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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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Planning activity in amygdala neurons: population data. (a,b) Planning activity (z-normalized) of 72 neurons encoding sequence value across all trials or specifically on first trials. (b) Population activity (magenta, n = 93 responses) reflected sequence value (r2 = 0.91, P < 0.0001, linear regression, n = 7) rather than sequence length (r2 = 0.38, P > 0.1). (c,b) Planning activity of 71 neurons encoding sequence length across all trials or specifically on first trials. (d) Population activity (magenta, n = 92 responses) reflected sequence length (r2 = 0.85, P = 0.0035, n = 7) rather than sequence value (r2= 0.14, P > 0.4). (e, f) Activity of neurons tested in the imperative task failed to reflect sequence value or sequence length when saving was instructed (data from 30 neurons encoding sequence value and 29 neurons encoding sequence length). (g) Regression betas for observed data (orange, n = 829 responses from 329 neurons, collapsed across sequence value and sequence length) and trial-shuffled data (black, scaled down 1,000 times). The distribution of observed data was shifted towards higher positive and negative values (Kolmogorov-Smirnov test). (h) Histological reconstruction of 72 sequence value neurons and 71 sequence length neurons. Green, white, pink, yellow and blue symbols: example neurons in Fig. 2 and Fig. 3a–d, respectively. Collapsing across anterior-posterior dimension resulted in symbol overlap. (i) Proportion of neurons with planning activity (n = 123 neurons, collapsed across sequence value and sequence length) in basolateral and centromedial amygdala (P = 0.005, χ2-test) and corresponding recording depths (reference: bregma).
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Figure 4: Planning activity in amygdala neurons: population data. (a,b) Planning activity (z-normalized) of 72 neurons encoding sequence value across all trials or specifically on first trials. (b) Population activity (magenta, n = 93 responses) reflected sequence value (r2 = 0.91, P < 0.0001, linear regression, n = 7) rather than sequence length (r2 = 0.38, P > 0.1). (c,b) Planning activity of 71 neurons encoding sequence length across all trials or specifically on first trials. (d) Population activity (magenta, n = 92 responses) reflected sequence length (r2 = 0.85, P = 0.0035, n = 7) rather than sequence value (r2= 0.14, P > 0.4). (e, f) Activity of neurons tested in the imperative task failed to reflect sequence value or sequence length when saving was instructed (data from 30 neurons encoding sequence value and 29 neurons encoding sequence length). (g) Regression betas for observed data (orange, n = 829 responses from 329 neurons, collapsed across sequence value and sequence length) and trial-shuffled data (black, scaled down 1,000 times). The distribution of observed data was shifted towards higher positive and negative values (Kolmogorov-Smirnov test). (h) Histological reconstruction of 72 sequence value neurons and 71 sequence length neurons. Green, white, pink, yellow and blue symbols: example neurons in Fig. 2 and Fig. 3a–d, respectively. Collapsing across anterior-posterior dimension resulted in symbol overlap. (i) Proportion of neurons with planning activity (n = 123 neurons, collapsed across sequence value and sequence length) in basolateral and centromedial amygdala (P = 0.005, χ2-test) and corresponding recording depths (reference: bregma).

Mentions: Among 329 task-related neurons, 123 (37%, 66/57 from animal A/B) showed planning activity related to sequence value or sequence length, either throughout saving sequences or specifically on initial trials (Fig. 4a–d, Table 1, Supplementary Tables 1–3, Supplementary Fig. 4). The average activity of sequence value neurons followed closely the average subjective value profile, which was a non-monotonic function of sequence length (r2 = 0.91, P<0.0001, linear regression; compare magenta curve and black bars in Fig. 4b). Analysis of trial-by-trial activity in these neurons confirmed this effect (P = 2.2 × 10−15, partial correlation factored out sequence length). By contrast, activity of sequence length neurons increased linearly with sequence length (r2 = 0.85, P = 0.0035, linear regression, Fig. 4d). Analysis of trial-by-trial activity in these neurons confirmed this effect (P = 7.4 × 10−5, partial correlation factored out sequence value). Supplementary analysis confirmed a graded, parametric representation of sequence value or sequence length, rather than sharp tuning to specific sequences (Supplementary Fig. 5). A subset of neurons with planning activity was tested in the imperative task. In most of them (53/57, 93%), planning activity was not found when saving was externally instructed (Fig. 4e,f). Thus, planning activity appeared to be largely specific for internally controlled saving behavior.


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

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

Planning activity in amygdala neurons: population data. (a,b) Planning activity (z-normalized) of 72 neurons encoding sequence value across all trials or specifically on first trials. (b) Population activity (magenta, n = 93 responses) reflected sequence value (r2 = 0.91, P < 0.0001, linear regression, n = 7) rather than sequence length (r2 = 0.38, P > 0.1). (c,b) Planning activity of 71 neurons encoding sequence length across all trials or specifically on first trials. (d) Population activity (magenta, n = 92 responses) reflected sequence length (r2 = 0.85, P = 0.0035, n = 7) rather than sequence value (r2= 0.14, P > 0.4). (e, f) Activity of neurons tested in the imperative task failed to reflect sequence value or sequence length when saving was instructed (data from 30 neurons encoding sequence value and 29 neurons encoding sequence length). (g) Regression betas for observed data (orange, n = 829 responses from 329 neurons, collapsed across sequence value and sequence length) and trial-shuffled data (black, scaled down 1,000 times). The distribution of observed data was shifted towards higher positive and negative values (Kolmogorov-Smirnov test). (h) Histological reconstruction of 72 sequence value neurons and 71 sequence length neurons. Green, white, pink, yellow and blue symbols: example neurons in Fig. 2 and Fig. 3a–d, respectively. Collapsing across anterior-posterior dimension resulted in symbol overlap. (i) Proportion of neurons with planning activity (n = 123 neurons, collapsed across sequence value and sequence length) in basolateral and centromedial amygdala (P = 0.005, χ2-test) and corresponding recording depths (reference: bregma).
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Figure 4: Planning activity in amygdala neurons: population data. (a,b) Planning activity (z-normalized) of 72 neurons encoding sequence value across all trials or specifically on first trials. (b) Population activity (magenta, n = 93 responses) reflected sequence value (r2 = 0.91, P < 0.0001, linear regression, n = 7) rather than sequence length (r2 = 0.38, P > 0.1). (c,b) Planning activity of 71 neurons encoding sequence length across all trials or specifically on first trials. (d) Population activity (magenta, n = 92 responses) reflected sequence length (r2 = 0.85, P = 0.0035, n = 7) rather than sequence value (r2= 0.14, P > 0.4). (e, f) Activity of neurons tested in the imperative task failed to reflect sequence value or sequence length when saving was instructed (data from 30 neurons encoding sequence value and 29 neurons encoding sequence length). (g) Regression betas for observed data (orange, n = 829 responses from 329 neurons, collapsed across sequence value and sequence length) and trial-shuffled data (black, scaled down 1,000 times). The distribution of observed data was shifted towards higher positive and negative values (Kolmogorov-Smirnov test). (h) Histological reconstruction of 72 sequence value neurons and 71 sequence length neurons. Green, white, pink, yellow and blue symbols: example neurons in Fig. 2 and Fig. 3a–d, respectively. Collapsing across anterior-posterior dimension resulted in symbol overlap. (i) Proportion of neurons with planning activity (n = 123 neurons, collapsed across sequence value and sequence length) in basolateral and centromedial amygdala (P = 0.005, χ2-test) and corresponding recording depths (reference: bregma).
Mentions: Among 329 task-related neurons, 123 (37%, 66/57 from animal A/B) showed planning activity related to sequence value or sequence length, either throughout saving sequences or specifically on initial trials (Fig. 4a–d, Table 1, Supplementary Tables 1–3, Supplementary Fig. 4). The average activity of sequence value neurons followed closely the average subjective value profile, which was a non-monotonic function of sequence length (r2 = 0.91, P<0.0001, linear regression; compare magenta curve and black bars in Fig. 4b). Analysis of trial-by-trial activity in these neurons confirmed this effect (P = 2.2 × 10−15, partial correlation factored out sequence length). By contrast, activity of sequence length neurons increased linearly with sequence length (r2 = 0.85, P = 0.0035, linear regression, Fig. 4d). Analysis of trial-by-trial activity in these neurons confirmed this effect (P = 7.4 × 10−5, partial correlation factored out sequence value). Supplementary analysis confirmed a graded, parametric representation of sequence value or sequence length, rather than sharp tuning to specific sequences (Supplementary Fig. 5). A subset of neurons with planning activity was tested in the imperative task. In most of them (53/57, 93%), planning activity was not found when saving was externally instructed (Fig. 4e,f). Thus, planning activity appeared to be largely specific for internally controlled saving behavior.

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