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. 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. In this perspective, I make the case for a possible second tier of neural activity that coexists with the well-established sensorimotor tier. The prominent physiological feature of the second tier is coordinated spike timing activity. The interplay of data supporting this hypothesis involves three puzzling yet highly intriguing experimental observations, without any obvious indication that they might actually represent different aspects of a single functional organization. First, consider the precision of spiking in individual neurons. 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. Second, high temporal resolution can also mediate spike timing-dependent plasticity (STDP) by controlling the relative timing of presynaptic and postsynaptic spikes at the millisecond scale. Third, we observe waves across many frequency bands traveling across the cortex. Strikingly, their timing is highly precise. Gamma waves, for example, which are triggered by attention, can plausibly trigger STDP that lasts for hours in cortical neurons. This temporary cortical network, ostensibly a second tier of functionality, rides astride the long-term sensorimotor network and could support cognitive processing and long-term working memory.