scholarly journals The basolateral nucleus of the amygdala regulates both the predictive and incentive motivational properties of reward cues

2019 ◽  
Author(s):  
Alice Servonnet ◽  
Giovanni Hernandez ◽  
Cynthia El Hage ◽  
Pierre-Paul Rompré ◽  
Anne-Noël Samaha

ABSTRACTReward-associated stimuli can acquire both predictive and incentive motivational properties. These conditioned stimuli (CS) can then guide reward-seeking behaviour in adaptive (e.g., locating food) and maladaptive (e.g., binge eating) ways. The basolateral amygdala (BLA) contributes to learning of the predictive value of CS, but less is known about BLA contributions to the incentive motivational properties of appetitive CS. Here we studied the influence of BLA neuron activity on both the predictive and incentive motivational effects of CS. Water-restricted male rats learned to associate a light-tone cue (CS) with water delivery into a port. We assessed the predictive value to the CS by measuring CS-evoked port entries during Pavlovian conditioning. We assessed CS-evoked incentive motivation by measuring lever-pressing for the CS during instrumental responding sessions. During Pavlovian conditioning, we paired CS presentations with photo-stimulation of channelrhodopsin-2 (ChR2)-expressing BLA neurons. This potentiated CS-evoked port entries during conditioning, but suppressed subsequent lever-pressing for the CS. This indicates increased conditioned responding to the CS, but an apparent decrease in incentive motivation for that CS. However, in rats previously naïve to photo-stimulation, pairing BLA-ChR2 stimulations during lever-pressing for the CS intensified responding, indicating enhanced motivation for the CS. Rats did not self-administer BLA-ChR2 stimulations, suggesting that BLA activation does not carry a primary reward signal. Lastly, intra-BLA infusions of d-amphetamine also intensified lever-pressing for the CS. These converging findings suggest that BLA mediated-activity enhances both the predictive and incentive motivational properties of CS, allowing BLA-dependent circuits to guide behaviour in the presence of reward-associated cues.SIGNIFICANCE STATEMENTCues paired with rewards can guide animals to valuable resources such as food. Cues can also promote dysfunctional reward-seeking behaviour, as in over-eating. Reward-paired cues influence reward seeking through two major mechanisms. First, reward-paired cues are predictive and thus evoke anticipation of future rewards. Second, reward-paired cues are powerful motivators and they can evoke pursuit in their own right. Here we show that increasing neural activity in the basolateral amygdala enhances both the predictive and motivational effects of reward-paired cues. The basolateral amygdala therefore facilitates cue-induced control over behaviour by both increasing anticipation for impending rewards and making reward cues more attractive.

2021 ◽  
Author(s):  
Caroline Garceau ◽  
Anne-Noël Samaha ◽  
Thomas Cordahi ◽  
Alice Servonnet ◽  
Shaun Yon-Seng Khoo

Rationale: Reward-associated cues can trigger incentive motivation for reward and invigorate reward-seeking behaviour via Pavlovian-to-instrumental transfer (PIT). Glutamate signaling within the basolateral amygdala (BLA) modulates cue-triggered increases in incentive motivation. However, the role of BLA metabotropic group II glutamate (mGlu2/3) receptors is largely unknown. Objectives: In Experiment 1, we characterized cue-triggered increases in incentive motivation for water reward using the PIT paradigm. In Experiment 2, we assessed the influence of intra-BLA microinjections of the mGlu2/3 receptor agonist LY379268 on this effect. Methods: Water-restricted male Sprague-Dawley rats learned to press a lever for water. Separately, they learned to associate one of two auditory cues with free water. On test days, rats could lever press under extinction conditions (no water), with intermittent, non-contingent CS+ and CS- presentations. In Experiment 1, rats were tested under baseline conditions. In Experiment 2, rats received intra-BLA microinjections of LY379268 (0, 3 and 6 μg/hemisphere) before testing. Results: Across experiments, CS+, but not CS- presentations increased water-associated lever pressing during testing, even though responding was reinforced neither by water nor the CS+. Intra-BLA LY379268 abolished both CS+ potentiated pressing on the water-associated lever and CS+ evoked conditioned approach to the site of water delivery. LY379268 did not influence locomotion or instrumental and Pavlovian response rates during intervals between CS presentations or during the CS-, indicating no motor effects. Conclusions: mGlu2/3 receptor activity in the BLA mediates CS-triggered potentiation of incentive motivation for reward, suppressing both CS-induced increases in instrumental pursuit of the reward and anticipatory approach behaviour.


2018 ◽  
Author(s):  
Kurt M. Fraser ◽  
Patricia H. Janak

AbstractThe context in which reward-paired cues are encountered sets the occasion for appropriate reward-seeking but may also spur inappropriate behaviors such as the renewal of drug-seeking. The psychological processes underlying occasion setting remain unclear as contexts are diffuse and difficult to isolate from other stimuli. To overcome this, we modeled a context as a phasic and discrete event – an occasion setter – which allowed for control over its presentation and influence on cue-driven reward-seeking. This allowed us to directly assess how occasion setters, like contexts, regulate the predictive and motivational significance of Pavlovian cues. Male rats (n=50) were trained in a Pavlovian paradigm where the presentation of an ambiguous conditioned stimulus was reinforced only if preceded by an occasion setting cue. We assessed the motivational value of the occasion setter and conditioned stimulus alone or in combination using conditioned reinforcement. Rats showed enhanced conditioned approach to the reward port during the reward-adjacent conditioned stimulus when it was preceded by the occasion setter. When allowed the opportunity, rats responded more to obtain presentations of the conditioned stimulus in combination with the occasion setter than the conditioned stimulus alone. Critically, rats also worked to obtain presentations of the occasion setter alone more than the conditioned stimulus, and this was resistant to manipulations of the value of the occasion setter. We conclude that occasion setting can act via incentive motivational mechanisms and that, apart from resolving predictive information about ambiguous reward-paired cues, occasion setters themselves generate states of appetitive motivation that can facilitate reward-seeking.


2020 ◽  
Author(s):  
Andrew T. Marshall ◽  
Nigel T. Maidment ◽  
Sean B. Ostlund

AbstractImpulsive behavior during adolescence may stem from a developmental imbalance between motivational and impulse control systems, producing greater urges to pursue reward and weakened capacities to inhibit such actions. Here, we developed a Pavlovian-instrumental transfer (PIT) protocol to assay rats’ ability to suppress cue-motivated reward seeking based on changes in reward expectancy. Traditionally, PIT studies focus on how reward-predictive cues motivate instrumental reward-seeking behavior (lever pressing). However, cues signaling imminent reward delivery also elicit countervailing focal-search responses (food-cup approach). We first examined how reward expectancy (cue-reward probability) influences expression of these competing behaviors. Adult male rats increased rates of lever pressing when presented with cues signaling lower probabilities of reward but focused their activity at the food cup on trials with cues that signaled higher probabilities of reward. We then compared adolescent and adult male rats in their responsivity to cues signaling different reward probabilities. In contrast to adults, adolescent rats did not flexibly adjust their pattern of responding based on the expected likelihood of reward delivery but increased their rate of lever pressing for both weak and strong cues. These findings indicate that impulse control over cue-motivated behavior is fundamentally dysregulated during adolescence, providing a model for studying neurobiological mechanisms of adolescent impulsivity.


2021 ◽  
Author(s):  
Caroline Garceau ◽  
Justine Marsault ◽  
Mike J F Robinson ◽  
Anne-Noël Samaha

AbstractRationaleReward-associated cues can acquire incentive motivational properties and invigorate reward-seeking actions via Pavlovian-to-instrumental transfer (PIT). Glutamatergic neurotransmission mediates the appetitive effects of reward-associated cues. We characterized the expression of PIT and its mediation by metabotropic group II glutamate (mGlu2/3) receptor activity in female and male rats.ObjectivesAcross the sexes, we used PIT procedures to determine i) cue-triggered increases in incentive motivation for water reward (Experiment 1), ii) the respective influences of the mGlu2/3 receptor agonist LY379268 and reward devaluation by satiation on this effect (Experiment 2).MethodsWater-restricted male and female Sprague-Dawley rats learned to lever press for water. Separately, they learned that one of two auditory stimuli predicts free water (CS+ vs CS-). On PIT test days, the CS+ and CS- were presented non-contingently, and we measured effects on lever pressing under extinction (no water). In Experiment 1, we characterized PIT across the sexes. In Experiment 2, we measured PIT after systemic LY379268 administration (0, 0.3 and 1 mg/kg), and water satiation, respectively.ResultsFemale and male rats showed similar PIT, with CS+ but not CS- presentations potentiating water-seeking behaviour. LY379268 (1 mg/kg) attenuated CS+ evoked increases in both water-associated lever pressing and conditioned approach to the water port. Reward devaluation attenuated both water-seeking and CS+ evoked conditioned approach behaviour.ConclusionsThe sexes show similar cue-triggered increases in reward ‘wanting’, and water devaluation suppresses both water seeking and cue-triggered anticipation of water reward. Finally, across the sexes, mGlu2/3 receptor activity mediates cue-triggered increases in reward ‘wanting’.


2006 ◽  
Vol 83 (3) ◽  
pp. 360-369 ◽  
Author(s):  
Timo Viitamaa ◽  
Antti Haapalinna ◽  
Anders Ågmo

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.


2021 ◽  
Vol 13 ◽  
Author(s):  
Danna Ellner ◽  
Bryana Hallam ◽  
Jude A. Frie ◽  
Hayley H. A. Thorpe ◽  
Muhammad Shoaib ◽  
...  

The endocannabinoid system is responsible for regulating a spectrum of physiological activities and plays a critical role in the developing brain. During adolescence, the endocannabinoid system is particularly sensitive to external insults that may change the brain’s developmental trajectory. Cannabinoid receptor type 2 (CB2R) was initially thought to predominantly function in the peripheral nervous system, but more recent studies have implicated its role in the mesolimbic pathway, a network largely attributed to reward circuitry and reward motivated behavior, which undergoes extensive changes during adolescence. It is therefore important to understand how CB2R modulation during adolescence can impact reward-related behaviors in adulthood. In this study, adolescent male rats (postnatal days 28–41) were exposed to a low or high dose of the CB2R antagonist/inverse agonist SR144528 and Pavlovian autoshaping and instrumental conditional behavioral outcomes were measured in adulthood. SR144528-treated rats had significantly slower acquisition of the autoshaping task, seen by less lever pressing behavior over time [F(2, 19) = 5.964, p = 0.010]. Conversely, there was no effect of adolescent SR144528 exposure on instrumental conditioning. These results suggest that modulation of the CB2R in adolescence differentially impacts reward-learning behaviors in adulthood.


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