Tuft dendrites of pyramidal neurons operate as feedback-modulated functional subunits

Florian Eberhardt, Andreas V M Herz and Stefan Häusler

PLOS Computational Biology, 2019, vol. 15, issue 3, 1-23

Abstract: Dendrites of pyramidal cells exhibit complex morphologies and contain a variety of ionic conductances, which generate non-trivial integrative properties. Basal and proximal apical dendrites have been shown to function as independent computational subunits within a two-layer feedforward processing scheme. The outputs of the subunits are linearly summed and passed through a final non-linearity. It is an open question whether this mathematical abstraction can be applied to apical tuft dendrites as well. Using a detailed compartmental model of CA1 pyramidal neurons and a novel theoretical framework based on iso-response methods, we first show that somatic sub-threshold responses to brief synaptic inputs cannot be described by a two-layer feedforward model. Then, we relax the core assumption of subunit independence and introduce non-linear feedback from the output layer to the subunit inputs. We find that additive feedback alone explains the somatic responses to synaptic inputs to most of the branches in the apical tuft. Individual dendritic branches bidirectionally modulate the thresholds of their input-output curves without significantly changing the gains. In contrast to these findings for precisely timed inputs, we show that neuronal computations based on firing rates can be accurately described by purely feedforward two-layer models. Our findings support the view that dendrites of pyramidal neurons possess non-linear analog processing capabilities that critically depend on the location of synaptic inputs. The iso-response framework proposed in this computational study is highly efficient and could be directly applied to biological neurons.Author summary: Pyramidal neurons are the principal cell type in the cerebral cortex. Revealing how these cells operate is key to understanding the dynamics and computations of cortical circuits. However, it is still a matter of debate how pyramidal neurons transform their synaptic inputs into spike outputs. Recent studies have proposed that individual dendritic branches or subtrees may function as independent computational subunits. Although experimental work consolidated this abstraction for basal and proximal apical dendrites, a rigorous test for tuft dendrites is still missing. By carrying out a computational study we demonstrate that dendritic branches in the tuft do not form independent subunits, however, their integrative properties can be captured by a model that incorporates modulatory feedback between these subunits. This conclusion has been reached using a novel theoretical framework that can be directly integrated into multi-electrode or photo-stimulation paradigms to reveal the dendritic computations of biological neurons.

Date: 2019
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Persistent link: https://EconPapers.repec.org/RePEc:plo:pcbi00:1006757

DOI: 10.1371/journal.pcbi.1006757

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