Encoding Predicted Outcome and Acquired Value in Orbitofrontal Cortex during Cue Sampling Depends upon Input from Basolateral Amygdala

Adaptive reward-related decision making often requires accurate and detailed representation of potential available rewards. Environmental reward-predictive stimuli can facilitate these representations, allowing one to infer which specific rewards might be available and choose accordingly. This process relies on encoded relationships between the cues and the sensory-specific details of the reward they predict. Here we interrogated the function of the basolateral amygdala (BLA) and its interaction with the lateral orbitofrontal cortex (lOFC) in the ability to learn such stimulus-outcome associations and use these memories to guide decision making. Using optical recording and inhibition approaches, Pavlovian cue-reward conditioning, and the outcome-selective Pavlovian-to-instrumental transfer (PIT) test in male rats, we found that the BLA is robustly activated at the time of stimulus-outcome learning and that this activity is necessary for sensory-specific stimulus-outcome memories to be encoded, so they can subsequently influence reward choices. Direct input from the lOFC was found to support the BLA in this function. Based on prior work, activity in BLA projections back to the lOFC was known to support the use of stimulus-outcome memories to influence decision making. By multiplexing optogenetic and chemogenetic inhibition we performed a serial circuit disconnection and found that the lOFCàBLA and BLAàlOFC pathways form a functional circuit regulating the encoding (lOFCàBLA) and subsequent use (BLAàlOFC) of the stimulus-dependent, sensory-specific reward memories that are critical for adaptive, appetitive decision making.

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All That Glitters … Dissociating Attention and Outcome Expectancy From Prediction Errors Signals

Journal of Neurophysiology ◽

10.1152/jn.00173.2010 ◽

2010 ◽

Vol 104 (2) ◽

pp. 587-595 ◽

Cited By ~ 39

Author(s):

Matthew R. Roesch ◽

Donna J. Calu ◽

Guillem R. Esber ◽

Geoffrey Schoenbaum

Keyword(s):

Orbitofrontal Cortex ◽

Basolateral Amygdala ◽

Ventral Striatum ◽

Recent Literature ◽

Neural Correlates ◽

Dopamine Neurons ◽

Outcome Expectancy ◽

Prediction Errors ◽

Signal Prediction ◽

Unexpected Outcomes

Initially reported in dopamine neurons, neural correlates of prediction errors have now been shown in a variety of areas, including orbitofrontal cortex, ventral striatum, and amygdala. Yet changes in neural activity to an outcome or cues that precede it can reflect other processes. We review the recent literature and show that although activity in dopamine neurons appears to signal prediction errors, similar activity in orbitofrontal cortex, basolateral amygdala, and ventral striatum does not. Instead, increased firing in basolateral amygdala to unexpected outcomes likely reflects attention, whereas activity in orbitofrontal cortex and ventral striatum is unaffected by prior expectations and may provide information on outcome expectancy. These results have important implications for how these areas interact to facilitate learning and guide behavior.

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Different Roles for Orbitofrontal Cortex and Basolateral Amygdala in a Reinforcer Devaluation Task

Journal of Neuroscience ◽

10.1523/jneurosci.23-35-11078.2003 ◽

2003 ◽

Vol 23 (35) ◽

pp. 11078-11084 ◽

Cited By ~ 220

Author(s):

Charles L. Pickens ◽

Michael P. Saddoris ◽

Barry Setlow ◽

Michela Gallagher ◽

Peter C. Holland ◽

...

Keyword(s):

Orbitofrontal Cortex ◽

Basolateral Amygdala ◽

Reinforcer Devaluation

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Complementary contributions of basolateral amygdala and orbitofrontal cortex to value learning under uncertainty

eLife ◽

10.7554/elife.27483 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 14

Author(s):

Alexandra Stolyarova ◽

Alicia Izquierdo

Keyword(s):

Orbitofrontal Cortex ◽

Basolateral Amygdala ◽

Previous Experience ◽

Wait Times ◽

Meaningful Change ◽

New Learning ◽

Expected Outcome ◽

Value Learning ◽

Expected Outcomes

We make choices based on the values of expected outcomes, informed by previous experience in similar settings. When the outcomes of our decisions consistently violate expectations, new learning is needed to maximize rewards. Yet not every surprising event indicates a meaningful change in the environment. Even when conditions are stable overall, outcomes of a single experience can still be unpredictable due to small fluctuations (i.e., expected uncertainty) in reward or costs. In the present work, we investigate causal contributions of the basolateral amygdala (BLA) and orbitofrontal cortex (OFC) in rats to learning under expected outcome uncertainty in a novel delay-based task that incorporates both predictable fluctuations and directional shifts in outcome values. We demonstrate that OFC is required to accurately represent the distribution of wait times to stabilize choice preferences despite trial-by-trial fluctuations in outcomes, whereas BLA is necessary for the facilitation of learning in response to surprising events.

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