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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

Illustration of temporally coordinating the retrieval of choice-relevant information through theta rhythmic activity. The blue line refers to the theta activity not in one particular “decision” area, but to local theta rhythms in all those areas whose concerted spike coordination influence which choice is made. The gray shaded area indicates the time window of the theta cycle at which spike output is generated and received from participating neurons. The theta rhythmic retrieval hypothesis suggests that a choice is formed when all relevant sources of evidence (arrows) functionally activate around a similar phase of the theta cycle (solid arrows at the time of choice), which takes three cycles in the sketched outline. Empirical evidence for theta synchronized information of context, reward, memory, and sensory evidence is surveyed in the text.
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Figure 1: Illustration of temporally coordinating the retrieval of choice-relevant information through theta rhythmic activity. The blue line refers to the theta activity not in one particular “decision” area, but to local theta rhythms in all those areas whose concerted spike coordination influence which choice is made. The gray shaded area indicates the time window of the theta cycle at which spike output is generated and received from participating neurons. The theta rhythmic retrieval hypothesis suggests that a choice is formed when all relevant sources of evidence (arrows) functionally activate around a similar phase of the theta cycle (solid arrows at the time of choice), which takes three cycles in the sketched outline. Empirical evidence for theta synchronized information of context, reward, memory, and sensory evidence is surveyed in the text.

Mentions: During awake and active states, neuronal activation patterns are prepared to evaluate input to link it to motor action. This prepared state is frequently governed by a behavioral goal of the organism, which per definition biases neuronal circuits to process and evaluate sensory inputs according to their values to achieve the goal (Miller and Cohen, 2001; Glimcher et al., 2009). Evaluating the value of information in relation to a behavioral goal involves a multitude of processes. These processes are reflected in neuronal activation patterns and are supposed to take place around the time when the organism is forming the decision about which behavioral route to take in the face of multiple alternatives. Among the multitude of processes involved, at least four major component processes have been experimentally well isolated and linked to rhythmic theta synchronization within and between neuronal circuits: (i) The evaluation of stimulus–reward associations, (ii) the retrieval of working memory representations, (iii) the retrieval of long-term memories relevant to inform the expected value of possible choices, and (iv) the representation of the task rules, which govern how incoming sensory input map onto possible responses. In the following, we show that these component processes are associated with and possibly realized by rhythmically synchronizing neuronal groups in distant brain areas at theta frequency with high temporal and spatial specificity. In particular, the outlined evidence suggests that multiple types of choice-relevant information is structured by the theta cycle as sketched in Figure 1. The following will document the accumulated evidence supporting the hypothesis that theta synchronization across multiple areas could be a neuronal prerequisite which underlies the actual formation of a choice.


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

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

Illustration of temporally coordinating the retrieval of choice-relevant information through theta rhythmic activity. The blue line refers to the theta activity not in one particular “decision” area, but to local theta rhythms in all those areas whose concerted spike coordination influence which choice is made. The gray shaded area indicates the time window of the theta cycle at which spike output is generated and received from participating neurons. The theta rhythmic retrieval hypothesis suggests that a choice is formed when all relevant sources of evidence (arrows) functionally activate around a similar phase of the theta cycle (solid arrows at the time of choice), which takes three cycles in the sketched outline. Empirical evidence for theta synchronized information of context, reward, memory, and sensory evidence is surveyed in the text.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Illustration of temporally coordinating the retrieval of choice-relevant information through theta rhythmic activity. The blue line refers to the theta activity not in one particular “decision” area, but to local theta rhythms in all those areas whose concerted spike coordination influence which choice is made. The gray shaded area indicates the time window of the theta cycle at which spike output is generated and received from participating neurons. The theta rhythmic retrieval hypothesis suggests that a choice is formed when all relevant sources of evidence (arrows) functionally activate around a similar phase of the theta cycle (solid arrows at the time of choice), which takes three cycles in the sketched outline. Empirical evidence for theta synchronized information of context, reward, memory, and sensory evidence is surveyed in the text.
Mentions: During awake and active states, neuronal activation patterns are prepared to evaluate input to link it to motor action. This prepared state is frequently governed by a behavioral goal of the organism, which per definition biases neuronal circuits to process and evaluate sensory inputs according to their values to achieve the goal (Miller and Cohen, 2001; Glimcher et al., 2009). Evaluating the value of information in relation to a behavioral goal involves a multitude of processes. These processes are reflected in neuronal activation patterns and are supposed to take place around the time when the organism is forming the decision about which behavioral route to take in the face of multiple alternatives. Among the multitude of processes involved, at least four major component processes have been experimentally well isolated and linked to rhythmic theta synchronization within and between neuronal circuits: (i) The evaluation of stimulus–reward associations, (ii) the retrieval of working memory representations, (iii) the retrieval of long-term memories relevant to inform the expected value of possible choices, and (iv) the representation of the task rules, which govern how incoming sensory input map onto possible responses. In the following, we show that these component processes are associated with and possibly realized by rhythmically synchronizing neuronal groups in distant brain areas at theta frequency with high temporal and spatial specificity. In particular, the outlined evidence suggests that multiple types of choice-relevant information is structured by the theta cycle as sketched in Figure 1. The following will document the accumulated evidence supporting the hypothesis that theta synchronization across multiple areas could be a neuronal prerequisite which underlies the actual formation of a choice.

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