---
_id: '8914'
abstract:
- lang: eng
  text: Amyotrophic lateral sclerosis (ALS) leads to a loss of specific motor neuron
    populations in the spinal cord and cortex. Emerging evidence suggests that interneurons
    may also be affected, but a detailed characterization of interneuron loss and
    its potential impacts on motor neuron loss and disease progression is lacking.
    To examine this issue, the fate of V1 inhibitory neurons during ALS was assessed
    in the ventral spinal cord using the SODG93A mouse model. The V1 population makes
    up ∼30% of all ventral inhibitory neurons, ∼50% of direct inhibitory synaptic
    contacts onto motor neuron cell bodies, and is thought to play a key role in modulating
    motor output, in part through recurrent and reciprocal inhibitory circuits. We
    find that approximately half of V1 inhibitory neurons are lost in SODG93A mice
    at late disease stages, but that this loss is delayed relative to the loss of
    motor neurons and V2a excitatory neurons. We further identify V1 subpopulations
    based on transcription factor expression that are differentially susceptible to
    degeneration in SODG93A mice. At an early disease stage, we show that V1 synaptic
    contacts with motor neuron cell bodies increase, suggesting an upregulation of
    inhibition before V1 neurons are lost in substantial numbers. These data support
    a model in which progressive changes in V1 synaptic contacts early in disease,
    and in select V1 subpopulations at later stages, represent a compensatory upregulation
    and then deleterious breakdown of specific interneuron circuits within the spinal
    cord.
acknowledgement: This work was made possible by the generous support of Project ALS.
  Imaging and related analyses were facilitated by The Waitt Advanced Biophotonics
  Center Core at the Salk Institute, supported by grants from NIH-NCI CCSG (P30 014195)
  and NINDS Neuroscience Center (NS072031). The authors would like to additionally
  thank Drs. Jane Dodd, Robert Brownstone, and Laskaro Zagoraiou for helpful comments
  on the manuscript. This manuscript is dedicated to Tom Jessell, an inspirational
  scientist, friend and mentor.
article_processing_charge: Yes (via OA deal)
article_type: original
author:
- first_name: Alina
  full_name: Salamatina, Alina
  last_name: Salamatina
- first_name: Jerry H
  full_name: Yang, Jerry H
  last_name: Yang
- first_name: Susan
  full_name: Brenner-Morton, Susan
  last_name: Brenner-Morton
- first_name: 'Jay B '
  full_name: 'Bikoff, Jay B '
  last_name: Bikoff
- first_name: Linjing
  full_name: Fang, Linjing
  last_name: Fang
- first_name: Christopher R
  full_name: Kintner, Christopher R
  last_name: Kintner
- first_name: Thomas M
  full_name: Jessell, Thomas M
  last_name: Jessell
- first_name: Lora Beatrice Jaeger
  full_name: Sweeney, Lora Beatrice Jaeger
  id: 56BE8254-C4F0-11E9-8E45-0B23E6697425
  last_name: Sweeney
  orcid: 0000-0001-9242-5601
citation:
  ama: Salamatina A, Yang JH, Brenner-Morton S, et al. Differential loss of spinal
    interneurons in a mouse model of ALS. <i>Neuroscience</i>. 2020;450:81-95. doi:<a
    href="https://doi.org/10.1016/j.neuroscience.2020.08.011">10.1016/j.neuroscience.2020.08.011</a>
  apa: Salamatina, A., Yang, J. H., Brenner-Morton, S., Bikoff, J. B., Fang, L., Kintner,
    C. R., … Sweeney, L. B. (2020). Differential loss of spinal interneurons in a
    mouse model of ALS. <i>Neuroscience</i>. Elsevier. <a href="https://doi.org/10.1016/j.neuroscience.2020.08.011">https://doi.org/10.1016/j.neuroscience.2020.08.011</a>
  chicago: Salamatina, Alina, Jerry H Yang, Susan Brenner-Morton, Jay B  Bikoff, Linjing
    Fang, Christopher R Kintner, Thomas M Jessell, and Lora B. Sweeney. “Differential
    Loss of Spinal Interneurons in a Mouse Model of ALS.” <i>Neuroscience</i>. Elsevier,
    2020. <a href="https://doi.org/10.1016/j.neuroscience.2020.08.011">https://doi.org/10.1016/j.neuroscience.2020.08.011</a>.
  ieee: A. Salamatina <i>et al.</i>, “Differential loss of spinal interneurons in
    a mouse model of ALS,” <i>Neuroscience</i>, vol. 450. Elsevier, pp. 81–95, 2020.
  ista: Salamatina A, Yang JH, Brenner-Morton S, Bikoff JB, Fang L, Kintner CR, Jessell
    TM, Sweeney LB. 2020. Differential loss of spinal interneurons in a mouse model
    of ALS. Neuroscience. 450, 81–95.
  mla: Salamatina, Alina, et al. “Differential Loss of Spinal Interneurons in a Mouse
    Model of ALS.” <i>Neuroscience</i>, vol. 450, Elsevier, 2020, pp. 81–95, doi:<a
    href="https://doi.org/10.1016/j.neuroscience.2020.08.011">10.1016/j.neuroscience.2020.08.011</a>.
  short: A. Salamatina, J.H. Yang, S. Brenner-Morton, J.B. Bikoff, L. Fang, C.R. Kintner,
    T.M. Jessell, L.B. Sweeney, Neuroscience 450 (2020) 81–95.
date_created: 2020-12-03T11:47:31Z
date_published: 2020-12-01T00:00:00Z
date_updated: 2024-01-31T10:15:34Z
day: '01'
ddc:
- '570'
department:
- _id: LoSw
doi: 10.1016/j.neuroscience.2020.08.011
external_id:
  isi:
  - '000595588700008'
  pmid:
  - '32858144'
file:
- access_level: open_access
  checksum: da7413c819e079720669c82451b49294
  content_type: application/pdf
  creator: dernst
  date_created: 2020-12-03T11:45:26Z
  date_updated: 2020-12-03T11:45:26Z
  file_id: '8915'
  file_name: 2020_Neuroscience_Salamatina.pdf
  file_size: 4071247
  relation: main_file
  success: 1
file_date_updated: 2020-12-03T11:45:26Z
has_accepted_license: '1'
intvolume: '       450'
isi: 1
language:
- iso: eng
license: https://creativecommons.org/licenses/by-nc-nd/4.0/
month: '12'
oa: 1
oa_version: Published Version
page: 81-95
pmid: 1
publication: Neuroscience
publication_identifier:
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
quality_controlled: '1'
scopus_import: '1'
status: public
title: Differential loss of spinal interneurons in a mouse model of ALS
tmp:
  image: /images/cc_by_nc_nd.png
  legal_code_url: https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode
  name: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
    (CC BY-NC-ND 4.0)
  short: CC BY-NC-ND (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 450
year: '2020'
...
---
_id: '2605'
abstract:
- lang: eng
  text: 'The granular layer of the cerebellar cortex consists of densely packed neuronal
    cells, classified into granule cells and large interneurons. In this study, we
    provide a comparative survey of large granular layer interneurons in the adult
    rat cerebellum based on both morphological and neurochemical criteria. To this
    end, double immunofluorescence histochemistry was performed by combining antibodies
    against the cytoplasmic antigen Rat-303, calretinin, the metabotropic glutamate
    receptor mGluR2 and somatostatin. Based on Rat-303/calretinin double immunohistochemistry,
    three distinct populations of large granular layer interneurons could be discerned:
    cells immunopositive for Rat-303, calretinin or both. Rat-303 or calretinin single-labeled
    cells represented Golgi cells and unipolar brush cells, respectively. Rat-303/calretinin
    double-labeled cells located just underneath the Purkinje cell layer represented
    Lugaro cells. Morphometrical analysis distinguished two populations of Rat-303-positive
    Golgi cells according to their location: vermis versus hemisphere. Immunostaining
    for the metabotropic glutamate receptor mGluR2 combined with Rat-303 or calretinin
    revealed that the majority of Golgi cells (about 90%) appeared to be mGluR2 positive.
    Lugaro cells were mGluR2 negative. In addition, a limited population of large
    polymorphous interneurons in the depth of the granular layer with morphological
    features resembling Golgi cells also displayed Rat-303/calretinin immunoreactivity
    and were mGluR2 negative. Double immunohistochemistry for Rat-303 and somatostatin
    revealed three populations of labeled cells in the depth of the granular layer.
    Besides double-labeled Golgi cells, Rat-303 or somatostatin single-labeled cells
    were present. Based on mGluR2/somatostatin and calretinin/somatostatin double
    immunostainings, Rat-303 single-labeled cells were found to correspond to Rat-303/calretinin-positive,
    mGluR2-negative Golgi-like cells, while the identity of somatostatin single-labeled
    cells remained unclear. The data presented in this article elaborate previous
    reports on the morphological and neurochemical differentiation of large interneurons
    in the rat cerebellar granular layer. In addition, they indicate that the current
    classification of these cells into Golgi cells, Lugaro cells and unipolar brush
    cells does not describe the observed neurochemical heterogeneity.'
article_processing_charge: No
article_type: original
author:
- first_name: Frederik
  full_name: Geurts, Frederik
  last_name: Geurts
- first_name: Jean
  full_name: Timmermans, Jean
  last_name: Timmermans
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
- first_name: Erik
  full_name: De Schutter, Erik
  last_name: De Schutter
citation:
  ama: Geurts F, Timmermans J, Shigemoto R, De Schutter E. Morphological and neurochemical
    differentiation of large granular layer interneurons in the adult rat cerebellum.
    <i>Neuroscience</i>. 2001;104(2):499-512. doi:<a href="https://doi.org/10.1016/S0306-4522(01)00058-6">10.1016/S0306-4522(01)00058-6</a>
  apa: Geurts, F., Timmermans, J., Shigemoto, R., &#38; De Schutter, E. (2001). Morphological
    and neurochemical differentiation of large granular layer interneurons in the
    adult rat cerebellum. <i>Neuroscience</i>. Elsevier. <a href="https://doi.org/10.1016/S0306-4522(01)00058-6">https://doi.org/10.1016/S0306-4522(01)00058-6</a>
  chicago: Geurts, Frederik, Jean Timmermans, Ryuichi Shigemoto, and Erik De Schutter.
    “Morphological and Neurochemical Differentiation of Large Granular Layer Interneurons
    in the Adult Rat Cerebellum.” <i>Neuroscience</i>. Elsevier, 2001. <a href="https://doi.org/10.1016/S0306-4522(01)00058-6">https://doi.org/10.1016/S0306-4522(01)00058-6</a>.
  ieee: F. Geurts, J. Timmermans, R. Shigemoto, and E. De Schutter, “Morphological
    and neurochemical differentiation of large granular layer interneurons in the
    adult rat cerebellum,” <i>Neuroscience</i>, vol. 104, no. 2. Elsevier, pp. 499–512,
    2001.
  ista: Geurts F, Timmermans J, Shigemoto R, De Schutter E. 2001. Morphological and
    neurochemical differentiation of large granular layer interneurons in the adult
    rat cerebellum. Neuroscience. 104(2), 499–512.
  mla: Geurts, Frederik, et al. “Morphological and Neurochemical Differentiation of
    Large Granular Layer Interneurons in the Adult Rat Cerebellum.” <i>Neuroscience</i>,
    vol. 104, no. 2, Elsevier, 2001, pp. 499–512, doi:<a href="https://doi.org/10.1016/S0306-4522(01)00058-6">10.1016/S0306-4522(01)00058-6</a>.
  short: F. Geurts, J. Timmermans, R. Shigemoto, E. De Schutter, Neuroscience 104
    (2001) 499–512.
date_created: 2018-12-11T11:58:38Z
date_published: 2001-05-10T00:00:00Z
date_updated: 2023-05-24T12:45:30Z
day: '10'
doi: 10.1016/S0306-4522(01)00058-6
extern: '1'
external_id:
  pmid:
  - '11377850'
intvolume: '       104'
issue: '2'
language:
- iso: eng
month: '05'
oa_version: None
page: 499 - 512
pmid: 1
publication: Neuroscience
publication_identifier:
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
publist_id: '4292'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Morphological and neurochemical differentiation of large granular layer interneurons
  in the adult rat cerebellum
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 104
year: '2001'
...
---
_id: '2608'
abstract:
- lang: eng
  text: The regulation of neurotransmitter receptors during synapse formation has
    been studied extensively at the neuromuscular junction, but little is known about
    the development of excitatory neurotransmitter receptors during synaptogenesis
    in central synapses. In this study we show qualitatively and quantitatively that
    a receptor undergoes changes in localisation on the surface of rat Purkinje cells
    during development in association with its excitatory synapses. The presence of
    mGluR1α at parallel and climbing fibre synapses on developing Purkinje cells was
    studied using high-resolution immunoelectron microscopy. Immunoreactivity for
    mGluR1α was detected from embryonic day 18 in Purkinje cells, and showed dramatic
    changes in its localisation with age. At early postnatal ages (P0 and P3), mGluR1α
    was found both in somata and stem dendrites but was not usually associated with
    synaptic contacts. At P7, mGluR1α became concentrated in somatic spines associated
    with climbing fibres and in the growing dendritic arborisation even before innervation
    by parallel fibres. During the second and third postnatal week, when spines and
    parallel fibre synapses were generated, mGluR1α became progressively concentrated
    in the molecular layer, particularly in the synaptic specialisations. As a result,
    during the fourth postnatal week, the pattern and level of mGluR1α expression
    became similar to the adult and mGluR1α appeared in high density in perisynaptic
    sites. Our results indicate that mGluR1α is present in the developing Purkinje
    cells prior to their innervation by climbing and parallel fibres and demonstrate
    that this receptor undergoes a dynamic and specific regulation during postnatal
    development in association with the establishment of synaptic inputs to Purkinje
    cell.
acknowledgement: öWe thank Drs. Paul Bolam, Ole Paulsen, Je¡ McIlhinney, Alfonso Faire¨n
  and Francisco Ciruela for reviewing a previous version of this manuscript and Mrs
  Alexandra Salewski for the English revision of the manuscript. We also want to thank
  Dr. Peter Somogyi for offering the facilities of the MRC Anatomical Neuropharmacology
  Unit to carry out part of this study. This work was supported by a Grant from the
  European Community (QLG3-CT-1999-00192 to R.L.) and the Spanish Ministry of Education
  (DGES PM 97-0082 to J.M.J.).
article_processing_charge: No
article_type: original
author:
- first_name: Guillermina
  full_name: López Bendito, Guillermina
  last_name: López Bendito
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
- first_name: Rafael
  full_name: Luján, Rafael
  last_name: Luján
- first_name: José
  full_name: Juíz, José
  last_name: Juíz
citation:
  ama: López Bendito G, Shigemoto R, Luján R, Juíz J. Developmental changes in the
    localisation of the mGluR1α subtype of metabotropic glutamate receptors in Purkinje
    cells. <i>Neuroscience</i>. 2001;105(2):413-429. doi:<a href="https://doi.org/10.1016/S0306-4522(01)00188-9">10.1016/S0306-4522(01)00188-9</a>
  apa: López Bendito, G., Shigemoto, R., Luján, R., &#38; Juíz, J. (2001). Developmental
    changes in the localisation of the mGluR1α subtype of metabotropic glutamate receptors
    in Purkinje cells. <i>Neuroscience</i>. Elsevier. <a href="https://doi.org/10.1016/S0306-4522(01)00188-9">https://doi.org/10.1016/S0306-4522(01)00188-9</a>
  chicago: López Bendito, Guillermina, Ryuichi Shigemoto, Rafael Luján, and José Juíz.
    “Developmental Changes in the Localisation of the MGluR1α Subtype of Metabotropic
    Glutamate Receptors in Purkinje Cells.” <i>Neuroscience</i>. Elsevier, 2001. <a
    href="https://doi.org/10.1016/S0306-4522(01)00188-9">https://doi.org/10.1016/S0306-4522(01)00188-9</a>.
  ieee: G. López Bendito, R. Shigemoto, R. Luján, and J. Juíz, “Developmental changes
    in the localisation of the mGluR1α subtype of metabotropic glutamate receptors
    in Purkinje cells,” <i>Neuroscience</i>, vol. 105, no. 2. Elsevier, pp. 413–429,
    2001.
  ista: López Bendito G, Shigemoto R, Luján R, Juíz J. 2001. Developmental changes
    in the localisation of the mGluR1α subtype of metabotropic glutamate receptors
    in Purkinje cells. Neuroscience. 105(2), 413–429.
  mla: López Bendito, Guillermina, et al. “Developmental Changes in the Localisation
    of the MGluR1α Subtype of Metabotropic Glutamate Receptors in Purkinje Cells.”
    <i>Neuroscience</i>, vol. 105, no. 2, Elsevier, 2001, pp. 413–29, doi:<a href="https://doi.org/10.1016/S0306-4522(01)00188-9">10.1016/S0306-4522(01)00188-9</a>.
  short: G. López Bendito, R. Shigemoto, R. Luján, J. Juíz, Neuroscience 105 (2001)
    413–429.
date_created: 2018-12-11T11:58:39Z
date_published: 2001-07-27T00:00:00Z
date_updated: 2023-05-24T09:31:48Z
day: '27'
doi: 10.1016/S0306-4522(01)00188-9
extern: '1'
external_id:
  pmid:
  - '11672608 '
intvolume: '       105'
issue: '2'
language:
- iso: eng
month: '07'
oa_version: None
page: 413 - 429
pmid: 1
publication: Neuroscience
publication_identifier:
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
publist_id: '4290'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Developmental changes in the localisation of the mGluR1α subtype of metabotropic
  glutamate receptors in Purkinje cells
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 105
year: '2001'
...
---
_id: '2609'
abstract:
- lang: eng
  text: 'The metabotropic glutamate receptors (mGluRs) have distinct distribution
    patterns in the CNS but subtypes within group I or group III mGluRs share similar
    ultrastructural localization relative to neurotransmitter release sites: group
    I mGluRs are concentrated in an annulus surrounding the edge of the postsynaptic
    density, whereas group III mGluRs are concentrated in the presynaptic active zone.
    One of the group II subtypes, mGluR2, is expressed in both pre- and postsynaptic
    elements, having no close association with synapses. In order to determine if
    such a distribution is common to another group II subtype, mGluR3, an antibody
    was raised against a carboxy-terminus of mGluR3 and used for light and electron
    microscopic immunohistochemistry in the mouse CNS. The antibody reacted strongly
    with mGluR3, but it also reacted, though only weakly, with mGluR2. Therefore,
    to examine mGluR3-selective distribution, we used mGluR2-deficient mice as well
    as wild-type mice. Strong immunoreactivity for mGluR3 was found in the cerebral
    cortex, striatum, dentate gyrus of the hippocampus, olfactory tubercle, lateral
    septal nucleus, lateral and basolateral amygdaloid nuclei, and nucleus of the
    lateral olfactory tract. Pre-embedding immunoperoxidase and immunogold methods
    revealed mGluR3 labeling in both presynaptic and postsynaptic elements, and also
    in glial profiles. Double labeling revealed that the vast majority of mGluR3 in
    presynaptic elements is not closely associated with glutamate and GABA release
    sites in the striatum and thalamus, respectively. However, in the spines of the
    dentate granule cells, the highest receptor density was found in perisynaptic
    sites (20% of immunogold particles within 60 nm from the edge of postsynaptic
    membrane specialization) followed by a decreasing receptor density away from the
    synapses (to ∼5% of particles per 60 nm). Furthermore, 19% of immunogold particles
    were located in asymmetrical postsynaptic specialization, indicating an association
    of mGluR3 to glutamatergic synapses. The present results indicate that the localization
    of mGluR3 is rather similar to that of group I mGluRs in the postsynaptic elements,
    suggesting a unique functional role of mGluR3 in glutamatergic neurotransmission
    in the CNS.'
acknowledgement: We are grateful to M. Yokoi and S. Nakanishi for kindly providing
  us with the mGluR2-de¢cient mice and F. Ferraguti for mGluR8b cDNA. The technical
  assistance of S. Doi and the photographic assistance of A. Uesugi are acknowledged.
  This work has been supported by research grants from the Ministry of Education,
  Sports, Culture, Science, and Technology of Japan.
article_processing_charge: No
article_type: original
author:
- first_name: Y
  full_name: Tamaru, Y
  last_name: Tamaru
- first_name: Sakashi
  full_name: Nomura, Sakashi
  last_name: Nomura
- first_name: Noboru
  full_name: Mizuno, Noboru
  last_name: Mizuno
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
citation:
  ama: 'Tamaru Y, Nomura S, Mizuno N, Shigemoto R. Distribution of metabotropic glutamate
    receptor mGluR3 in the mouse CNS: Differential location relative to pre- and postsynaptic
    sites. <i>Neuroscience</i>. 2001;106(3):481-503. doi:<a href="https://doi.org/10.1016/S0306-4522(01)00305-0">10.1016/S0306-4522(01)00305-0</a>'
  apa: 'Tamaru, Y., Nomura, S., Mizuno, N., &#38; Shigemoto, R. (2001). Distribution
    of metabotropic glutamate receptor mGluR3 in the mouse CNS: Differential location
    relative to pre- and postsynaptic sites. <i>Neuroscience</i>. Elsevier. <a href="https://doi.org/10.1016/S0306-4522(01)00305-0">https://doi.org/10.1016/S0306-4522(01)00305-0</a>'
  chicago: 'Tamaru, Y, Sakashi Nomura, Noboru Mizuno, and Ryuichi Shigemoto. “Distribution
    of Metabotropic Glutamate Receptor MGluR3 in the Mouse CNS: Differential Location
    Relative to Pre- and Postsynaptic Sites.” <i>Neuroscience</i>. Elsevier, 2001.
    <a href="https://doi.org/10.1016/S0306-4522(01)00305-0">https://doi.org/10.1016/S0306-4522(01)00305-0</a>.'
  ieee: 'Y. Tamaru, S. Nomura, N. Mizuno, and R. Shigemoto, “Distribution of metabotropic
    glutamate receptor mGluR3 in the mouse CNS: Differential location relative to
    pre- and postsynaptic sites,” <i>Neuroscience</i>, vol. 106, no. 3. Elsevier,
    pp. 481–503, 2001.'
  ista: 'Tamaru Y, Nomura S, Mizuno N, Shigemoto R. 2001. Distribution of metabotropic
    glutamate receptor mGluR3 in the mouse CNS: Differential location relative to
    pre- and postsynaptic sites. Neuroscience. 106(3), 481–503.'
  mla: 'Tamaru, Y., et al. “Distribution of Metabotropic Glutamate Receptor MGluR3
    in the Mouse CNS: Differential Location Relative to Pre- and Postsynaptic Sites.”
    <i>Neuroscience</i>, vol. 106, no. 3, Elsevier, 2001, pp. 481–503, doi:<a href="https://doi.org/10.1016/S0306-4522(01)00305-0">10.1016/S0306-4522(01)00305-0</a>.'
  short: Y. Tamaru, S. Nomura, N. Mizuno, R. Shigemoto, Neuroscience 106 (2001) 481–503.
date_created: 2018-12-11T11:58:39Z
date_published: 2001-09-27T00:00:00Z
date_updated: 2023-05-24T08:51:17Z
day: '27'
doi: 10.1016/S0306-4522(01)00305-0
extern: '1'
external_id:
  pmid:
  - '11591452'
intvolume: '       106'
issue: '3'
language:
- iso: eng
month: '09'
oa_version: None
page: 481 - 503
pmid: 1
publication: Neuroscience
publication_identifier:
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
publist_id: '4289'
quality_controlled: '1'
scopus_import: '1'
status: public
title: 'Distribution of metabotropic glutamate receptor mGluR3 in the mouse CNS: Differential
  location relative to pre- and postsynaptic sites'
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 106
year: '2001'
...
---
_id: '2611'
abstract:
- lang: eng
  text: Research using animal models of neuropathic pain has revealed sympathetic
    sprouting onto dorsal root ganglion cells. More recently, sensory fibre sprouting
    onto dorsal root ganglion cells has also been observed. Previous work in our laboratory
    demonstrated persistent sympathetic fibre sprouting in the skin of the rat lower
    lip following sensory denervation of this region. Therefore, we applied immunocytochemistry
    to determine the effects of sympathectomies on the terminal fields of sensory
    fibres. The superior cervical ganglia were removed bilaterally and the effects
    on the innervation of the skin of the rat lower lip were observed 1, 2, 3, 4,
    6 and 8 weeks post-surgery. Substance P and dopamine-β-hydroxylase immunoreactivities
    were used to identify a subset of sensory and sympathetic fibres, respectively.
    We also assessed neurokinin-1 receptor immunoreactivity. Quantitative data was
    obtained with the aid of an image analysis system. In controls, the epidermis
    and upper dermis were innervated by substance P-immunoreactive fibres only and
    upper dermal blood vessels possessed the highest density of neurokinin-1 receptor
    immunoreactivity. Blood vessels in the lower dermis were innervated by both substance
    P- and dopamine-β-hydroxylase-immunoreactive fibres. Following sympathectomies,
    substance P-immunoreactive fibres in the epidermis and upper dermis were more
    intensely labelled only 1 and 2 weeks post-surgery when compared to sham controls.
    The length of substance P-immunoreactive fibres in this region was also increased
    only on the second week. Neurokinin-1 receptor immunoreactivity in the upper dermis
    was slightly decreased 1 and 2 weeks post-surgery. In the lower dermis, substance
    P-immunoreactive fibres associated with blood vessels were more intensely labelled
    only 1 and 2 weeks post-surgery, and at all post-surgical time points studied,
    blood vessels in this region were devoid of dopamine-β-hydroxylase-immunoreactive
    fibres. The length of substance P-immunoreactive fibres was increased from the
    first to the third week post-surgery in the lower dermis. These results indicate
    that sympathectomies lead to transient changes in substance P-immunoreactive fibre
    innervation and neurokinin-1 receptor expression in rat lower lip skin. The effects
    are most prominent in the lower dermis probably due to a greater local concentration
    of nerve growth factor in this region. The plasticity of the interactions between
    sensory and sympathetic fibres may prove important in the regulation of skin microcirculation
    and in the generation of painful sensations under normal conditions or following
    peripheral nerve injuries.
acknowledgement: 'The work contained in this manuscript was sponsored by the Canadian
  MRC, Grants # MT-12170 and MoP-38093. The authors would like to thank Sylvain Cote
  for technical assistance and Sid Parkinson for editorial assistance.'
article_processing_charge: No
article_type: original
author:
- first_name: Isabella
  full_name: Ruocco, Isabella
  last_name: Ruocco
- first_name: Augusto
  full_name: Cuello, Augusto
  last_name: Cuello
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
- first_name: Alfredo
  full_name: Ribeiro Da Silva, Alfredo
  last_name: Ribeiro Da Silva
citation:
  ama: Ruocco I, Cuello A, Shigemoto R, Ribeiro Da Silva A. Sympathectomies lead to
    transient substance P-immunoreactive sensory fibre plasticity in the rat skin.
    <i>Neuroscience</i>. 2001;108(1):157-166. doi:<a href="https://doi.org/10.1016/S0306-4522(01)00158-0">10.1016/S0306-4522(01)00158-0</a>
  apa: Ruocco, I., Cuello, A., Shigemoto, R., &#38; Ribeiro Da Silva, A. (2001). Sympathectomies
    lead to transient substance P-immunoreactive sensory fibre plasticity in the rat
    skin. <i>Neuroscience</i>. Elsevier. <a href="https://doi.org/10.1016/S0306-4522(01)00158-0">https://doi.org/10.1016/S0306-4522(01)00158-0</a>
  chicago: Ruocco, Isabella, Augusto Cuello, Ryuichi Shigemoto, and Alfredo Ribeiro
    Da Silva. “Sympathectomies Lead to Transient Substance P-Immunoreactive Sensory
    Fibre Plasticity in the Rat Skin.” <i>Neuroscience</i>. Elsevier, 2001. <a href="https://doi.org/10.1016/S0306-4522(01)00158-0">https://doi.org/10.1016/S0306-4522(01)00158-0</a>.
  ieee: I. Ruocco, A. Cuello, R. Shigemoto, and A. Ribeiro Da Silva, “Sympathectomies
    lead to transient substance P-immunoreactive sensory fibre plasticity in the rat
    skin,” <i>Neuroscience</i>, vol. 108, no. 1. Elsevier, pp. 157–166, 2001.
  ista: Ruocco I, Cuello A, Shigemoto R, Ribeiro Da Silva A. 2001. Sympathectomies
    lead to transient substance P-immunoreactive sensory fibre plasticity in the rat
    skin. Neuroscience. 108(1), 157–166.
  mla: Ruocco, Isabella, et al. “Sympathectomies Lead to Transient Substance P-Immunoreactive
    Sensory Fibre Plasticity in the Rat Skin.” <i>Neuroscience</i>, vol. 108, no.
    1, Elsevier, 2001, pp. 157–66, doi:<a href="https://doi.org/10.1016/S0306-4522(01)00158-0">10.1016/S0306-4522(01)00158-0</a>.
  short: I. Ruocco, A. Cuello, R. Shigemoto, A. Ribeiro Da Silva, Neuroscience 108
    (2001) 157–166.
date_created: 2018-12-11T11:58:40Z
date_published: 2001-12-05T00:00:00Z
date_updated: 2023-05-22T12:15:44Z
day: '05'
doi: 10.1016/S0306-4522(01)00158-0
extern: '1'
external_id:
  pmid:
  - '11738139'
intvolume: '       108'
issue: '1'
language:
- iso: eng
month: '12'
oa_version: None
page: 157 - 166
pmid: 1
publication: Neuroscience
publication_identifier:
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
publist_id: '4286'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Sympathectomies lead to transient substance P-immunoreactive sensory fibre
  plasticity in the rat skin
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 108
year: '2001'
...
---
_id: '3515'
abstract:
- lang: eng
  text: Oscillations in neuronal networks are assumed to serve various physiological
    functions, from coordination of motor patterns to perceptual binding of sensory
    information. Here, we describe an ultra-slow oscillation (0.025 Hz) in the hippocampus.
    Extracellular and intracellular activity was recorded from the CA1 and subicular
    regions in rats of the Wistar and Sprague-Dawley strains. anesthetized with urethane.
    in a subgroup of Wistar rats (23%), spontaneous afterdischarges (4.7 +/- 1.6 s)
    occurred regularly at 40.8 +/- 15.7 s. The afterdischarge was initiated by a fast
    increase of population synchrony (100-250 Hz oscillation; “tonic” phase), followed
    by large-amplitude rhythmic waves and associated action potentials at gamma and
    beta frequency (15-50 Hz; “clonic” phase). The afterdischarges were bilaterally
    synchronous and terminated relatively abruptly without post-ictal depression.
    Single-pulse stimulation of the commissural input could trigger afterdischarges,
    but only at times when they were about to occur. Commissural stimulation evoked
    inhibitory postsynaptic potentials in pyramidal cells. However, when the stimulus
    triggered an afterdischarge, the inhibitory postsynaptic potential was absent
    and the cells remained depolarized during most of the afterdischarge. Afterdischarges
    were not observed in the Sprague-Dawley rats. Long-term analysis of interneuronal
    activity in intact, drug-free rats also revealed periodic excitability changes
    in the hippocampal network at 0.025 Hz. These findings indicate the presence of
    an ultra-slow oscillation in the hippocampal formation. The ultra-slow clock induced
    afterdischarges in susceptible animals. We hypothesize that a transient failure
    of GABAergic inhibition in a subset of Wistar rats is responsible for the emergence
    of epileptiform patterns. (C) 1999 IBRO. Published by Elsevier Science Ltd.
acknowledgement: This work was supported by the Academy of Finland (32391) and the
  NIH (NS34994, MH54671).
article_processing_charge: No
article_type: original
author:
- first_name: Markku
  full_name: Penttonen, Markku
  last_name: Penttonen
- first_name: Nina
  full_name: Nurminen, Nina
  last_name: Nurminen
- first_name: Riitta
  full_name: Miettinen, Riitta
  last_name: Miettinen
- first_name: Jouni
  full_name: Sirviö, Jouni
  last_name: Sirviö
- first_name: Darrell
  full_name: Henze, Darrell
  last_name: Henze
- first_name: Jozsef L
  full_name: Csicsvari, Jozsef L
  id: 3FA14672-F248-11E8-B48F-1D18A9856A87
  last_name: Csicsvari
  orcid: 0000-0002-5193-4036
- first_name: György
  full_name: Buzsáki, György
  last_name: Buzsáki
citation:
  ama: Penttonen M, Nurminen N, Miettinen R, et al. Ultra-slow oscillation (0.025
    Hz) triggers hippocampal afterdischarges in Wistar rats. <i>Neuroscience</i>.
    1999;94(3):735-743. doi:<a href="https://doi.org/10.1016/S0306-4522(99)00367-X">10.1016/S0306-4522(99)00367-X</a>
  apa: Penttonen, M., Nurminen, N., Miettinen, R., Sirviö, J., Henze, D., Csicsvari,
    J. L., &#38; Buzsáki, G. (1999). Ultra-slow oscillation (0.025 Hz) triggers hippocampal
    afterdischarges in Wistar rats. <i>Neuroscience</i>. Elsevier. <a href="https://doi.org/10.1016/S0306-4522(99)00367-X">https://doi.org/10.1016/S0306-4522(99)00367-X</a>
  chicago: Penttonen, Markku, Nina Nurminen, Riitta Miettinen, Jouni Sirviö, Darrell
    Henze, Jozsef L Csicsvari, and György Buzsáki. “Ultra-Slow Oscillation (0.025
    Hz) Triggers Hippocampal Afterdischarges in Wistar Rats.” <i>Neuroscience</i>.
    Elsevier, 1999. <a href="https://doi.org/10.1016/S0306-4522(99)00367-X">https://doi.org/10.1016/S0306-4522(99)00367-X</a>.
  ieee: M. Penttonen <i>et al.</i>, “Ultra-slow oscillation (0.025 Hz) triggers hippocampal
    afterdischarges in Wistar rats,” <i>Neuroscience</i>, vol. 94, no. 3. Elsevier,
    pp. 735–743, 1999.
  ista: Penttonen M, Nurminen N, Miettinen R, Sirviö J, Henze D, Csicsvari JL, Buzsáki
    G. 1999. Ultra-slow oscillation (0.025 Hz) triggers hippocampal afterdischarges
    in Wistar rats. Neuroscience. 94(3), 735–743.
  mla: Penttonen, Markku, et al. “Ultra-Slow Oscillation (0.025 Hz) Triggers Hippocampal
    Afterdischarges in Wistar Rats.” <i>Neuroscience</i>, vol. 94, no. 3, Elsevier,
    1999, pp. 735–43, doi:<a href="https://doi.org/10.1016/S0306-4522(99)00367-X">10.1016/S0306-4522(99)00367-X</a>.
  short: M. Penttonen, N. Nurminen, R. Miettinen, J. Sirviö, D. Henze, J.L. Csicsvari,
    G. Buzsáki, Neuroscience 94 (1999) 735–743.
date_created: 2018-12-11T12:03:44Z
date_published: 1999-10-01T00:00:00Z
date_updated: 2022-09-07T13:16:01Z
day: '01'
doi: 10.1016/S0306-4522(99)00367-X
extern: '1'
external_id:
  pmid:
  - '10579564'
intvolume: '        94'
issue: '3'
language:
- iso: eng
month: '10'
oa_version: None
page: 735 - 743
pmid: 1
publication: Neuroscience
publication_identifier:
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
publist_id: '2870'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Ultra-slow oscillation (0.025 Hz) triggers hippocampal afterdischarges in Wistar
  rats
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 94
year: '1999'
...
---
_id: '3541'
abstract:
- lang: eng
  text: 'The contribution of the various hippocampal regions to the maintenance of
    epileptic activity, induced by stimulation of the perforant path or commissural
    system, was examined in the awake rat. Combination of multiple-site recordings
    with silicon probes, current source density analysis and unit recordings allowed
    for a high spatial resolution of the field events. Following perforant path stimulation,
    seizures began in the dentate gyrus, followed by events in the CA3-CA1 regions.
    After commissural stimulation, rhythmic bursts in the CA3-CA1 circuitry preceded
    the activation of the dentate gyrus. Correlation of events in the different subregions
    indicated that the sustained rhythmic afterdischarge (2-6 Hz) could not be explained
    by a cycle-by-cycle excitation of principal cell populations in the hippocampal-entorhinal
    loop. The primary afterdischarge always terminated in the CA1 region, followed
    by the dentate gyrus, CA3 region and the entorhinal cortex. The duration and pattern
    of the hippocampal afterdischarge was essentially unaffected by removal of the
    entorhinal cortex. The emergence of large population spike bursts coincided with
    a decreased discharge of interneurons in both CAI and hilar regions. The majority
    of hilar interneurons displayed a strong amplitude decrement prior to the onset
    of population spike phase of the afterdischarge. These findings suggest that (i)
    afterdischarges can independently arise in the CA3-CA1 and entorhinal-dentate
    gyrus circuitries, (ii) reverberation of excitation in the hippocampal-entorhinal
    loop is not critical for the maintenance of afterdischarges and (iii) decreased
    activity of the interneuronal network may release population bursting of principal
    cells. '
acknowledgement: We thank K. Wise and J. Hetke for providing us the silicon probes,
  J. J. Chrobak, S. L-W. Leung, G. G. Somjen and R. D. Traub for their comments on
  the manuscript. This work was supported by NINDS (NS34994; 1P41RR09754; NS33310)
  and the Whitehall Foundation. M. Penttonen was a visiting scholar at Rutgers University,
  supported by the Finnish Academy of Sciences and the A. I. Virtanen Institute.
article_processing_charge: No
article_type: original
author:
- first_name: Anatol
  full_name: Bragin, Anatol
  last_name: Bragin
- first_name: Jozsef L
  full_name: Csicsvari, Jozsef L
  id: 3FA14672-F248-11E8-B48F-1D18A9856A87
  last_name: Csicsvari
  orcid: 0000-0002-5193-4036
- first_name: Markku
  full_name: Penttonen, Markku
  last_name: Penttonen
- first_name: György
  full_name: Buzsáki, György
  last_name: Buzsáki
citation:
  ama: 'Bragin A, Csicsvari JL, Penttonen M, Buzsáki G. Epileptic afterdischarge in
    the hippocampal-entorhinal system: Current source density and unit studies. <i>Neuroscience</i>.
    1997;76(4):1187-1203. doi:<a href="https://doi.org/10.1016/S0306-4522(96)00446-0">10.1016/S0306-4522(96)00446-0</a>'
  apa: 'Bragin, A., Csicsvari, J. L., Penttonen, M., &#38; Buzsáki, G. (1997). Epileptic
    afterdischarge in the hippocampal-entorhinal system: Current source density and
    unit studies. <i>Neuroscience</i>. Elsevier. <a href="https://doi.org/10.1016/S0306-4522(96)00446-0">https://doi.org/10.1016/S0306-4522(96)00446-0</a>'
  chicago: 'Bragin, Anatol, Jozsef L Csicsvari, Markku Penttonen, and György Buzsáki.
    “Epileptic Afterdischarge in the Hippocampal-Entorhinal System: Current Source
    Density and Unit Studies.” <i>Neuroscience</i>. Elsevier, 1997. <a href="https://doi.org/10.1016/S0306-4522(96)00446-0">https://doi.org/10.1016/S0306-4522(96)00446-0</a>.'
  ieee: 'A. Bragin, J. L. Csicsvari, M. Penttonen, and G. Buzsáki, “Epileptic afterdischarge
    in the hippocampal-entorhinal system: Current source density and unit studies,”
    <i>Neuroscience</i>, vol. 76, no. 4. Elsevier, pp. 1187–1203, 1997.'
  ista: 'Bragin A, Csicsvari JL, Penttonen M, Buzsáki G. 1997. Epileptic afterdischarge
    in the hippocampal-entorhinal system: Current source density and unit studies.
    Neuroscience. 76(4), 1187–1203.'
  mla: 'Bragin, Anatol, et al. “Epileptic Afterdischarge in the Hippocampal-Entorhinal
    System: Current Source Density and Unit Studies.” <i>Neuroscience</i>, vol. 76,
    no. 4, Elsevier, 1997, pp. 1187–203, doi:<a href="https://doi.org/10.1016/S0306-4522(96)00446-0">10.1016/S0306-4522(96)00446-0</a>.'
  short: A. Bragin, J.L. Csicsvari, M. Penttonen, G. Buzsáki, Neuroscience 76 (1997)
    1187–1203.
date_created: 2018-12-11T12:03:52Z
date_published: 1997-01-15T00:00:00Z
date_updated: 2022-08-19T11:53:06Z
day: '15'
doi: 10.1016/S0306-4522(96)00446-0
extern: '1'
external_id:
  pmid:
  - '9027878'
intvolume: '        76'
issue: '4'
language:
- iso: eng
month: '01'
oa_version: None
page: 1187 - 1203
pmid: 1
publication: Neuroscience
publication_identifier:
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
publist_id: '2844'
quality_controlled: '1'
status: public
title: 'Epileptic afterdischarge in the hippocampal-entorhinal system: Current source
  density and unit studies'
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 76
year: '1997'
...
---
_id: '2492'
abstract:
- lang: eng
  text: The metabotropic glutamate receptor subtypes mGluR2 and mGluR5, which are
    thought to be coupled respectively to the inhibitory cyclic adenosine monophosphate
    (cAMP) cascade and the phosphatidylinositol hydrolysis/Ca2+ cascade, are known
    to be expressed on Golgi cells in the granular layer of the rat cerebellar cortex.
    In the present immunohistochemical study with a monoclonal antibody against mGluR2
    and a polyclonal antibody for mGluR5, we examined whether or not mGluR2- and mGluR5-like
    immunoreactivities were both present in single Golgi cells in the rat cerebellar
    cortex. In double immunofluorescence histochemistry, no Golgi cells showed mGluR2-
    and mGluR5-like immunoreactivities simultaneously. Of the total number of Golgi
    cells immunoreactive for mGluR2 or mGluR5, about 90% were mGluR2-like immunoreactive,
    and about 10% were mGluR5-like immunoreactive. Golgi cells with mGluR2-like immunoreactivity
    were distributed evenly in the granular layer of all the cerebellar regions, while
    those with mGluR5-like immunoreactivity were distributed more frequently in the
    I, II, VII-X lobules of the vermis and the copula pyramidis of the hemisphere
    than in other cerebellar regions. The results indicate that Golgi cells containing
    mGluR2 are segregated from those possessing mGluR5. These two populations of Golgi
    cells, each equipped with a different metabolic glutamate receptor coupled to
    a different intracellular signal transduction system, may play different roles
    in the glutamatergic neuronal circuits in the cerebellar cortex.
acknowledgement: We thank Mr Akira Uesugi for expert photographic assistance. We also
  thank Dr Jeremy M. Henley for a critical reading of the manuscript.
article_processing_charge: No
article_type: original
author:
- first_name: Akio
  full_name: Neki, Akio
  last_name: Neki
- first_name: Hitoshi
  full_name: Ohishi, Hitoshi
  last_name: Ohishi
- first_name: Takeshi
  full_name: Kaneko, Takeshi
  last_name: Kaneko
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
- first_name: Shigetada
  full_name: Nakanishi, Shigetada
  last_name: Nakanishi
- first_name: Noboru
  full_name: Mizuno, Noboru
  last_name: Mizuno
citation:
  ama: Neki A, Ohishi H, Kaneko T, Shigemoto R, Nakanishi S, Mizuno N. Metabotropic
    glutamate receptors mGluR2 and mGluR5 are expressed in two non-overlapping populations
    of Golgi cells in the rat cerebellum. <i>Neuroscience</i>. 1996;75(3):815-826.
    doi:<a href="https://doi.org/10.1016/0306-4522(96)00316-8">10.1016/0306-4522(96)00316-8</a>
  apa: Neki, A., Ohishi, H., Kaneko, T., Shigemoto, R., Nakanishi, S., &#38; Mizuno,
    N. (1996). Metabotropic glutamate receptors mGluR2 and mGluR5 are expressed in
    two non-overlapping populations of Golgi cells in the rat cerebellum. <i>Neuroscience</i>.
    Elsevier. <a href="https://doi.org/10.1016/0306-4522(96)00316-8">https://doi.org/10.1016/0306-4522(96)00316-8</a>
  chicago: Neki, Akio, Hitoshi Ohishi, Takeshi Kaneko, Ryuichi Shigemoto, Shigetada
    Nakanishi, and Noboru Mizuno. “Metabotropic Glutamate Receptors MGluR2 and MGluR5
    Are Expressed in Two Non-Overlapping Populations of Golgi Cells in the Rat Cerebellum.”
    <i>Neuroscience</i>. Elsevier, 1996. <a href="https://doi.org/10.1016/0306-4522(96)00316-8">https://doi.org/10.1016/0306-4522(96)00316-8</a>.
  ieee: A. Neki, H. Ohishi, T. Kaneko, R. Shigemoto, S. Nakanishi, and N. Mizuno,
    “Metabotropic glutamate receptors mGluR2 and mGluR5 are expressed in two non-overlapping
    populations of Golgi cells in the rat cerebellum,” <i>Neuroscience</i>, vol. 75,
    no. 3. Elsevier, pp. 815–826, 1996.
  ista: Neki A, Ohishi H, Kaneko T, Shigemoto R, Nakanishi S, Mizuno N. 1996. Metabotropic
    glutamate receptors mGluR2 and mGluR5 are expressed in two non-overlapping populations
    of Golgi cells in the rat cerebellum. Neuroscience. 75(3), 815–826.
  mla: Neki, Akio, et al. “Metabotropic Glutamate Receptors MGluR2 and MGluR5 Are
    Expressed in Two Non-Overlapping Populations of Golgi Cells in the Rat Cerebellum.”
    <i>Neuroscience</i>, vol. 75, no. 3, Elsevier, 1996, pp. 815–26, doi:<a href="https://doi.org/10.1016/0306-4522(96)00316-8">10.1016/0306-4522(96)00316-8</a>.
  short: A. Neki, H. Ohishi, T. Kaneko, R. Shigemoto, S. Nakanishi, N. Mizuno, Neuroscience
    75 (1996) 815–826.
date_created: 2018-12-11T11:57:59Z
date_published: 1996-12-01T00:00:00Z
date_updated: 2022-08-12T12:11:03Z
day: '01'
doi: 10.1016/0306-4522(96)00316-8
extern: '1'
external_id:
  pmid:
  - '8951875'
intvolume: '        75'
issue: '3'
language:
- iso: eng
month: '12'
oa_version: None
page: 815 - 826
pmid: 1
publication: Neuroscience
publication_identifier:
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
publist_id: '4409'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Metabotropic glutamate receptors mGluR2 and mGluR5 are expressed in two non-overlapping
  populations of Golgi cells in the rat cerebellum
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 75
year: '1996'
...
---
_id: '2488'
abstract:
- lang: eng
  text: Substance P receptor-expressing neurons in the rat cerebral neocortex were
    examined by single- and double-immunolabeling methods with an affinity-purified
    specific antibody to substance P receptor. Substance P receptor immunoreactivity
    was observed exclusively in non-pyramidal neurons. About a quarter of these substance
    P receptor-positive neocortical neurons showed intense immunoreactivity, and the
    other three quarters displayed weak substance P receptor immunoreactivity. The
    neurons showing intense substance P receptor immunoreactivity were large multipolar
    cells with a few long aspiny or sparsely-spiny dendrites, and were scattered throughout
    the neocortical layers except for layer I, and also in the underlying white matter.
    The weakly immunoreactive neurons were medium-sized multipolar cells with oval
    to round somata and aspiny varicose dendrites, and were distributed in all cortical
    layers with a bias to layers II-III and the superficial part of layer V. The double-immunofluorescence
    study revealed that almost all substance P receptor-positive neurons were immunoreactive
    for GABA, but negative for glutaminase. Substance P receptor immunoreactivity
    in GABAergic neocortical neurons were further examined by the double-immunofluorescence
    method with antibodies to markers for subgroups of GABAergic neurons. Somatostatin
    immunoreactivity was found in 89% of neurons with intense substance P receptor
    immunoreactivity, and in 1.5% of neurons with weak substance P receptor immunoreactivity.
    Neuropeptide Y immunoreactivity was also observed in 92% of neurons with intense
    immunoreactivity for substance P receptor, and in 1.6% of neurons with weak immunoreactivity
    for substance P receptor. In contrast, parvalbumin immunoreactivity was seen in
    1.3% of neurons with intense substance P receptor immunoreactivity, and in 59%
    of weak substance P receptor immunoreactivity. Calbindin D28k immunoreactivity
    was found in 12 and 19% of neurons, respectively, with weak and intense immunoreactivities
    for substance P receptor. Virtually no cells showing substance P receptor immunoreactivity
    displayed immunoreactivity for vasoactive intestinal polypeptide or choline acetyltransferase.
    These results indicate that the neocortical neurons expressing substance P receptor
    constitute a subpopulation of GABAergic non-pyramidal cells, and are segregated
    into neurons with intense immunoreactivity and those with weak immunoreactivity
    for substance P receptor; the vast majority of neurons with intense substance
    P receptor immunoreactivity contain somatostatin and neuropeptide Y, and the majority
    of neurons with weak substance P receptor immunoreactivity have parvalbumin.
acknowledgement: We are grateful for photographic help of Mr A. Uesugi, and the support
  of Drs S. Fukuchi, T. Fukuda, R. Hayashi, M. Katsurada, Y. Kitani, K. Kumagai, H.
  Kuroda, H. Matsubara, H. Matsushima, C. Minakuchi, M. Nishio, G. Niwa, H. Ckla,
  M. Ohbayashi, S. Ohbayashi, H. Ohtsuka, S. Tamaki, E. Watanabe, K. Yoshino and Y.
  Yoshino. This work was supported in part by Grants-in-Aid for Scientific Research
  on Priority Areas 05248207 and 05267104, and Scientific Research (B) 05454658 and
  (C) 05680658 from the Ministry of Education, Science and Culture of Japan.
article_processing_charge: No
article_type: original
author:
- first_name: Takeshi
  full_name: Kaneko, Takeshi
  last_name: Kaneko
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
- first_name: Shigetada
  full_name: Nakanishi, Shigetada
  last_name: Nakanishi
- first_name: Noboru
  full_name: Mizuno, Noboru
  last_name: Mizuno
citation:
  ama: Kaneko T, Shigemoto R, Nakanishi S, Mizuno N. Morphological and chemical characteristics
    of substance P receptor immunoreactive neurons in the rat neocortex. <i>Neuroscience</i>.
    1994;60(1):199-211. doi:<a href="https://doi.org/10.1016/0306-4522(94)90215-1">10.1016/0306-4522(94)90215-1</a>
  apa: Kaneko, T., Shigemoto, R., Nakanishi, S., &#38; Mizuno, N. (1994). Morphological
    and chemical characteristics of substance P receptor immunoreactive neurons in
    the rat neocortex. <i>Neuroscience</i>. Elsevier. <a href="https://doi.org/10.1016/0306-4522(94)90215-1">https://doi.org/10.1016/0306-4522(94)90215-1</a>
  chicago: Kaneko, Takeshi, Ryuichi Shigemoto, Shigetada Nakanishi, and Noboru Mizuno.
    “Morphological and Chemical Characteristics of Substance P Receptor Immunoreactive
    Neurons in the Rat Neocortex.” <i>Neuroscience</i>. Elsevier, 1994. <a href="https://doi.org/10.1016/0306-4522(94)90215-1">https://doi.org/10.1016/0306-4522(94)90215-1</a>.
  ieee: T. Kaneko, R. Shigemoto, S. Nakanishi, and N. Mizuno, “Morphological and chemical
    characteristics of substance P receptor immunoreactive neurons in the rat neocortex,”
    <i>Neuroscience</i>, vol. 60, no. 1. Elsevier, pp. 199–211, 1994.
  ista: Kaneko T, Shigemoto R, Nakanishi S, Mizuno N. 1994. Morphological and chemical
    characteristics of substance P receptor immunoreactive neurons in the rat neocortex.
    Neuroscience. 60(1), 199–211.
  mla: Kaneko, Takeshi, et al. “Morphological and Chemical Characteristics of Substance
    P Receptor Immunoreactive Neurons in the Rat Neocortex.” <i>Neuroscience</i>,
    vol. 60, no. 1, Elsevier, 1994, pp. 199–211, doi:<a href="https://doi.org/10.1016/0306-4522(94)90215-1">10.1016/0306-4522(94)90215-1</a>.
  short: T. Kaneko, R. Shigemoto, S. Nakanishi, N. Mizuno, Neuroscience 60 (1994)
    199–211.
date_created: 2018-12-11T11:57:58Z
date_published: 1994-05-01T00:00:00Z
date_updated: 2022-06-09T12:22:16Z
day: '01'
doi: 10.1016/0306-4522(94)90215-1
extern: '1'
external_id:
  pmid:
  - '8052413'
intvolume: '        60'
issue: '1'
language:
- iso: eng
main_file_link:
- url: https://www.sciencedirect.com/science/article/pii/0306452294902151?via%3Dihub
month: '05'
oa_version: None
page: 199 - 211
pmid: 1
publication: Neuroscience
publication_identifier:
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
publist_id: '4413'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Morphological and chemical characteristics of substance P receptor immunoreactive
  neurons in the rat neocortex
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 60
year: '1994'
...
---
_id: '2490'
abstract:
- lang: eng
  text: Distribution of the messenger RNA for the prostaglandin E receptor subtype
    EP3 was investigated by in situ hybridization in the nervous system of the mouse.
    The hybridization signals for EP3 were widely distributed in the brain and sensory
    ganglia and specifically localized to neurons. In the dorsal root and trigeminal
    ganglia, about half of the neurons were labeled intensely. In the brain, intensely
    labeled neurons were found in Ammon's horn, the preoptic nuclei, lateral hypothalamic
    area, dorsomedial hypothalamic nucleus, lateral mammillary nucleus, entopeduncular
    nucleus, substantia nigra pars compacta, locus coeruleus and raphe nuclei. Moderately
    labeled neurons were seen in the mitral cell layer of the main olfactory bulb,
    layer V of the entorhinal and parasubicular cortices, layers V and VI of the cerebral
    neocortex, nuclei of the diagonal band, magnocellular preoptic nucleus, globus
    pallidus and lateral parabrachial nucleus. In the thalamus, moderately labeled
    neurons were distributed in the anterior, ventromedial, laterodorsal, paraventricular
    and central medial nuclei. Based on these distributions, we suggest that EP3 not
    only mediates prostaglandin E2 signals evoked by blood-borne cytokines in the
    areas poor in the blood-brain barrier, but also responds to those formed intrinsically
    within the brain to modulate various neuronal activities. Possible EP3 actions
    are discussed in relation to the reported neuronal activities of prostaglandin
    E2 in the brain.
acknowledgement: 'This work was supported in part by Grants-in-aid for Scientific
  Research 05404020, 04255103. 05771975, 05671816 and 05454568 from the Ministry of
  Education, Science and Culture of Japan and by grants from the Mitsubishi Foundation
  and the Takeda Science Foundation. We are grateful to Mr Akira Uesugi for photographic
  help. We also thank Drs Chihiro Akazawa, Hitoshi Ohishi and Masabumi Minami for
  helpful discussions. '
article_processing_charge: No
article_type: original
author:
- first_name: Yukihiko
  full_name: Sugimoto, Yukihiko
  last_name: Sugimoto
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
- first_name: Tsunehisa
  full_name: Namba, Tsunehisa
  last_name: Namba
- first_name: Manabu
  full_name: Negishi, Manabu
  last_name: Negishi
- first_name: Noboru
  full_name: Mizuno, Noboru
  last_name: Mizuno
- first_name: Shuh
  full_name: Narumiya, Shuh
  last_name: Narumiya
- first_name: Atsushi
  full_name: Ichikawa, Atsushi
  last_name: Ichikawa
citation:
  ama: Sugimoto Y, Shigemoto R, Namba T, et al. Distribution of the messenger rna
    for the prostaglandin e receptor subtype ep3 in the mouse nervous system. <i>Neuroscience</i>.
    1994;62(3):919-928. doi:<a href="https://doi.org/10.1016/0306-4522(94)90483-9">10.1016/0306-4522(94)90483-9</a>
  apa: Sugimoto, Y., Shigemoto, R., Namba, T., Negishi, M., Mizuno, N., Narumiya,
    S., &#38; Ichikawa, A. (1994). Distribution of the messenger rna for the prostaglandin
    e receptor subtype ep3 in the mouse nervous system. <i>Neuroscience</i>. Elsevier.
    <a href="https://doi.org/10.1016/0306-4522(94)90483-9">https://doi.org/10.1016/0306-4522(94)90483-9</a>
  chicago: Sugimoto, Yukihiko, Ryuichi Shigemoto, Tsunehisa Namba, Manabu Negishi,
    Noboru Mizuno, Shuh Narumiya, and Atsushi Ichikawa. “Distribution of the Messenger
    Rna for the Prostaglandin e Receptor Subtype Ep3 in the Mouse Nervous System.”
    <i>Neuroscience</i>. Elsevier, 1994. <a href="https://doi.org/10.1016/0306-4522(94)90483-9">https://doi.org/10.1016/0306-4522(94)90483-9</a>.
  ieee: Y. Sugimoto <i>et al.</i>, “Distribution of the messenger rna for the prostaglandin
    e receptor subtype ep3 in the mouse nervous system,” <i>Neuroscience</i>, vol.
    62, no. 3. Elsevier, pp. 919–928, 1994.
  ista: Sugimoto Y, Shigemoto R, Namba T, Negishi M, Mizuno N, Narumiya S, Ichikawa
    A. 1994. Distribution of the messenger rna for the prostaglandin e receptor subtype
    ep3 in the mouse nervous system. Neuroscience. 62(3), 919–928.
  mla: Sugimoto, Yukihiko, et al. “Distribution of the Messenger Rna for the Prostaglandin
    e Receptor Subtype Ep3 in the Mouse Nervous System.” <i>Neuroscience</i>, vol.
    62, no. 3, Elsevier, 1994, pp. 919–28, doi:<a href="https://doi.org/10.1016/0306-4522(94)90483-9">10.1016/0306-4522(94)90483-9</a>.
  short: Y. Sugimoto, R. Shigemoto, T. Namba, M. Negishi, N. Mizuno, S. Narumiya,
    A. Ichikawa, Neuroscience 62 (1994) 919–928.
date_created: 2018-12-11T11:57:58Z
date_published: 1994-10-01T00:00:00Z
date_updated: 2022-06-09T11:56:23Z
day: '01'
doi: 10.1016/0306-4522(94)90483-9
extern: '1'
external_id:
  pmid:
  - '7870313'
intvolume: '        62'
issue: '3'
language:
- iso: eng
main_file_link:
- url: https://www.sciencedirect.com/science/article/pii/0306452294904839?via%3Dihub
month: '10'
oa_version: None
page: 919 - 928
pmid: 1
publication: Neuroscience
publication_identifier:
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
publist_id: '4411'
quality_controlled: '1'
status: public
title: Distribution of the messenger rna for the prostaglandin e receptor subtype
  ep3 in the mouse nervous system
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 62
year: '1994'
...
---
_id: '2540'
abstract:
- lang: eng
  text: Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2,
    which is coupled to the inhibitory cyclic AMP cascade, was investigated in the
    central nervous system of the adult rat by in situ hybridization. Transcripts
    of mGluR2 were specifically localized to neuronal cells of the brain. Although
    the hybridization signals were widely distributed in the brain, the most prominent
    expression of mGluR2 messenger RNA was seen in Golgi cells of the cerebellum.
    Marked expression of mGluR2 messenger RNA was further observed in the mitral cells
    of the accessory olfactory bulb, neurons in the external part of the anterior
    olfactory nucleus, and pyramidal neurons in the entorhinal and parasubicular cortical
    regions. The granule cells of the accessory olfactory bulb, and many pyramidal
    and non-pyramidal neurons in the neocortical, cingulate, retrosplenial and subicular
    cortices, were moderately labeled. All of the granule cells in the dentate gyrus
    were also labeled moderately, whereas no significant hybridization signals were
    detected in Ammon's horn. In the basal forebrain regions, moderately labeled neurons
    were distributed in the triangular septal nucleus, in the lateral, basolateral
    and basomedial amygdaloid nuclei, and in the medial mammillary nucleus. Weakly
    labeled neurons were sparsely scattered in the striatum, globus pallidus, ventral
    pallidum and claustrum. The subthalamic nucleus was also labeled weakly. No significant
    labeling was found in the entopeduncular nucleus and substantia nigra. In the
    thalamus, moderately labeled neurons were distributed in the anterodorsal, anteromedial,
    ventromedial, intralaminar and midline nuclei; the ventrolateral part of the anteroventral
    nucleus and the rostral pole of the ventrolateral nucleus also contained moderately
    labeled neurons. No significant labeling was found in the thalamic reticular,
    submedius, ventroposterior, lateral geniculate and medial geniculate nuclei. In
    the lower brainstem, labeling was generally weak. No significant hybridization
    signals were found in the spinal cord. Some neurons in the inner part of the inner
    nuclear layer of the retina and some retinal ganglion cells were labeled moderately.
    The pattern of distribution of mGluR2 messenger RNA revealed in the present study
    indicates specific roles of mGluR2 in the glutamatergic system in the brain.
acknowledgement: We are grateful for the photographic help of Mr Akira Uesugi and
  the support of Drs Ryosuke Fujimori, Satoru Fukuchi, Toshio Fukuda, Ritsu Hayashi,
  Sozaburo Hayashi, Mizuho Katsurada, Yutaka Kitani, Keiko Kumagai, Hiroshi Kuroda,
  Toshio Kuroda, Hiroshi Matsubara. Hiroshi Matsushima. Chisato Minakuchi. Masatoshi
  ‘Nishio, Gonpei Niwa, Hajime Oda, Masahiko Ohbayashi, Seiichi Ohbayashi, Hiroyasu
  Ohtsuka, Shigeo Tamaki, Eizo Watanabe, Kazuo Yoshino and Toshiaki Yoshino. This
  work was supported in part by Grants-in-Aid from the Ministry of Education, Science
  and Culture of Japan.
article_processing_charge: No
article_type: original
author:
- first_name: Hitoshi
  full_name: Ohishi, Hitoshi
  last_name: Ohishi
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
- first_name: Shigetada
  full_name: Nakanishi, Shigetada
  last_name: Nakanishi
- first_name: Noboru
  full_name: Mizuno, Noboru
  last_name: Mizuno
citation:
  ama: Ohishi H, Shigemoto R, Nakanishi S, Mizuno N. Distribution of the messenger
    RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system
    of the rat. <i>Neuroscience</i>. 1993;53(4):1009-1018. doi:<a href="https://doi.org/10.1016/0306-4522(93)90485-X">10.1016/0306-4522(93)90485-X</a>
  apa: Ohishi, H., Shigemoto, R., Nakanishi, S., &#38; Mizuno, N. (1993). Distribution
    of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central
    nervous system of the rat. <i>Neuroscience</i>. Elsevier. <a href="https://doi.org/10.1016/0306-4522(93)90485-X">https://doi.org/10.1016/0306-4522(93)90485-X</a>
  chicago: Ohishi, Hitoshi, Ryuichi Shigemoto, Shigetada Nakanishi, and Noboru Mizuno.
    “Distribution of the Messenger RNA for a Metabotropic Glutamate Receptor, MGluR2,
    in the Central Nervous System of the Rat.” <i>Neuroscience</i>. Elsevier, 1993.
    <a href="https://doi.org/10.1016/0306-4522(93)90485-X">https://doi.org/10.1016/0306-4522(93)90485-X</a>.
  ieee: H. Ohishi, R. Shigemoto, S. Nakanishi, and N. Mizuno, “Distribution of the
    messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous
    system of the rat,” <i>Neuroscience</i>, vol. 53, no. 4. Elsevier, pp. 1009–1018,
    1993.
  ista: Ohishi H, Shigemoto R, Nakanishi S, Mizuno N. 1993. Distribution of the messenger
    RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system
    of the rat. Neuroscience. 53(4), 1009–1018.
  mla: Ohishi, Hitoshi, et al. “Distribution of the Messenger RNA for a Metabotropic
    Glutamate Receptor, MGluR2, in the Central Nervous System of the Rat.” <i>Neuroscience</i>,
    vol. 53, no. 4, Elsevier, 1993, pp. 1009–18, doi:<a href="https://doi.org/10.1016/0306-4522(93)90485-X">10.1016/0306-4522(93)90485-X</a>.
  short: H. Ohishi, R. Shigemoto, S. Nakanishi, N. Mizuno, Neuroscience 53 (1993)
    1009–1018.
date_created: 2018-12-11T11:58:16Z
date_published: 1993-01-01T00:00:00Z
date_updated: 2022-03-31T12:19:44Z
day: '01'
doi: 10.1016/0306-4522(93)90485-X
extern: '1'
external_id:
  pmid:
  - '8389425'
intvolume: '        53'
issue: '4'
language:
- iso: eng
main_file_link:
- url: https://www.sciencedirect.com/science/article/pii/030645229390485X?via%3Dihub
month: '01'
oa_version: None
page: 1009 - 1018
pmid: 1
publication: Neuroscience
publication_identifier:
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
publist_id: '4358'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2,
  in the central nervous system of the rat
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 53
year: '1993'
...
---
_id: '2479'
abstract:
- lang: eng
  text: Distribution of putative glutamatergic neurons in the lower brainstem and
    cerebellum of the rat was examined immunocytochemically by using a monoclonal
    antibody against phosphate-activated glutaminase, which has been proposed to be
    a major synthetic enzyme of transmitter glutamate and so may serve as a marker
    for glutamatergic neurons in the central nervous system. Intensely-immunolabeled
    neuronal cell bodies were densely distributed in the main precerebellar nuclei
    sending mossy fibers to the cerebellum; in the pontine nuclei, pontine tegmental
    reticular nucleus of Bechterew, external cuneate nucleus, and lateral reticular
    nucleus of the medulla oblongata. Phosphate-activated glutaminase-immunoreactive
    granular deposits were densely seen in the brachium pontis and restiform body,
    suggesting the immunolabeling of mossy fibers of passage. In the cerebellum, neuropil
    within the granule cell layer of the cerebellar cortex displayed intense phosphate-activated
    glutaminase-immunoreactivity, and that within the deep cerebellar nuclei showed
    moderate immunoreactivity. These results indicate that many mossy fiber terminals
    originate from phosphate-activated glutaminase-containing neurons and utilize
    phosphate-activated glutaminase for the synthesis of transmitter glutamate. Intensely-immunostained
    neuronal cell bodies were further observed in other regions which have been reported
    to contain neurons sending mossy fibers to the cerebellum; in the dorsal part
    of the principal sensory trigeminal nucleus, dorsomedial part of the oral subnucleus
    of the spinal trigeminal nucleus, interpolar subnucleus of the spinal trigeminal
    nucleus, paratrigeminal nucleus, supragenual nucleus, regions dorsal to the abducens
    nucleus and genu of the facial nerve, superior and medial vestibular nuclei, cell
    groups f, x and y, hypoglossal prepositus nucleus, intercalated nucleus, nucleus
    of Roller, reticular regions intercalated between the motor trigeminal and principal
    sensory trigeminal nuclei, linear nucleus, and gigantocellular and paramedian
    reticular formation. Neuronal cell bodies with intense phosphate-activated glutaminase-immunoreactivity
    were also found in other brainstem regions, such as the paracochlear glial substance,
    posterior ventral cochlear nucleus, and cell group e. Although it is still controversial
    whether all glutamatergic neurons use phosphate-activated glutaminase in a transmitter-related
    process and whether phosphate-activated glutaminase is involved in other metabolism-related
    processes, the neurons showing intense phosphate-activated glutaminase-immuno-reactivity
    in the present study were suggested to be putative glutamatergic neurons.
acknowledgement: 'The authors wish to thank Mr. Akira Uesugi and Mr. Ken’ichi Uesugi
  for their photographic help. This work was partly supported by grants-in-aid from
  the Ministry of Education, science and Culture of Japan for Special Project Research
  63112003. Special Research Project on Priority-Areas 63623505, Special Research
  62480098 and Encouragement of Young Scientist 63770043. The support of the Niwa
  Medical Research Foundation, Dr. Satoru Fukuchi, Dr. Toshio Fukuda, Dr. Ritsu Hayashi,
  Dr. Yutaka Kitani, Dr. Hiroshi Matsushima, Dr. Gonpei Niwa, Dr. Hiroyasu Ohtsuka,
  Dr. Shigeo Tamaki, and Dr. Eizo Watanabe are gratefully acknowledged. '
article_processing_charge: No
article_type: original
author:
- first_name: Takeshi
  full_name: Kaneko, Takeshi
  last_name: Kaneko
- first_name: Kazuo
  full_name: Itoh, Kazuo
  last_name: Itoh
- first_name: Ryuichi
  full_name: Shigemoto, Ryuichi
  id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
  last_name: Shigemoto
  orcid: 0000-0001-8761-9444
- first_name: Noboru
  full_name: Mizuno, Noboru
  last_name: Mizuno
citation:
  ama: Kaneko T, Itoh K, Shigemoto R, Mizuno N. Glutaminase-like immunoreactivity
    in the lower brainstem and cerebellum of the adult rat. <i>Neuroscience</i>. 1989;32(1):79-98.
    doi:<a href="https://doi.org/10.1016/0306-4522(89)90109-7">10.1016/0306-4522(89)90109-7</a>
  apa: Kaneko, T., Itoh, K., Shigemoto, R., &#38; Mizuno, N. (1989). Glutaminase-like
    immunoreactivity in the lower brainstem and cerebellum of the adult rat. <i>Neuroscience</i>.
    Elsevier. <a href="https://doi.org/10.1016/0306-4522(89)90109-7">https://doi.org/10.1016/0306-4522(89)90109-7</a>
  chicago: Kaneko, Takeshi, Kazuo Itoh, Ryuichi Shigemoto, and Noboru Mizuno. “Glutaminase-like
    Immunoreactivity in the Lower Brainstem and Cerebellum of the Adult Rat.” <i>Neuroscience</i>.
    Elsevier, 1989. <a href="https://doi.org/10.1016/0306-4522(89)90109-7">https://doi.org/10.1016/0306-4522(89)90109-7</a>.
  ieee: T. Kaneko, K. Itoh, R. Shigemoto, and N. Mizuno, “Glutaminase-like immunoreactivity
    in the lower brainstem and cerebellum of the adult rat,” <i>Neuroscience</i>,
    vol. 32, no. 1. Elsevier, pp. 79–98, 1989.
  ista: Kaneko T, Itoh K, Shigemoto R, Mizuno N. 1989. Glutaminase-like immunoreactivity
    in the lower brainstem and cerebellum of the adult rat. Neuroscience. 32(1), 79–98.
  mla: Kaneko, Takeshi, et al. “Glutaminase-like Immunoreactivity in the Lower Brainstem
    and Cerebellum of the Adult Rat.” <i>Neuroscience</i>, vol. 32, no. 1, Elsevier,
    1989, pp. 79–98, doi:<a href="https://doi.org/10.1016/0306-4522(89)90109-7">10.1016/0306-4522(89)90109-7</a>.
  short: T. Kaneko, K. Itoh, R. Shigemoto, N. Mizuno, Neuroscience 32 (1989) 79–98.
date_created: 2018-12-11T11:57:54Z
date_published: 1989-01-01T00:00:00Z
date_updated: 2022-02-15T09:47:08Z
day: '01'
doi: 10.1016/0306-4522(89)90109-7
extern: '1'
external_id:
  pmid:
  - '2586753'
intvolume: '        32'
issue: '1'
language:
- iso: eng
main_file_link:
- url: https://www.sciencedirect.com/science/article/pii/0306452289901097?via%3Dihub
month: '01'
oa_version: None
page: 79 - 98
pmid: 1
publication: Neuroscience
publication_identifier:
  eissn:
  - 1873-7544
  issn:
  - 0306-4522
publication_status: published
publisher: Elsevier
publist_id: '4422'
quality_controlled: '1'
scopus_import: '1'
status: public
title: Glutaminase-like immunoreactivity in the lower brainstem and cerebellum of
  the adult rat
type: journal_article
user_id: ea97e931-d5af-11eb-85d4-e6957dddbf17
volume: 32
year: '1989'
...
