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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.

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Related in: MedlinePlus

Reward anticipation in orbitofrontal cortex conveyed through theta synchronized spike output. (A,B) LFP traces and accompanying action potentials during the anticipation period in example trials when a rodent awaited a sucrose (A), or quinine (B) outcome. Colored/gray lines show theta band filtered and raw LFP traces. (C) Time-frequency distribution of spike-LFP phase locking during the anticipation period (before reward delivery) shows selective theta band synchronization. (D) Timing and strength of theta band activity reverses with reversal of trial outcome associations. y-Axis denote trials relative to reversal; The upper two panels show transition from preferred (sucrose) reward to aversive outcome, while the bottom two panel shows the reversal back to the preferred outcome. Adapted with permission from van Wingerden et al. (2010).
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Figure 4: Reward anticipation in orbitofrontal cortex conveyed through theta synchronized spike output. (A,B) LFP traces and accompanying action potentials during the anticipation period in example trials when a rodent awaited a sucrose (A), or quinine (B) outcome. Colored/gray lines show theta band filtered and raw LFP traces. (C) Time-frequency distribution of spike-LFP phase locking during the anticipation period (before reward delivery) shows selective theta band synchronization. (D) Timing and strength of theta band activity reverses with reversal of trial outcome associations. y-Axis denote trials relative to reversal; The upper two panels show transition from preferred (sucrose) reward to aversive outcome, while the bottom two panel shows the reversal back to the preferred outcome. Adapted with permission from van Wingerden et al. (2010).

Mentions: Within rodent orbitofrontal cortex, a recent study has shown that part of the reward predicting signal is the synchronized firing of neurons to an underlying theta activity, evolving in close correspondence to the degree to which stimulus–reward associations are learned and become predictable for the brain (van Wingerden et al., 2010). In this study rodents had to discriminate one of two odors during an odor sampling period in order to decide to either approach or withhold approaching to a food well. When approaching the food well, rodents had to wait for 1 s before the trial outcome was disclosed with either a positive outcome (sucrose reward) upon correctly approaching, or a negative feedback (quinine) when approaching was incorrect. Figure 4A illustrates that during the correct anticipation of reward, theta activity emerged with spike output locked to the positive flanks of the theta oscillation. In contrast, during trials when reward anticipation was not maximal, there was no spike-LFP locking signature in the waiting period Figure 4B. Notably this pattern of enhance spike-LFP phase locking was evident for more than half of the recorded sites within OFC, was unaffected by overt movement confounds, and emerged with high temporal specificity during anticipation (Figure 4C). Interestingly, it was most strongly expressed, both, during the anticipation and consumption of a reward, in a selective group of anticipation cells. Notably, the latency of predictive theta activity varied in close correspondence with the predictability of the reward: When the specific odor associated with the preferred reward was reversed to indicate a non-preferred reward, theta activity decreased and vanished in few trials (Figure 4D). During the same time, trials with the second odor now predicting the preferred reward resulted in progressively increased anticipatory theta activity, evolving initially late during anticipation, and progressively shifting to early periods over trials (Figure 4D). These findings therefore reveal that reward anticipation is available to other systems in theta-synchronized spiking responses. Critically, theta synchronized output from the OFC about the anticipated reward in this described study was indicative of the type of outcome expected, rather than indicating a general state of un-selective reward expectation. Such reward selectivity is required to learn the stimulus–reward association in the first place, but also to inform other neuronal groups about the expected value of possible actions prior to choosing to engage in a particular action.


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

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

Reward anticipation in orbitofrontal cortex conveyed through theta synchronized spike output. (A,B) LFP traces and accompanying action potentials during the anticipation period in example trials when a rodent awaited a sucrose (A), or quinine (B) outcome. Colored/gray lines show theta band filtered and raw LFP traces. (C) Time-frequency distribution of spike-LFP phase locking during the anticipation period (before reward delivery) shows selective theta band synchronization. (D) Timing and strength of theta band activity reverses with reversal of trial outcome associations. y-Axis denote trials relative to reversal; The upper two panels show transition from preferred (sucrose) reward to aversive outcome, while the bottom two panel shows the reversal back to the preferred outcome. Adapted with permission from van Wingerden et al. (2010).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Reward anticipation in orbitofrontal cortex conveyed through theta synchronized spike output. (A,B) LFP traces and accompanying action potentials during the anticipation period in example trials when a rodent awaited a sucrose (A), or quinine (B) outcome. Colored/gray lines show theta band filtered and raw LFP traces. (C) Time-frequency distribution of spike-LFP phase locking during the anticipation period (before reward delivery) shows selective theta band synchronization. (D) Timing and strength of theta band activity reverses with reversal of trial outcome associations. y-Axis denote trials relative to reversal; The upper two panels show transition from preferred (sucrose) reward to aversive outcome, while the bottom two panel shows the reversal back to the preferred outcome. Adapted with permission from van Wingerden et al. (2010).
Mentions: Within rodent orbitofrontal cortex, a recent study has shown that part of the reward predicting signal is the synchronized firing of neurons to an underlying theta activity, evolving in close correspondence to the degree to which stimulus–reward associations are learned and become predictable for the brain (van Wingerden et al., 2010). In this study rodents had to discriminate one of two odors during an odor sampling period in order to decide to either approach or withhold approaching to a food well. When approaching the food well, rodents had to wait for 1 s before the trial outcome was disclosed with either a positive outcome (sucrose reward) upon correctly approaching, or a negative feedback (quinine) when approaching was incorrect. Figure 4A illustrates that during the correct anticipation of reward, theta activity emerged with spike output locked to the positive flanks of the theta oscillation. In contrast, during trials when reward anticipation was not maximal, there was no spike-LFP locking signature in the waiting period Figure 4B. Notably this pattern of enhance spike-LFP phase locking was evident for more than half of the recorded sites within OFC, was unaffected by overt movement confounds, and emerged with high temporal specificity during anticipation (Figure 4C). Interestingly, it was most strongly expressed, both, during the anticipation and consumption of a reward, in a selective group of anticipation cells. Notably, the latency of predictive theta activity varied in close correspondence with the predictability of the reward: When the specific odor associated with the preferred reward was reversed to indicate a non-preferred reward, theta activity decreased and vanished in few trials (Figure 4D). During the same time, trials with the second odor now predicting the preferred reward resulted in progressively increased anticipatory theta activity, evolving initially late during anticipation, and progressively shifting to early periods over trials (Figure 4D). These findings therefore reveal that reward anticipation is available to other systems in theta-synchronized spiking responses. Critically, theta synchronized output from the OFC about the anticipated reward in this described study was indicative of the type of outcome expected, rather than indicating a general state of un-selective reward expectation. Such reward selectivity is required to learn the stimulus–reward association in the first place, but also to inform other neuronal groups about the expected value of possible actions prior to choosing to engage in a particular action.

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