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1 Biology, University of Texas at San Antonio, San Antonio, Texas, United States
2 Department of Biology, University of Texas San Antonio, San Antonio, Texas, United States
* To whom correspondence should be addressed. E-mail: josh{at}biocontrol.co.il.
The responsiveness of rhythmically-firing neurons to synaptic inputs is characterized by their phase response curve (PRC), which relates how weak somatic perturbations affect the timing of the next action potential. The shape of the somatic PRC is an important determinant of collective network dynamics. Here we study theoretically and experimentally the impact of distally-located synapses and dendritic nonlinearities on the synchronization properties of rhythmically firing neurons. Combining the theories of quasi-active cables and phase-coupled oscillators we derive an approximation for the dendritic responsiveness, captured by the neuron's dendritic PRC (dPRC). This closed-form expression indicates that the dPRCs are linearly-filtered versions of the somatic PRC, and that the filter characteristics are determined by the passive and active properties of the dendrite. The passive properties induce leftward shifts in the dPRCs and attenuate them. Our analysis yields a single dimensionless parameter that classifies active dendritic conductances as either regenerative conductances that counter the passive properties by boosting the dPRCs, or restorative conductances that high-pass filter the dPRCs. Thus, dendritic properties can generate a qualitative difference between the somatic and dendritic PRCs. As a result collective dynamics can be qualitatively different depending on the location of the synapse, the neuronal firing rates and the dendritic nonlinearities. Finally, we use dual whole-cell recordings from the soma and apical dendrite of cortical pyramidal neurons to test these predictions and find that empirical dPRCs are shifted leftward as predicted, but may also display high-pass characteristics due to the restorative dendritic HCN (h) current.
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