Cerebral Cortex, Vol. 12, No. 4, 395-410,
April 2002
© 2002 Oxford University Press
Anatomical, Physiological, Molecular and Circuit Properties of Nest Basket Cells in the Developing Somatosensory Cortex
1 Section of Neurobiology, Yale University School of Medicine, New Haven, CT 06520-8001, USA and , 2 Department of Neurobiology, Weizmann Institute of Science, 76100 Rehovot, Israel
Henry Markram, Department of Neuro-biology, Weizmann Institute of Science, 76100 Rehovot, Israel. Email: henry.markram{at}weizmann.ac.il.
Anatomical, electrophysiological and molecular diversity of basket cell-like interneurons in layers II–IV of rat somatosensory cortex were studied using patch-clamp electrodes filled with biocytin. This multiparametric study shows that neocortical basket cells (BCs) are composed of three distinct subclasses: classical large (LBC) and small (SBC) basket cells and a third subclass, the nest basket cell (NBC). Anatomically, NBCs were distinct from LBCs and SBCs in that they formed simpler dendritic arbors and an axonal plexus of inter-mediate density, composed of a few long, smooth axonal branches. Electrophysiologically, NBCs exhibited diverse discharge responses to depolarizing current injections including accommodation, non-accommodation and stuttering. Single-cell multiplex RT-PCR revealed distinct mRNA expression patterns for the calcium binding proteins parvalbumin (PV), calbindin (CB) and calretinin (CR), and the neuropeptides somatostatin (SOM), vasoactive intestinal peptide (VIP), cholecystokinin (CCK) and neuropeptide Y (NPY) for each BC-subclass. SBCs lacked NPY expression but invariably expressed VIP, whereas neither VIP, CR nor SOM expression was detected in LBCs, and VIP and CR expression was absent in NBCs. Electro-physiologically distinct types of NBCs formed GABAergic synapses with specific dynamics onto pyramidal cells (PCs) and received either strongly facilitating or depressing synaptic inputs from PCs. Finally, NBCs were found to be the most common basket cell in layers II/III, while LBCs were the most common in layer IV. These data provide multiparametric distinguishing features of three major subclasses of basket cells and indicate that NBCs are powerful interneurons that provide most of the (peri-)somatic inhibition in the supragranular layers.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. V. Zaitsev, N. V. Povysheva, G. Gonzalez-Burgos, D. Rotaru, K. N. Fish, L. S. Krimer, and D. A. Lewis Interneuron Diversity in Layers 2-3 of Monkey Prefrontal Cortex Cereb Cortex, July 1, 2009; 19(7): 1597 - 1615. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Caputi, A. Rozov, M. Blatow, and H. Monyer Two Calretinin-Positive GABAergic Cell Types in Layer 2/3 of the Mouse Neocortex Provide Different Forms of Inhibition Cereb Cortex, June 1, 2009; 19(6): 1345 - 1359. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Q.-Q. Sun, Z. Zhang, Y. Jiao, C. Zhang, G. Szabo, and F. Erdelyi Differential Metabotropic Glutamate Receptor Expression and Modulation in Two Neocortical Inhibitory Networks J Neurophysiol, May 1, 2009; 101(5): 2679 - 2692. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Z. J. Huang Activity-dependent development of inhibitory synapses and innervation pattern: role of GABA signalling and beyond J. Physiol., May 1, 2009; 587(9): 1881 - 1888. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Helmstaedter, B. Sakmann, and D. Feldmeyer The Relation between Dendritic Geometry, Electrical Excitability, and Axonal Projections of L2/3 Interneurons in Rat Barrel Cortex Cereb Cortex, April 1, 2009; 19(4): 938 - 950. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Helmstaedter, B. Sakmann, and D. Feldmeyer L2/3 Interneuron Groups Defined by Multiparameter Analysis of Axonal Projection, Dendritic Geometry, and Electrical Excitability Cereb Cortex, April 1, 2009; 19(4): 951 - 962. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Karagiannis, T. Gallopin, C. David, D. Battaglia, H. Geoffroy, J. Rossier, E. M. C. Hillman, J. F. Staiger, and B. Cauli Classification of NPY-Expressing Neocortical Interneurons J. Neurosci., March 18, 2009; 29(11): 3642 - 3659. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Kumar and O. Ohana Inter- and Intralaminar Subcircuits of Excitatory and Inhibitory Neurons in Layer 6a of the Rat Barrel Cortex J Neurophysiol, October 1, 2008; 100(4): 1909 - 1922. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Helmstaedter, J. F. Staiger, B. Sakmann, and D. Feldmeyer Efficient Recruitment of Layer 2/3 Interneurons by Layer 4 Input in Single Columns of Rat Somatosensory Cortex J. Neurosci., August 13, 2008; 28(33): 8273 - 8284. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. I. Krook-Magnuson, P. Li, S. M. Paluszkiewicz, and M. M. Huntsman Tonically Active Inhibition Selectively Controls Feedforward Circuits in Mouse Barrel Cortex J Neurophysiol, August 1, 2008; 100(2): 932 - 944. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Morita Possible Role of Dendritic Compartmentalization in the Spatial Working Memory Circuit J. Neurosci., July 23, 2008; 28(30): 7699 - 7724. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. A. Atencio and C. E. Schreiner Spectrotemporal Processing Differences between Auditory Cortical Fast-Spiking and Regular-Spiking Neurons J. Neurosci., April 9, 2008; 28(15): 3897 - 3910. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Uematsu, Y. Hirai, F. Karube, S. Ebihara, M. Kato, K. Abe, K. Obata, S. Yoshida, M. Hirabayashi, Y. Yanagawa, et al. Quantitative Chemical Composition of Cortical GABAergic Neurons Revealed in Transgenic Venus-Expressing Rats Cereb Cortex, February 1, 2008; 18(2): 315 - 330. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. B. Glickstein, H. Moore, B. Slowinska, J. Racchumi, M. Suh, N. Chuhma, and M. E. Ross Selective cortical interneuron and GABA deficits in cyclin D2-null mice Development, November 15, 2007; 134(22): 4083 - 4093. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Miyoshi, S. J. B. Butt, H. Takebayashi, and G. Fishell Physiologically Distinct Temporal Cohorts of Cortical Interneurons Arise from Telencephalic Olig2-Expressing Precursors J. Neurosci., July 18, 2007; 27(29): 7786 - 7798. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. B. Ali, A. P. Bannister, and A. M. Thomson Robust correlations between action potential duration and the properties of synaptic connections in layer 4 interneurones in neocortical slices from juvenile rats and adult rat and cat J. Physiol., April 1, 2007; 580(1): 149 - 169. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Dumitriu, R. Cossart, J. Huang, and R. Yuste Correlation Between Axonal Morphologies and Synaptic Input Kinetics of Interneurons from Mouse Visual Cortex Cereb Cortex, January 1, 2007; 17(1): 81 - 91. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Yano, T. Subkhankulova, F. J. Livesey, and H. P. C. Robinson Electrophysiological and gene expression profiling of neuronal cell types in mammalian neocortex J. Physiol., September 1, 2006; 575(2): 361 - 365. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Takahata, Y. Komatsu, A. Watakabe, T. Hashikawa, S. Tochitani, and T. Yamamori Activity-dependent Expression of occ1 in Excitatory Neurons Is a Characteristic Feature of the Primate Visual Cortex Cereb Cortex, July 1, 2006; 16(7): 929 - 940. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Ma, H. Hu, A. S. Berrebi, P. H. Mathers, and A. Agmon Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J. Neurosci., May 10, 2006; 26(19): 5069 - 5082. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Kawaguchi, F. Karube, and Y. Kubota Dendritic Branch Typing and Spine Expression Patterns in Cortical Nonpyramidal Cells Cereb Cortex, May 1, 2006; 16(5): 696 - 711. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Q.-Q. Sun, J. R. Huguenard, and D. A. Prince Barrel Cortex Microcircuits: Thalamocortical Feedforward Inhibition in Spiny Stellate Cells Is Mediated by a Small Number of Fast-Spiking Interneurons J. Neurosci., January 25, 2006; 26(4): 1219 - 1230. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. S. Krimer, A. V. Zaitsev, G. Czanner, S. Kroner, G. Gonzalez-Burgos, N. V. Povysheva, S. Iyengar, G. Barrionuevo, and D. A. Lewis Cluster Analysis-Based Physiological Classification and Morphological Properties of Inhibitory Neurons in Layers 2-3 of Monkey Dorsolateral Prefrontal Cortex J Neurophysiol, November 1, 2005; 94(5): 3009 - 3022. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Toledo-Rodriguez, P. Goodman, M. Illic, C. Wu, and H. Markram Neuropeptide and calcium-binding protein gene expression profiles predict neuronal anatomical type in the juvenile rat J. Physiol., September 1, 2005; 567(2): 401 - 413. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Zilberter, T. Harkany, and C. D. Holmgren Dendritic Release of Retrograde Messengers Controls Synaptic Transmission in Local Neocortical Networks Neuroscientist, August 1, 2005; 11(4): 334 - 344. [Abstract] [PDF]
|
|
|
|
|
|
H. Wang, I. M. Hitron, C. Iadecola, and V. M. Pickel Synaptic and Vascular Associations of Neurons Containing Cyclooxygenase-2 and Nitric Oxide Synthase in Rat Somatosensory Cortex Cereb Cortex, August 1, 2005; 15(8): 1250 - 1260. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. D. Traub, D. Contreras, M. O. Cunningham, H. Murray, F. E. N. LeBeau, A. Roopun, A. Bibbig, W. B. Wilent, M. J. Higley, and M. A. Whittington Single-Column Thalamocortical Network Model Exhibiting Gamma Oscillations, Sleep Spindles, and Epileptogenic Bursts J Neurophysiol, April 1, 2005; 93(4): 2194 - 2232. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Gonzalez-Burgos, L. S. Krimer, N. V. Povysheva, G. Barrionuevo, and D. A. Lewis Functional Properties of Fast Spiking Interneurons and Their Synaptic Connections With Pyramidal Cells in Primate Dorsolateral Prefrontal Cortex J Neurophysiol, February 1, 2005; 93(2): 942 - 953. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Palma, D. A. Lim, N. Dahmane, P. Sanchez, T. C. Brionne, C. D. Herzberg, Y. Gitton, A. Carleton, A. Alvarez-Buylla, and A. R. i Altaba Sonic hedgehog controls stem cell behavior in the postnatal and adult brain Development, January 15, 2005; 132(2): 335 - 344. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Korngreen, K. M. M. Kaiser, and Y. Zilberter Subthreshold inactivation of voltage-gated K+ channels modulates action potentials in neocortical bitufted interneurones from rats J. Physiol., January 15, 2005; 562(2): 421 - 437. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Toledo-Rodriguez, B. Blumenfeld, C. Wu, J. Luo, B. Attali, P. Goodman, and H. Markram Correlation Maps Allow Neuronal Electrical Properties to be Predicted from Single-cell Gene Expression Profiles in Rat Neocortex Cereb Cortex, December 1, 2004; 14(12): 1310 - 1327. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Wang, M. Toledo-Rodriguez, A. Gupta, C. Wu, G. Silberberg, J. Luo, and H. Markram Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat J. Physiol., November 15, 2004; 561(1): 65 - 90. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Chattopadhyaya, G. Di Cristo, H. Higashiyama, G. W. Knott, S. J. Kuhlman, E. Welker, and Z. J. Huang Experience and Activity-Dependent Maturation of Perisomatic GABAergic Innervation in Primary Visual Cortex during a Postnatal Critical Period J. Neurosci., October 27, 2004; 24(43): 9598 - 9611. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. A. Fortin, J. Trettel, and E. S. Levine Brief Trains of Action Potentials Enhance Pyramidal Neuron Excitability Via Endocannabinoid-Mediated Suppression of Inhibition J Neurophysiol, October 1, 2004; 92(4): 2105 - 2112. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Jolivet, T. J. Lewis, and W. Gerstner Generalized Integrate-and-Fire Models of Neuronal Activity Approximate Spike Trains of a Detailed Model to a High Degree of Accuracy J Neurophysiol, August 1, 2004; 92(2): 959 - 976. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. F. Staiger, I. Flagmeyer, D. Schubert, K. Zilles, R. Kotter, and H. J. Luhmann Functional Diversity of Layer IV Spiny Neurons in Rat Somatosensory Cortex: Quantitative Morphology of Electrophysiologically Characterized and Biocytin Labeled Cells Cereb Cortex, June 1, 2004; 14(6): 690 - 701. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Harkany, C. Holmgren, W. Hartig, T. Qureshi, F. A. Chaudhry, J. Storm-Mathisen, M. B. Dobszay, P. Berghuis, G. Schulte, K. M. Sousa, et al. Endocannabinoid-Independent Retrograde Signaling at Inhibitory Synapses in Layer 2/3 of Neocortex: Involvement of Vesicular Glutamate Transporter 3 J. Neurosci., May 26, 2004; 24(21): 4978 - 4988. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Gonzalez-Burgos, L. S. Krimer, N. N. Urban, G. Barrionuevo, and D. A. Lewis Synaptic Efficacy during Repetitive Activation of Excitatory Inputs in Primate Dorsolateral Prefrontal Cortex Cereb Cortex, May 1, 2004; 14(5): 530 - 542. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Wang and P. S. Goldman-Rakic D2 receptor regulation of synaptic burst firing in prefrontal cortical pyramidal neurons PNAS, April 6, 2004; 101(14): 5093 - 5098. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Karube, Y. Kubota, and Y. Kawaguchi Axon Branching and Synaptic Bouton Phenotypes in GABAergic Nonpyramidal Cell Subtypes J. Neurosci., March 24, 2004; 24(12): 2853 - 2865. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Gonchar and A. Burkhalter Distinct GABAergic Targets of Feedforward and Feedback Connections Between Lower and Higher Areas of Rat Visual Cortex J. Neurosci., November 26, 2003; 23(34): 10904 - 10912. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Beierlein, J. R. Gibson, and B. W. Connors Two Dynamically Distinct Inhibitory Networks in Layer 4 of the Neocortex J Neurophysiol, November 1, 2003; 90(5): 2987 - 3000. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Bacci, U. Rudolph, J. R. Huguenard, and D. A. Prince Major Differences in Inhibitory Synaptic Transmission onto Two Neocortical Interneuron Subclasses J. Neurosci., October 22, 2003; 23(29): 9664 - 9674. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Holmgren, T. Harkany, B. Svennenfors, and Y. Zilberter Pyramidal cell communication within local networks in layer 2/3 of rat neocortex J. Physiol., August 15, 2003; 551(1): 139 - 153. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. C. Angulo, J. F. Staiger, J. Rossier, and E. Audinat Distinct Local Circuits Between Neocortical Pyramidal Cells and Fast-Spiking Interneurons in Young Adult Rats J Neurophysiol, February 1, 2003; 89(2): 943 - 953. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Bacci, J. R. Huguenard, and D. A. Prince Functional Autaptic Neurotransmission in Fast-Spiking Interneurons: A Novel Form of Feedback Inhibition in the Neocortex J. Neurosci., February 1, 2003; 23(3): 859 - 866. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Thomson and A. P. Bannister Interlaminar Connections in the Neocortex Cereb Cortex, January 1, 2003; 13(1): 5 - 14. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Thomson, D. C. West, Y. Wang, and A. P. Bannister Synaptic Connections and Small Circuits Involving Excitatory and Inhibitory Neurons in Layers 2-5 of Adult Rat and Cat Neocortex: Triple Intracellular Recordings and Biocytin Labelling In Vitro Cereb Cortex, September 1, 2002; 12(9): 936 - 953. [Abstract] [Full Text] [PDF]
|
|