Neuronal Signals in the Monkey Basolateral Amygdala during Reward Schedules

Sugase-Miyamoto, Yasuko; Richmond, Barry J.

doi:10.1523/jneurosci.1796-05.2005

Cited by 91 publications

(93 citation statements)

References 51 publications

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“…S3), and many choice-predictive neurons did not track them (SI Results). Third, a previous study showed that reward expectation-related activity in amygdala neurons covaried with the temporal distance to reward receipt (24). By contrast, activity in many choice-predictive neurons in the present study did not covary with distance to reward (SI Results).…”

Section: Discussioncontrasting

confidence: 70%

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Prediction of economic choice by primate amygdala neurons

Grabenhorst

Hernádi

Schultz

2012

Proc. Natl. Acad. Sci. U.S.A.

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The amygdala is a key structure of the brain's reward system. Existing theories view its role in decision-making as restricted to an early valuation stage that provides input to decision mechanisms in downstream brain structures. However, the extent to which the amygdala itself codes information about economic choices is unclear. Here, we report that individual neurons in the primate amygdala predict behavioral choices in an economic decision task. We recorded the activity of amygdala neurons while monkeys chose between saving liquid reward with interest and spending the accumulated reward. In addition to known value-related responses, we found that activity in a group of amygdala neurons predicted the monkeys' upcoming save-spend choices with an average accuracy of 78%. This choicepredictive activity occurred early in trials, even before information about specific actions associated with save-spend choices was available. For a substantial number of neurons, choice-differential activity was specific for free, internally generated economic choices and not observed in a control task involving forced imperative choices. A subgroup of choice-predictive neurons did not show relationships to value, movement direction, or visual stimulus features. Choicepredictive activity in some amygdala neurons was preceded by transient periods of value coding, suggesting value-to-choice transitions and resembling decision processes in other brain systems. These findings suggest that the amygdala might play an active role in economic decisions. Current views of amygdala function should be extended to incorporate a role in decision-making beyond valuation.neurophysiology | abstract representation | subjective value | emotion

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Section: Discussioncontrasting

confidence: 70%

“…S7). We were unable to identify systematic differences between recording sites (nonsignificant χ 2 tests); therefore, in line with previous studies (6,24), we present the neuronal data as one set.…”

Section: Resultsmentioning

confidence: 59%

Prediction of economic choice by primate amygdala neurons

Grabenhorst

Hernádi

Schultz

2012

Proc. Natl. Acad. Sci. U.S.A.

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“…Moreover, posterior orbitofrontal areas target dual systems in the amygdala that can potentially increase or decrease autonomic drive, activated perhaps according to the emotional significance of the situation or environment (Ghashghaei and Barbas, 2002;Barbas et al, 2003;Arana et al, 2003;Sugase-Miyamoto and Richmond, 2005;Wellman et al, 2005;Paton et al, 2006). Decision for action based on the significance of the environment is a complex process that likely involves many structures, including communication between caudal lateral prefrontal cortices, which are thought to have executive functions, and orbitofrontal and medial prefrontal cortices associated with processing the value of stimuli [(Wallis and Miller, 2003;PadoaSchioppa and Assad, 2006); reviewed in (Miller and Cohen, 2001)].…”

Section: Sequence Of Information Processing For Emotionsmentioning

confidence: 99%

Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala

2007

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The prefrontal cortex and the amygdala have synergistic roles in regulating purposive behavior, effected through bidirectional pathways. Here we investigated the largely unknown extent and laminar relationship of prefrontal input-output zones linked with the amygdala using neural tracers injected in the amygdala in rhesus monkeys. Prefrontal areas varied vastly in their connections with the amygdala, with the densest connections found in posterior orbitofrontal and posterior medial cortices, and the sparsest in anterior lateral prefrontal areas, especially area 10. Prefrontal projection neurons directed to the amygdala originated in layer 5, but significant numbers were also found in layers 2 and 3 in posterior medial and orbitofrontal cortices. Amygdalar axonal terminations in prefrontal cortex were most frequently distributed in bilaminar bands in the superficial and deep layers, by columns spanning the entire cortical depth, and less frequently as small patches centered in the superficial or deep layers. Heavy terminations in layers 1−2 overlapped with calbindin positive inhibitory neurons. A comparison of the relationship of input to output projections revealed that among the most heavily connected cortices, cingulate areas 25 and 24 issued comparatively more projections to the amygdala than they received, whereas caudal orbitofrontal areas were more receivers than senders. Further, there was a significant relationship between the proportion of 'feedforward' cortical projections from layers 2−3 to 'feedback' terminations innervating the superficial layers of prefrontal cortices. These findings indicate that the connections between prefrontal cortices and the amygdala follow similar patterns as corticocortical connections, and by analogy suggest pathways underlying the sequence of information processing for emotions.The amygdala and the prefrontal cortex have synergistic roles in regulating purposive behavior [(Schoenbaum et al., 2000;Izquierdo and Murray, 2005); reviewed in (Barbas, 2000;Bechara et al., 2000)]. The amygdala appears to extract the affective significance of stimuli, and the prefrontal cortex guides goal-directed behavior (Damasio, 1994;Petrides, 1996;Roberts and Wallis, 2000;Levy and Goldman-Rakic, 2000;Fuster, 2000;Barbas et al., 2002). Communication between the amygdala and the prefrontal cortex is bidirectional [e.g., (Nauta, 1961;Pandya et al., 1973;Jacobson and Trojanowski, 1975;Aggleton et al., 1980;Porrino et al., e Current address: Department of Molecular Biomedical Sciences, School of Veterinary Medicine, North Carolina State University, Raleigh, NC. * Corresponding author. Dept. Health Sciences, Boston University, 635 Commonwealth Ave. Room 431, Boston, MA 02215. E-mail address: barbas@bu.edu Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is p...

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“…That is, monkeys get the reward whether or not lipping occurs. In earlier studies conducted in this laboratory, licking responses were monitored in monkeys performing the same reward schedule task with the spout being positioned outside of the monkey's mouth (Sugase-Miyamoto and Richmond 2005). In those conditions, cueevoked licking was stronger in rewarded trials of the schedules.…”

Section: Operant and Instinctive Behaviors In The Reward Schedulesmentioning

confidence: 99%

Relation of Locus Coeruleus Neurons in Monkeys to Pavlovian and Operant Behaviors

Bouret

Richmond²

2009

Journal of Neurophysiology

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Bouret S, Richmond BJ. Relation of locus coeruleus neurons in monkeys to Pavlovian and operant behaviors. J Neurophysiol 101: 898 -911, 2009. First published December 17, 2008 doi:10.1152/jn.91048.2008. Noradrenaline is released throughout the forebrain from locus coeruleus (LC) projections in close temporal proximity to emotional and goal-directed events. To examine interactive influences of these processes on LC neuronal activity, we used a task where Pavlovian and operant processes vary and can be easily identified. We recorded 69 single LC neurons from two monkeys performing a task where cues indicate the progression through schedules of one, two, or three operant trials. Pavlovian responses and phasic LC activations occur following the appearance of conditioned visual cues (54/69 neurons), especially those at the beginning of new schedules, whether the current trial will be rewarded (single trial schedule) or not (2 or 3 trial schedules), and after visual imperative signals eliciting the operant response (64/69 neurons), whether the current trial will be rewarded or not. The modulation of LC responses seems to be relatively independent of attention or motivation, because the responses do not covary with operant performance in the task. The magnitude of LC responses across the schedules varied in close relation to the intensity of Pavlovian behavior but these responses were also modulated by operant processes. Our conclusion is that LC activation occurs when task-relevant stimuli evoke a conditioned instinctive (Pavlovian) response, with the strength of the activation also being modulated by goal-directed processes. Thus locus coeruleus neurons broadcast information about stimulus-elicited primitive and goal-directed behaviors to forebrain structures important for executive functions and emotions.

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Neuronal Signals in the Monkey Basolateral Amygdala during Reward Schedules

Cited by 91 publications

References 51 publications

Prediction of economic choice by primate amygdala neurons

Prediction of economic choice by primate amygdala neurons

Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala

Relation of Locus Coeruleus Neurons in Monkeys to Pavlovian and Operant Behaviors

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