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

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Ana C Sias ◽  
Ashleigh K Morse ◽  
Sherry Wang ◽  
Venuz Y Greenfield ◽  
Caitlin M Goodpaster ◽  
...  

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.

2021 ◽  
Author(s):  
Ana C Sias ◽  
Ashleigh K Morse ◽  
Sherry Wang ◽  
Venuz Y Greenfield ◽  
Caitlin M Goodpaster ◽  
...  

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.


2021 ◽  
Author(s):  
Nina T. Lichtenberg ◽  
Linnea Sepe-Forrest ◽  
Zachary T. Pennington ◽  
Alexander C. Lamparelli ◽  
Venuz Y. Greenfield ◽  
...  

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.


2013 ◽  
Vol 24 ◽  
pp. e28
Author(s):  
Lena Wischhof ◽  
Kerstin Wernecke ◽  
Ellen Irrsack ◽  
Malte Feja ◽  
Michael Koch

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
L. Van Schaik ◽  
C. Kettle ◽  
R. Green ◽  
W. Sievers ◽  
M. W. Hale ◽  
...  

AbstractThe role of central orexin in the sympathetic control of interscapular brown adipose tissue (iBAT) thermogenesis has been established in rodents. Stimulatory doses of caffeine activate orexin positive neurons in the lateral hypothalamus, a region of the brain implicated in stimulating BAT thermogenesis. This study tests the hypothesis that central administration of caffeine is sufficient to activate BAT. Low doses of caffeine administered either systemically (intravenous [IV]; 10 mg/kg) and centrally (intracerebroventricular [ICV]; 5–10 μg) increases BAT thermogenesis, in anaesthetised (1.5 g/kg urethane, IV) free breathing male rats. Cardiovascular function was monitored via an indwelling intra-arterial cannula and exhibited no response to the caffeine. Core temperature did not significantly differ after administration of caffeine via either route of administration. Caffeine administered both IV and ICV increased neuronal activity, as measured by c-Fos-immunoreactivity within subregions of the hypothalamic area, previously implicated in regulating BAT thermogenesis. Significantly, there appears to be no neural anxiety response to the low dose of caffeine as indicated by no change in activity in the basolateral amygdala. Having measured the physiological correlate of thermogenesis (heat production) we have not measured indirect molecular correlates of BAT activation. Nevertheless, our results demonstrate that caffeine, at stimulatory doses, acting via the central nervous system can increase thermogenesis, without adverse cardio-dynamic impact.


Author(s):  
Susanne Koot ◽  
Magdalini Koukou ◽  
Annemarie Baars ◽  
Peter Hesseling ◽  
José van ’t Klooster ◽  
...  

2019 ◽  
Author(s):  
Bhargav Teja Nallapu ◽  
Frédéric Alexandre

AbstractIn the context of flexible and adaptive animal behavior, the orbitofrontal cortex (OFC) is found to be one of the crucial regions in the prefrontal cortex (PFC) influencing the downstream processes of decision-making and learning in the sub-cortical regions. Although OFC has been implicated to be important in a variety of related behavioral processes, the exact mechanisms are unclear, through which the OFC encodes or processes information related to decision-making and learning. Here, we propose a systems-level view of the OFC, positioning it at the nexus of sub-cortical systems and other prefrontal regions. Particularly we focus on one of the most recent implications of neuroscientific evidences regarding the OFC - possible functional dissociation between two of its sub-regions : lateral and medial. We present a system-level computational model of decision-making and learning involving the two sub-regions taking into account their individual roles as commonly implicated in neuroscientific studies. We emphasize on the role of the interactions between the sub-regions within the OFC as well as the role of other sub-cortical structures which form a network with them. We leverage well-known computational architecture of thalamo-cortical basal ganglia loops, accounting for recent experimental findings on monkeys with lateral and medial OFC lesions, performing a 3-arm bandit task. First we replicate the seemingly dissociate effects of lesions to lateral and medial OFC during decision-making as a function of value-difference of the presented options. Further we demonstrate and argue that such an effect is not necessarily due to the dissociate roles of both the subregions, but rather a result of complex temporal dynamics between the interacting networks in which they are involved.Author summaryWe first highlight the role of the Orbitofrontal Cortex (OFC) in value-based decision making and goal-directed behavior in primates. We establish the position of OFC at the intersection of cortical mechanisms and thalamo-basal ganglial circuits. In order to understand possible mechanisms through which the OFC exerts emotional control over behavior, among several other possibilities, we consider the case of dissociate roles of two of its topographical subregions - lateral and medial parts of OFC. We gather predominant roles of each of these sub-regions as suggested by numerous experimental evidences in the form of a system-level computational model that is based on existing neuronal architectures. We argue that besides possible dissociation, there could be possible interaction of these sub-regions within themselves and through other sub-cortical structures, in distinct mechanisms of choice and learning. The computational framework described accounts for experimental data and can be extended to more comprehensive detail of representations required to understand the processes of decision-making, learning and the role of OFC and subsequently the regions of prefrontal cortex in general.


2020 ◽  
Author(s):  
Dannia Islas-Preciado ◽  
Steven R. Wainwright ◽  
Julia Sniegocki ◽  
Stephane E. Lieblich ◽  
Shunya Yagi ◽  
...  

AbstractDecision-making is a complex process essential to daily adaptation in many species. Risk is an inherent aspect of decision-making and it is influenced by gonadal hormones. Testosterone and 17β-estradiol may modulate decision making and impact the mesocorticolimbic dopamine pathway. Here, we explored sex differences, the effect of gonadal hormones and the dopamine agonist amphetamine on risk-based decision making. Intact or gonadectomised (GDX) male and female rats underwent to a probabilistic discounting task. High and low doses of testosterone propionate (1.0 or 0.2 mg) and 17β-estradiol benzoate (0.3 μg) were administered to assess acute effects on risk-based decision making. After 3-days of washout period, intact and GDX rats received high or low (0.5 or 0.125 mg/kg) doses of amphetamine and re-tested in the probabilistic discounting task. Under baseline conditions, males made more risky choices during probability discounting compared to female rats, particularly in the lower probability blocks, but GDX did not influence risky choice. The high, but not the low dose, of testosterone modestly reduced risky decision making in GDX male rats. Conversely, 17β-estradiol had no significant effect on risky choice regardless of GDX status in either sex. Lastly, a higher dose of amphetamine increased risky decision making in both intact males and females, but had no effect in GDX rats. These findings demonstrated sex differences in risk-based decision making, with males showing a stronger bias towards larger, uncertain rewards. GDX status influenced the effects of amphetamine, suggesting different dopaminergic regulation in risk-based choices among males and females.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Sean E Cavanagh ◽  
Joni D Wallis ◽  
Steven W Kennerley ◽  
Laurence T Hunt

Correlates of value are routinely observed in the prefrontal cortex (PFC) during reward-guided decision making. In previous work (Hunt et al., 2015), we argued that PFC correlates of chosen value are a consequence of varying rates of a dynamical evidence accumulation process. Yet within PFC, there is substantial variability in chosen value correlates across individual neurons. Here we show that this variability is explained by neurons having different temporal receptive fields of integration, indexed by examining neuronal spike rate autocorrelation structure whilst at rest. We find that neurons with protracted resting temporal receptive fields exhibit stronger chosen value correlates during choice. Within orbitofrontal cortex, these neurons also sustain coding of chosen value from choice through the delivery of reward, providing a potential neural mechanism for maintaining predictions and updating stored values during learning. These findings reveal that within PFC, variability in temporal specialisation across neurons predicts involvement in specific decision-making computations.


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