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Identifying the principles of neuronal information processing is one of the most important and most controversially discussed issues in neuroscience. In the neocortex, the emission of any single action potential depends on the cooperativity of a large number of active inputs. Cooperativity has been proposed in various forms, ranging from simple coactivation (Hebb assembly) to precise temporal synchrony like synfire chains or the synchronization of high-frequency oscillations. We have recently reported that both, coactivation of distributed neuronal populations on slow time scales of hundreds of milliseconds as well as synchronization of multi-unit activity with beta- and gamma-frequency oscillations occur in a task dependent fashion during visual short-term memory in prefrontal cortex. Here we present the analysis of the same data on temporally precise spike synchronization. To this end we employ the recently introduced NeuroXidence method that allows for the detection and robust significance estimation of coordinated firing of large numbers of units. The behavioral paradigm comprises two periods with stimulus drive and a long delay period during which neuronal activity is purely intrinsic. We analyzed the activity of 122 units recorded in 12 sessions from 2 monkeys. We first identified synchronous firing on a time scale of 3 ms and corrected for rate modulation on a time scale of 15 ms and slower. We then tested each pattern for being a significant modulation of synchronous firing with respect to behavioral performance or stimulus specificity. We found a total of 18150 different patterns that changed the level of synchrony in a performance related way (all test levels 1%) and which involved up to 8 units simultaneously. Stimulus specific modulation of synchrony occurred in 15273 patterns involving up to 6 units. Individual neurons participated in up to 350 times per second in synchronous patterns. This observation suggests that synchronous spike firing might be a much more salient and informative signal than changes in spike rate if measured across large populations of neurons. Grand average statistics show that both performance related and stimulus specific modulation are highly significant during stimulus presentation and early delay with z-scores (baseline corrected and corrected by shuffled conditions) above 4.2 (Bonferroni corrected) and up to 10. In conclusion, cooperativity occurs at various time scales and is informative about both behavioral performance and memory content. Which time scale is relevant for specific neuronal processes like attention, maintenance or plasticity remains to be determined by selective experimental manipulations.
