Dynamical Mechanisms for Coordinating Long-term Working Memory Based on the Precision of Spike-timing in Cortical Neurons

In the last century, most sensorimotor studies of cortical neurons relied on average firing rates. Rate coding is efficient for fast sensorimotor processing that occurs within a few seconds. Much less is known about the neural mechanisms underlying long-term working memory with a time scale of hours (Ericsson and Kintsch, 1995). Cognitive states may not have sensory or motor correlates. For example, you can sit in a quiet room making plans without moving or sensory processing. You can also make plans while out walking. This suggests that the neural substrate for cognitive states neither depends on nor interferes with ongoing sensorimotor brain activity. In this perspective, I make the case for a possible second tier of neural activity that coexists with the well-established sensorimotor tier, based on coordinated spike-timing activity. The discovery of millisecond-precision spike initiation in cortical neurons was unexpected (Mainen and Sejnowski, 1995). Even more striking was the precision of spiking in vivo, in response to rapidly fluctuating sensory inputs, suggesting that neural circuits could preserve and manipulate sensory information through spike timing. High temporal resolution enables a broader range of neural codes. The relative timing of spikes between presynaptic and postsynaptic neurons in the millisecond range triggers spike-timing-dependent plasticity (STDP). What spike-timing mechanisms could engage STDP in vivo? Cortical traveling waves have been observed across many frequency bands with high temporal precision, and neural mechanisms can plausibly enable traveling waves to trigger STDP lasting for hours in cortical neurons. This temporary cortical network, riding astride the long-term sensorimotor network, could support cognitive processing and long-term working memory.