Effects of synaptic synchrony on the neuronal input-output relationship

Abstract

The firing rate of individual neurons depends on the firing frequency of their distributed synaptic inputs, with linear and nonlinear relations subserving different computational functions. This letter explores the relationship between the degree of synchrony among excitatory synapses and the linearity of the response using detailed compartmental models of cortical pyramidal cells. Synchronous input resulted in a linear input-output relationship, while asynchronous stimulation yielded sub- and supraproportional outputs at low and high frequencies, respectively. The dependence of input-output linearity on synchrony was sigmoidal and considerably robust with respect to dendritic location, stimulus irregularity, and alteration of active and synaptic properties. Moreover, synchrony affected firing rate differently at lower and higher input frequencies. A reduced integrate-and-fire model suggested a mechanism explaining these results based on spatiotemporal integration, with fundamental implications relating synchrony to memory encoding.

Fig. 1

A) Input-output relation of one neuron with fully synchronous or asynchronous inputs. Inset: neuronal morphology and the synaptic distribution area on the apical tree (scale bar: 100 μm). B) Axonal voltage recordings with asynchronous and synchronous inputs at two representative frequencies. C) Raster plots showing 1000 synapses activated with the grouping synchronization method at the value of 50 (i.e., 20 groups of 50 synapses each). D) Recruiting method with recruiting value of 400. E) Proportionality is expressed as a function of the deviation of the output firing rate from the linear regression (through the origin) of the input frequency (see Methods). F) Increase of I/O proportionality with the grouping value (apical stimulation, Type I model). Mean and standard error over 8 cells fitted by a sigmoidal function (see Table 1 for formula and parameter values).

Fig. 2

Effect of synaptic synchrony on I/O (apical synapses, regular stimulation). A) Amount of synchronization (measured by synaptic cross-correlation) as a function of grouping and recruiting values. B) Proportionality with intermediate levels of grouping and recruiting (Type I model) replotted versus synchrony values obtained from Fig. 2A. C) Representative single-neuron data relating output firing rate to synchrony: output frequency vs. grouping at various synaptic input levels. D) Data from panel C normalized to unity at grouping value of 50. E) Output frequency vs. recruiting at various synaptic input levels. F) Data from E normalized to unity at recruiting value of 800.