TY - JOUR
T1 - Dendritic computations captured by an effective point neuron model
AU - Li, Songting
AU - Liu, Nan
AU - Zhang, Xiaohui
AU - McLaughlin, David W.
AU - Zhou, Douglas
AU - Cai, David
N1 - Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.
PY - 2019/7/23
Y1 - 2019/7/23
N2 - Complex dendrites in general present formidable challenges to understanding neuronal information processing. To circumvent the difficulty, a prevalent viewpoint simplifies the neuronal morphology as a point representing the soma, and the excitatory and inhibitory synaptic currents originated from the dendrites are treated as linearly summed at the soma. Despite its extensive applications, the validity of the synaptic current description remains unclear, and the existing point neuron framework fails to characterize the spatiotemporal aspects of dendritic integration supporting specific computations. Using electrophysiological experiments, realistic neuronal simulations, and theoretical analyses, we demonstrate that the traditional assumption of linear summation of synaptic currents is oversimplified and underestimates the inhibition effect. We then derive a form of synaptic integration current within the point neuron framework to capture dendritic effects. In the derived form, the interaction between each pair of synaptic inputs on the dendrites can be reliably parameterized by a single coefficient, suggesting the inherent low-dimensional structure of dendritic integration. We further generalize the form of synaptic integration current to capture the spatiotemporal interactions among multiple synaptic inputs and show that a point neuron model with the synaptic integration current incorporated possesses the computational ability of a spatial neuron with dendrites, including direction selectivity, coincidence detection, logical operation, and a bilinear dendritic integration rule discovered in experiment. Our work amends the modeling of synaptic inputs and improves the computational power of a modeling neuron within the point neuron framework.
AB - Complex dendrites in general present formidable challenges to understanding neuronal information processing. To circumvent the difficulty, a prevalent viewpoint simplifies the neuronal morphology as a point representing the soma, and the excitatory and inhibitory synaptic currents originated from the dendrites are treated as linearly summed at the soma. Despite its extensive applications, the validity of the synaptic current description remains unclear, and the existing point neuron framework fails to characterize the spatiotemporal aspects of dendritic integration supporting specific computations. Using electrophysiological experiments, realistic neuronal simulations, and theoretical analyses, we demonstrate that the traditional assumption of linear summation of synaptic currents is oversimplified and underestimates the inhibition effect. We then derive a form of synaptic integration current within the point neuron framework to capture dendritic effects. In the derived form, the interaction between each pair of synaptic inputs on the dendrites can be reliably parameterized by a single coefficient, suggesting the inherent low-dimensional structure of dendritic integration. We further generalize the form of synaptic integration current to capture the spatiotemporal interactions among multiple synaptic inputs and show that a point neuron model with the synaptic integration current incorporated possesses the computational ability of a spatial neuron with dendrites, including direction selectivity, coincidence detection, logical operation, and a bilinear dendritic integration rule discovered in experiment. Our work amends the modeling of synaptic inputs and improves the computational power of a modeling neuron within the point neuron framework.
KW - Dendritic computation
KW - Point neuron model
KW - Single-neuron dynamics
KW - Synaptic current
KW - Synaptic integration
UR - http://www.scopus.com/inward/record.url?scp=85069736390&partnerID=8YFLogxK
U2 - 10.1073/pnas.1904463116
DO - 10.1073/pnas.1904463116
M3 - Article
C2 - 31292252
AN - SCOPUS:85069736390
SN - 0027-8424
VL - 116
SP - 15244
EP - 15252
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 30
ER -