University of Washington and Stanford University.
Visual cortical neurons receive an abundance of excitatory synaptic input. Estimates of the number, strength and reliability of such excitatory input suggest that cortical neurons should saturate their response in the absence of some balancing inhibitory input. Rough parity between excitatory and inhibitory inputs allows cortical neurons to respond in a graded fashion in the face of massive excitation; this buffering process can be nicely modeled by considering membrane depolarization as a rectified random walk (RRW) between resting potential and threshold. According to this model, variation in response rate is due to comodulation of excitatory and inhibitory inputs to the neuron. The desired buffering comes at a price, however-interspike intervals (ISIs) generated by the model become random. Thus, postsynaptic spikes are effectively dissociated from the exact timing of individual inputs, implying that spike timing information is not conserved precisely.
A major problem posed by random ISIs is that the timing of sensory events can be estimated precisely only by pooling the responses from many neurons carrying redundant information in their firing rates (as in a cortical column). Such neurons are likely to receive many inputs in common. We have recently explored the consequences of such common input on pairs of neurons modeled by the RRW. A surprisingly large amount of shared input-on the order of -is needed to simulate the modest peaks in cross correlograms typically observed in real cortical neurons. The same model explains the weak covariation in response rate (noise correlation) measured from pairs of neurons (r 0.15). The levels of synchrony observed in the cortex, therefore, can be reasonably understood as an obligatory consequence of common input-the design architecture that permits rate information to be transmitted quickly and reliably through ensembles of neurons. Changes in synchrony evoked by different stimulus configurations may simply reflect changes in the proportion of common input activated in the different conditions. (Supported by The McKnight Foundation, RR00166 and EY05603)