Organized growth of thalamocortical axons from the deep tier of terminations into layer IV of developing mouse barrel cortex

QUICK SEARCH:

[advanced]

	Author:		Keyword(s):
Year:		Vol:		Page:

HOME | SEARCH | ARCHIVE | SUBSCRIBE | CONTACT | HELP

This Article

Full Text (PDF)

Submit an eLetter

Alert me when this article is cited

Alert me when eLetters are posted

Alert me if a correction is posted

Citation Map

Services

Email this article to a friend

Similar articles in this journal

Similar articles in PubMed

Alert me to new issues of the journal

Download to citation manager

Citing Articles

Citing Articles via HighWire

Citing Articles via Google Scholar

Google Scholar

Articles by Agmon, A.

Articles by Jones, E. G.

Search for Related Content

PubMed

PubMed Citation

Articles by Agmon, A.

Articles by Jones, E. G.

Previous Article | Next Article

Journal of Neuroscience, Vol 13, 5365-5382, Copyright © 1993 by Society for Neuroscience

ARTICLE

Organized growth of thalamocortical axons from the deep tier of terminations into layer IV of developing mouse barrel cortex

A Agmon, LT Yang, DK O'Dowd and EG Jones
Department of Anatomy, University of California, Irvine 92717.
The thalamocortical projection to rodent somatosensory ("barrell") cortex is highly ordered in both the radial and the tangential dimensions. During a brief period of postnatal development, thalamocortical axons establish two tiers of terminations, in the deep layers and in layer IV, and form whisker-specific clusters within layer IV; however, little is known about the cues that guide them to their appropriate radial and tangential positions. To gain insight into potential mechanisms underlying this process, we studied the development of thalamocortical termination patterns in mouse barrel cortex at high spatial resolution. Developing thalamocortical axons were labeled in fixed slices with the lipophilic carbocyanine dye Dil and imaged with a laser scanning confocal microscope. On the day of birth (postnatal day 0, P0) axons coursed through layers VI and V, with little or no branching. By P2 the lower tier of terminations, at the border of layers VI and V, was clearly identifiable. Below this tier axons coursed obliquely or tangentially, forming a dense meshwork of intersecting fibers, but with no apparent branching. By P4 the upper tier of terminations, in layer IV, was clearly recognizable, and consisted of periodic, dense clusters of terminal arborizations. In marked contrast to the oblique and apparently disorderly course followed by axons in layer VI and lower layer V, axons in upper layer V heading toward the upper tier were organized in loose bundles running radially, suggesting that axons destined to terminate in a particular layer IV barrel had already reached their appropriate tangential coordinates within the lower tier. Thus, the pattern of thalamocortical terminations in layer IV seems to be projected from the deep tier of terminations, and does not develop from an initially profuse arborization pattern through pruning of inappropriate branches.

This article has been cited by other articles:

Y. Hayano and N. Yamamoto
Activity-Dependent Thalamocortical Axon Branching
Neuroscientist, August 1, 2008; 14(4): 359 - 368.
[Abstract] [PDF]

T. Iwasato, M. Inan, H. Kanki, R. S. Erzurumlu, S. Itohara, and M. C. Crair
Cortical Adenylyl Cyclase 1 Is Required for Thalamocortical Synapse Maturation and Aspects of Layer IV Barrel Development
J. Neurosci., June 4, 2008; 28(23): 5931 - 5943.
[Abstract] [Full Text] [PDF]

C. Takasaki, R. Okada, A. Mitani, M. Fukaya, M. Yamasaki, Y. Fujihara, T. Shirakawa, K. Tanaka, and M. Watanabe
Glutamate Transporters Regulate Lesion-Induced Plasticity in the Developing Somatosensory Cortex
J. Neurosci., May 7, 2008; 28(19): 4995 - 5006.
[Abstract] [Full Text] [PDF]

Z. Tan, H. Hu, Z. J. Huang, and A. Agmon
Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons
PNAS, February 12, 2008; 105(6): 2187 - 2192.
[Abstract] [Full Text] [PDF]

M. J. Galazo, V. Martinez-Cerdeno, C. Porrero, and F. Clasca
Embryonic and Postnatal Development of the Layer I-Directed ("Matrix") Thalamocortical System in the Rat
Cereb Cortex, February 1, 2008; 18(2): 344 - 363.
[Abstract] [Full Text] [PDF]

C. P. J. de Kock, R. M. Bruno, H. Spors, and B. Sakmann
Layer- and cell-type-specific suprathreshold stimulus representation in rat primary somatosensory cortex
J. Physiol., May 15, 2007; 581(1): 139 - 154.
[Abstract] [Full Text] [PDF]

N. Uesaka, Y. Hayano, A. Yamada, and N. Yamamoto
Interplay between Laminar Specificity and Activity-Dependent Mechanisms of Thalamocortical Axon Branching
J. Neurosci., May 9, 2007; 27(19): 5215 - 5223.
[Abstract] [Full Text] [PDF]

Y. Kubota, S. Hatada, S. Kondo, F. Karube, and Y. Kawaguchi
Neocortical Inhibitory Terminals Innervate Dendritic Spines Targeted by Thalamocortical Afferents
J. Neurosci., January 31, 2007; 27(5): 1139 - 1150.
[Abstract] [Full Text] [PDF]

F. Gheorghita, R. Kraftsik, R. Dubois, and E. Welker
Structural Basis for Map Formation in the Thalamocortical Pathway of the Barrelless Mouse
J. Neurosci., September 27, 2006; 26(39): 10057 - 10067.
[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]

D. F. McLaughlin and S. L. Juliano
Disruption of Layer 4 Development Alters Laminar Processing in Ferret Somatosensory Cortex
Cereb Cortex, November 1, 2005; 15(11): 1791 - 1803.
[Abstract] [Full Text] [PDF]

S. Higashi, K. Hioki, T. Kurotani, N. Kasim, and Z. Molnar
Functional Thalamocortical Synapse Reorganization from Subplate to Layer IV during Postnatal Development in the Reeler-Like Mutant Rat (Shaking Rat Kawasaki)
J. Neurosci., February 9, 2005; 25(6): 1395 - 1406.
[Abstract] [Full Text] [PDF]

K. M. Jacobs and D. A. Prince
Excitatory and Inhibitory Postsynaptic Currents in a Rat Model of Epileptogenic Microgyria
J Neurophysiol, February 1, 2005; 93(2): 687 - 696.
[Abstract] [Full Text] [PDF]

S. B. Mierau, R. M. Meredith, A. L. Upton, and O. Paulsen
Dissociation of experience-dependent and -independent changes in excitatory synaptic transmission during development of barrel cortex
PNAS, October 26, 2004; 101(43): 15518 - 15523.
[Abstract] [Full Text] [PDF]

Y. Zhong, M. Takemoto, T. Fukuda, Y. Hattori, F. Murakami, D. Nakajima, M. Nakayama, and N. Yamamoto
Identification of the Genes that are Expressed in the Upper Layers of the Neocortex
Cereb Cortex, October 1, 2004; 14(10): 1144 - 1152.
[Abstract] [Full Text] [PDF]

K. J. Bender, J. Rangel, and D. E. Feldman
Development of Columnar Topography in the Excitatory Layer 4 to Layer 2/3 Projection in Rat Barrel Cortex
J. Neurosci., September 24, 2003; 23(25): 8759 - 8770.
[Abstract] [Full Text] [PDF]

Y.-Q. Ding, J. Yin, H.-M. Xu, M. F. Jacquin, and Z.-F. Chen
Formation of Whisker-Related Principal Sensory Nucleus-Based Lemniscal Pathway Requires a Paired Homeodomain Transcription Factor, Drg11
J. Neurosci., August 13, 2003; 23(19): 7246 - 7254.
[Abstract] [Full Text] [PDF]

Z. Molnar, S. Higashi, and G. Lopez-Bendito
Choreography of Early Thalamocortical Development
Cereb Cortex, June 1, 2003; 13(6): 661 - 669.
[Abstract] [Full Text] [PDF]

D. F. McLaughlin and S. L. Juliano
Developmental Regulation of Plasticity in the Forepaw Representation of Ferret Somatosensory Cortex
J Neurophysiol, April 1, 2003; 89(4): 2289 - 2298.
[Abstract] [Full Text] [PDF]

K. Poskanzer, L. A. Needleman, O. Bozdagi, and G. W. Huntley
N-Cadherin Regulates Ingrowth and Laminar Targeting of Thalamocortical Axons
J. Neurosci., March 15, 2003; 23(6): 2294 - 2305.
[Abstract] [Full Text] [PDF]

F. Mann, C. Peuckert, F. Dehner, R. Zhou, and J. Bolz
Ephrins regulate the formation of terminal axonal arbors during the development of thalamocortical projections
Development, March 10, 2003; 129(16): 3945 - 3955.
[Abstract] [Full Text] [PDF]

Z. Molnar, G. Lopez-Bendito, J. Small, L. D. Partridge, C. Blakemore, and M. C. Wilson
Normal Development of Embryonic Thalamocortical Connectivity in the Absence of Evoked Synaptic Activity
J. Neurosci., December 1, 2002; 22(23): 10313 - 10323.
[Abstract] [Full Text] [PDF]

M. Beierlein, C. P. Fall, J. Rinzel, and R. Yuste
Thalamocortical Bursts Trigger Recurrent Activity in Neocortical Networks: Layer 4 as a Frequency-Dependent Gate
J. Neurosci., November 15, 2002; 22(22): 9885 - 9894.
[Abstract] [Full Text] [PDF]

A. Rebsam, I. Seif, and P. Gaspar
Refinement of Thalamocortical Arbors and Emergence of Barrel Domains in the Primary Somatosensory Cortex: A Study of Normal and Monoamine Oxidase A Knock-Out Mice
J. Neurosci., October 1, 2002; 22(19): 8541 - 8552.
[Abstract] [Full Text] [PDF]

I. L. Hanganu, W. Kilb, and H. J. Luhmann
Functional Synaptic Projections onto Subplate Neurons in Neonatal Rat Somatosensory Cortex
J. Neurosci., August 15, 2002; 22(16): 7165 - 7176.
[Abstract] [Full Text] [PDF]

J. DeFelipe, J.I. Arellano, A. Merchan-Perez, M.C. Gonzalez-Albo, K. Walton, and R. Llinas
Spaceflight Induces Changes in the Synaptic Circuitry of the Postnatal Developing Neocortex
Cereb Cortex, August 1, 2002; 12(8): 883 - 891.
[Abstract] [Full Text] [PDF]

T. Vitalis, O. Cases, K. Gillies, N. Hanoun, M. Hamon, I. Seif, P. Gaspar, P. Kind, and D. J. Price
Interactions between TrkB Signaling and Serotonin Excess in the Developing Murine Somatosensory Cortex: A Role in Tangential and Radial Organization of Thalamocortical Axons
J. Neurosci., June 15, 2002; 22(12): 4987 - 5000.
[Abstract] [Full Text] [PDF]

S. Iyengar and S. W. Bottjer
Development of Individual Axon Arbors in a Thalamocortical Circuit Necessary for Song Learning in Zebra Finches
J. Neurosci., February 1, 2002; 22(3): 901 - 911.
[Abstract] [Full Text] [PDF]

S. Iyengar and S. W. Bottjer
The Role of Auditory Experience in the Formation of Neural Circuits Underlying Vocal Learning in Zebra Finches
J. Neurosci., February 1, 2002; 22(3): 946 - 958.
[Abstract] [Full Text] [PDF]

R. R. Llinas, E. Leznik, and F. J. Urbano
Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: A voltage-dependent dye-imaging study in mouse brain slices
PNAS, January 1, 2002; (2002) 12604899.
[Abstract] [Full Text] [PDF]

X. Jin, P. H. Mathers, G. Szabo, Z. Katarova, and A. Agmon
Vertical Bias in Dendritic Trees of Non-pyramidal Neocortical Neurons Expressing GAD67-GFP In Vitro
Cereb Cortex, July 1, 2001; 11(7): 666 - 678.
[Abstract] [Full Text] [PDF]

S. C. Noctor, S. L. Palmer, D. F. McLaughlin, and S. L. Juliano
Disruption of Layers 3 and 4 during Development Results in Altered Thalamocortical Projections in Ferret Somatosensory Cortex
J. Neurosci., May 1, 2001; 21(9): 3184 - 3195.
[Abstract] [Full Text] [PDF]

J. T. Porter, C. K. Johnson, and A. Agmon
Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex
J. Neurosci., April 15, 2001; 21(8): 2699 - 2710.
[Abstract] [Full Text] [PDF]

N. Salichon, P. Gaspar, A. L. Upton, S. Picaud, N. Hanoun, M. Hamon, E. De Maeyer, D. L. Murphy, R. Mossner, K. P. Lesch, et al.
Excessive Activation of Serotonin (5-HT) 1B Receptors Disrupts the Formation of Sensory Maps in Monoamine Oxidase A and 5-HT Transporter Knock-Out Mice
J. Neurosci., February 1, 2001; 21(3): 884 - 896.
[Abstract] [Full Text] [PDF]

N. Yamamoto, K. Inui, Y. Matsuyama, A. Harada, K. Hanamura, F. Murakami, E. S. Ruthazer, U. Rutishauser, and T. Seki
Inhibitory Mechanism by Polysialic Acid for Lamina-Specific Branch Formation of Thalamocortical Axons
J. Neurosci., December 15, 2000; 20(24): 9145 - 9151.
[Abstract] [Full Text] [PDF]

I. Skaliora, R. Adams, and C. Blakemore
Morphology and Growth Patterns of Developing Thalamocortical Axons
J. Neurosci., May 15, 2000; 20(10): 3650 - 3662.
[Abstract] [Full Text] [PDF]

A. Gaillard and M. Roger
Early Commitment of Embryonic Neocortical Cells to Develop Area-specific Thalamic Connections
Cereb Cortex, May 1, 2000; 10(5): 443 - 453.
[Abstract] [Full Text] [PDF]

Y. Gitton, M. Cohen-Tannoudji, and M. Wassef
Role of Thalamic Axons in the Expression of H-2Z1, a Mouse Somatosensory Cortex Specific Marker
Cereb Cortex, September 1, 1999; 9(6): 611 - 620.
[Abstract] [Full Text] [PDF]

D. L. Maier, S. Mani, S. L. Donovan, D. Soppet, L. Tessarollo, J. S. McCasland, and K. F. Meiri
Disrupted cortical map and absence of cortical barrels in growth-associated protein (GAP)-43 knockout mice
PNAS, August 3, 1999; 96(16): 9397 - 9402.
[Abstract] [Full Text] [PDF]

S. Iyengar, S. S. Viswanathan, and S. W. Bottjer
Development of Topography within Song Control Circuitry of Zebra Finches during the Sensitive Period for Song Learning
J. Neurosci., July 15, 1999; 19(14): 6037 - 6057.
[Abstract] [Full Text] [PDF]

C. Hedin-Pereira, R. Lent, and S. Jhaveri
Morphogenesis of Callosal Arbors in the Parietal Cortex of Hamsters
Cereb Cortex, January 1, 1999; 9(1): 50 - 64.
[Abstract] [Full Text] [PDF]

K. M. Pedersen, B. Finsen, J. E. Celis, and N. A. Jensen
Expression of a Novel Murine Phospholipase D Homolog Coincides with Late Neuronal Development in the Forebrain
J. Biol. Chem., November 20, 1998; 273(47): 31494 - 31504.
[Abstract] [Full Text] [PDF]

Z. Molnar, R. Adams, and C. Blakemore
Mechanisms Underlying the Early Establishment of Thalamocortical Connections in the Rat
J. Neurosci., August 1, 1998; 18(15): 5723 - 5745.
[Abstract] [Full Text] [PDF]

K. Krug, A. L. Smith, and I. D. Thompson
The Development of Topography in the Hamster Geniculo-Cortical Projection
J. Neurosci., August 1, 1998; 18(15): 5766 - 5776.
[Abstract] [Full Text] [PDF]

P. Golshani, R. A. Warren, and E. G. Jones
Progression of Change in NMDA, non-NMDA, and Metabotropic Glutamate Receptor Function at the Developing Corticothalamic Synapse
J Neurophysiol, July 1, 1998; 80(1): 143 - 154.
[Abstract] [Full Text] [PDF]

L. A. Hutton, G. Gu, and R. B. Simerly
Development of a Sexually Dimorphic Projection from the Bed Nuclei of the Stria Terminalis to the Anteroventral Periventricular Nucleus in the Rat
J. Neurosci., April 15, 1998; 18(8): 3003 - 3013.
[Abstract] [Full Text] [PDF]

N. Yamamoto, S. Higashi, and K. Toyama
Stop and Branch Behaviors of Geniculocortical Axons: A Time-Lapse Study in Organotypic Cocultures
J. Neurosci., May 15, 1997; 17(10): 3653 - 3663.
[Abstract] [Full Text] [PDF]

R. A. Warren and E. G. Jones
Maturation of Neuronal Form and Function in a Mouse Thalamo-Cortical Circuit
J. Neurosci., January 1, 1997; 17(1): 277 - 295.
[Abstract] [Full Text] [PDF]

A. Agmon, G. Hollrigel, and D. K. O'Dowd
Functional GABAergic Synaptic Connection in Neonatal Mouse Barrel Cortex
J. Neurosci., August 1, 1996; 16(15): 4684 - 4695.
[Abstract] [Full Text] [PDF]

R. S. Broide, R. T. Robertson, and F. M. Leslie
Regulation of alpha 7 Nicotinic Acetylcholine Receptors in the Developing Rat Somatosensory Cortex by Thalamocortical Afferents
J. Neurosci., May 1, 1996; 16(9): 2956 - 2971.
[Abstract] [Full Text] [PDF]

L. B. Thomas and D. A. Steindler
Review : Glial Boundaries and Scars: Programs for Normal Development and Wound Healing in the Brain
Neuroscientist, May 1, 1995; 1(3): 142 - 154.
[Abstract] [PDF]

D. Emerling and A. Lander
Laminar specific attachment and neurite outgrowth of thalamic neurons on cultured slices of developing cerebral neocortex
Development, January 10, 1994; 120(10): 2811 - 2822.
[Abstract] [PDF]

R. R. Llinas, E. Leznik, and F. J. Urbano
Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: A voltage-dependent dye-imaging study in mouse brain slices
PNAS, January 8, 2002; 99(1): 449 - 454.
[Abstract] [Full Text] [PDF]