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Selective theta-synchronization of choice-relevant information subserves goal-directed behavior.

Womelsdorf T, Vinck M, Leung LS, Everling S - Front Hum Neurosci (2010)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Pharmacology, University of Western Ontario London, ON, Canada.

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.

No MeSH data available.


Related in: MedlinePlus

Task rule selective theta activity in macaque anterior cingulate cortex just before a “decision point.” (A) Time-frequency distribution of statistical reliable task selectivity of LFP power. Time zero marks the onset of a peripheral stimulus on either right/left side and requiring either a pro-, or an anti-saccade response. (B) Task selective theta activity emerged early in those correct trials, where the task representation had to be re-established following an error response (bottom left, and red line), compared to correct trials following other correct trials (top left and blue line). Adapted with permission from Womelsdorf et al. (2010).
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Figure 3: Task rule selective theta activity in macaque anterior cingulate cortex just before a “decision point.” (A) Time-frequency distribution of statistical reliable task selectivity of LFP power. Time zero marks the onset of a peripheral stimulus on either right/left side and requiring either a pro-, or an anti-saccade response. (B) Task selective theta activity emerged early in those correct trials, where the task representation had to be re-established following an error response (bottom left, and red line), compared to correct trials following other correct trials (top left and blue line). Adapted with permission from Womelsdorf et al. (2010).

Mentions: Importantly, the neuronal representation of relevant SR mapping is structured in time by theta rhythmic synchronization in ACC (Womelsdorf et al., 2010). In this study, macaque monkeys performed blocks of two different tasks requiring them to either saccade toward or away from a peripheral stimulus (pro-saccade and anti-saccade tasks). Both tasks differed only in how a peripheral stimulus (randomly presented in the left or right hemifield) mapped onto a response. The SR mapping stayed constant over 30 consecutive trials before it was switched, forcing the monkeys to retain an internal representation of the currently relevant SR mapping rule and retrieving this representation prior to processing the sensory stimulus for efficient task performance, i.e., during a time akin to a decision point. Notably, at this decision point selective changes in theta activity in ACC predicted which SR mapping the monkey was about to apply upon peripheral stimulus onset (Figure 3A). In spatially separate neuronal groups, theta activity and synchronized spiking to LFP theta emerged for one versus the other SR mapping rule at 0.4 s before peripheral stimulus onset. Interestingly, a previous study reported that task selectivity becomes evident also in average firing rates from 0.4 s before stimulus onset, but the latency of task selective firing changed over trials on the same task in anterior cingulate and prefrontal cortex (Johnston et al., 2007): In ACC, firing rates were signaling the task rule at 0.4 s only in the immediate trials after task rules were switched, but its latency declined with trials on the same rule. Neurons in prefrontal cortex showed the reverse pattern: Task selectivity became apparent at 0.4 s before stimulus onset only after some trials on the same rule (Johnston et al., 2007). This pattern of results shows that LFP theta activity within ACC translated into higher spike counts only when the task demands had recently changed, i.e., after a task rule switch, and when prefrontal neurons did not yet fire selectively for one task versus the other. During the higher task demands to establish a new task rule, LFP theta activity and firing patterns were the earliest task selective signal recorded, likely reflecting a genuine local contribution of ACC circuitry for cognitive control. However, when task demands were established after few trials on the same task rule, the spike output contribution of the ACC declined, suggesting that task selective LFP theta activity reflected partly the input from prefrontal projections or other nodes of a larger cognitive control network.


Selective theta-synchronization of choice-relevant information subserves goal-directed behavior.

Womelsdorf T, Vinck M, Leung LS, Everling S - Front Hum Neurosci (2010)

Task rule selective theta activity in macaque anterior cingulate cortex just before a “decision point.” (A) Time-frequency distribution of statistical reliable task selectivity of LFP power. Time zero marks the onset of a peripheral stimulus on either right/left side and requiring either a pro-, or an anti-saccade response. (B) Task selective theta activity emerged early in those correct trials, where the task representation had to be re-established following an error response (bottom left, and red line), compared to correct trials following other correct trials (top left and blue line). Adapted with permission from Womelsdorf et al. (2010).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2991127&req=5

Figure 3: Task rule selective theta activity in macaque anterior cingulate cortex just before a “decision point.” (A) Time-frequency distribution of statistical reliable task selectivity of LFP power. Time zero marks the onset of a peripheral stimulus on either right/left side and requiring either a pro-, or an anti-saccade response. (B) Task selective theta activity emerged early in those correct trials, where the task representation had to be re-established following an error response (bottom left, and red line), compared to correct trials following other correct trials (top left and blue line). Adapted with permission from Womelsdorf et al. (2010).
Mentions: Importantly, the neuronal representation of relevant SR mapping is structured in time by theta rhythmic synchronization in ACC (Womelsdorf et al., 2010). In this study, macaque monkeys performed blocks of two different tasks requiring them to either saccade toward or away from a peripheral stimulus (pro-saccade and anti-saccade tasks). Both tasks differed only in how a peripheral stimulus (randomly presented in the left or right hemifield) mapped onto a response. The SR mapping stayed constant over 30 consecutive trials before it was switched, forcing the monkeys to retain an internal representation of the currently relevant SR mapping rule and retrieving this representation prior to processing the sensory stimulus for efficient task performance, i.e., during a time akin to a decision point. Notably, at this decision point selective changes in theta activity in ACC predicted which SR mapping the monkey was about to apply upon peripheral stimulus onset (Figure 3A). In spatially separate neuronal groups, theta activity and synchronized spiking to LFP theta emerged for one versus the other SR mapping rule at 0.4 s before peripheral stimulus onset. Interestingly, a previous study reported that task selectivity becomes evident also in average firing rates from 0.4 s before stimulus onset, but the latency of task selective firing changed over trials on the same task in anterior cingulate and prefrontal cortex (Johnston et al., 2007): In ACC, firing rates were signaling the task rule at 0.4 s only in the immediate trials after task rules were switched, but its latency declined with trials on the same rule. Neurons in prefrontal cortex showed the reverse pattern: Task selectivity became apparent at 0.4 s before stimulus onset only after some trials on the same rule (Johnston et al., 2007). This pattern of results shows that LFP theta activity within ACC translated into higher spike counts only when the task demands had recently changed, i.e., after a task rule switch, and when prefrontal neurons did not yet fire selectively for one task versus the other. During the higher task demands to establish a new task rule, LFP theta activity and firing patterns were the earliest task selective signal recorded, likely reflecting a genuine local contribution of ACC circuitry for cognitive control. However, when task demands were established after few trials on the same task rule, the spike output contribution of the ACC declined, suggesting that task selective LFP theta activity reflected partly the input from prefrontal projections or other nodes of a larger cognitive control network.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Pharmacology, University of Western Ontario London, ON, Canada.

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.

No MeSH data available.


Related in: MedlinePlus