Discharge Synchrony during the Transition of Behavioral Goal Representations Encoded by Discharge Rates of Prefrontal Neurons

Abstract

To investigate the temporal relationship between synchrony in the discharge of neuron pairs and modulation of the discharge rate, we recorded the neuronal activity of the lateral prefrontal cortex of monkeys performing a behavioral task that required them to plan an immediate goal of action to attain a final goal. Information about the final goal was retrieved via visual instruction signals, whereas information about the immediate goal was generated internally. The synchrony of neuron pair discharges was analyzed separately from changes in the firing rate of individual neurons during a preparatory period. We focused on neuron pairs that exhibited a representation of the final goal followed by a representation of the immediate goal at a later stage. We found that changes in synchrony and discharge rates appeared to be complementary at different phases of the behavioral task. Synchrony was maximized during a specific phase in the preparatory period corresponding to a transitional stage when the neuronal activity representing the final goal was replaced with that representing the immediate goal. We hypothesize that the transient increase in discharge synchrony is an indication of a process that facilitates dynamic changes in the prefrontal neural circuits in order to undergo profound state changes.

Long-Term Modifications in Motor Cortical Dynamics Induced by Intensive Practice

“…However, it is much less clear how these networks organize dynamically their activity in space and time. The concept of cell assemblies (Hebb, 1949;Aertsen et al, 1986;Gerstein et al, 1989;Abeles, 1991) uses synchrony as an additional dimension to the rate code, suggesting that the system may retrieve much more information from a given neuronal activity pattern (Riehle et al, 1997;Hatsopoulos et al, 1998;Baker et al, 2001;Sakamoto et al, 2008). We have shown that the strength of precise spike synchrony modulates in time, independent of rate modulations (Riehle et al, 1997).…”

“…It is thus tempting to speculate that the increase in synchrony related to this specific moment reflects a cognitive state, an internal representation of (the nonappearance of) an expected event. Alternatively, it could be related to a shift in the cognitive state necessary for movement reprogramming, because the time of go signal also indicates movement direction in this task (Sakamoto et al, 2008).…”

“…It has been proposed that synchrony and firing rate may be involved in different processing types (Riehle et al, 1997;Riehle, 1999, 2003;Baker et al, 2001;Sakamoto et al, 2008;Tsujimoto et al, 2008). Transient synchrony, strengthened by learning, has been suggested to facilitate interstructural communication (Paz et al, 2007) or to promote the transition between different cognitive states determined by firing rate modulations .…”

The potential of multilateral analyses of neuronal activities in future brain-machine interface research

“…For example, we have reported that neurons in the monkey prefrontal cortex exhibited representational shifts in behavioral goals encoded by firing rate (Fig. 1) [6,7]. A path-planning task is a demanding task in which monkeys plan an immediate goal of action to attain a final goal presented early in the preparatory period of the trial (see Methods).…”

Spatiotemporal patterns of current source density in the prefrontal cortex of a behaving monkey

“…That is, the PFC is responsible for determining actions or action plans according to sensory and mnemonic inputs rather than merely responding to them. Correspondingly, recent physiological and theoretical studies have revealed that the output properties of neurons in PFC circuits dynamically change depending on their supposed inputs (Katori et al, 2011;Machens, Romo, & Brody, 2005;Sakamoto et al, 2013Sakamoto et al, , 2008. However, signals obtained from conventional single-unit recordings are spikes that reflect the output of neurons or neuronal circuits, and signals that directly reflect the inputs to them are unclear.…”