The DOI matches its Crossref record; 5 of the 5 references it cites were found in a registry or an index.
Local circuit neurons immunoreactive for calretinin, calbindin D‐28k or parvalbumin in monkey prefronatal cortex: Distribution and morphology
Abstract
In the cerebral cortex, local circuit neurons provide critical inhibitory control over the activity of pyramidal neurons, the major class of excitatory efferent cortical cells. The calciumbinding proteins, calretinin, calbindin, and parvalbumin, are expressed in a variety of cortical local circuit neurons. However, in the primate prefrontal cortex, relatively little is known, especially with regard to calretinin, about the specific classes or distribution of local circuit neurons that contain these calcium‐binding proteins. In this study, we used immunohistochemical techniques to characterize and compare the morphological features and distribution in macaque monkey prefrontal cortex of local circuit neurons that contain each of these calcium‐binding proteins. On the basis of the axonal features of the labeled neurons, and correlations with previous Golgi studies, calretinin appeared to be present in double‐bouquet neurons, calbindin in neurogliaform neurons and Martinotti cells, and parvalbumin in chandelier and wide arbor (basket) neurons. Calretinin was also found in other cell populations, such as a distinctive group of large neurons in the infragranular layers, but it was not possible to assign these neurons to a known cell class. In addition, although the animals studied were adults, immunoreactivity for both calretinin and calbindin was found in Cajal‐Retzius neurons of layer I. Dual labeling studies confirmed that with the exception of the Cajal‐Retzius neurons, each calcium‐binding protein was expressed in separate populations of prefrontal cortical neurons. Comparisons of the laminar distributions of the labeled neurons also indicated that these calcium‐binding proteins were segregated into discrete neuronal populations. Calretinin‐positive neurons were present in greatest density in deep layer I and layer II, calbindin‐immuno‐reactive cells were most dense in layers II‐superficial III, and parvalbumin‐containing neurons were present in greatest density in the middle cortical layers. In addition, the relative density of calretinin‐labeled neurons was approximately twice that of the calbindin‐ and parvalbumin‐positive neurons. However, within each group of labeled neurons, their laminar distribution and relative density did not differ substantially across regions of the prefrontal cortex. These findings demonstrate that calretinin, calbindin, and parvalbumin are markers of separate populations of local circuit neurons in monkey prefrontal cortex, and that they may be useful tools in unraveling the intrinsic inhibitory circuitry of the primate prefrontal cortex in both normal and disease states.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Somogyi, P., Kisvárday, Z. F., Martin, K. A. C., & Whitteridge, D. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90133-1 · Cited by 423
DeFelipe, J., Hendry, S. H. C., Hashikawa, T., Molinari, M., & Jones, E. G. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90097-n · Cited by 231
Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity
DeFelipe, J., Hendry, S. H. C., & Jones, E. G. (1989) · Brain Research · doi:10.1016/0006-8993(89)91702-2 · Cited by 226
De Lima, A. D., & Morrison, J. H. (1989) · Journal of Comparative Neurology · doi:10.1002/cne.902830205 · Cited by 91
Hayes, T. L., & Lewis, D. A. (1992) · Cerebral Cortex · doi:10.1093/cercor/2.1.56 · Cited by 80
Self-citation
Cited by
Cortical inhibitory neurons and schizophrenia
Lewis, D. A., Hashimoto, T., & Volk, D. W. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1648 · Cited by 2,297
Self-citationStructural and molecular interrogation of intact biological systems
Chung, K., Wallace, J., Kim, S.-Y., Kalyanasundaram, S., Andalman, A. S., Davidson, T. J., Mirzabekov, J. J., Zalocusky, K. A., Mattis, J., Denisin, A. K., et al. (2013) · Nature · doi:10.1038/nature12107 · Cited by 2,008
NEURONAL CIRCUITS OF THE NEOCORTEX
Douglas, R. J., & Martin, K. A. C. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144152 · Cited by 1,886
Reconstruction and Simulation of Neocortical Microcircuitry
Markram, H., Muller, E., Ramaswamy, S., Reimann, M. W., Abdellah, M., Sanchez, C. A., Ailamaki, A., Alonso-Nanclares, L., Antille, N., Arsever, S., et al. (2015) · Cell · doi:10.1016/j.cell.2015.09.029 · Cited by 1,557
GABAergic cell subtypes and their synaptic connections in rat frontal cortex
Kawaguchi, Y. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.6.476 · Cited by 1,416
GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder
Benes, F. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00225-1 · Cited by 1,082
Hashimoto, T., Volk, D. W., Eggan, S. M., Mirnics, K., Pierri, J. N., Sun, Z., Sampson, A. R., & Lewis, D. A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-15-06315.2003 · Cited by 938
Self-citationGhashghaei, H. T., & Barbas, H. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00446-3 · Cited by 785
Burt, J. B., Demirtaş, M., Eckner, W. J., Navejar, N. M., Ji, J. L., Martin, W. J., Bernacchia, A., Anticevic, A., & Murray, J. D. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0195-0 · Cited by 657
Brunel, N., & Wang, X.-J. (2001) · Journal of Computational Neuroscience · doi:10.1023/a:1011204814320 · Cited by 620
Ketamine-Induced Loss of Phenotype of Fast-Spiking Interneurons Is Mediated by NADPH-Oxidase
Behrens, M. M., Ali, S. S., Dao, D. N., Lucero, J., Shekhtman, G., Quick, K. L., & Dugan, L. L. (2007) · Science · doi:10.1126/science.1148045 · Cited by 585
DeFelipe, J. (1997) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(97)10013-8 · Cited by 550
Jakab, R. L., & Goldman-Rakic, P. S. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.2.735 · Cited by 536
Wang, Y., Toledo‐Rodriguez, M., Gupta, A., Wu, C., Silberberg, G., Luo, J., & Markram, H. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.073353 · Cited by 491
Emerging principles of altered neural circuitry in schizophrenia
Benes, F. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00041-7 · Cited by 513
Hashimoto, T., Arion, D., Unger, T., Maldonado-Avilés, J. G., Morris, H. M., Volk, D. W., Mirnics, K., & Lewis, D. A. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002011 · Cited by 490
Self-citationHashimoto, T., Bazmi, H. H., Mirnics, K., Wu, Q., Sampson, A. R., & Lewis, D. A. (2008) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.07081223 · Cited by 457
Self-citationFunctional maps of neocortical local circuitry.
Thomson, A. M. (2007) · Frontiers in Neuroscience · doi:10.3389/neuro.01.1.1.002.2007 · Cited by 434
Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics
BEASLEY, C., & REYNOLDS, G. (1997) · Schizophrenia Research · doi:10.1016/s0920-9964(96)00122-3 · Cited by 426
Rajkowska, G., O'Dwyer, G., Teleki, Z., Stockmeier, C. A., & Miguel-Hidalgo, J. J. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301234 · Cited by 430
Eze, U. C., Bhaduri, A., Haeussler, M., Nowakowski, T. J., & Kriegstein, A. R. (2021) · Nature Neuroscience · doi:10.1038/s41593-020-00794-1 · Cited by 427
Modeling Sleep and Wakefulness in the Thalamocortical System
Hill, S., & Tononi, G. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00915.2004 · Cited by 417
Woo, T.-U. W., Walsh, J. P., & Benes, F. M. (2004) · Archives of General Psychiatry · doi:10.1001/archpsyc.61.7.649 · Cited by 411
Lewis, D. (1997) · Neuropsychopharmacology · doi:10.1016/s0893-133x(96)00277-1 · Cited by 388
Self-citationAnatomy of the Prefrontal Cortex
Fuster, J. M. (2008) · The Prefrontal Cortex · doi:10.1016/b978-0-12-373644-4.00002-5 · Cited by 364
Altered neural connectivity in excitatory and inhibitory cortical circuits in autism
Zikopoulos, B., & Barbas, H. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00609 · Cited by 313
Hashemi, E., Ariza, J., Rogers, H., Noctor, S. C., & Martínez-Cerdeño, V. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw021 · Cited by 322
Gorelova, N., Seamans, J. K., & Yang, C. R. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00335.2002 · Cited by 302
GABAergic local circuit neurons and prefrontal cortical dysfunction in schizophrenia
Lewis, D. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00042-9 · Cited by 257
Self-citationLewis, D., Volk, D., & Hashimoto, T. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1673-x · Cited by 253
Self-citationAnderson, S. A., Classey, J. D., Condé, F., Lund, J. S., & Lewis, D. A. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00051-j · Cited by 245
Self-citationQuantitative Architecture Distinguishes Prefrontal Cortical Systems in the Rhesus Monkey
Dombrowski, S. M. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.10.975 · Cited by 240
Smucny, J., Dienel, S. J., Lewis, D. A., & Carter, C. S. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01089-0 · Cited by 231
Self-citationReduced level of glutamic acid decarboxylase-67 kDa in the prefrontal cortex in major depression
Karolewicz, B., Maciag, D., O'Dwyer, G., Stockmeier, C. A., Feyissa, A. M., & Rajkowska, G. (2010) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145709990587 · Cited by 203
Caballero, A., Flores-Barrera, E., Cass, D. K., & Tseng, K. Y. (2014) · Brain Structure and Function · doi:10.1007/s00429-013-0508-8 · Cited by 178
Morphology and physiology of cortical neurons in layer I
Hestrin, S., & Armstrong, W. E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-17-05290.1996 · Cited by 194
Lumer, E. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.3.207 · Cited by 186
Cntnap4 differentially contributes to GABAergic and dopaminergic synaptic transmission
Karayannis, T., Au, E., Patel, J. C., Kruglikov, I., Markx, S., Delorme, R., Héron, D., Salomon, D., Glessner, J., Restituito, S., et al. (2014) · Nature · doi:10.1038/nature13248 · Cited by 183
Glutamatergic Synaptic Dysregulation in Schizophrenia: Therapeutic Implications
Coyle, J. T., Basu, A., Benneyworth, M., Balu, D., & Konopaske, G. (2012) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-642-25758-2_10 · Cited by 180
Powell, S. B., Sejnowski, T. J., & Behrens, M. M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.049 · Cited by 164
Wang, C. Z., Yang, S. F., Xia, Y., & Johnson, K. M. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301647 · Cited by 161
Chung, D. W., Fish, K. N., & Lewis, D. A. (2016) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2016.16010025 · Cited by 148
“Excitatory synapses on PV interneurons predict PV and GAD67 expression levels in human DLPFC Finally, we assessed whether the density of excitatory synapses on PV+ neurons predicted levels of PV and GAD67, molecular markers of PV interneuron activity.”
BackgroundMethodInfluentialSelf-citationGlausier, J. R., Fish, K. N., & Lewis, D. A. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.152 · Cited by 147
Self-citationBelmalih, A., Borra, E., Contini, M., Gerbella, M., Rozzi, S., & Luppino, G. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21892 · Cited by 142
Cortical basket cell dysfunction in schizophrenia
Curley, A. A., & Lewis, D. A. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.224659 · Cited by 136
Self-citationComparative density of CCK- and PV-GABA cells within the cortex and hippocampus
Whissell, P. D., Cajanding, J. D., Fogel, N., & Kim, J. C. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00124 · Cited by 118
The Relationship Between Synchronization Among Neuronal Populations and Their Mean Activity Levels
Chawla, D., Lumer, E. D., & Friston, K. J. (1999) · Neural Computation · doi:10.1162/089976699300016287 · Cited by 125
Connectivity of GABAergic Calretinin-immunoreactive Neurons in Rat Primary Visual Cortex
Gonchar, Y. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.7.683 · Cited by 117
Cruz, D. A., Eggan, S. M., & Lewis, D. A. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10833 · Cited by 118
Self-citationSakai, T., Oshima, A., Nozaki, Y., Ida, I., Haga, C., Akiyama, H., Nakazato, Y., & Mikuni, M. (2008) · Neuropathology · doi:10.1111/j.1440-1789.2007.00867.x · Cited by 118
A disinhibitory circuit motif and flexible information routing in the brain
Wang, X.-J., & Yang, G. R. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.01.002 · Cited by 113
Barbas, H., Medalla, M., Alade, O., Suski, J., Zikopoulos, B., & Lera, P. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi018 · Cited by 112
Erickson, S. L., & Lewis, D. A. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10249 · Cited by 104
Self-citationCabungcal, J.-H., Nicolas, D., Kraftsik, R., Cuénod, M., Do, K. Q., & Hornung, J.-P. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.01.003 · Cited by 96
Paspalas, C. D., & Goldman-Rakic, P. S. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3436-04.2005 · Cited by 94
Pérez-Cremades, D., Hernández, S., Blasco-Ibáñez, J. M., Crespo, C., Nacher, J., & Varea, E. (2010) · Journal of Neural Transmission · doi:10.1007/s00702-010-0376-9 · Cited by 85
Spatio-temporal extension in site of origin for cortical calretinin neurons in primates
Hladnik, A., Džaja, D., Darmopil, S., Jovanov-MiloÅ¡ević, N., & Petanjek, Z. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00050 · Cited by 72
Specificity in inhibitory systems associated with prefrontal pathways to temporal cortex in Primates
Medalla, M., Lera, P., Feinberg, M., & Barbas, H. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm068 · Cited by 69
Povysheva, N. V., & Johnson, J. W. (2012) · Journal of Neurophysiology · doi:10.1152/jn.01017.2011 · Cited by 62
Wędzony, K., & Chocyk, A. (2009) · Pharmacological Reports · doi:10.1016/s1734-1140(09)70161-6 · Cited by 50
Curley, A. A., Eggan, S. M., Lazarus, M. S., Huang, Z. J., Volk, D. W., & Lewis, D. A. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.10.018 · Cited by 51
Self-citationPathways for Contextual Memory: The Primate Hippocampal Pathway to Anterior Cingulate Cortex
Wang, J., John, Y., & Barbas, H. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhaa333 · Cited by 39
Disney, A. A., & Reynolds, J. H. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23456 · Cited by 40
“This contrasts with PV expression in macaque prefrontal cortex and in the rodent neocortex, where only 50% of GABAergic neurons express PV (Conde et al., 1994; Gonchar and Burkhalter, 1997).”
BackgroundLemmens, M. A. M., Sierksma, A. S. R., Rutten, B. P. F., Dennissen, F., Steinbusch, H. W. M., Lucassen, P. J., & Schmitz, C. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0305-1 · Cited by 37
Disney, A. A., Alasady, H. A., & Reynolds, J. H. (2014) · Brain and Behavior · doi:10.1002/brb3.225 · Cited by 28
Neuropathology of Schizophrenia
Harrison, P. J., Lewis, D. A., & Kleinman, J. E. (2010) · Schizophrenia · doi:10.1002/9781444327298.ch18 · Cited by 26
Self-citationBenchmarking macaque brain gene expression for horizontal and vertical translation
Luppi, A. I., Liu, Z.-Q., Hansen, J. Y., Cofre, R., Niu, M., Kuzmin, E., Froudist-Walsh, S., Palomero-Gallagher, N., & Misic, B. (2025) · Science Advances · doi:10.1126/sciadv.ads6967 · Cited by 14
McDonald, A. J., Hamilton, P. G., & Barnstable, C. J. (2018) · Brain Structure and Function · doi:10.1007/s00429-017-1542-8 · Cited by 11
Metadata
- Authors
- Condé, F., Lund, J. S., Jacobowitz, D. M., Baimbridge, K. G., & Lewis, D. A.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 1994-03
- Volume
- 341
- Issue
- 1
- Pages
- 95-116
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2032742540
- Cited by
- 500
- References
- 5
- FWCI
- 7.73
- Type
- journal article
- Language
- en
- Open access
- closed
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.