Chaos-induced modulation of reliability boosts output firing rate in downstream cortical areas

The reproducibility of neural spike train responses to an identical stimulus across different presentations (trials) has been studied extensively. Reliability, the degree of reproducibility of spike trains, was found to depend in part on the amplitude and frequency content of the stimulus [J. Hunter and J. Milton, J. Neurophysiol. 90, 387 (2003)]. The responses across different trials can sometimes be interpreted as the response of an ensemble of similar neurons to a single stimulus presentation. How does the reliability of the activity of neural ensembles affect information transmission between different cortical areas? We studied a model neural system consisting of two ensembles of neurons with Hodgkin-Huxley-type channels. The first ensemble was driven by an injected sinusoidal current that oscillated in the gamma-frequency range (40 Hz) and its output spike trains in turn drove the second ensemble by fast excitatory synaptic potentials with short term depression. We determined the relationship between the reliability of the first ensemble and the response of the second ensemble. In our paradigm the neurons in the first ensemble were initially in a chaotic state with unreliable and imprecise spike trains. The neurons became entrained to the oscillation and responded reliably when the stimulus power was increased by less than 10%. The firing rate of the first ensemble increased by 30%, whereas that of the second ensemble could increase by an order of magnitude. We also determined the response of the second ensemble when its input spike trains, which had non-Poisson statistics, were replaced by an equivalent ensemble of Poisson spike trains. The resulting output spike trains were significantly different from the original response, as assessed by the metric introduced by Victor and Purpura [J. Neurophysiol. 76, 1310 (1996)]. These results are a proof of principle that weak temporal modulations in the power of gamma-frequency oscillations in a given cortical area can strongly affect firing rate responses downstream by way of reliability in spite of rather modest changes in firing rate in the originating area.