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Planning activity for internally generated reward goals in monkey amygdala neurons.

Hernádi I, Grabenhorst F, Schultz W - Nat. Neurosci. (2015)

Bottom Line: The best rewards are often distant and can only be achieved by planning and decision-making over several steps.Such prospective activity could underlie the formation and pursuit of internal plans characteristic of goal-directed behavior.The existence of neuronal planning activity in the amygdala suggests that this structure is important in guiding behavior toward internally generated, distant goals.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK.

ABSTRACT
The best rewards are often distant and can only be achieved by planning and decision-making over several steps. We designed a multi-step choice task in which monkeys followed internal plans to save rewards toward self-defined goals. During this self-controlled behavior, amygdala neurons showed future-oriented activity that reflected the animal's plan to obtain specific rewards several trials ahead. This prospective activity encoded crucial components of the animal's plan, including value and length of the planned choice sequence. It began on initial trials when a plan would be formed, reappeared step by step until reward receipt, and readily updated with a new sequence. It predicted performance, including errors, and typically disappeared during instructed behavior. Such prospective activity could underlie the formation and pursuit of internal plans characteristic of goal-directed behavior. The existence of neuronal planning activity in the amygdala suggests that this structure is important in guiding behavior toward internally generated, distant goals.

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Relationship between amygdala planning activity and behavioral performance. (a) Relationship to saving efficiency. Stronger planning activity (sign-corrected regression betas, collapsed across responses encoding sequence value or sequence length across all trials, n = 116) predicted behavioral saving efficiency (accumulated sequence value per unit time, normalized, linear regression). This effect was confirmed in a partial correlation analysis (P < 0.001) that factored out potential confounding variables. (b) Relationship to performance errors. Bars show regression betas (± s.e.m) from a population analysis (combining sequence value and sequence length responses, n = 116) for trials immediately preceding errors (Pre−), error trials (Error), and trials following errors (Post−). The relationship between activity and planning variables was significantly reduced on error trials, when the animals failed to progress towards their saving goal (t1453 = −2.69, P < 0.01, dependent-samples t-test comparing betas on pre-error and error trials), and subsequently reappeared after error correction (t1453 = 3.47, P < 0.001, dependent-samples t-test comparing betas on error and post-error trials).
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Figure 6: Relationship between amygdala planning activity and behavioral performance. (a) Relationship to saving efficiency. Stronger planning activity (sign-corrected regression betas, collapsed across responses encoding sequence value or sequence length across all trials, n = 116) predicted behavioral saving efficiency (accumulated sequence value per unit time, normalized, linear regression). This effect was confirmed in a partial correlation analysis (P < 0.001) that factored out potential confounding variables. (b) Relationship to performance errors. Bars show regression betas (± s.e.m) from a population analysis (combining sequence value and sequence length responses, n = 116) for trials immediately preceding errors (Pre−), error trials (Error), and trials following errors (Post−). The relationship between activity and planning variables was significantly reduced on error trials, when the animals failed to progress towards their saving goal (t1453 = −2.69, P < 0.01, dependent-samples t-test comparing betas on pre-error and error trials), and subsequently reappeared after error correction (t1453 = 3.47, P < 0.001, dependent-samples t-test comparing betas on error and post-error trials).

Mentions: If planning activity in the amygdala participated in guiding the animals’ behavior, it should fluctuate with behavioral performance. We tested this hypothesis by regressing a measure of the animals’ reward-saving efficiency on the standardized neuronal regression coefficients for sequence value and sequence length. We measured reward-saving efficiency as the accumulated sequence value per unit time, which indicated the extent to which the animals maximized subjective value. Across neuronal responses, stronger planning activity in a given testing session predicted more efficient reward-saving (r = 0.39, P = 2.9 ×10−5, linear regression, Fig. 6a). This relationship remained highly significant after factoring out alternative variables, including interest rate, juice amount, error rate, number of trials, and reward range (P < 0.001, partial correlation). Thus, the strength of planning activity in amygdala neurons explained variation in the animals’ saving efficiency.


Planning activity for internally generated reward goals in monkey amygdala neurons.

Hernádi I, Grabenhorst F, Schultz W - Nat. Neurosci. (2015)

Relationship between amygdala planning activity and behavioral performance. (a) Relationship to saving efficiency. Stronger planning activity (sign-corrected regression betas, collapsed across responses encoding sequence value or sequence length across all trials, n = 116) predicted behavioral saving efficiency (accumulated sequence value per unit time, normalized, linear regression). This effect was confirmed in a partial correlation analysis (P < 0.001) that factored out potential confounding variables. (b) Relationship to performance errors. Bars show regression betas (± s.e.m) from a population analysis (combining sequence value and sequence length responses, n = 116) for trials immediately preceding errors (Pre−), error trials (Error), and trials following errors (Post−). The relationship between activity and planning variables was significantly reduced on error trials, when the animals failed to progress towards their saving goal (t1453 = −2.69, P < 0.01, dependent-samples t-test comparing betas on pre-error and error trials), and subsequently reappeared after error correction (t1453 = 3.47, P < 0.001, dependent-samples t-test comparing betas on error and post-error trials).
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Figure 6: Relationship between amygdala planning activity and behavioral performance. (a) Relationship to saving efficiency. Stronger planning activity (sign-corrected regression betas, collapsed across responses encoding sequence value or sequence length across all trials, n = 116) predicted behavioral saving efficiency (accumulated sequence value per unit time, normalized, linear regression). This effect was confirmed in a partial correlation analysis (P < 0.001) that factored out potential confounding variables. (b) Relationship to performance errors. Bars show regression betas (± s.e.m) from a population analysis (combining sequence value and sequence length responses, n = 116) for trials immediately preceding errors (Pre−), error trials (Error), and trials following errors (Post−). The relationship between activity and planning variables was significantly reduced on error trials, when the animals failed to progress towards their saving goal (t1453 = −2.69, P < 0.01, dependent-samples t-test comparing betas on pre-error and error trials), and subsequently reappeared after error correction (t1453 = 3.47, P < 0.001, dependent-samples t-test comparing betas on error and post-error trials).
Mentions: If planning activity in the amygdala participated in guiding the animals’ behavior, it should fluctuate with behavioral performance. We tested this hypothesis by regressing a measure of the animals’ reward-saving efficiency on the standardized neuronal regression coefficients for sequence value and sequence length. We measured reward-saving efficiency as the accumulated sequence value per unit time, which indicated the extent to which the animals maximized subjective value. Across neuronal responses, stronger planning activity in a given testing session predicted more efficient reward-saving (r = 0.39, P = 2.9 ×10−5, linear regression, Fig. 6a). This relationship remained highly significant after factoring out alternative variables, including interest rate, juice amount, error rate, number of trials, and reward range (P < 0.001, partial correlation). Thus, the strength of planning activity in amygdala neurons explained variation in the animals’ saving efficiency.

Bottom Line: The best rewards are often distant and can only be achieved by planning and decision-making over several steps.Such prospective activity could underlie the formation and pursuit of internal plans characteristic of goal-directed behavior.The existence of neuronal planning activity in the amygdala suggests that this structure is important in guiding behavior toward internally generated, distant goals.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK.

ABSTRACT
The best rewards are often distant and can only be achieved by planning and decision-making over several steps. We designed a multi-step choice task in which monkeys followed internal plans to save rewards toward self-defined goals. During this self-controlled behavior, amygdala neurons showed future-oriented activity that reflected the animal's plan to obtain specific rewards several trials ahead. This prospective activity encoded crucial components of the animal's plan, including value and length of the planned choice sequence. It began on initial trials when a plan would be formed, reappeared step by step until reward receipt, and readily updated with a new sequence. It predicted performance, including errors, and typically disappeared during instructed behavior. Such prospective activity could underlie the formation and pursuit of internal plans characteristic of goal-directed behavior. The existence of neuronal planning activity in the amygdala suggests that this structure is important in guiding behavior toward internally generated, distant goals.

Show MeSH
Related in: MedlinePlus