.48637",
      "volume-title": "Histologie du Syst\u00e8me Nerveux de l'Homme et des Vert\u00e9br\u00e9s",
      "author": "Ram\u00f3n y Cajal S.",
      "year": "1909"
    },
    {
      "key": "e_1_2_1_48_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901720307"
    },
    {
      "key": "e_1_2_1_49_1",
      "first-page": "269",
      "article-title": "The terminal arborization pattern of primary afferent fibers in the substantia gelatinosa of the spinal cord in the cat",
      "volume": "73",
      "author": "R\u00e9thelyi M.",
      "year": "1977",
      "journal-title": "J. Physiol. (Paris)"
    },
    {
      "key": "e_1_2_1_50_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00239033"
    },
    {
      "key": "e_1_2_1_51_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901850403"
    },
    {
      "key": "e_1_2_1_52_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.900960303"
    },
    {
      "key": "e_1_2_1_53_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(68)90256-4"
    },
    {
      "key": "e_1_2_1_54_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(69)90258-3"
    },
    {
      "key": "e_1_2_1_55_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.54936"
    },
    {
      "key": "e_1_2_1_56_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(67)90144-8"
    },
    {
      "key": "e_1_2_1_57_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.901220207"
    },
    {
      "key": "e_1_2_1_58_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(75)90518-1"
    },
    {
      "key": "e_1_2_1_59_1",
      "doi-asserted-by": "crossref",
      "first-page": "750",
      "DOI": "10.1152/jn.1973.36.4.750",
      "article-title": "Location of cells of origin of spinothalamic tract in lumbar enlargement of the monkey",
      "volume": "36",
      "author": "Trevino D. L.",
      "year": "1973",
      "journal-title": "J. Neurophysiol."
    },
    {
      "key": "e_1_2_1_60_1",
      "volume-title": "Pain: Its Mechanisms and Neurosurgical Control",
      "author": "White J. C.",
      "year": "1955"
    },
    {
      "key": "e_1_2_1_61_1",
      "doi-asserted-by": "crossref",
      "first-page": "358",
      "DOI": "10.1152/jn.1974.37.2.358",
      "article-title": "Responses of primate spinothalamic tract nuerons to natural stimulation of hindlimb",
      "volume": "37",
      "author": "Willis W. D.",
      "year": "1974",
      "journal-title": "J. Neurophysiol."
    }
  ],
  "container-title": "Journal of Comparative Neurology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1002%2Fcne.901860203",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1002/cne.901860203",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        11,
        12
      ]
    ],
    "date-time": "2023-11-12T23:00:37Z",
    "timestamp": 1699830037000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1002/cne.901860203"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1979,
        7,
        15
      ]
    ]
  },
  "references-count": 60,
  "journal-issue": {
    "issue": "2",
    "published-print": {
      "date-parts": [
        [
          1979,
          7,
          15
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1002/cne.901860203"
  ],
  "URL": "http://dx.doi.org/10.1002/cne.901860203",
  "relation": {},
  "ISSN": [
    "0021-9967",
    "1096-9861"
  ],
  "subject": [],
  "container-title-short": "J of Comparative Neurology",
  "published": {
    "date-parts": [
      [
        1979,
        7,
        15
      ]
    ]
  }
}