Sensitivity to Stimulus Irregularity Is Inherent in Neural Networks

Abstract

Behavior is controlled by complex neural networks in which neurons process thousands of inputs. However, even short spike trains evoked in a single cortical neuron were demonstrated to be sufficient to influence behavior in vivo. Specifically, irregular sequences of interspike intervals (ISIs) had a more reliable influence on behavior despite their resemblance to stochastic activity. Similarly, irregular tactile stimulation led to higher rates of behavioral responses. In this study, we identify the mechanisms enabling this sensitivity to stimulus irregularity (SSI) on the neuronal and network levels using simulated spiking neural networks. Matching in vivo experiments, we find that irregular stimulation elicits more detectable network events (bursts) than regular stimulation. Dissecting the stimuli, we identify short ISIs—occurring more frequently in irregular stimulations—as the main drivers of SSI rather than complex irregularity per se. In addition, we find that short-term plasticity modulates SSI. We subsequently eliminate the different mechanisms in turn to assess their role in generating SSI. Removing inhibitory interneurons, we find that SSI is retained, suggesting that SSI is not dependent on inhibition. Removing recurrency, we find that SSI is retained due to the ability of individual neurons to integrate activity over short timescales (“cell memory”). Removing single-neuron dynamics, we find that SSI is retained based on the short-term retention of activity within the recurrent network structure (“network memory”). Finally, using a further simplified probabilistic model, we find that local network structure is not required for SSI. Hence, SSI is identified as a general property that we hypothesize to be ubiquitous in neural networks with different structures and biophysical properties. Irregular sequences contain shorter ISIs, which are the main drivers underlying SSI. The experimentally observed SSI should thus generalize to other systems, suggesting a functional role for irregular activity in cortex.