Synaptic Self-Organization of Spatio-Temporal Pattern Selectivity

ABSTRACT Spiking model neurons can be set up to respond selectively to specific spatio-temporal spike patterns by optimization of their input weights. It is unknown, however, if existing synaptic plasticity mechanisms can achieve this temporal mode of neuronal coding and computation. Here it is shown that changes of synaptic efficacies which tend to balance excitatory and inhibitory synaptic inputs can make neurons sensitive to particular input spike patterns. Simulations demonstrate that a combination of Hebbian mechanisms, hetero-synaptic plasticity and synaptic scaling is sufficient for self-organizing sensitivity for spatio-temporal spike patterns that repeat in the input. In networks inclusion of hetero-synaptic plasticity leads to specialization and faithful representation of pattern sequences by a group of target neurons. Pattern detection is robust against a range of distortions and noise. The proposed combination of Hebbian mechanisms, hetero-synaptic plasticity and synaptic scaling is found to protect the memories for specific patterns from being overwritten by ongoing learning during extended periods when the patterns are not present. This suggests a novel explanation for the long term robustness of memory traces despite ongoing activity with substantial synaptic plasticity. Taken together, our result promote the plausibility of precise temporal coding in the brain. Author summary Neurons communicate using action potentials, that are pulses localized in time. There is evidence that the exact timing of these so called spikes carries information. The hypothesis, however, that computations in brains are indeed based on precise patterns of spikes is debated, particularly because this would require the existence of suitable detectors. While theoretically, individual neurons can perform spike pattern detection when their input synapses are carefully adjusted, it is not known if existing synaptic plasticity mechanisms indeed support this coding principle. Here, a combination of basic but realistic mechanisms is demonstrated to self-organize the synaptic input efficacies such that individual neurons become detectors of patterns repeating in the input. The proposed combination of learning mechanisms yields a balance of excitation and inhibition similar to observations in cortex, robustness of detection against perturbations and noise, and persistence of memory against plasticity during ongoing activity without the learned patterns. The proposed learning mechanism enables groups of neurons to incrementally acquire sets of patterns thereby faithfully representing their ’which’ and ’when’ in sequences. These results suggest that computations based on spatio-temporal spike patterns might emerge without any supervision from the synaptic plasticity mechanisms present in the brain.