DOI: 10.1523/jneurosci.20-04-01597.2000. Tactile Coactivation-Induced Changes in Spatial Discrimination Performance

Tactile Coactivation-Induced Changes in Spatial Discrimination Performance

10.1523/jneurosci.20-04-01597.2000

Crossref journal-article

Society for Neuroscience

The Journal of Neuroscience (393)

Abstract

We studied coactivation-based cortical plasticity at a psychophysical level in humans. For induction of plasticity, we used a protocol of simultaneous pairing of tactile stimulation to follow as closely as possible the idea of Hebbian learning. We reported previously that a few hours of tactile coactivation resulted in selective and reversible reorganization of receptive fields and cortical maps of the hindpaw representation of the somatosensory cortex of adult rats (Godde et al., 1996). In the present study, simultaneous spatial two-point discrimination was tested on the tip of the right index finger in human subjects as a marker of plastic changes. After 2 hr of coactivation we found a significant improvement in discrimination performance that was reversible within 8 hr. Reduction of the duration of the coactivation protocol revealed that 30 min was not sufficient to drive plastic changes. Repeated application of coactivation over 3 consecutive days resulted in a delayed recovery indicating stabilization of the improvement over time. Perceptual changes were highly selective because no transfer of improved performance to fingers that were not stimulated was found. The results demonstrate the potential role of sensory input statistics (i.e., their probability of occurrence and spatiotemporal relationships) in the induction of cortical plasticity without involving cognitive factors such as attention or reinforcement.

Bibliography

Godde, B., Stauffenberg, B., Spengler, F., & Dinse, H. R. (2000). Tactile Coactivation-Induced Changes in Spatial Discrimination Performance. The Journal of Neuroscience, 20(4), 1597â1604.

Authors 4

Ben Godde (first)
Beate Stauffenberg (additional)
Friederike Spengler (additional)
Hubert R. Dinse (additional)

References 62 Referenced 180

10.1073/pnas.90.12.5718
10.1126/science.1529342
10.1016/S0028-3908(98)00068-9
10.1152/jn.1991.66.3.1048
10.1073/pnas.93.20.11219
10.1007/BF00332921
10.1016/S0306-4522(97)00064-X
10.1037/0735-7044.112.3.467
10.1016/S0304-3940(98)00948-3
10.1523/JNEUROSCI.19-16-06748.1999 / J Neurosci / Distinct functional types of associative long-term potentiation in neocortical and hippocampal pyramidal neurons. by Buonomano (1999)
10.1038/332444a0
{'key': '2023041302441802000_20.4.1597.12', 'first-page': '187', 'article-title': 'Plasticity of cortical motor output organization following deafferentation, cerebral lesions, and skill acquisition.', 'volume': '63', 'author': 'Cohen', 'year': '1993', 'journal-title': 'Adv Neurol'} / Adv Neurol / Plasticity of cortical motor output organization following deafferentation, cerebral lesions, and skill acquisition. by Cohen (1993)
10.1152/jn.1997.78.6.2889 / J Neurophysiol / Perceptual learning of spatial localization: specificity for orientation, position, and context. by Crist (1997)
10.1016/S0165-0173(96)00015-X
10.1523/JNEUROSCI.16-02-00861.1996
10.1523/JNEUROSCI.15-03-01631.1995
10.1073/pnas.90.5.2082
{'key': '2023041302441802000_20.4.1597.18', 'first-page': '159', 'article-title': 'Short-term functional plasticity of cortical and thalamic sensory representations and its implication for information processing.', 'volume': '73', 'author': 'Dinse', 'year': '1997', 'journal-title': 'Adv Neurol'} / Adv Neurol / Short-term functional plasticity of cortical and thalamic sensory representations and its implication for information processing. by Dinse (1997)
10.1016/S0928-4257(97)81437-4
10.1007/BF00241531 / Exp Brain Res / Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex. by Edeline (1994)
10.1126/science.270.5234.305
10.1007/s004220050349
Eurich CW Dinse HR Dicke U Godde B Schwegler H (1997) Coarse coding accounts for improvement of spatial discrimination after plastic reorganization in rats and humans. in Artificial neural networks, Proceedings of ICANN 1997, eds Gerstner W Germond A Hasler M Nicaud JD (Springer, New York), pp 55–60. (10.1007/BFb0020132)
10.1073/pnas.94.17.9428
10.1016/S0042-6989(96)00308-2
10.1523/JNEUROSCI.15-12-08083.1995
10.1126/science.282.5391.1117
10.1038/333367a0
10.1126/science.3749885
10.1097/00001756-199612200-00056
10.1146/annurev.psych.49.1.585
10.3758/BF03201438
Hebb DO (1949) The organization of behavior. (Wiley, New York).
Hinton GE McClelland JL Rumelhart DE (1986) Distributed representations. in Parallel distributed processing. Exploration in the microstructure of cognition, Vol I, Foundations, eds Feldman JA Hayes PJ Rumelhart DE (MIT, Cambridge, MA), pp 77–109.
10.1016/S0896-6273(00)80499-7
James W (1890) Psychology: brief course. (Harvard UP, Cambridge, MA).
10.1523/JNEUROSCI.19-20-09016.1999
10.1126/science.282.5391.1121
10.1073/pnas.96.14.7622
10.1073/pnas.88.11.4966
10.1126/science.279.5357.1714
10.1073/pnas.96.14.8200
10.1093/cercor/2.2.81
10.1007/s002210050700
10.1016/S0306-4522(97)00333-3
10.1515/REVNEURO.1998.9.3.213 / Rev Neurosci / Potential circuit mechanisms underlying concurrent thalamic and cortical plasticity. by Nicolelis (1998)
10.1038/33918
10.1093/brain/116.1.39
10.1007/BF00248353 / Exp Brain Res / Long-term enhancement of evoked potentials in cat somatosensory cortex produced by co-activation of the basal forebrain and cutaneous receptors. by Rasmusson (1988)
10.1152/jn.1992.67.5.1015 / J Neurophysiol / Progressive improvement in discriminative abilities in adult owl monkeys performing a tactile frequency discrimination task. by Recanzone (1992)
10.1152/jn.1992.67.5.1031 / J Neurophysiol / Topographic reorganization of the hand representation in cortical area 3b of owl monkeys trained in a frequency discrimination task. by Recanzone (1992)
10.1152/jn.1998.79.6.3216 / J Neurophysiol / Role of the basal forebrain cholinergic projection in somatosensory cortical plasticity. by Sachdev (1998)
10.1007/BF00962720
10.1007/s002210050263
10.1113/jphysiol.1995.sp020623
10.1016/0042-6989(94)00295-W
10.1523/JNEUROSCI.18-11-04417.1998
10.1152/jn.1998.80.6.3272 / J Neurophysiol / Response of anterior parietal cortex to different modes of same-site skin stimulation. by Tommerdahl (1998)
10.1038/378071a0
10.1146/annurev.ne.18.030195.001021
10.1007/BF00238525 / Exp Brain Res / Cooperative neural processes involved in stereoscopic acuity. by Westheimer (1979)
10.1523/JNEUROSCI.19-17-07578.1999

Dates

Type	When
Created	7 years, 5 months ago (April 3, 2018, 1:33 p.m.)
Deposited	2 years, 4 months ago (April 13, 2023, 9:11 a.m.)
Indexed	1 month ago (Aug. 6, 2025, 8:46 a.m.)
Issued	25 years, 6 months ago (Feb. 15, 2000)
Published	25 years, 6 months ago (Feb. 15, 2000)
Published Online	25 years, 6 months ago (Feb. 15, 2000)
Published Print	25 years, 6 months ago (Feb. 15, 2000)

Funders 0

None

BibTeX

@article{Godde_2000, title={Tactile Coactivation-Induced Changes in Spatial Discrimination Performance}, volume={20}, ISSN={1529-2401}, url={http://dx.doi.org/10.1523/jneurosci.20-04-01597.2000}, DOI={10.1523/jneurosci.20-04-01597.2000}, number={4}, journal={The Journal of Neuroscience}, publisher={Society for Neuroscience}, author={Godde, Ben and Stauffenberg, Beate and Spengler, Friederike and Dinse, Hubert R.}, year={2000}, month=feb, pages={1597–1604} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        6
      ]
    ],
    "date-time": "2025-08-06T12:46:10Z",
    "timestamp": 1754484370714
  },
  "reference-count": 62,
  "publisher": "Society for Neuroscience",
  "issue": "4",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2000,
            8,
            15
          ]
        ],
        "date-time": "2000-08-15T00:00:00Z",
        "timestamp": 966297600000
      },
      "content-version": "vor",
      "delay-in-days": 182,
      "URL": "https://creativecommons.org/licenses/by-nc-sa/4.0/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2000,
        2,
        15
      ]
    ]
  },
  "abstract": "<jats:p>We studied coactivation-based cortical plasticity at a psychophysical level in humans. For induction of plasticity, we used a protocol of simultaneous pairing of tactile stimulation to follow as closely as possible the idea of Hebbian learning. We reported previously that a few hours of tactile coactivation resulted in selective and reversible reorganization of receptive fields and cortical maps of the hindpaw representation of the somatosensory cortex of adult rats (Godde et al., 1996). In the present study, simultaneous spatial two-point discrimination was tested on the tip of the right index finger in human subjects as a marker of plastic changes. After 2 hr of coactivation we found a significant improvement in discrimination performance that was reversible within 8 hr. Reduction of the duration of the coactivation protocol revealed that 30 min was not sufficient to drive plastic changes. Repeated application of coactivation over 3 consecutive days resulted in a delayed recovery indicating stabilization of the improvement over time. Perceptual changes were highly selective because no transfer of improved performance to fingers that were not stimulated was found. The results demonstrate the potential role of sensory input statistics (i.e., their probability of occurrence and spatiotemporal relationships) in the induction of cortical plasticity without involving cognitive factors such as attention or reinforcement.</jats:p>",
  "DOI": "10.1523/jneurosci.20-04-01597.2000",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2018,
        4,
        3
      ]
    ],
    "date-time": "2018-04-03T17:33:19Z",
    "timestamp": 1522776799000
  },
  "page": "1597-1604",
  "source": "Crossref",
  "is-referenced-by-count": 180,
  "title": "Tactile Coactivation-Induced Changes in Spatial Discrimination Performance",
  "prefix": "10.1523",
  "volume": "20",
  "author": [
    {
      "given": "Ben",
      "family": "Godde",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Beate",
      "family": "Stauffenberg",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Friederike",
      "family": "Spengler",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Hubert R.",
      "family": "Dinse",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "393",
  "published-online": {
    "date-parts": [
      [
        2000,
        2,
        15
      ]
    ]
  },
  "reference": [
    {
      "key": "2023041302441802000_20.4.1597.1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.90.12.5718"
    },
    {
      "key": "2023041302441802000_20.4.1597.2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1529342"
    },
    {
      "key": "2023041302441802000_20.4.1597.3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0028-3908(98)00068-9"
    },
    {
      "key": "2023041302441802000_20.4.1597.4",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.1991.66.3.1048"
    },
    {
      "key": "2023041302441802000_20.4.1597.5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.93.20.11219"
    },
    {
      "key": "2023041302441802000_20.4.1597.6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00332921"
    },
    {
      "key": "2023041302441802000_20.4.1597.7",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0306-4522(97)00064-X"
    },
    {
      "key": "2023041302441802000_20.4.1597.8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1037/0735-7044.112.3.467"
    },
    {
      "key": "2023041302441802000_20.4.1597.9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0304-3940(98)00948-3"
    },
    {
      "key": "2023041302441802000_20.4.1597.10",
      "doi-asserted-by": "crossref",
      "first-page": "6748",
      "DOI": "10.1523/JNEUROSCI.19-16-06748.1999",
      "article-title": "Distinct functional types of associative long-term potentiation in neocortical and hippocampal pyramidal neurons.",
      "volume": "19",
      "author": "Buonomano",
      "year": "1999",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041302441802000_20.4.1597.11",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/332444a0"
    },
    {
      "key": "2023041302441802000_20.4.1597.12",
      "first-page": "187",
      "article-title": "Plasticity of cortical motor output organization following deafferentation, cerebral lesions, and skill acquisition.",
      "volume": "63",
      "author": "Cohen",
      "year": "1993",
      "journal-title": "Adv Neurol"
    },
    {
      "key": "2023041302441802000_20.4.1597.13",
      "doi-asserted-by": "crossref",
      "first-page": "2889",
      "DOI": "10.1152/jn.1997.78.6.2889",
      "article-title": "Perceptual learning of spatial localization: specificity for orientation, position, and context.",
      "volume": "78",
      "author": "Crist",
      "year": "1997",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "2023041302441802000_20.4.1597.14",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0165-0173(96)00015-X"
    },
    {
      "key": "2023041302441802000_20.4.1597.15",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.16-02-00861.1996"
    },
    {
      "key": "2023041302441802000_20.4.1597.16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.15-03-01631.1995"
    },
    {
      "key": "2023041302441802000_20.4.1597.17",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.90.5.2082"
    },
    {
      "key": "2023041302441802000_20.4.1597.18",
      "first-page": "159",
      "article-title": "Short-term functional plasticity of cortical and thalamic sensory representations and its implication for information processing.",
      "volume": "73",
      "author": "Dinse",
      "year": "1997",
      "journal-title": "Adv Neurol"
    },
    {
      "key": "2023041302441802000_20.4.1597.19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0928-4257(97)81437-4"
    },
    {
      "key": "2023041302441802000_20.4.1597.20",
      "doi-asserted-by": "crossref",
      "first-page": "373",
      "DOI": "10.1007/BF00241531",
      "article-title": "Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex.",
      "volume": "97",
      "author": "Edeline",
      "year": "1994",
      "journal-title": "Exp Brain Res"
    },
    {
      "key": "2023041302441802000_20.4.1597.21",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.270.5234.305"
    },
    {
      "key": "2023041302441802000_20.4.1597.22",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s004220050349"
    },
    {
      "key": "2023041302441802000_20.4.1597.23",
      "doi-asserted-by": "crossref",
      "unstructured": "Eurich CW Dinse HR Dicke U Godde B Schwegler H (1997) Coarse coding accounts for improvement of spatial discrimination after plastic reorganization in rats and humans. in Artificial neural networks, Proceedings of ICANN 1997, eds Gerstner W Germond A Hasler M Nicaud JD (Springer, New York), pp 55\u201360.",
      "DOI": "10.1007/BFb0020132"
    },
    {
      "key": "2023041302441802000_20.4.1597.24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.94.17.9428"
    },
    {
      "key": "2023041302441802000_20.4.1597.25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0042-6989(96)00308-2"
    },
    {
      "key": "2023041302441802000_20.4.1597.26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.15-12-08083.1995"
    },
    {
      "key": "2023041302441802000_20.4.1597.27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.282.5391.1117"
    },
    {
      "key": "2023041302441802000_20.4.1597.28",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/333367a0"
    },
    {
      "key": "2023041302441802000_20.4.1597.29",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3749885"
    },
    {
      "key": "2023041302441802000_20.4.1597.30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00001756-199612200-00056"
    },
    {
      "key": "2023041302441802000_20.4.1597.31",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.psych.49.1.585"
    },
    {
      "key": "2023041302441802000_20.4.1597.32",
      "doi-asserted-by": "publisher",
      "DOI": "10.3758/BF03201438"
    },
    {
      "key": "2023041302441802000_20.4.1597.33",
      "unstructured": "Hebb DO (1949) The organization of behavior. (Wiley, New York)."
    },
    {
      "key": "2023041302441802000_20.4.1597.34",
      "unstructured": "Hinton GE McClelland JL Rumelhart DE (1986) Distributed representations. in Parallel distributed processing. Exploration in the microstructure of cognition, Vol I, Foundations, eds Feldman JA Hayes PJ Rumelhart DE (MIT, Cambridge, MA), pp 77\u2013109."
    },
    {
      "key": "2023041302441802000_20.4.1597.35",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0896-6273(00)80499-7"
    },
    {
      "key": "2023041302441802000_20.4.1597.36",
      "unstructured": "James W (1890) Psychology: brief course. (Harvard UP, Cambridge, MA)."
    },
    {
      "key": "2023041302441802000_20.4.1597.37",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.19-20-09016.1999"
    },
    {
      "key": "2023041302441802000_20.4.1597.38",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.282.5391.1121"
    },
    {
      "key": "2023041302441802000_20.4.1597.39",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.96.14.7622"
    },
    {
      "key": "2023041302441802000_20.4.1597.40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.88.11.4966"
    },
    {
      "key": "2023041302441802000_20.4.1597.41",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.279.5357.1714"
    },
    {
      "key": "2023041302441802000_20.4.1597.42",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.96.14.8200"
    },
    {
      "key": "2023041302441802000_20.4.1597.43",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/cercor/2.2.81"
    },
    {
      "key": "2023041302441802000_20.4.1597.44",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s002210050700"
    },
    {
      "key": "2023041302441802000_20.4.1597.45",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0306-4522(97)00333-3"
    },
    {
      "key": "2023041302441802000_20.4.1597.46",
      "doi-asserted-by": "crossref",
      "first-page": "213",
      "DOI": "10.1515/REVNEURO.1998.9.3.213",
      "article-title": "Potential circuit mechanisms underlying concurrent thalamic and cortical plasticity.",
      "volume": "9",
      "author": "Nicolelis",
      "year": "1998",
      "journal-title": "Rev Neurosci"
    },
    {
      "key": "2023041302441802000_20.4.1597.47",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/33918"
    },
    {
      "key": "2023041302441802000_20.4.1597.48",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/brain/116.1.39"
    },
    {
      "key": "2023041302441802000_20.4.1597.49",
      "doi-asserted-by": "crossref",
      "first-page": "276",
      "DOI": "10.1007/BF00248353",
      "article-title": "Long-term enhancement of evoked potentials in cat somatosensory cortex produced by co-activation of the basal forebrain and cutaneous receptors.",
      "volume": "70",
      "author": "Rasmusson",
      "year": "1988",
      "journal-title": "Exp Brain Res"
    },
    {
      "key": "2023041302441802000_20.4.1597.50",
      "doi-asserted-by": "crossref",
      "first-page": "1015",
      "DOI": "10.1152/jn.1992.67.5.1015",
      "article-title": "Progressive improvement in discriminative abilities in adult owl monkeys performing a tactile frequency discrimination task.",
      "volume": "67",
      "author": "Recanzone",
      "year": "1992",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "2023041302441802000_20.4.1597.51",
      "doi-asserted-by": "crossref",
      "first-page": "1031",
      "DOI": "10.1152/jn.1992.67.5.1031",
      "article-title": "Topographic reorganization of the hand representation in cortical area 3b of owl monkeys trained in a frequency discrimination task.",
      "volume": "67",
      "author": "Recanzone",
      "year": "1992",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "2023041302441802000_20.4.1597.52",
      "doi-asserted-by": "crossref",
      "first-page": "3216",
      "DOI": "10.1152/jn.1998.79.6.3216",
      "article-title": "Role of the basal forebrain cholinergic projection in somatosensory cortical plasticity.",
      "volume": "79",
      "author": "Sachdev",
      "year": "1998",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "2023041302441802000_20.4.1597.53",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00962720"
    },
    {
      "key": "2023041302441802000_20.4.1597.54",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s002210050263"
    },
    {
      "key": "2023041302441802000_20.4.1597.55",
      "doi-asserted-by": "publisher",
      "DOI": "10.1113/jphysiol.1995.sp020623"
    },
    {
      "key": "2023041302441802000_20.4.1597.56",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0042-6989(94)00295-W"
    },
    {
      "key": "2023041302441802000_20.4.1597.57",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.18-11-04417.1998"
    },
    {
      "key": "2023041302441802000_20.4.1597.58",
      "doi-asserted-by": "crossref",
      "first-page": "3272",
      "DOI": "10.1152/jn.1998.80.6.3272",
      "article-title": "Response of anterior parietal cortex to different modes of same-site skin stimulation.",
      "volume": "80",
      "author": "Tommerdahl",
      "year": "1998",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "2023041302441802000_20.4.1597.59",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/378071a0"
    },
    {
      "key": "2023041302441802000_20.4.1597.60",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.ne.18.030195.001021"
    },
    {
      "key": "2023041302441802000_20.4.1597.61",
      "doi-asserted-by": "crossref",
      "first-page": "585",
      "DOI": "10.1007/BF00238525",
      "article-title": "Cooperative neural processes involved in stereoscopic acuity.",
      "volume": "36",
      "author": "Westheimer",
      "year": "1979",
      "journal-title": "Exp Brain Res"
    },
    {
      "key": "2023041302441802000_20.4.1597.62",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.19-17-07578.1999"
    }
  ],
  "container-title": "The Journal of Neuroscience",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://syndication.highwire.org/content/doi/10.1523/JNEUROSCI.20-04-01597.2000",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        4,
        13
      ]
    ],
    "date-time": "2023-04-13T13:11:01Z",
    "timestamp": 1681391461000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.jneurosci.org/lookup/doi/10.1523/JNEUROSCI.20-04-01597.2000"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2000,
        2,
        15
      ]
    ]
  },
  "references-count": 62,
  "journal-issue": {
    "issue": "4",
    "published-online": {
      "date-parts": [
        [
          2000,
          2,
          15
        ]
      ]
    },
    "published-print": {
      "date-parts": [
        [
          2000,
          2,
          15
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1523/JNEUROSCI.20-04-01597.2000"
  ],
  "URL": "http://dx.doi.org/10.1523/JNEUROSCI.20-04-01597.2000",
  "relation": {},
  "ISSN": [
    "0270-6474",
    "1529-2401"
  ],
  "subject": [],
  "container-title-short": "J. Neurosci.",
  "published": {
    "date-parts": [
      [
        2000,
        2,
        15
      ]
    ]
  }
}