Dissociable Roles for the Basolateral Amygdala and Orbitofrontal Cortex in Decision-Making under Risk of Punishment

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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The medial orbitofrontal cortex - basolateral amygdala circuit regulates the influence of reward cues on adaptive behavior and choice

10.1101/2021.04.27.441665 ◽

2021 ◽

Author(s):

Nina T. Lichtenberg ◽

Linnea Sepe-Forrest ◽

Zachary T. Pennington ◽

Alexander C. Lamparelli ◽

Venuz Y. Greenfield ◽

...

Keyword(s):

Decision Making ◽

Adaptive Behavior ◽

Orbitofrontal Cortex ◽

Basolateral Amygdala ◽

Outcome Expectations ◽

Mental Illnesses ◽

Male Rats ◽

Course Of Action ◽

Current Availability ◽

Environmental Events

ABSTRACTAdaptive reward-related decision making requires accurate prospective consideration of the current availability and desirability of potential rewarding options. Often this information must be inferred based on the presence of predictive environmental events. The basolateral amygdala (BLA) and medial orbitofrontal cortex (mOFC) are two key nodes in the circuitry supporting such outcome guided behavior, but very little is known about the function of direct connections between these regions. Here, in male rats, we first anatomically confirmed the existence of bidirectional, direct projections between the mOFC and BLA and found that BLA projections to mOFC are distinct from those to lateral OFC (lOFC). Next, using pathway-specific chemogenetic inhibition and the outcome-selective Pavlovian-to-instrumental transfer and devaluation tests, we interrogated the function of the bidirectional mOFC→BLA connections in reward-directed behavior. We found evidence that the mOFC→BLA pathway mediates the use of environmental cues to predict which reward is available, information needed to infer which action to choose, and how desirable that reward is to ensure adaptive cue responses. By contrast, the BLA→mOFC pathway is not needed to use cues to know which reward is available but is needed to use the current desirability of that reward to infer how advantageous it would be to respond to the cue. These functions differ from those we previously identified for the lOFC-BLA circuit. Collectively, these data reveal the mOFC-BLA circuit as critical for the cue-dependent reward outcome expectations that influence adaptive behavior and decision making.SIGNIFICANCE STATEMENTTo make good decisions we evaluate how advantageous a particular course of action would be. This requires understanding what rewarding events might be available and how desirable those events are currently. Such prospective considerations are critical for adaptive decision making but are disrupted in many psychiatric diseases. Here we reveal that direct connections between the medial orbitofrontal cortex and basolateral amygdala mediate these functions. These findings are especially important in light of evidence of dysfunction in this circuit in substance use disorder and mental illnesses marked by poor decision making.

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A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories

10.1101/2021.03.20.436233 ◽

2021 ◽

Author(s):

Ana C Sias ◽

Ashleigh K Morse ◽

Sherry Wang ◽

Venuz Y Greenfield ◽

Caitlin M Goodpaster ◽

...

Keyword(s):

Decision Making ◽

Orbitofrontal Cortex ◽

Basolateral Amygdala ◽

Optical Recording ◽

Male Rats ◽

Work Activity ◽

Specific Stimulus ◽

Reward Conditioning ◽

Environmental Reward ◽

Direct Input

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 an 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 that 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 to perform a serial circuit disconnection, we found that activity in lOFC→BLA projections regulates the encoding of the same components of the stimulus-outcome memory that are later used to allow cues to guide choice via activity in BLA→lOFC projections. Thus, the lOFC→BLA→lOFC circuit regulates the encoding (lOFC→BLA) and subsequent use (BLA→lOFC) of the stimulus-dependent, sensory-specific reward memories that are critical for adaptive, appetitive decision making.

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