Selective Theta-Synchronization of Choice-Relevant Information Subserves Goal-Directed Behavior

Abstract

Theta activity reflects a state of rhythmic modulation of excitability at the level of single neuron membranes, within local neuronal groups and between distant nodes of a neuronal network. A wealth of evidence has shown that during theta states distant neuronal groups synchronize, forming networks of spatially confined neuronal clusters at specific time periods during task performance. Here, we show that a functional commonality of networks engaging in theta rhythmic states is that they emerge around decision points, reflecting rhythmic synchronization of choice-relevant information. Decision points characterize a point in time shortly before a subject chooses to select one action over another, i.e., when automatic behavior is terminated and the organism reactivates multiple sources of information to evaluate the evidence for available choices. As such, decision processes require the coordinated retrieval of choice-relevant information including (i) the retrieval of stimulus evaluations (stimulus–reward associations) and reward expectancies about future outcomes, (ii) the retrieval of past and prospective memories (e.g., stimulus–stimulus associations), (iii) the reactivation of contextual task rule representations (e.g., stimulus–response mappings), along with (iv) an ongoing assessment of sensory evidence. An increasing number of studies reveal that retrieval of these multiple types of information proceeds within few theta cycles through synchronized spiking activity across limbic, striatal, and cortical processing nodes. The outlined evidence suggests that evolving spatially and temporally specific theta synchronization could serve as the critical correlate underlying the selection of a choice during goal-directed behavior.

Neural processes for action observation

“…Overall, our finding was in line with the theory that theta band is involved in sensorimotor integration and that it reflects computational processes near behavioural decision points (Cruikshank et al, 2012;Rawle et al, 2012;Womelsdorf et al, 2010).…”

“…Several previous experiments explained central theta power increases with neural processing related to either sensorimotor integration or to behavioural decision points (Cheyne et al, 2012;Cruikshank et al, 2012;Rawle et al, 2012;Womelsdorf et al, 2010). Furthermore, experiments reported increased theta activity during action initiation compared to action preparation (Cheyne et al, 2012;Cruikshank et al, 2012).…”

“…Theoretical models hypothesise that theta activity is strongest around behavioural decision points because this oscillatory band is involved in the selection or decision processes related to movements (for a review see Womelsdorf et al, 2010).…”

“…Working-memory related brain processes are often linked to increase in theta power over parietal electrodes, contralateral to the visual hemifield where to-be-memorised items are located (Klaver et al, 1999;Vogel & Machizawa, 2004). Recent theories claim that theta activity is involved in the integration of memory representations with current motor plans, rather than working-memory activity per se (Rawle et al, 2012, Womelsdorf et al, 2010. For example, Rawle and colleagues (2012) reported stronger theta power increase over parietal areas after participants observed a precue, and stronger theta power at frontal sites following a response signal.…”

Losing Control Under Ketamine: Suppressed Cortico-Hippocampal Drive Following Acute Ketamine in Rats

“…For example, numerous investigations of prefrontal and hippocampal circuits in both rodents and humans highlight the importance of theta (4-10 Hz) and gamma (32-150 Hz) rhythms and their interaction for the successful integration of both spatial and non-spatial information during goal-directed behaviors (Jones and Wilson, 2005;Sirota et al, 2008;Anderson et al, 2010;Benchenane et al, 2010;Hyman et al, 2010;Womelsdorf et al, 2010;Brockmann et al, 2011). These oscillatory rhythms emerge from interactions between excitatory glutamatergic and inhibitory GABAergic neurotransmission, which are in turn subject to behavior-dependent neuromodulation.…”