Intermittent rate coding and cue-specific neuronal ensembles support working memory

Persistent, memorandum-specific neuronal spiking activity has long been
hypothesized to underlie working memory. However, emerging evidence
suggests a possible role for ‘activity-silent’, synaptic mechanisms. This
issue remains controversial because evidence for either view has largely
relied on datasets that fail to capture single-trial population dynamics
or on indirect measures of neuronal spiking. We addressed this by
examining the dynamics of mnemonic information on single trials obtained
from large, local populations of lateral prefrontal neurons recorded
simultaneously in monkeys performing a working memory task. 
Here, we show that mnemonic information does not persist in the spiking
activity of neuronal populations during memory delays, but instead
alternates between coordinated ‘On’ and ‘Off’ states. At the level of
single neurons, Off states are driven both by a loss of selectivity for
memoranda and a return of firing rates to spontaneous levels. Further
exploiting the large-scale recordings, we show that mnemonic information
is available in the patterns of functional connections among neuronal
ensembles during Off states. Our results suggest that intermittent periods
of memoranda-specific spiking coexist with synaptic mechanisms to support
working memory.