Anatomical and Functional Connectivity at the Dendrodendritic Reciprocal Mitral Cell-Granule Cell Synapse: Impact on Recurrent and Lateral Inhibition

Aghvami, S. Sara and Kubota, Yoshiyuki and Egger, Veronica (2022) Anatomical and Functional Connectivity at the Dendrodendritic Reciprocal Mitral Cell-Granule Cell Synapse: Impact on Recurrent and Lateral Inhibition. FRONTIERS IN NEURAL CIRCUITS, 16: 933201. ISSN 1662-5110

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Abstract

In the vertebrate olfactory bulb, reciprocal dendrodendritic interactions between its principal neurons, the mitral and tufted cells, and inhibitory interneurons in the external plexiform layer mediate both recurrent and lateral inhibition, with the most numerous of these interneurons being granule cells. Here, we used recently established anatomical parameters and functional data on unitary synaptic transmission to simulate the strength of recurrent inhibition of mitral cells specifically from the reciprocal spines of rat olfactory bulb granule cells in a quantitative manner. Our functional data allowed us to derive a unitary synaptic conductance on the order of 0.2 nS. The simulations predicted that somatic voltage deflections by even proximal individual granule cell inputs are below the detection threshold and that attenuation with distance is roughly linear, with a passive length constant of 650 mu m. However, since recurrent inhibition in the wake of a mitral cell action potential will originate from hundreds of reciprocal spines, the summated recurrent IPSP will be much larger, even though there will be substantial mutual shunting across the many inputs. Next, we updated and refined a preexisting model of connectivity within the entire rat olfactory bulb, first between pairs of mitral and granule cells, to estimate the likelihood and impact of recurrent inhibition depending on the distance between cells. Moreover, to characterize the substrate of lateral inhibition, we estimated the connectivity via granule cells between any two mitral cells or all the mitral cells that belong to a functional glomerular ensemble (i.e., which receive their input from the same glomerulus), again as a function of the distance between mitral cells and/or entire glomerular mitral cell ensembles. Our results predict the extent of the three regimes of anatomical connectivity between glomerular ensembles: high connectivity within a glomerular ensemble and across the first four rings of adjacent glomeruli, substantial connectivity to up to eleven glomeruli away, and negligible connectivity beyond. Finally, in a first attempt to estimate the functional strength of granule-cell mediated lateral inhibition, we combined this anatomical estimate with our above simulation results on attenuation with distance, resulting in slightly narrowed regimes of a functional impact compared to the anatomical connectivity.

Item Type: Article
Uncontrolled Keywords: RAT OLFACTORY-BULB; EXTERNAL PLEXIFORM LAYER; SHORT-AXON CELLS; TUFTED CELLS; FEEDFORWARD INHIBITION; INTERNEURON NETWORKS; MITRAL/TUFTED CELLS; ACTION-POTENTIALS; TERM PLASTICITY; NEURONS; olfactory bulb; recurrent inhibition; lateral inhibition; network model; mitral cell; granule cell; reciprocal synapse; glomerular column
Subjects: 500 Science > 590 Zoological sciences
Divisions: Biology, Preclinical Medicine > Institut für Zoologie > Neurophysiologie (Prof. Dr. Veronica Egger)
Depositing User: Dr. Gernot Deinzer
Date Deposited: 07 Feb 2024 10:19
Last Modified: 07 Feb 2024 10:19
URI: https://pred.uni-regensburg.de/id/eprint/57198

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