 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, May 15, 1999, 19(10):3827-3835
Developmental Switch in the Short-Term Modification of Unitary EPSPs Evoked in Layer 2/3 and Layer 5 Pyramidal Neurons of Rat Neocortex
Alex Reyes and Bert Sakmann Abteilung Zellphysiologie, Max-Planck-Institut für medizinische Forschung, D-69120 Heidelberg, Germany
Amplitudes of EPSPs evoked by repetitive presynaptic action potentials can either decrease (synaptic depression) or increase (synaptic facilitation). To determine whether facilitation and depression in the connections between neocortical pyramidal cells varied with the identity of the pre- or the postsynaptic cell and whether they changed during postnatal development, whole-cell voltage recordings were made simultaneously from two or three pyramidal cells in layers 2/3 and 5 of the rat sensorimotor cortex. Unitary EPSPs were evoked when pre- and postsynaptic neurons were in the same and in different layers. In young [postnatal day 14 (P14)] cortex, EPSPs evoked in all connected neurons depressed. The degree of depression was layer specific and was determined by the identity of the presynaptic cell. EPSPs evoked by stimulation of presynaptic layer 5 neurons depressed significantly more than did those evoked by stimulation of layer 2/3 neurons. In mature cortex (P28), however, the EPSPs evoked in these connected neurons facilitated to a comparable degree regardless of the layer in which pre- and postsynaptic neurons were located. The results suggest that in young cortex the degree of synaptic depression in connected pyramidal cells is determined primarily by whether the presynaptic cell was in layer 2/3 or 5 and that maturation of the cortex involves a developmental switch from depression to facilitation between P14 and P28 that eliminates the layer-specific differences. A functional consequence of this switch is that in mature cortex the spread of excitation between neocortical pyramidal neurons is enhanced when action potentials occur in bursts.
Key words: neocortex; development; facilitation; depression; synapses; postsynaptic potentials
Copyright © 1999 Society for Neuroscience 0270-6474/99/19103827-09$05.00/0
This article has been cited by other articles:
J. de Marchena, A. C. Roberts, P. G. Middlebrooks, V. Valakh, K. Yashiro, L. R. Wilfley, and B. D. Philpot
NMDA Receptor Antagonists Reveal Age-Dependent Differences in the Properties of Visual Cortical Plasticity
J Neurophysiol, October 1, 2008; 100(4): 1936 - 1948.
[Abstract] [Full Text] [PDF]
A.-M. M. Oswald and A. D. Reyes
Maturation of Intrinsic and Synaptic Properties of Layer 2/3 Pyramidal Neurons in Mouse Auditory Cortex
J Neurophysiol, June 1, 2008; 99(6): 2998 - 3008.
[Abstract] [Full Text] [PDF]
M. I. Chelaru and V. Dragoi
Asymmetric Synaptic Depression in Cortical Networks
Cereb Cortex, April 1, 2008; 18(4): 771 - 788.
[Abstract] [Full Text] [PDF]
A. Frick, D. Feldmeyer, M. Helmstaedter, and B. Sakmann
Monosynaptic Connections between Pairs of L5A Pyramidal Neurons in Columns of Juvenile Rat Somatosensory Cortex
Cereb Cortex, February 1, 2008; 18(2): 397 - 406.
[Abstract] [Full Text] [PDF]
S. R. Williams and S. E. Atkinson
Pathway-specific use-dependent dynamics of excitatory synaptic transmission in rat intracortical circuits
J. Physiol., December 15, 2007; 585(3): 759 - 777.
[Abstract] [Full Text] [PDF]
A. Frick, D. Feldmeyer, and B. Sakmann
Postnatal development of synaptic transmission in local networks of L5A pyramidal neurons in rat somatosensory cortex
J. Physiol., November 15, 2007; 585(1): 103 - 116.
[Abstract] [Full Text] [PDF]
P. Krieger, T. Kuner, and B. Sakmann
Synaptic Connections between Layer 5B Pyramidal Neurons in Mouse Somatosensory Cortex Are Independent of Apical Dendrite Bundling
J. Neurosci., October 24, 2007; 27(43): 11473 - 11482.
[Abstract] [Full Text] [PDF]
R. Corlew, Y. Wang, H. Ghermazien, A. Erisir, and B. D. Philpot
Developmental Switch in the Contribution of Presynaptic and Postsynaptic NMDA Receptors to Long-Term Depression
J. Neurosci., September 12, 2007; 27(37): 9835 - 9845.
[Abstract] [Full Text] [PDF]
N. R. Hardingham, G. E. Hardingham, K. D. Fox, and J. J. B. Jack
Presynaptic Efficacy Directs Normalization of Synaptic Strength in Layer 2/3 Rat Neocortex After Paired Activity
J Neurophysiol, April 1, 2007; 97(4): 2965 - 2975.
[Abstract] [Full Text] [PDF]
A. J. Borgdorff, J. F. A. Poulet, and C. C. H. Petersen
Facilitating Sensory Responses in Developing Mouse Somatosensory Barrel Cortex
J Neurophysiol, April 1, 2007; 97(4): 2992 - 3003.
[Abstract] [Full Text] [PDF]
Y. Pankratov, U. Lalo, A. Verkhratsky, and R. A. North
Quantal Release of ATP in Mouse Cortex
J. Gen. Physiol., March 26, 2007; 129(3): 257 - 265.
[Abstract] [Full Text] [PDF]
E. Erazo-Fischer, J. Striessnig, and H. Taschenberger
The Role of Physiological Afferent Nerve Activity during In Vivo Maturation of the Calyx of Held Synapse
J. Neurosci., February 14, 2007; 27(7): 1725 - 1737.
[Abstract] [Full Text] [PDF]
Y. Katz, J. E. Heiss, and I. Lampl
Cross-Whisker Adaptation of Neurons in the Rat Barrel Cortex
J. Neurosci., December 20, 2006; 26(51): 13363 - 13372.
[Abstract] [Full Text] [PDF]
J. J. Letzkus, B. M. Kampa, and G. J. Stuart
Learning Rules for Spike Timing-Dependent Plasticity Depend on Dendritic Synapse Location
J. Neurosci., October 11, 2006; 26(41): 10420 - 10429.
[Abstract] [Full Text] [PDF]
D. Feldmeyer, J. Lubke, and B. Sakmann
Efficacy and connectivity of intracolumnar pairs of layer 2/3 pyramidal cells in the barrel cortex of juvenile rats
J. Physiol., September 1, 2006; 575(2): 583 - 602.
[Abstract] [Full Text] [PDF]
N. Hardingham and K. Fox
The role of nitric oxide and GluR1 in presynaptic and postsynaptic components of neocortical potentiation.
J. Neurosci., July 12, 2006; 26(28): 7395 - 7404.
[Abstract] [Full Text] [PDF]
D. Arsenault and Z.-w. Zhang
Developmental remodelling of the lemniscal synapse in the ventral basal thalamus of the mouse
J. Physiol., May 15, 2006; 573(1): 121 - 132.
[Abstract] [Full Text] [PDF]
R. Reig, R. Gallego, L. G. Nowak, and M. V. Sanchez-Vives
Impact of Cortical Network Activity on Short-term Synaptic Depression
Cereb Cortex, May 1, 2006; 16(5): 688 - 695.
[Abstract] [Full Text] [PDF]
R. B. Levy, A. D. Reyes, and C. Aoki
Nicotinic and Muscarinic Reduction of Unitary Excitatory Postsynaptic Potentials in Sensory Cortex; Dual Intracellular Recording In Vitro
J Neurophysiol, April 1, 2006; 95(4): 2155 - 2166.
[Abstract] [Full Text] [PDF]
D. Schubert, R. Kotter, H.J. Luhmann, and J.F. Staiger
Morphology, Electrophysiology and Functional Input Connectivity of Pyramidal Neurons Characterizes a Genuine Layer Va in the Primary Somatosensory Cortex
Cereb Cortex, February 1, 2006; 16(2): 223 - 236.
[Abstract] [Full Text] [PDF]
D. C. West, A. Mercer, S. Kirchhecker, O. T. Morris, and A. M. Thomson
Layer 6 Cortico-thalamic Pyramidal Cells Preferentially Innervate Interneurons and Generate Facilitating EPSPs
Cereb Cortex, February 1, 2006; 16(2): 200 - 211.
[Abstract] [Full Text] [PDF]
H. J. Rose and R. Metherate
Auditory Thalamocortical Transmission Is Reliable and Temporally Precise
J Neurophysiol, September 1, 2005; 94(3): 2019 - 2030.
[Abstract] [Full Text] [PDF]
C. E. Boudreau and D. Ferster
Short-Term Depression in Thalamocortical Synapses of Cat Primary Visual Cortex
J. Neurosci., August 3, 2005; 25(31): 7179 - 7190.
[Abstract] [Full Text] [PDF]
B. S. Gutkin, G. B. Ermentrout, and A. D. Reyes
Phase-Response Curves Give the Responses of Neurons to Transient Inputs
J Neurophysiol, August 1, 2005; 94(2): 1623 - 1635.
[Abstract] [Full Text] [PDF]
C. J. Price, B. Cauli, E. R. Kovacs, A. Kulik, B. Lambolez, R. Shigemoto, and M. Capogna
Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area
J. Neurosci., July 20, 2005; 25(29): 6775 - 6786.
[Abstract] [Full Text] [PDF]
O. Beck, M. Chistiakova, K. Obermayer, and M. Volgushev
Adaptation at Synaptic Connections to Layer 2/3 Pyramidal Cells in Rat Visual Cortex
J Neurophysiol, July 1, 2005; 94(1): 363 - 376.
[Abstract] [Full Text] [PDF]
S. R. Williams
Encoding and Decoding of Dendritic Excitation during Active States in Pyramidal Neurons
J. Neurosci., June 22, 2005; 25(25): 5894 - 5902.
[Abstract] [Full Text] [PDF]
G. M. G. Shepherd and K. Svoboda
Laminar and Columnar Organization of Ascending Excitatory Projections to Layer 2/3 Pyramidal Neurons in Rat Barrel Cortex
J. Neurosci., June 15, 2005; 25(24): 5670 - 5679.
[Abstract] [Full Text] [PDF]
H. Oviedo and A. D. Reyes
Variation of Input-Output Properties along the Somatodendritic Axis of Pyramidal Neurons
J. Neurosci., May 18, 2005; 25(20): 4985 - 4995.
[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]
E. D. Nosyreva and K. M. Huber
Developmental Switch in Synaptic Mechanisms of Hippocampal Metabotropic Glutamate Receptor-Dependent Long-Term Depression
J. Neurosci., March 16, 2005; 25(11): 2992 - 3001.
[Abstract] [Full Text] [PDF]
H. Li, A. E. Bandrowski, and D. A. Prince
Cortical Injury Affects Short-Term Plasticity of Evoked Excitatory Synaptic Currents
J Neurophysiol, January 1, 2005; 93(1): 146 - 156.
[Abstract] [Full Text] [PDF]
P. Wasling, E. Hanse, and B. Gustafsson
Developmental Changes in Release Properties of the CA3-CA1 Glutamate Synapse in Rat Hippocampus
J Neurophysiol, November 1, 2004; 92(5): 2714 - 2724.
[Abstract] [Full Text] [PDF]
H.-X. Chen and S. N. Roper
Tonic Activity of Metabotropic Glutamate Receptors Is Involved in Developmental Modification of Short-Term Plasticity in the Neocortex
J Neurophysiol, August 1, 2004; 92(2): 838 - 844.
[Abstract] [Full Text] [PDF]
P. Fuentealba, S. Crochet, I. Timofeev, and M. Steriade
Synaptic Interactions Between Thalamic and Cortical Inputs Onto Cortical Neurons In Vivo
J Neurophysiol, May 1, 2004; 91(5): 1990 - 1998.
[Abstract] [Full Text] [PDF]
J.-C. Beique, E. M. Chapin-Penick, L. Mladenovic, and R. Andrade
Serotonergic facilitation of synaptic activity in the developing rat prefrontal cortex
J. Physiol., May 1, 2004; 556(3): 739 - 754.
[Abstract] [Full Text] [PDF]
I. D. Manns, B. Sakmann, and M. Brecht
Sub- and suprathreshold receptive field properties of pyramidal neurones in layers 5A and 5B of rat somatosensory barrel cortex
J. Physiol., April 15, 2004; 556(2): 601 - 622.
[Abstract] [Full Text] [PDF]
Z.-w. Zhang
Maturation of Layer V Pyramidal Neurons in the Rat Prefrontal Cortex: Intrinsic Properties and Synaptic Function
J Neurophysiol, March 1, 2004; 91(3): 1171 - 1182.
[Abstract] [Full Text] [PDF]
J. Lubke, A. Roth, D. Feldmeyer, and B. Sakmann
Morphometric Analysis of the Columnar Innervation Domain of Neurons Connecting Layer 4 and Layer 2/3 of Juvenile Rat Barrel Cortex
Cereb Cortex, October 1, 2003; 13(10): 1051 - 1063.
[Abstract] [Full Text] [PDF]
C. I. O. Myme, K. Sugino, G. G. Turrigiano, and S. B. Nelson
The NMDA-to-AMPA Ratio at Synapses Onto Layer 2/3 Pyramidal Neurons Is Conserved Across Prefrontal and Visual Cortices
J Neurophysiol, August 1, 2003; 90(2): 771 - 779.
[Abstract] [Full Text] [PDF]
Z.-w. Zhang
Serotonin Induces Tonic Firing in Layer V Pyramidal Neurons of Rat Prefrontal Cortex during Postnatal Development
J. Neurosci., April 15, 2003; 23(8): 3373 - 3384.
[Abstract] [Full Text] [PDF]
C. C. H. Petersen, A. Grinvald, and B. Sakmann
Spatiotemporal Dynamics of Sensory Responses in Layer 2/3 of Rat Barrel Cortex Measured In Vivo by Voltage-Sensitive Dye Imaging Combined with Whole-Cell Voltage Recordings and Neuron Reconstructions
J. Neurosci., February 15, 2003; 23(4): 1298 - 1309.
[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. M. Thomson and D. C. West
Presynaptic Frequency Filtering in the Gamma Frequency Band; Dual Intracellular Recordings in Slices of Adult Rat and Cat Neocortex
Cereb Cortex, February 1, 2003; 13(2): 136 - 143.
[Abstract] [Full Text] [PDF]
H.-X. Chen and S. N. Roper
Reduction of Spontaneous Inhibitory Synaptic Activity in Experimental Heterotopic Gray Matter
J Neurophysiol, January 1, 2003; 89(1): 150 - 158.
[Abstract] [Full Text] [PDF]
Y. Li and R. E. Burke
Developmental Changes in Short-Term Synaptic Depression in the Neonatal Mouse Spinal Cord
J Neurophysiol, December 1, 2002; 88(6): 3218 - 3231.
[Abstract] [Full Text] [PDF]
M. Beierlein and B. W. Connors
Short-Term Dynamics of Thalamocortical and Intracortical Synapses Onto Layer 6 Neurons in Neocortex
J Neurophysiol, October 1, 2002; 88(4): 1924 - 1932.
[Abstract] [Full Text] [PDF]
M. Galarreta and S. Hestrin
Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex
PNAS, September 17, 2002; 99(19): 12438 - 12443.
[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]
M. E. Larkum and J. J. Zhu
Signaling of Layer 1 and Whisker-Evoked Ca2+ and Na+ Action Potentials in Distal and Terminal Dendrites of Rat Neocortical Pyramidal Neurons In Vitro and In Vivo
J. Neurosci., August 15, 2002; 22(16): 6991 - 7005.
[Abstract] [Full Text] [PDF]
C. C. H. Petersen
Short-Term Dynamics of Synaptic Transmission Within the Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex
J Neurophysiol, June 1, 2002; 87(6): 2904 - 2914.
[Abstract] [Full Text] [PDF]
Q. Li, S. Clark, D. V. Lewis, and W. A. Wilson
NMDA Receptor Antagonists Disinhibit Rat Posterior Cingulate and Retrosplenial Cortices: A Potential Mechanism of Neurotoxicity
J. Neurosci., April 15, 2002; 22(8): 3070 - 3080.
[Abstract] [Full Text] [PDF]
Y. Wang, A. Gupta, M. Toledo-Rodriguez, C. Z. Wu, and H. Markram
Anatomical, Physiological, Molecular and Circuit Properties of Nest Basket Cells in the Developing Somatosensory Cortex
Cereb Cortex, April 1, 2002; 12(4): 395 - 410.
[Abstract] [Full Text] [PDF]
M. G. Mozhayeva, Y. Sara, X. Liu, and E. T. Kavalali
Development of Vesicle Pools during Maturation of Hippocampal Synapses
J. Neurosci., February 1, 2002; 22(3): 654 - 665.
[Abstract] [Full Text] [PDF]
S. S. Kumar and J. R. Huguenard
Properties of Excitatory Synaptic Connections Mediated by the Corpus Callosum in the Developing Rat Neocortex
J Neurophysiol, December 1, 2001; 86(6): 2973 - 2985.
[Abstract] [Full Text] [PDF]
C. Rozas, H. Frank, A. J. Heynen, B. Morales, M. F. Bear, and A. Kirkwood
Developmental Inhibitory Gate Controls the Relay of Activity to the Superficial Layers of the Visual Cortex
J. Neurosci., September 1, 2001; 21(17): 6791 - 6801.
[Abstract] [Full Text] [PDF]
D. Schubert, J. F. Staiger, N. Cho, R. Kotter, K. Zilles, and H. J. Luhmann
Layer-Specific Intracolumnar and Transcolumnar Functional Connectivity of Layer V Pyramidal Cells in Rat Barrel Cortex
J. Neurosci., May 15, 2001; 21(10): 3580 - 3592.
[Abstract] [Full Text] [PDF]
K. Toth, G. Suares, J. J. Lawrence, E. Philips-Tansey, and C. J. McBain
Differential Mechanisms of Transmission at Three Types of Mossy Fiber Synapse
J. Neurosci., November 15, 2000; 20(22): 8279 - 8289.
[Abstract] [Full Text] [PDF]
Y. Yoshimura, H. Sato, K. Imamura, and Y. Watanabe
Properties of Horizontal and Vertical Inputs to Pyramidal Cells in the Superficial Layers of the Cat Visual Cortex
J. Neurosci., March 1, 2000; 20(5): 1931 - 1940.
[Abstract] [Full Text] [PDF]
