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

Abstract

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.

Dopamine in the Dorsal Bed Nucleus of Stria Terminalis signals Pavlovian sign-tracking and reward violations

“…However, other studies find evidence for sensory specific signaling in dopamine function and signaling (Sharpe, Chang et al 2017, Takahashi, Batchelor et al 2017). This suggests BNST DA signals may carry sensory specific information that is critical for higher order learning processes (Burke, Franz et al 2007, Burke, Franz et al 2008, Malvaez, Greenfield et al 2015, Lichtenberg, Pennington et al 2017, Sharpe, Chang et al 2017, Takahashi, Batchelor et al 2017, Malvaez, Shieh et al 2019, Keefer, Gyawali et al 2021, Lichtenberg, Sepe-Forrest et al 2021, Sias, Morse et al 2021).…”

Orbitofrontal cortex populations are differentially recruited to support actions

“…The unstructured, self-paced nature of our task allowed us to identify patterns of lOFC activity that reflected prior action information as well as other sources of experience. As OFC populations have been shown to process cue-related and reward-predictive information, 25,26,20,21,16,91,22 our findings suggest that OFC can also represent and encode action-related information to guide adaptive behavior depending on the behavioral context.…”

Basolateral amygdala to insular cortex activity makes sign-tracking behavior insensitive to outcome value

“…Additional studies indicate that communication between the BLA and OFC are necessary for outcome devaluation (Baxter et al, 2000; Fiuzat et al, 2017), and direct projections from the BLA to OFC and from the OFC to BLA are critical for Pavlovian, but not instrumental, outcome devaluation (Lichtenberg et al, 2017; Malvaez et al, 2019). Similarly, communication between the BLA and OFC is necessary for other behavioral flexibility paradigms, such as over-expectation (Lucantonio et al, 2015), outcome-specific Pavlovian-to-Instrumental transfer (Lichtenberg et al, 2017; Sias et al, 2021), and risky decision making (Zeeb & Winstanley, 2013; see Keefer et al, 2021 for review).…”