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  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex

Markram, H., Lübke, J. H. R., Frotscher, M., Roth, A., & Sakmann, B. (1997). Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. Journal of Physiology, 500(2), 409-440. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid%3D1159394.

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Alternative Title : Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex

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Markram, Henry1, Author           
Lübke, Joachim H. R., Author
Frotscher, Michael, Author
Roth, Arnd1, Author           
Sakmann, Bert1, Author           
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1Department of Cell Physiology, Max Planck Institute for Medical Research, Max Planck Society, ou_1497701              

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 Abstract: 1. Dual voltage recordings were made from pairs of adjacent, synaptically connected thick tufted layer 5 pyramidal neurones in brain slices of young rat (14-16 days) somatosensory cortex to examine the physiological properties of unitary EPSPs. Pre- and postsynaptic neurones were filled with biocytin and examined in the light and electron microscope to quantify the morphology of axonal and dendritic arbors and the number and location of synaptic contacts on the target neurone. 2. In 138 synaptic connections between pairs of pyramidal neurones 96 (70%) were unidirectional and 42 (30%) were bidirectional. The probability of finding a synaptic connection in dual recordings was 0.1. Unitary EPSPs evoked by a single presynaptic action potential (AP) had a mean peak amplitude ranging from 0.15 to 5.5 mV in different connections with a mean of 1.3 +/- 1.1 mV, a latency of 1.7 +/- 0.9 ms, a 20-80% rise time of 2.9 +/- 2.3 ms and a decay time constant of 40 +/- 18 ms at 32-24 degrees C and -60 +/- 2 mV membrane potential. 3. Peak amplitudes of unitary EPSPs fluctuated randomly from trial to trial. The coefficient of variation (c.v.) of the unitary EPSP amplitudes ranged from 0.13 to 2.8 in different synaptic connections (mean, 0.52; median, 0.41). The percentage of failures of single APs to evoke a unitary EPSP ranged from 0 to 73% (mean, 14%; median, 7%). Both c.v. and percentage of failures decreased with increasing mean EPSP amplitude. 4. Postsynaptic glutamate receptors which mediate unitary EPSPs at -60 mV were predominantly of the L-alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptor type. Receptors of the N-methyl-D-aspartate (NMDA) type contributed only a small fraction (< 20%) to the voltage-time integral of the unitary EPSP at -60 mV, but their contribution increased at more positive membrane potentials. 5. Branching patterns of dendrites and axon collaterals of forty-five synaptically connected neurones, when examined in the light microscope, indicated that the axonal and dendritic anatomy of both projecting and target neurones and of uni- and bidirectionally connected neurones was uniform. 6. The number of potential synaptic contacts formed by a presynaptic neurone on a target neurone varied between four and eight (mean, 5.5 +/- 1.1 contacts; n = 19 connections). Synaptic contacts were preferentially located on basal dendrites (63%, 82 +/- 35 microns from the soma, n = 67) and apical oblique dendrites (27%, 145 +/- 59 microns, n = 29), and 35% of all contacts were located on tertiary basal dendritic branches. The mean geometric distances (from the soma) of the contacts of a connection varied between 80 and 585 microns (mean, 147 microns; median, 105 microns). The correlation between EPSP amplitude and the number of morphologically determined synaptic contacts or the mean geometric distances from the soma was only weak (correlation coefficients were 0.2 and 0.26, respectively). 7. Compartmental models constructed from camera lucida drawings of eight target neurones showed that synaptic contacts were located at mean electrotonic distances between 0.07 and 0.33 from the soma (mean, 0.13). Simulations of unitary EPSPs, assuming quantal conductance changes with fast rise time and short duration, indicated that amplitudes of quantal EPSPs at the soma were attenuated, on average, to < 10% of dendritic EPSPs and varied in amplitude up to 10-fold depending on the dendritic location of synaptic contacts. The inferred quantal peak conductance increase varied between 1.5 and 5.5 nS (mean, 3 nS). 8. The combined physiological and morphological measurements in conjunction with EPSP simulations indicated that the 20-fold range in efficacy of the synaptic connections between thick tufted pyramidal neurones, which have their synaptic contacts preferentially located on basal and apical oblique dendrites, was due to differences in transmitter release probability of the projecting neurones and, to a lesser extent, to differencdifferences in the number of release sites per bouton or quantal size. 9. The continuum of efficacies in their synaptic connections implies that layer 5 pyramidal neurones can be recruited to ensemble electrical activity via their axon collaterals if as few as five of the strongly and reliably connected neighbouring neurones are active synchronously, whereas coincident APs of as many as 100 of the weakly connected pyramidal neurones are necessary.

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Language(s): eng - English
 Dates: 1996-09-121996-12-101997-04-15
 Publication Status: Published in print
 Pages: 32
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 Table of Contents: -
 Rev. Type: Peer
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Title: Journal of Physiology
Source Genre: Journal
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Publ. Info: London : Cambridge University Press
Pages: - Volume / Issue: 500 (2) Sequence Number: - Start / End Page: 409 - 440 Identifier: ISSN: 0022-3751
CoNE: https://pure.mpg.de/cone/journals/resource/954925334693