Intrinsic morphological diversity of thick-tufted layer 5 pyramidal neurons ensures robust and invariant properties of in silico synaptic connections.

ABSTRACT

The morphology of neocortical pyramidal neurons is not only highly characteristic but also displays an intrinsic diversity that renders each neuron morphologically unique. We investigated the significance of this intrinsic morphological diversity in in silico networks composed of thick-tufted layer 5 (TTL5) pyramidal neurons, by comparing the in silico and in vitro properties of TTL5 synaptic connections. The synaptic locations of in silico connections were determined by placing 3D reconstructed TTL5 neurons randomly in a volume equivalent to that of layer 5 in the juvenile rat somatosensory cortex and using a 'collision-detection' algorithm to identify the incidental loci of axo-dendritic overlap. The activation time of the modelled synapses and their biophysical properties were characterized based on experimental measurements. We found that the anatomical loci of synapses and the physiological properties of the somatically recorded EPSPs closely matched those recorded experimentally without the need for any fine-tuning. Furthermore, perturbations to both the physiological or anatomical parameters of the model did not alter the average physiological properties of the population of modelled synaptic connections. This microcircuit-level robust behaviour was due to the intrinsic diversity of the morphology of pyramidal neurons in the microcircuit. We conclude that synaptic transmission in a network of TTL5 neurons is highly invariant across microcircuits suggesting that intrinsic diversity is a mechanism to ensure the same average synaptic properties in different animals of the same species. Finally, we show that the average physiological properties of the TTL5 microcircuit are surprisingly robust to anatomical and physiological perturbations also partly due to the intrinsic diversity of pyramidal neuron morphology.