Effects of early life and current housing on sensitivity to reward loss in a successive negative contrast test in pigs.

Animals in a negative affective state seem to be more sensitive to reward loss, i.e. an unexpected decrease in reward size. The aim of this study was to investigate whether early-life and current enriched vs. barren housing conditions affect the sensitivity to reward loss in pigs using a successive negative contrast test. Pigs (n = 64 from 32 pens) were housed in barren or enriched conditions from birth onwards, and at 7 weeks of age experienced either a switch in housing conditions (from barren to enriched or vice versa) or not. Allotting pigs to the different treatments was balanced for coping style (proactive vs. reactive). One pig per pen was trained to run for a large reward and one for a small reward. Reward loss was introduced for pigs receiving the large reward after 11 days (reward downshift), i.e. from then onwards, they received the small reward. Pigs housed in barren conditions throughout life generally had a lower probability and higher latency to get the reward than other pigs. Proactive pigs ran overall slower than reactive pigs. After the reward downshift, all pigs ran slower. Nevertheless, reward downshift increased the latency and reduced the probability to get to the reward, but only in pigs exposed to barren conditions in early life, which thus were more sensitive to reward loss than pigs from enriched early life housing. In conclusion, barren housed pigs seemed overall less motivated for the reward, and early life housing conditions had long-term effects on the sensitivity to reward loss.

Consummatory Successive Negative Contrast in Rats.

Using animal models in addiction and pain research is pivotal to unravel new pathways and mechanisms for the treatment of these disorders. Reward devaluation through a consummatory successive negative contrast (cSNC) task has shown the ability to reduce physical pain sensitivity (hypoalgesia) and increase oral ethanol consumption in rats. The procedure is based on exposing the experimental animals to a 32% sucrose solution during several sessions (preshift sessions) followed by a devaluation to 4% sucrose during the next few sessions (postshift sessions). The cSNC effect can be monitored by comparing the experimental group to an unshifted control that had access to 4% sucrose throughout the entire experiment (preshift and postshift sessions). The cSNC phenomenon is defined by lower consumption of sucrose in the downshifted group than in the unshifted group during postshfit sessions.

Lateral habenula lesions disrupt appetitive extinction, but do not affect voluntary alcohol consumption.

This study analyzed the effects of LHb lesions on appetitive extinction and alcohol consumption. Eighteen male Wistar rats received neurochemical lesions of the LHb (quinolinic acid) and 12 received a vehicle infusion (PBS). In a runway instrumental task, rats received acquisition (12 pellets/trial, 6 trials/session, 10 sessions) and extinction training (5 sessions). In a consummatory task, rats had daily access to 32% sucrose (5 min, 10 sessions) followed by access to water (5 sessions). Then, animals received 2 h preference tests with escalating alcohol concentrations (2%-24%), followed by two 24 h preference tests with 24% alcohol. Relative to Shams, LHb lesions delayed extinction, as indicated by lower response latencies (instrumental task) and higher fluid consumption (consummatory task). LHb lesions did not affect alcohol consumption regardless of alcohol concentration or test duration. The LHb modulates appetitive extinction and needs to be considered as part of the brain circuit underlying reward loss.

Reward loss and addiction: Opportunities for cross-pollination.

Paradigms used to study the response to and consequences of exposure to reward loss have been underutilized in approaches to the psychobiology of substance use disorders. We propose here that bringing these two areas into contact will help expanding our understanding of both reward loss and addictive behavior, hence opening up opportunities for cross-pollination. This review focuses on two lines of research that point to parallels. First, several neurochemical systems involved in addiction are also involved in the modulation of the behavioral effects of reward loss, including opioid, GABA, and dopamine receptors. Second, there are extensive overlaps in the brain circuitry underlying both reward loss and addiction. Common components of this system include, at least, the amygdala, ventral and dorsal striatum, and various prefrontal cortex regions. Four emerging avenues of research that benefit from emphasis on the common ground between reward loss and addiction are reviewed, namely, the neural circuitry involved in reward devaluation, the influence of genetic and reward history on the behavioral vulnerability and resilience, the role of competing natural rewards, and emotional self-medication. An understanding of the role of reward loss in addiction will point to a deeper understanding of the initiation and maintenance of substance use disorders.

Reward loss and the basolateral amygdala: A function in reward comparisons.

The neural circuitry underlying behavior in reward loss situations is poorly understood. We considered two such situations: reward devaluation (from large to small rewards) and reward omission (from large rewards to no rewards). There is evidence that the central nucleus of the amygdala (CeA) plays a role in the negative emotion accompanying reward loss. However, little is known about the function of the basolateral nucleus (BLA) in reward loss. Two hypotheses of BLA function in reward loss, negative emotion and reward comparisons, were tested in an experiment involving pretraining excitotoxic BLA lesions followed by training in four tasks: consummatory successive negative contrast (cSNC), autoshaping (AS) acquisition and extinction, anticipatory negative contrast (ANC), and open field testing (OF). Cell counts in the BLA (but not in the CeA) were significantly lower in animals with lesions vs. shams. BLA lesions eliminated cSNC and ANC, and accelerated extinction of lever pressing in AS. BLA lesions had no effect on OF testing: higher activity in the periphery than in the central area. This pattern of results provides support for the hypothesis that BLA neurons are important for reward comparison. The three affected tasks (cSNC, ANC, and AS extinction) involve reward comparisons. However, ANC does not seem to involve negative emotions and it was affected, whereas OF activity is known to involve negative emotion, but it was not affected. It is hypothesized that a circuit involving the thalamus, insular cortex, and BLA is critically involved in the mechanism comparing current and expected rewards.

Listening to music in a risk-reward context: The roles of the temporoparietal junction and the orbitofrontal/insular cortices in reward-anticipation, reward-gain, and reward-loss.

Artificial rewards, such as visual arts and music, produce pleasurable feelings. Popular songs in the verse-chorus form provide a useful model for understanding the neural mechanisms underlying the processing of artificial rewards, because the chorus is usually the most rewarding element of a song. In this functional magnetic resonance imaging (fMRI) study, the stimuli were excerpts of 10 popular songs with a tensioned verse-to-chorus transition. We examined the neural correlates of three phases of reward processing: (1) reward-anticipation during the verse-to-chorus transition, (2) reward-gain during the first phrase of the chorus, and (3) reward-loss during the unexpected noise followed by the verse-to-chorus transition. Participants listened to these excerpts in a risk-reward context because the verse was followed by either the chorus or noise with equal probability. The results showed that reward-gain and reward-loss were associated with left- and right-biased temporoparietal junction activation, respectively. The bilateral temporoparietal junctions were active during reward-anticipation. Moreover, we observed left-biased lateral orbitofrontal activation during reward-anticipation, whereas the medial orbitofrontal cortex was activated during reward-gain. The findings are discussed in relation to the cognitive and emotional aspects of reward processing.

Neural mechanisms of negative reinforcement in children and adolescents with autism spectrum disorders.

BACKGROUND: Previous research has found accumulating evidence for atypical reward processing in autism spectrum disorders (ASD), particularly in the context of social rewards. Yet, this line of research has focused largely on positive social reinforcement, while little is known about the processing of negative reinforcement in individuals with ASD. METHODS: The present study examined neural responses to social negative reinforcement (a face displaying negative affect) and non-social negative reinforcement (monetary loss) in children with ASD relative to typically developing children, using functional magnetic resonance imaging (fMRI). RESULTS: We found that children with ASD demonstrated hypoactivation of the right caudate nucleus while anticipating non-social negative reinforcement and hypoactivation of a network of frontostriatal regions (including the nucleus accumbens, caudate nucleus, and putamen) while anticipating social negative reinforcement. In addition, activation of the right caudate nucleus during non-social negative reinforcement was associated with individual differences in social motivation. CONCLUSIONS: These results suggest that atypical responding to negative reinforcement in children with ASD may contribute to social motivational deficits in this population.

Behavioral neuroscience of psychological pain.

Pain is a common word used to refer to a wide range of physical and mental states sharing hedonic aversive value. Three types of pain are distinguished in this article: Physical pain, an aversive state related to actual or potential injury and disease; social pain, an aversive emotion associated to social exclusion; and psychological pain, a negative emotion induced by incentive loss. This review centers on psychological pain as studied in nonhuman animals. After covering issues of terminology, the article briefly discusses the daily-life significance of psychological pain and then centers on a discussion of the results originating from two procedures involving incentive loss: successive negative contrast-the unexpected devaluation of a reward-and appetitive extinction-the unexpected omission of a reward. The evidence reviewed points to substantial commonalities, but also some differences and interactions between physical and psychological pains. This evidence is discussed in relation to behavioral, pharmacological, neurobiological, and genetic factors that contribute to the multidimensional experience of psychological pain.

Identifying profiles of recovery from reward devaluation in rats.

In humans and other mammals, the unexpected loss of a resource can lead to emotional conflict. Consummatory successive negative contrast (cSNC) is a laboratory model of reward devaluation meant to capture that conflict. In this paradigm, animals are exposed to a sharp reduction in the sucrose concentration of a solution after several days of access. This downshift in sucrose content leads to behavioral responses such as the suppression of consumption and physiologic responses including elevation of corticosterone levels. However, response heterogeneity in cSNC has yet to be explored and may be relevant for increasing the validity of this model, as humans demonstrate clinically meaningful heterogeneity in response to resource loss. The current analysis applied latent growth mixture modeling to test for and characterize heterogeneity in recovery from cSNC among rats (N=262). Although most animals exhibited recovery of consummatory behavior after a sharp drop in consumption in the first postshift trial (Recovery class; 83%), two additional classes were identified including animals that did not change their consumption levels after downshift (No Contrast class; 6%), and animals that exhibited an initial response similar to that of the Recovery class but did not recover to preshift consumption levels (No Recovery class; 11%). These results indicate heterogeneity in recovery from reward loss among rats, which may increase the translatability of this animal model to understand diverse responses to loss among humans.