A mechanism for graded, dynamically routable current propagation in pulse-gated synfire chains and implications for information coding

Neural oscillations can enhance feature recognition (Azouz and Gray Proceedings of the National Academy of Sciences of the United States of America, 97, 8110–8115 2000), modulate interactions between neurons (Womelsdorf et al. Science, 316, 1609–01612 2007), and improve learning and memory (Markowska et al. The Journal of Neuroscience, 15, 2063–2073 1995). Numerical studies have shown that coherent spiking can give rise to windows in time during which information transfer can be enhanced in neuronal networks (Abeles Israel Journal of Medical Sciences, 18, 83–92 1982; Lisman and Idiart Science, 267, 1512–1515 1995, Salinas and Sejnowski Nature Reviews. Neuroscience, 2, 539–550 2001). Unanswered questions are: 1) What is the transfer mechanism? And 2) how well can a transfer be executed? Here, we present a pulse-based mechanism by which a graded current amplitude may be exactly propagated from one neuronal population to another. The mechanism relies on the downstream gating of mean synaptic current amplitude from one population of neurons to another via a pulse. Because transfer is pulse-based, information may be dynamically routed through a neural circuit with fixed connectivity. We demonstrate the transfer mechanism in a realistic network of spiking neurons and show that it is robust to noise in the form of pulse timing inaccuracies, random synaptic strengths and finite size effects. We also show that the mechanism is structurally robust in that it may be implemented using biologically realistic pulses. The transfer mechanism may be used as a building block for fast, complex information processing in neural circuits. We show that the mechanism naturally leads to a framework wherein neural information coding and processing can be considered as a product of linear maps under the active control of a pulse generator. Distinct control and processing components combine to form the basis for the binding, propagation, and processing of dynamically routed information within neural pathways. Using our framework, we construct example neural circuits to 1) maintain a short-term memory, 2) compute time-windowed Fourier transforms, and 3) perform spatial rotations. We postulate that such circuits, with automatic and stereotyped control and processing of information, are the neural correlates of Crick and Koch’s zombie modes.