Lesions of the nucleus accumbens disrupt reinforcement omission effects in rats

Judice-Daher, Danielle Marcilio; Bueno, José Lino Oliveira

doi:10.1016/j.bbr.2013.06.028

Cited by 10 publications

(9 citation statements)

References 41 publications

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“…NAc activity also encodes information about reward (26, 39-41), and is critical for appropriate responses to reward omissions (42, 43). Here, reward omission differentially elicited excitatory phasic responses, proportions of which were modulated by NAc region and risk preference.…”

Section: Discussionmentioning

confidence: 99%

Nucleus Accumbens Neurons Track Behavioral Preferences and Reward Outcomes During Risky Decision Making

Sugam¹,

Saddoris²,

Carelli³

2014

Biological Psychiatry

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Background In order to make appropriate decisions, organisms must evaluate the risks and benefits of action selection. The nucleus accumbens (NAc) has been shown to be critical for this processing, and is necessary for appropriate risk-based decision making behavior. However, it is not clear how NAc neurons encode this information to promote appropriate behavioral responding. Methods Here, rats (n=17) were trained to perform a risky decision making task in which discrete visual cues predicted the availability to respond for a smaller certain (safer) or larger uncertain (riskier) reward. Electrophysiological recordings were made in the NAc core and shell to evaluate neural activity during task performance. Results At test, animals exhibited individual differences in risk-taking behavior; some displayed a preference for the risky option, some the safe option, and some did not have a preference. Electrophysiological analysis indicated that NAc neurons differentially encoded information related to risk versus safe outcomes. Further, during free choice trials, neural activity during reward-predictive cues reflected individual behavioral preferences. In addition, neural encoding of reward outcomes was correlated with risk taking behavior, with safe-preferring and risk-preferring rats showing differential activity in the NAc core and shell during reward omissions. Conclusions Consistent with previously demonstrated alterations in prospective reward value with effort and delay, NAc neurons encode information during reward-predictive cues and outcomes in a risk task that tracked the rats’ preferred responses. This processing appears to contribute to subjective encoding of anticipated outcomes, and thus may function to bias future risk-based decisions.

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Section: Discussionmentioning

confidence: 99%

Nucleus Accumbens Neurons Track Behavioral Preferences and Reward Outcomes During Risky Decision Making

Sugam¹,

Saddoris²,

Carelli³

2014

Biological Psychiatry

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“…The NAcc and the medial caudate nucleus robustly activate during reward anticipation (Deadwyler et al, 2004), while the rostroventral putamen most reliably deactivates in response to non-reward delivery (McClure et al, 2003; O'Doherty et al, 2003). Lesions of NAcc have recently been shown to disrupt reinforcement-omission effects (Judice-Daher and Bueno, 2013). However, no cellular recordings have yet shown that NAcc cells react specifically to reward omission.…”

Section: Methodsmentioning

confidence: 99%

Timing and expectation of reward: a neuro-computational model of the afferents to the ventral tegmental area

Vitay

Hamker

2014

Front. Neurorobot.

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Neural activity in dopaminergic areas such as the ventral tegmental area is influenced by timing processes, in particular by the temporal expectation of rewards during Pavlovian conditioning. Receipt of a reward at the expected time allows to compute reward-prediction errors which can drive learning in motor or cognitive structures. Reciprocally, dopamine plays an important role in the timing of external events. Several models of the dopaminergic system exist, but the substrate of temporal learning is rather unclear. In this article, we propose a neuro-computational model of the afferent network to the ventral tegmental area, including the lateral hypothalamus, the pedunculopontine nucleus, the amygdala, the ventromedial prefrontal cortex, the ventral basal ganglia (including the nucleus accumbens and the ventral pallidum), as well as the lateral habenula and the rostromedial tegmental nucleus. Based on a plausible connectivity and realistic learning rules, this neuro-computational model reproduces several experimental observations, such as the progressive cancelation of dopaminergic bursts at reward delivery, the appearance of bursts at the onset of reward-predicting cues or the influence of reward magnitude on activity in the amygdala and ventral tegmental area. While associative learning occurs primarily in the amygdala, learning of the temporal relationship between the cue and the associated reward is implemented as a dopamine-modulated coincidence detection mechanism in the nucleus accumbens.

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“…Furthermore, the response rates during LH showed an opposite distribution. These data characterize the pattern of behavior in FI LH signaled schedules (7,8,10,9,23,24) and can be explained by evoked expectations and the delivery of reinforcement (15,25).…”

Section: Discussionmentioning

confidence: 82%

“…KA was infused with a 5 µL Hamilton syringe over a 2-min period according to the following coordinates: SNc (n=27): –4.3 mm posterior to bregma and 2.2 mm from the midline, with infusions to a depth of 7.4 mm from the skull surface (0.25 µL per site) (19). The Sham-SNc (n=16) groups received the same surgical treatment, with the exception that no solution was infused (7,8,10,11,20,21). After surgery, all rats received a single subcutaneous injection of 0.1 mL per 100 g body mass (2.15 mg/mL) of Flunixin Meglumine (Banamine®, 50 mg/mL, Intervet, Brazil) for pain relief and were allowed to recover from the surgery for 5–7 days before behavioral testing.…”

Section: Methodsmentioning

confidence: 99%

Reinforcement omission effects in rats with bilateral lesions in the substantia nigra pars compacta and ventral tegmental area

Tavares

Judice-Daher

Bueno

2019

Braz J Med Biol Res

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Reinforcement omission effects (ROEs) are characterized by higher response rates after reinforcement omission than after reinforcement delivery. This pattern of behavior is interpreted in terms of motivational and attentional processes. Recent studies from our laboratory have shown that the amygdala, nucleus accumbens, and medial prefrontal cortex are involved in ROE modulation. Also, the literature has demonstrated a role of other areas such as substantia nigra pars compacta (SNc) and the ventral tegmental area (VTA) in processes related to surprising events, such as prediction error and presentation or omission of an event (exteroceptive stimulus and reinforcement). Since these structures send projections to areas related to ROE modulation such as the amygdala, nucleus accumbens, and prefrontal cortex, the objective of the present study was to determine whether the SNc and VTA also integrate the circuit involved in ROE modulation. Rats were trained on a fixed-interval 12 s with limited-hold 6 s signaled schedule of reinforcement (Pre-lesion training). After acquisition of stable performance, the rats received bilateral neurotoxic lesions of the SNc (Experiment 1) and VTA (Experiment 2). Following postoperative recovery, the rats were submitted to two refresher sessions (Post-lesion training). Subsequently, the training was changed from a 100 to a 50% schedule of reinforcement (Post-lesion testing). In both experiments, the results showed that there was no difference in performance between sham rats and rats with bilateral lesions of the SNc or the VTA.

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Lesions of the nucleus accumbens disrupt reinforcement omission effects in rats

Cited by 10 publications

References 41 publications

Nucleus Accumbens Neurons Track Behavioral Preferences and Reward Outcomes During Risky Decision Making

Nucleus Accumbens Neurons Track Behavioral Preferences and Reward Outcomes During Risky Decision Making

Timing and expectation of reward: a neuro-computational model of the afferents to the ventral tegmental area

Reinforcement omission effects in rats with bilateral lesions in the substantia nigra pars compacta and ventral tegmental area

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