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
Open Access
- 1 February 2002
- journal article
- research article
- Published by Wiley in The Journal of Physiology
- Vol. 538 (3), 803-822
- https://doi.org/10.1113/jphysiol.2001.012959
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 μm (range, 16–196 μm). 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.Keywords
This publication has 69 references indexed in Scilit:
- Synaptic efficacy and reliability of excitatory connections between the principal neurones of the input (layer 4) and output layer (layer 5) of the neocortexThe Journal of Physiology, 2000
- Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single ‘barrel’ of developing rat somatosensory cortexThe Journal of Physiology, 1999
- Learning through maps: Functional significance of topographic organization in primary sensory cortexJournal of Neurobiology, 1999
- Developmental and regional expression in the rat brain and functional properties of four NMDA receptorsNeuron, 1994
- Thalamic Afferents of the Rat Barrel Cortex: A Light-and Electron-Microscopic Study Using Phaseolus vulgaris Leucoagglutinin as an Anterograde TracerSomatosensory & Motor Research, 1993
- Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortexJournal of Comparative Neurology, 1989
- Functional architecture of cortex revealed by optical imaging of intrinsic signalsNature, 1986
- Morphology of Golgi‐Cox‐impregnated barrel neurons in rat SmI cortexJournal of Comparative Neurology, 1984
- Widespread Periodic Intrinsic Connections in the Tree Shrew Visual CortexScience, 1982
- Dendritic plasticity in mouse barrel cortex following postnatal vibrissa follicle damageJournal of Comparative Neurology, 1981