Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells

M. Megías, Z. Emri, T. Freund, A. I. Gulyás

Research output: Contribution to journalArticle

569 Citations (Scopus)

Abstract

The integrative properties of neurons depend strongly on the number, proportions and distribution of excitatory and inhibitory synaptic inputs they receive. In this study the three-dimensional geometry of dendritic trees and the density of symmetrical and asymmetrical synapses on different cellular compartments of rat hippocampal CA1 area pyramidal cells was measured to calculate the total number and distribution of excitatory and inhibitory inputs on a single cell. A single pyramidal cell has ∼12,000 μm dendrites and receives around 30,000 excitatory and 1700 inhibitory inputs, of which 40% are concentrated in the perisomatic region and 20% on dendrites in the stratum lacunosum-moleculare. The pre- and post-synaptic features suggest that CA1 pyramidal cell dendrites are heterogeneous. Strata radiatum and oriens dendrites are similar and differ from stratum lacunosum-moleculare dendrites. Proximal apical and basal strata radiatum and oriens dendrites are spine-free or sparsely spiny. Distal strata radiatum and oriens dendrites (forming 68.5% of the pyramidal cells' dendritic tree) are densely spiny; their excitatory inputs terminate exclusively on dendritic spines, while inhibitory inputs target only dendritic shafts. The proportion of inhibitory inputs on distal spiny strata radiatum and oriens dendrites is low (∼3%). In contrast, proximal dendritic segments receive mostly (70-100%) inhibitory inputs. Only inhibitory inputs innervate the somata (77-103 per cell) and axon initial segments. Dendrites in the stratum lacunosum-moleculare possess moderate to small amounts of spines. Excitatory synapses on stratum lacunosum-moleculare dendrites are larger than the synapses in other layers, are frequently perforated (∼40%) and can be located on dendritic shafts. Inhibitory inputs, whose percentage is relatively high (∼14-17%), also terminate on dendritic spines. Our results indicate that: (i) the highly convergent excitation arriving onto the distal dendrites of pyramidal cells is primarily controlled by proximally located inhibition; (ii) the organization of excitatory and inhibitory inputs in layers receiving Schaffer collateral input (radiatum/oriens) versus perforant path input (lacunosum-moleculare) is significantly different.

Original languageEnglish
Pages (from-to)527-540
Number of pages14
JournalNeuroscience
Volume102
Issue number3
DOIs
Publication statusPublished - Feb 5 2001

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Pyramidal Cells
Dendrites
Synapses
Dendritic Spines
Spine
Perforant Pathway
Hippocampal CA1 Region
Carisoprodol
Hippocampus
Neurons

Keywords

  • 3D
  • Database for modeling
  • Dendrite geometry
  • Electron microscopy
  • Serial reconstruction
  • Synaptic convergence

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. / Megías, M.; Emri, Z.; Freund, T.; Gulyás, A. I.

In: Neuroscience, Vol. 102, No. 3, 05.02.2001, p. 527-540.

Research output: Contribution to journalArticle

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N2 - The integrative properties of neurons depend strongly on the number, proportions and distribution of excitatory and inhibitory synaptic inputs they receive. In this study the three-dimensional geometry of dendritic trees and the density of symmetrical and asymmetrical synapses on different cellular compartments of rat hippocampal CA1 area pyramidal cells was measured to calculate the total number and distribution of excitatory and inhibitory inputs on a single cell. A single pyramidal cell has ∼12,000 μm dendrites and receives around 30,000 excitatory and 1700 inhibitory inputs, of which 40% are concentrated in the perisomatic region and 20% on dendrites in the stratum lacunosum-moleculare. The pre- and post-synaptic features suggest that CA1 pyramidal cell dendrites are heterogeneous. Strata radiatum and oriens dendrites are similar and differ from stratum lacunosum-moleculare dendrites. Proximal apical and basal strata radiatum and oriens dendrites are spine-free or sparsely spiny. Distal strata radiatum and oriens dendrites (forming 68.5% of the pyramidal cells' dendritic tree) are densely spiny; their excitatory inputs terminate exclusively on dendritic spines, while inhibitory inputs target only dendritic shafts. The proportion of inhibitory inputs on distal spiny strata radiatum and oriens dendrites is low (∼3%). In contrast, proximal dendritic segments receive mostly (70-100%) inhibitory inputs. Only inhibitory inputs innervate the somata (77-103 per cell) and axon initial segments. Dendrites in the stratum lacunosum-moleculare possess moderate to small amounts of spines. Excitatory synapses on stratum lacunosum-moleculare dendrites are larger than the synapses in other layers, are frequently perforated (∼40%) and can be located on dendritic shafts. Inhibitory inputs, whose percentage is relatively high (∼14-17%), also terminate on dendritic spines. Our results indicate that: (i) the highly convergent excitation arriving onto the distal dendrites of pyramidal cells is primarily controlled by proximally located inhibition; (ii) the organization of excitatory and inhibitory inputs in layers receiving Schaffer collateral input (radiatum/oriens) versus perforant path input (lacunosum-moleculare) is significantly different.

AB - The integrative properties of neurons depend strongly on the number, proportions and distribution of excitatory and inhibitory synaptic inputs they receive. In this study the three-dimensional geometry of dendritic trees and the density of symmetrical and asymmetrical synapses on different cellular compartments of rat hippocampal CA1 area pyramidal cells was measured to calculate the total number and distribution of excitatory and inhibitory inputs on a single cell. A single pyramidal cell has ∼12,000 μm dendrites and receives around 30,000 excitatory and 1700 inhibitory inputs, of which 40% are concentrated in the perisomatic region and 20% on dendrites in the stratum lacunosum-moleculare. The pre- and post-synaptic features suggest that CA1 pyramidal cell dendrites are heterogeneous. Strata radiatum and oriens dendrites are similar and differ from stratum lacunosum-moleculare dendrites. Proximal apical and basal strata radiatum and oriens dendrites are spine-free or sparsely spiny. Distal strata radiatum and oriens dendrites (forming 68.5% of the pyramidal cells' dendritic tree) are densely spiny; their excitatory inputs terminate exclusively on dendritic spines, while inhibitory inputs target only dendritic shafts. The proportion of inhibitory inputs on distal spiny strata radiatum and oriens dendrites is low (∼3%). In contrast, proximal dendritic segments receive mostly (70-100%) inhibitory inputs. Only inhibitory inputs innervate the somata (77-103 per cell) and axon initial segments. Dendrites in the stratum lacunosum-moleculare possess moderate to small amounts of spines. Excitatory synapses on stratum lacunosum-moleculare dendrites are larger than the synapses in other layers, are frequently perforated (∼40%) and can be located on dendritic shafts. Inhibitory inputs, whose percentage is relatively high (∼14-17%), also terminate on dendritic spines. Our results indicate that: (i) the highly convergent excitation arriving onto the distal dendrites of pyramidal cells is primarily controlled by proximally located inhibition; (ii) the organization of excitatory and inhibitory inputs in layers receiving Schaffer collateral input (radiatum/oriens) versus perforant path input (lacunosum-moleculare) is significantly different.

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