Dopamine errors drive excitatory and inhibitory components of backward conditioning in an outcome-specific manner.

For over two decades, phasic activity in midbrain dopamine neurons was considered synonymous with the prediction error in temporal-difference reinforcement learning.1-4 Central to this proposal is the notion that reward-predictive stimuli become endowed with the scalar value of predicted rewards. When these cues are subsequently encountered, their predictive value is compared to the value of the actual reward received, allowing for the calculation of prediction errors.5,6 Phasic firing of dopamine neurons was proposed to reflect this computation,1,2 facilitating the backpropagation of value from the predicted reward to the reward-predictive stimulus, thus reducing future prediction errors. There are two critical assumptions of this proposal: (1) that dopamine errors can only facilitate learning about scalar value and not more complex features of predicted rewards, and (2) that the dopamine signal can only be involved in anticipatory cue-reward learning in which cues or actions precede rewards. Recent work7-15 has challenged the first assumption, demonstrating that phasic dopamine signals across species are involved in learning about more complex features of the predicted outcomes, in a manner that transcends this value computation. Here, we tested the validity of the second assumption. Specifically, we examined whether phasic midbrain dopamine activity would be necessary for backward conditioning-when a neutral cue reliably follows a rewarding outcome.16-20 Using a specific Pavlovian-to-instrumental transfer (PIT) procedure,21-23 we show rats learn both excitatory and inhibitory components of a backward association, and that this association entails knowledge of the specific identity of the reward and cue. We demonstrate that brief optogenetic inhibition of VTADA neurons timed to the transition between the reward and cue reduces both of these components of backward conditioning. These findings suggest VTADA neurons are capable of facilitating associations between contiguously occurring events, regardless of the content of those events. We conclude that these data may be in line with suggestions that the VTADA error acts as a universal teaching signal. This may provide insight into why dopamine function has been implicated in myriad psychological disorders that are characterized by very distinct reinforcement-learning deficits.

Elements of a compound elicit little conditioned reinforcement.

The acquisition of instrumental responding can be supported by primary reinforcers or by conditional (also known as secondary) reinforcers that themselves have an association to a primary reinforcer. While primary reinforcement has been heavily studied for the past century, the associative basis of conditioned reinforcement has received comparatively little experimental examination. Yet conditioned reinforcement has been employed as an important behavioral assay in neuroscience studies, and thus an analysis of its associative basis is called for. We evaluated the extent to which an element from a previously trained compound would facilitate conditioned reinforcement. Three groups of rats received Pavlovian conditioning with a visual-auditory compound cue followed by food. After training, a lever was made available that, when pressed, produced the same trained compound (group compound), only the auditory cue (group element), or a novel auditory cue (group control). The rats in group compound pressed the lever at a higher rate than did rats in either group element or group control, demonstrating a strong conditioned reinforcement effect only in group compound. Interestingly, there was almost no difference in responding between group element and group control. The implications of this generalization decrement in conditioned reinforcement are discussed-particularly as they relate to research in behavioral neuroscience. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Higher-Order Conditioning and Dopamine: Charting a Path Forward.

Higher-order conditioning involves learning causal links between multiple events, which then allows one to make novel inferences. For example, observing a correlation between two events (e.g., a neighbor wearing a particular sports jersey), later helps one make new predictions based on this knowledge (e.g., the neighbor's wife's favorite sports team). This type of learning is important because it allows one to benefit maximally from previous experiences and perform adaptively in complex environments where many things are ambiguous or uncertain. Two procedures in the lab are often used to probe this kind of learning, second-order conditioning (SOC) and sensory preconditioning (SPC). In second-order conditioning (SOC), we first teach subjects that there is a relationship between a stimulus and an outcome (e.g., a tone that predicts food). Then, an additional stimulus is taught to precede the predictive stimulus (e.g., a light leads to the food-predictive tone). In sensory preconditioning (SPC), this order of training is reversed. Specifically, the two neutral stimuli (i.e., light and tone) are first paired together and then the tone is paired separately with food. Interestingly, in both SPC and SOC, humans, rodents, and even insects, and other invertebrates will later predict that both the light and tone are likely to lead to food, even though they only experienced the tone directly paired with food. While these processes are procedurally similar, a wealth of research suggests they are associatively and neurobiologically distinct. However, midbrain dopamine, a neurotransmitter long thought to facilitate basic Pavlovian conditioning in a relatively simplistic manner, appears critical for both SOC and SPC. These findings suggest dopamine may contribute to learning in ways that transcend differences in associative and neurological structure. We discuss how research demonstrating that dopamine is critical to both SOC and SPC places it at the center of more complex forms of cognition (e.g., spatial navigation and causal reasoning). Further, we suggest that these more sophisticated learning procedures, coupled with recent advances in recording and manipulating dopamine neurons, represent a new path forward in understanding dopamine's contribution to learning and cognition.

Eating behavior as a new frontier in memory research.

The study of memory is commonly associated with neuroscience, aging, education, and eyewitness testimony. Here we discuss how eating behavior is also heavily intertwined-and yet considerably understudied in its relation to memory processes. Both are influenced by similar neuroendocrine signals (e.g., leptin and ghrelin) and are dependent on hippocampal functions. While learning processes have long been implicated in influencing eating behavior, recent research has shown how memory of recent eating modulates future consumption. In humans, obesity is associated with impaired memory performance, and in rodents, dietary-induced obesity causes rapid decrements to memory. Lesions to the hippocampus disrupt memory but also induce obesity, highlighting a cyclic relationship between obesity and memory impairment. Enhancing memory of eating has been shown to reduce future eating and yet, little is known about what influences memory of eating or how memory of eating differs from memory for other behaviors. We discuss recent advancements in these areas and highlight fruitful research pursuits afforded by combining the study of memory with the study of eating behavior.

Using touchscreen equipped operant chambers to study animal cognition. Benefits, limitations, and advice.

Operant chambers are small enclosures used to test animal behavior and cognition. While traditionally reliant on simple technologies for presenting stimuli (e.g., lights and sounds) and recording responses made to basic manipulanda (e.g., levers and buttons), an increasing number of researchers are beginning to use Touchscreen-equipped Operant Chambers (TOCs). These TOCs have obvious advantages, namely by allowing researchers to present a near infinite number of visual stimuli as well as increased flexibility in the types of responses that can be made and recorded. We trained wild-caught adult and juvenile great-tailed grackles (Quiscalus mexicanus) to complete experiments using a TOC. We learned much from these efforts, and outline the advantages and disadvantages of our protocols. Our training data are summarized to quantify the variables that might influence participation and success, and we discuss important modifications to facilitate animal engagement and participation in various tasks. Finally, we provide a "training guide" for creating experiments using PsychoPy, a free and open-source software that was incredibly useful during these endeavors. This article, therefore, should serve as a resource to those interested in switching to or maintaining a TOC, or who similarly wish to use a TOC to test the cognitive abilities of non-model species or wild-caught individuals.

The pandemic exposes human nature: 10 evolutionary insights.

Humans and viruses have been coevolving for millennia. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2, the virus that causes COVID-19) has been particularly successful in evading our evolved defenses. The outcome has been tragic-across the globe, millions have been sickened and hundreds of thousands have died. Moreover, the quarantine has radically changed the structure of our lives, with devastating social and economic consequences that are likely to unfold for years. An evolutionary perspective can help us understand the progression and consequences of the pandemic. Here, a diverse group of scientists, with expertise from evolutionary medicine to cultural evolution, provide insights about the pandemic and its aftermath. At the most granular level, we consider how viruses might affect social behavior, and how quarantine, ironically, could make us susceptible to other maladies, due to a lack of microbial exposure. At the psychological level, we describe the ways in which the pandemic can affect mating behavior, cooperation (or the lack thereof), and gender norms, and how we can use disgust to better activate native "behavioral immunity" to combat disease spread. At the cultural level, we describe shifting cultural norms and how we might harness them to better combat disease and the negative social consequences of the pandemic. These insights can be used to craft solutions to problems produced by the pandemic and to lay the groundwork for a scientific agenda to capture and understand what has become, in effect, a worldwide social experiment.

Evidence that novel flavors unconditionally suppress weight gain in the absence of flavor-calorie associations.

Beginning with Pavlov (1927), there has been great interest in how associative learning processes affect eating behavior. For instance, flavors can become preferred when paired with calories or, conversely, become aversive when paired with illness. This relationship between flavors and caloric or toxic outcomes has been investigated by a number of theorists. We studied the effect of daily consumption of a flavor that was either paired or unpaired with calories provided by sugar on body weight change and daily food consumption over a 21-day period. Over three experiments, we observed an unanticipated attenuation of weight gain following consumption of flavored liquid solutions, particularly when those solutions were non-caloric. However, we did not find any impact of consuming the flavored liquid solutions on appetite. Given differences in weight gain in the absence of differences in the amount of food consumed, we suggest that unconditioned metabolic responses are elicited to initially novel flavor stimuli, even if those flavors are not followed by caloric outcomes. Potential dieting interventions based on these findings are discussed as is how they inform our understanding of the balance between unconditioned and conditioned responses.

Adaptive Memory: Generality of the Parent Processing Effect and Effects of Biological Relatedness on Recall.

The adaptive memory framework posits that human memory is an evolved cognitive feature, in which stimuli relevant to fitness are better remembered than neutral stimuli. There is now substantial evidence that processing a neutral stimulus in terms of its relevancy to an imagined ancestral survival scenario enhances recall, although there is still disagreement concerning the proximate mechanisms responsible for this effect. Several other mnemonic biases have recently been discovered that similarly appear to reflect evolutionary pressures, including a bias to remember items relevant to an imagined parenting scenario. We tested the generality of this parent processing effect by varying the biological relatedness of the imagined child. We also varied the biological relatedness of a child during an imagined third-person survival processing scenario. Across four experiments, we found evidence that simply altering the described biological relatedness of a child in the parenting scenario and third-person survival processing scenario can affect recall, such that items are better remembered when made relevant to a biological child compared to an adopted child. How these findings inform the general adaptive memory framework is discussed.

Adaptive memory: Is there a reproduction-processing effect?

Like all biological systems, human memory is likely to have been influenced by evolutionary processes, and its abilities have been subjected to selective mechanisms. Consequently, human memory should be primed to better remember information relevant to one's evolutionary fitness. Supporting this view, participants asked to rate words based on their relevance to an imaginary survival situation better recall those words (even the words rated low in relevancy) than the same words rated with respect to non-survival situations. This mnemonic advantage is called the "survival-processing effect," and presumably it was selected for because it contributed to evolutionary fitness. The same reasoning suggests that there should be an advantage for recall of information that has been rated for relevancy to reproduction and/or mate seeking, although little evidence has existed to assess this proposition. We used an experimental design similar to that in the original survival-processing effect study (Nairne, Thompson, & Pandeirada, 2007) and across 3 experiments tested several newly designed scenarios to determine whether a reproduction-processing effect could be found in an ancestral environment, a modern mating environment, and an ancestral environment in which the emphasis was on raising offspring as opposed to finding a mate. Our results replicated the survival-processing effect but provided no evidence of a reproduction-processing effect when the scenario emphasized finding a mate. However, when rating items on their relevancy to raising one's offspring in an ancestral environment, a mnemonic advantage comparable to that of the survival-processing effect was found. (PsycINFO Database Record