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Cited by 656Neuroscience and Neuropharmacology ResearchNeural dynamics and brain functionMemory and Neural Mechanisms

Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column.

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Feldmeyer, Dirk, Lübke, Joachim, Silver, R. Angus, Sakmann, Bert·2002·The Journal of Physiology
DOI 10.1113/jphysiol.2001.012959PMC PMC2290091
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Abstract

Whole-cell voltage recordings were obtained from 64 synaptically coupled excitatory layer 4 (L4) spiny neurones and L2/3 pyramidal cells in acute slices of the somatosensory cortex ('barrel' cortex) of 17- to 23-days-old rats. Single action potentials (APs) in the L4 spiny neurone evoked single unitary EPSPs in the L2/3 pyramidal cell with a peak amplitude of 0.7 +/- 0.6 mV. The average latency was 2.1 +/- 0.6 ms, the rise time was 0.8 +/- 0.3 ms and the decay time constant was 12.7 +/- 3.5 ms. The percentage of failures of an AP in a L4 spiny neurone to evoke a unitary EPSP in the L2/3 pyramidal cell was 4.9 +/- 8.8 % and the coefficient of variation (c.v.) of the unitary EPSP amplitude was 0.27 +/- 0.13. Both c.v. and percentage of failures decreased with increased average EPSP amplitude. Postsynaptic glutamate receptors (GluRs) in L2/3 pyramidal cells were of the N-methyl-D-aspartate (NMDA) receptor (NMDAR) and the non-NMDAR type. At -60 mV in the presence of extracellular Mg2+ (1 mM), 29 +/- 15 % of the EPSP voltage-time integral was blocked by NMDAR antagonists. In 0 Mg2+, the NMDAR/AMPAR ratio of the EPSC was 0.50 +/- 0.29, about half the value obtained for L4 spiny neurone connections. Burst stimulation of L4 spiny neurones showed that EPSPs in L2/3 pyramidal cells depressed over a wide range of frequencies (1-100 s(-1) ). However, at higher frequencies (30 s(-1)) EPSP summation overcame synaptic depression so that the summed EPSP was larger than the first EPSP amplitude in the train. The number of putative synaptic contacts established by the axonal collaterals of the L4 projection neurone with the target neurone in layer 2/3 varied between 4 and 5, with an average of 4.5 +/- 0.5 (n = 13 pairs). Synapses were established on basal dendrites of the pyramidal cell. Their mean geometric distance from the pyramidal cell soma was 67 +/- 34 microm (range, 16-196 microm). The results suggest that each connected L4 spiny neurone produces a weak but reliable EPSP in the pyramidal cell. Therefore transmission of signals to layer 2/3 is likely to have a high threshold requiring simultaneous activation of many L4 neurons, implying that L4 spiny neurone to L2/3 pyramidal cell synapses act as a gate for the lateral spread of excitation in layer 2/3.

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  • Synaptic connections of axons that arise within the same cortical column in the neocortex preferentially innervate the proximal basal dendrites of pyramidal cells.

    “For example, the synaptic connections of axons that arise within the same cortical column in the neocortex preferentially innervate the proximal basal dendrites of pyramidal cells (Markram et al., 1997; Feldmeyer et al., 2002).”

    From The influence of phospho-tau on dendritic spines of cortical pyramidal neurons in patients with Alzheimer’s disease (2013) · cites this paper as Feldmeyer et al., 2002

  • Neurons in layer 2/3 are capable of approximating a computation similar to a weighted sum of lateral connections multiplied by a bottom-up input.

    “We found several data points suggesting that neurons in layer 2/3 are capable of approximating a similar computation.”

    From Towards a mathematical theory of cortical micro-circuits (2009) · cites this paper as [50]

  • Projections of layer 4 spiny neurons to layer 2/3 pyramidal neurons act as a gate for the lateral spread of excitation in layer 2/3.

    “Another study [50] suggested that the projections of layer 4 spiny neurons to layer 2/3 pyramidal neurons act as a gate for the lateral spread of excitation in layer 2/3.”

    From Towards a mathematical theory of cortical micro-circuits (2009) · cites this paper as [50]

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Authors
Feldmeyer, D., Lübke, J., Silver, R. A., & Sakmann, B.
Affiliations
  • Max Planck Institute for Medical Research (DE)
  • University of Freiburg (DE)
  • University College London (GB)
Corresponding author
Feldmeyer, Dirk
ORCID
Venue
The Journal of Physiology
Publisher
Wiley
Published
2002-02
Volume
538
Issue
3
Pages
803-822
ISSN
  • 0022-3751 (ISSN-L)
  • 1469-7793
DOI
10.1113/jphysiol.2001.012959
PMC
PMC2290091
OpenAlex
W2063812162
Cited by
656
References
66
Citations by year
2026: 6 · 2025: 7 · 2024: 16 · 2023: 12 · 2022: 15 · 2021: 20 · 2020: 19 · 2019: 17 · 2018: 14 · 2017: 24 · 2016: 13 · 2015: 33 · 2014: 25 · 2013: 31 · 2012: 33
FWCI
14.29
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • The Journal of Physiology (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Max Planck Institute for Plasma Physics (submittedVersion)
  • UCL Discovery (University College London) (submittedVersion)
  • FreiDok plus (Universitätsbibliothek Freiburg) (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Funders
  • Wellcome Trust
  • Max-Planck-Gesellschaft
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
layer 2/3 pyramidal cells, barrel cortex, somatosensory cortex, EPSPS, NMDA receptor, AMPA receptors, synaptic depression, axon collaterals, synaptic connectivity, young rats, cortical columns, glutamate receptors
MeSH terms
Action Potentials, Afferent Pathways, Animals, Electric Conductivity, Synaptic Transmission, Neuronal Plasticity, Neurons, Afferent, Reaction Time, Somatosensory Cortex, Synapses, Vibrissae, Signal Transduction, Receptors, N-Methyl-D-Aspartate, Rats, Wistar, Pyramidal Cells, Receptors, AMPA, Excitatory Postsynaptic Potentials, Rats, In Vitro Techniques

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