Limits...
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.

Show MeSH

Related in: MedlinePlus

A single amygdala neuron with prospective activity that reflected the value of the monkey’s internal saving plan. (a) Activity during step-by-step saving depended on the final saving sequence that the animal eventually produced. Specifically, activity depended on the subjective value of the current sequence (‘sequence value’), which would only be achieved several trials ahead. Upper panels: activity (spike density functions) during three saving sequences of different lengths. Activity during fixation (yellow area) was highest for the sequence in which the monkey would eventually spend on the fifth trial, as this sequence had the highest subjective value (Imp/s: impulses per second; raster display: ticks indicate impulses, rows indicate trials). Lower panel: activity averages for all sequence lengths (e.g. light-pink activation indicates mean fixation activity for all five-trial sequences, averaged over trials one to five). Activity reflected sequence value (magenta curve, normalized), rather than linear sequence length or objective reward amount (green curve, normalized). Behaviorally derived sequence values reflected the animal’s preferences for different combinations of sequence length and final reward—five-trial sequences had the highest value as the monkey chose them most frequently. Saving sequences were freely determined by the animal; visual stimulation was constant across sequences. (b) Within-trial activity sorted according to sequence value (terciles). (c) Linear regression of activity on sequence value. Different value levels resulted from different sequence lengths as shown in (a). (d) Multiple regression coefficients (betas ± s.e.m., Eq. 6). (e) Activity in the imperative task, when saving was instructed, did not reflect sequence value.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC4340753&req=5

Figure 2: A single amygdala neuron with prospective activity that reflected the value of the monkey’s internal saving plan. (a) Activity during step-by-step saving depended on the final saving sequence that the animal eventually produced. Specifically, activity depended on the subjective value of the current sequence (‘sequence value’), which would only be achieved several trials ahead. Upper panels: activity (spike density functions) during three saving sequences of different lengths. Activity during fixation (yellow area) was highest for the sequence in which the monkey would eventually spend on the fifth trial, as this sequence had the highest subjective value (Imp/s: impulses per second; raster display: ticks indicate impulses, rows indicate trials). Lower panel: activity averages for all sequence lengths (e.g. light-pink activation indicates mean fixation activity for all five-trial sequences, averaged over trials one to five). Activity reflected sequence value (magenta curve, normalized), rather than linear sequence length or objective reward amount (green curve, normalized). Behaviorally derived sequence values reflected the animal’s preferences for different combinations of sequence length and final reward—five-trial sequences had the highest value as the monkey chose them most frequently. Saving sequences were freely determined by the animal; visual stimulation was constant across sequences. (b) Within-trial activity sorted according to sequence value (terciles). (c) Linear regression of activity on sequence value. Different value levels resulted from different sequence lengths as shown in (a). (d) Multiple regression coefficients (betas ± s.e.m., Eq. 6). (e) Activity in the imperative task, when saving was instructed, did not reflect sequence value.

Mentions: The neuron in Fig. 2 had phasic trial-by-trial activity during the fixation period that was highest during sequences in which the animal would eventually spend on the fifth trial, and lower for shorter or longer sequences (Fig. 2a). This activity profile resembled closely the distribution of sequence values derived from the animal’s choice preferences (Fig. 2a magenta curve): for this interest rate, five-trial sequences had the highest value as the animal chose them most frequently. Within trials, the prospective activity appeared during ocular fixation and continued beyond the cue period when a save-spend choice was made (Fig. 2b). Linear regression indicated a better relationship to sequence value (r2 = 0.54, P = 1.4 × 10−8, n = 40, Fig. 2c) than to sequence length (r2 = 0.21, P = 0.003) or final juice amount (r2 = 0.07, P = 0.09). Multiple regression confirmed a relationship between neuronal activity and sequence value (P = 3.8 × 10−6, Eq. 6) and factored out other variables, including subjective values related to single trial choices (P > 0.05, Fig. 2d, Supplementary Fig. 3). The relationship between activity and sequence value disappeared in externally cued trials when saving was instructed (Fig. 2e, P > 0.05, multiple regression), despite comparable behavioral outcome anticipation (regression of sequence length on reaction times: P < 0.05; Supplementary Fig. 2d). Thus, during internally controlled step-by-step saving, the neuron showed prospective activity related to the subjective value of the animal’s saving plan.


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

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

A single amygdala neuron with prospective activity that reflected the value of the monkey’s internal saving plan. (a) Activity during step-by-step saving depended on the final saving sequence that the animal eventually produced. Specifically, activity depended on the subjective value of the current sequence (‘sequence value’), which would only be achieved several trials ahead. Upper panels: activity (spike density functions) during three saving sequences of different lengths. Activity during fixation (yellow area) was highest for the sequence in which the monkey would eventually spend on the fifth trial, as this sequence had the highest subjective value (Imp/s: impulses per second; raster display: ticks indicate impulses, rows indicate trials). Lower panel: activity averages for all sequence lengths (e.g. light-pink activation indicates mean fixation activity for all five-trial sequences, averaged over trials one to five). Activity reflected sequence value (magenta curve, normalized), rather than linear sequence length or objective reward amount (green curve, normalized). Behaviorally derived sequence values reflected the animal’s preferences for different combinations of sequence length and final reward—five-trial sequences had the highest value as the monkey chose them most frequently. Saving sequences were freely determined by the animal; visual stimulation was constant across sequences. (b) Within-trial activity sorted according to sequence value (terciles). (c) Linear regression of activity on sequence value. Different value levels resulted from different sequence lengths as shown in (a). (d) Multiple regression coefficients (betas ± s.e.m., Eq. 6). (e) Activity in the imperative task, when saving was instructed, did not reflect sequence value.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4340753&req=5

Figure 2: A single amygdala neuron with prospective activity that reflected the value of the monkey’s internal saving plan. (a) Activity during step-by-step saving depended on the final saving sequence that the animal eventually produced. Specifically, activity depended on the subjective value of the current sequence (‘sequence value’), which would only be achieved several trials ahead. Upper panels: activity (spike density functions) during three saving sequences of different lengths. Activity during fixation (yellow area) was highest for the sequence in which the monkey would eventually spend on the fifth trial, as this sequence had the highest subjective value (Imp/s: impulses per second; raster display: ticks indicate impulses, rows indicate trials). Lower panel: activity averages for all sequence lengths (e.g. light-pink activation indicates mean fixation activity for all five-trial sequences, averaged over trials one to five). Activity reflected sequence value (magenta curve, normalized), rather than linear sequence length or objective reward amount (green curve, normalized). Behaviorally derived sequence values reflected the animal’s preferences for different combinations of sequence length and final reward—five-trial sequences had the highest value as the monkey chose them most frequently. Saving sequences were freely determined by the animal; visual stimulation was constant across sequences. (b) Within-trial activity sorted according to sequence value (terciles). (c) Linear regression of activity on sequence value. Different value levels resulted from different sequence lengths as shown in (a). (d) Multiple regression coefficients (betas ± s.e.m., Eq. 6). (e) Activity in the imperative task, when saving was instructed, did not reflect sequence value.
Mentions: The neuron in Fig. 2 had phasic trial-by-trial activity during the fixation period that was highest during sequences in which the animal would eventually spend on the fifth trial, and lower for shorter or longer sequences (Fig. 2a). This activity profile resembled closely the distribution of sequence values derived from the animal’s choice preferences (Fig. 2a magenta curve): for this interest rate, five-trial sequences had the highest value as the animal chose them most frequently. Within trials, the prospective activity appeared during ocular fixation and continued beyond the cue period when a save-spend choice was made (Fig. 2b). Linear regression indicated a better relationship to sequence value (r2 = 0.54, P = 1.4 × 10−8, n = 40, Fig. 2c) than to sequence length (r2 = 0.21, P = 0.003) or final juice amount (r2 = 0.07, P = 0.09). Multiple regression confirmed a relationship between neuronal activity and sequence value (P = 3.8 × 10−6, Eq. 6) and factored out other variables, including subjective values related to single trial choices (P > 0.05, Fig. 2d, Supplementary Fig. 3). The relationship between activity and sequence value disappeared in externally cued trials when saving was instructed (Fig. 2e, P > 0.05, multiple regression), despite comparable behavioral outcome anticipation (regression of sequence length on reaction times: P < 0.05; Supplementary Fig. 2d). Thus, during internally controlled step-by-step saving, the neuron showed prospective activity related to the subjective value of the animal’s saving plan.

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