Contribution of apical and basal dendrites to orientation encoding in mouse V1 L2/3 pyramidal neurons

Jiyoung Park,Athanasia Papoutsi,Miguel A Marin,Ryan T Ash,Stelios M Smirnakis,Panayiota Poirazi

doi:10.1038/s41467-019-13029-0

Abstract

Pyramidal neurons integrate synaptic inputs from basal and apical dendrites to generate stimulus-specific responses. It has been proposed that feed-forward inputs to basal dendrites drive a neuron’s stimulus preference, while feedback inputs to apical dendrites sharpen selectivity. However, how a neuron’s dendritic domains relate to its functional selectivity has not been demonstrated experimentally. We performed 2-photon dendritic micro-dissection on layer-2/3 pyramidal neurons in mouse primary visual cortex. We found that removing the apical dendritic tuft did not alter orientation-tuning. Furthermore, orientation-tuning curves were remarkably robust to the removal of basal dendrites: ablation of 2 basal dendrites was needed to cause a small shift in orientation preference, without significantly altering tuning width. Computational modeling corroborated our results and put limits on how orientation preferences among basal dendrites differ in order to reproduce the post-ablation data. In conclusion, neuronal orientation-tuning appears remarkably robust to loss of dendritic input.

Highlights

Pyramidal neurons integrate synaptic inputs from basal and apical dendrites to generate stimulus-specific responses
We showed that orientation selectivity in layer 2/3 (L2/3) pyramidal neurons, as measured by orientation preference, tuning-width and OSI, is robust to a complete loss of the apical tuft
This is surprising given that apical dendrites receive orientation-tuned input[11], with at least four input sources accessible to apical dendrites that could potentially modulate orientation selectivity in V1: (1) feedback cortico-cortical projections from extrastriate cortex thought to refine orientation selectivity[9,10,23,24], (2) direction-selective projections from the LGN12, (3) thalamo-cortical projections from lateral posterior thalamus[13], and (4) dendrite-targeting inhibitory inputs[25,26]

Summary

Introduction

Pyramidal neurons integrate synaptic inputs from basal and apical dendrites to generate stimulus-specific responses. Mouse primary visual cortex (V1) L2/3 pyramidal neurons generate action potentials in response to a narrow range of orientations[5] despite receiving highly heterogeneous input and poorly tuned subthreshold responses[4], making them ideal for studying the relationship between dendritic input and functional selectivity. Recent evidence suggests that apical tuft dendritic spikes serve to narrow the orientation tuning function, increasing orientation selectivity of area V1 L2/3 pyramidal neurons[6]. We employ in vivo two photon microdissection[14,15,16,17] to systematically remove individual dendrites from layer 2/3 mouse V1 pyramidal neurons, allowing us to assess the causal relationship between inputs arriving in different dendritic arbors and the computation of orientation selectivity at the soma

Methods

Results

Conclusion