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Axo-dendritic overlap and laminar projection can explain interneuron connectivity to pyramidal cells.

ABSTRACT: Neocortical GABAergic interneurons have important roles in the normal and pathological states of the circuit. Recent work has revealed that somatostatin-positive (SOM) and parvalbumin-positive (PV) interneurons connect promiscuously to pyramidal cells (PCs). We investigated whether Peters' rule, that is, the spatial overlap of axons and dendrites, could explain this unspecific connectivity. We reconstructed the morphologies of P11-17 mouse SOM and PV interneurons and their PC targets, and performed Monte Carlo simulations to build maps of predicted connectivity based on Peters' rule. We then compared the predicted with the real connectivity maps, measured with 2-photon uncaging experiments, and found no statistical differences between them in the probability of connection as a function of distance and in the spatial structure of the maps. Finally, using reconstructions of connected SOM-PCs and PV-PCs, we investigated the subcellular targeting specificity, by analyzing the postsynaptic position of the contacts, and found that their spatial distributions match the distribution of postsynaptic PC surface area, in agreement with Peters' rule. Thus, the spatial profile of the connectivity maps and even the postsynaptic position of interneuron contacts could result from the mere overlap of axonal and dendritic arborizations and their laminar projections patterns.

SUBMITTER: Packer AM

PROVIDER: S-EPMC3968298 | biostudies-literature | 2013 Dec

REPOSITORIES: biostudies-literature

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Axo-dendritic overlap and laminar projection can explain interneuron connectivity to pyramidal cells.

Packer Adam M AM McConnell Daniel J DJ Fino Elodie E Yuste Rafael R

Cerebral cortex (New York, N.Y. : 1991) 20120831 12

Neocortical GABAergic interneurons have important roles in the normal and pathological states of the circuit. Recent work has revealed that somatostatin-positive (SOM) and parvalbumin-positive (PV) interneurons connect promiscuously to pyramidal cells (PCs). We investigated whether Peters' rule, that is, the spatial overlap of axons and dendrites, could explain this unspecific connectivity. We reconstructed the morphologies of P11-17 mouse SOM and PV interneurons and their PC targets, and perfor ...[more]

PMID: 22941716

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Project description:Neurons display a wide range of intrinsic firing patterns. A particularly relevant pattern for neuronal signaling and synaptic plasticity is burst firing, the generation of clusters of action potentials with short interspike intervals. Besides ion-channel composition, dendritic morphology appears to be an important factor modulating firing pattern. However, the underlying mechanisms are poorly understood, and the impact of morphology on burst firing remains insufficiently known. Dendritic morphology is not fixed but can undergo significant changes in many pathological conditions. Using computational models of neocortical pyramidal cells, we here show that not only the total length of the apical dendrite but also the topological structure of its branching pattern markedly influences inter- and intraburst spike intervals and even determines whether or not a cell exhibits burst firing. We found that there is only a range of dendritic sizes that supports burst firing, and that this range is modulated by dendritic topology. Either reducing or enlarging the dendritic tree, or merely modifying its topological structure without changing total dendritic length, can transform a cell's firing pattern from bursting to tonic firing. Interestingly, the results are largely independent of whether the cells are stimulated by current injection at the soma or by synapses distributed over the dendritic tree. By means of a novel measure called mean electrotonic path length, we show that the influence of dendritic morphology on burst firing is attributable to the effect both dendritic size and dendritic topology have, not on somatic input conductance, but on the average spatial extent of the dendritic tree and the spatiotemporal dynamics of the dendritic membrane potential. Our results suggest that alterations in size or topology of pyramidal cell morphology, such as observed in Alzheimer's disease, mental retardation, epilepsy, and chronic stress, could change neuronal burst firing and thus ultimately affect information processing and cognition.

Dataset Information

Axo-dendritic overlap and laminar projection can explain interneuron connectivity to pyramidal cells.

Publications

Axo-dendritic overlap and laminar projection can explain interneuron connectivity to pyramidal cells.

Similar Datasets

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