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Nature Neuroscience Jun 2021Social interactions and relationships are often rewarding, but the neural mechanisms through which social interaction drives positive experience remain poorly...
Social interactions and relationships are often rewarding, but the neural mechanisms through which social interaction drives positive experience remain poorly understood. In this study, we developed an automated operant conditioning system to measure social reward in mice and found that adult mice of both sexes display robust reinforcement of social interaction. Through cell-type-specific manipulations, we identified a crucial role for GABAergic neurons in the medial amygdala (MeA) in promoting the positive reinforcement of social interaction. Moreover, MeA GABAergic neurons mediate social reinforcement behavior through their projections to the medial preoptic area (MPOA) and promote dopamine release in the nucleus accumbens. Finally, activation of this MeA-to-MPOA circuit can robustly overcome avoidance behavior. Together, these findings establish the MeA as a key node for regulating social reward in both sexes, providing new insights into the regulation of social reward beyond the classic mesolimbic reward system.
Topics: Amygdala; Animals; Conditioning, Operant; Female; Hypothalamus; Male; Mice; Mice, Inbred C57BL; Mice, Transgenic; Nerve Net; Optogenetics; Reinforcement, Psychology; Reward; Social Behavior
PubMed: 33820999
DOI: 10.1038/s41593-021-00828-2 -
A corticoamygdalar pathway controls reward devaluation and depression using dynamic inhibition code.Neuron Dec 2023Reward devaluation adaptively controls reward intake. It remains unclear how cortical circuits causally encode reward devaluation in healthy and depressed states. Here,...
Reward devaluation adaptively controls reward intake. It remains unclear how cortical circuits causally encode reward devaluation in healthy and depressed states. Here, we show that the neural pathway from the anterior cingulate cortex (ACC) to the basolateral amygdala (BLA) employs a dynamic inhibition code to control reward devaluation and depression. Fiber photometry and imaging of ACC pyramidal neurons reveal reward-induced inhibition, which weakens during satiation and becomes further attenuated in depression mouse models. Ablating or inhibiting these neurons desensitizes reward devaluation, causes reward intake increase and ultimate obesity, and ameliorates depression, whereas activating the cells sensitizes reward devaluation, suppresses reward consumption, and produces depression-like behaviors. Among various ACC neuron subpopulations, the BLA-projecting subset bidirectionally regulates reward devaluation and depression-like behaviors. Our study thus uncovers a corticoamygdalar circuit that encodes reward devaluation via blunted inhibition and suggests that enhancing inhibition within this circuit may offer a therapeutic approach for treating depression.
Topics: Animals; Mice; Conditioning, Operant; Depression; Reward; Basolateral Nuclear Complex; Satiation
PubMed: 37734380
DOI: 10.1016/j.neuron.2023.08.022 -
Behavioural Processes Mar 2023Learning to stop responding is an important process that allows behavior to adapt to a changing and variable environment. This article reviews recent research in this... (Review)
Review
Learning to stop responding is an important process that allows behavior to adapt to a changing and variable environment. This article reviews recent research in this laboratory and others that has studied how animals learn to stop responding in operant extinction, punishment, and feature-negative learning. Extinction and punishment are shown to be similar in two fundamental ways. First, the response-suppressing effects of both are highly context-specific. Second, the response-suppressing effects of both can be remarkably response-specific: Inhibition of one response transfers little to other responses. Learning to inhibit the response so specifically may result from the correction of "response error," the difference between the level of responding and what the current reinforcer supports. In contrast, the inhibition of responding that develops in feature-negative learning, where the response is reinforced during one discriminative stimulus (A) but not in a compound of A and stimulus B, is less response-specific: The inhibition of responding by stimulus B transfers and inhibits a second response, especially if the second response has itself been inhibited before. The results thus indicate both response-specific and response-general forms of behavioral inhibition. One possibility is that response-specific inhibition is learned when the circumstances encourage the organism to pay attention to the response-to what it is actually doing-as behavioral suppression is learned.
Topics: Animals; Conditioning, Operant; Extinction, Psychological; Learning; Punishment; Inhibition, Psychological
PubMed: 36702436
DOI: 10.1016/j.beproc.2023.104830 -
Behavioural Processes Apr 2024It is generally believed that termites can't learn and are not "intelligent". This study aimed to test whether termites could have any form of memory. A Y-shaped test...
It is generally believed that termites can't learn and are not "intelligent". This study aimed to test whether termites could have any form of memory. A Y-shaped test device with one release chamber and two identical test chambers was designed and constructed by 3D printing. A colony of damp wood termites was harvested from the wild. Worker termites were randomly selected for experiment. Repellent odors that could mimic the alarm pheromone for termites were first identified. Among all substances tested, a tea tree oil and lemon juice were found to contain repellent odors for the tested termites, as they significantly reduced the time that termites spent in the chamber treated with these substances. As control, a trail pheromone was found to be attractive. Subsequently, a second cohort of termites were operant conditioned by punishment using both tea tree oil and lemon juice, and then tested for their ability to remember the path that could lead to the repellant odors. The test device was thoroughly cleaned between trials. It was found that conditioned termites displayed a reduced tendency to choose the path that led to expectant punishment as compared with naïve termites. Thus, it is concluded that damp wood termites are capable of learning and forming "fear memory", indicative of "intelligence" in termites. This result challenges established presumption about termites' intelligence.
Topics: Isoptera; Animals; Odorants; Conditioning, Operant; Pheromones; Memory; Learning; Tea Tree Oil; Citrus; Insect Repellents; Behavior, Animal; Punishment
PubMed: 38493970
DOI: 10.1016/j.beproc.2024.105012 -
Journal of the Experimental Analysis of... Jan 2024Voluntary behaviors (operants) can come in two varieties: Goal-directed actions, which are emitted based on the remembered value of the reinforcer, and habits, which are... (Review)
Review
Voluntary behaviors (operants) can come in two varieties: Goal-directed actions, which are emitted based on the remembered value of the reinforcer, and habits, which are evoked by antecedent cues and performed without the reinforcer's value in active memory. The two are perhaps most clearly distinguished with the reinforcer-devaluation test: Goal-directed actions are suppressed when the reinforcer is separately devalued and responding is tested in extinction, and habitual behaviors are not. But what is the function of habit learning? Habits are often thought to be strong and unusually persistent. The present selective review examines this idea by asking whether habits identified by the reinforcer-devaluation test are more resistant to extinction, resistant to the effects of other contingency change, vulnerable to relapse, resistant to the weakening effects of context change, or permanently in place once they are learned. Surprisingly little evidence supports the idea that habits are permanent or more persistent. Habits are more context-specific than goal-directed actions are. Methods that make behavior persistent do not necessarily work by encouraging habit. The function of habit learning may not be to make a behavior strong or more persistent but to make it automatic and efficient in a particular context.
Topics: Conditioning, Operant; Motivation; Habits; Cues
PubMed: 38149526
DOI: 10.1002/jeab.894 -
Journal of the Experimental Analysis of... Nov 2023The three principles of reinforcement are (1) events such as incentives and reinforcers increase the activity of an organism; (2) that activity is bounded by competition... (Review)
Review
The three principles of reinforcement are (1) events such as incentives and reinforcers increase the activity of an organism; (2) that activity is bounded by competition from other responses; and (3) animals approach incentives and their signs, guided by their temporal and physical conditions, together called the "contingencies of reinforcement." Mathematical models of each of these principles comprised mathematical principles of reinforcement (MPR; Killeen, 1994). Over the ensuing decades, MPR was extended to new experimental contexts. This article reviews the basic theory and its extensions to satiation, warm-up, extinction, sign tracking, pausing, and sequential control in progressive-ratio and multiple schedules. In the latter cases, a single equation balancing target and competing responses governs behavioral contrast and behavioral momentum. Momentum is intrinsic in the fundamental equations, as behavior unspools more slowly from highly aroused responses conditioned by higher rates of incitement than it does from responses from leaner contexts. Habits are responses that have accrued substantial behavioral momentum. Operant responses, being predictors of reinforcement, are approached by making them: The sight and feel of a paw on a lever is approached by placing paw on lever, as attempted for any sign of reinforcement. Behavior in concurrent schedules is governed by approach to momentarily richer patches (melioration). Applications of MPR in behavioral pharmacology and delay discounting are noted.
Topics: Animals; Reinforcement Schedule; Conditioning, Operant; Reinforcement, Psychology; Motivation; Models, Theoretical
PubMed: 37706228
DOI: 10.1002/jeab.880 -
Annual Review of Clinical Psychology May 2020Pain is considered a hardwired signal of bodily disturbance belonging to a basic motivational system that urges the individual to act and to restore the body's... (Review)
Review
Pain is considered a hardwired signal of bodily disturbance belonging to a basic motivational system that urges the individual to act and to restore the body's integrity, rather than just a sensory and emotional experience. Given its eminent survival value, pain is a strong motivator for learning. Response to repeated pain increases when harm risks are high (sensitization) and decreases in the absence of such risks (habituation). Discovering relations between pain and other events provides the possibility to predict (Pavlovian conditioning) and control (operant conditioning) harmful events. Avoidance is adaptive in the short term but paradoxically may have detrimental long-term effects. Pain and pain-related responses compete with other demands in the environment. Exposure-based treatments share the aim of facilitating or restoring the pursuit of individual valued life goals in the face of persistent pain, and further improvements in pain treatment may require a paradigm shift toward more personalized approaches.
Topics: Avoidance Learning; Central Nervous System Sensitization; Chronic Pain; Conditioning, Classical; Conditioning, Operant; Fear; Habituation, Psychophysiologic; Humans; Motivation
PubMed: 31821023
DOI: 10.1146/annurev-clinpsy-050718-095744 -
Brain Research Bulletin Aug 2022Steve Fowler is best known for his contributions to neuroscience and pharmacology, especially in the behavioral characterization of antipsychotic drugs, which he pursued... (Review)
Review
Steve Fowler is best known for his contributions to neuroscience and pharmacology, especially in the behavioral characterization of antipsychotic drugs, which he pursued with great skill and ingenuity. The present review highlights some of his important contributions in understanding the interactions between pharmacology and learning systems, in particular operant learning. Much of Steve's work resulted in novel measurement systems that offered important insights about behavior that were not accessible with traditional operant approaches, which tend to emphasize response rate and interresponse times. A brief review of the emergence of response rate and temporal features of behavior as the dominant measures in operant learning is presented. Then, Steve's approach to behavioral measurement, grounded in his work under Joe Notterman, is developed. I will review selected aspects of his research program as they touch upon and illuminate the dopamine and the anhedonia hypothesis, behavioral characterizations of typical and atypical antipsychotics, the functional roles of response force in learning, and finally the nature of the operant itself.
Topics: Antipsychotic Agents; Conditioning, Operant; Humans; Learning; Male
PubMed: 35644432
DOI: 10.1016/j.brainresbull.2022.05.009 -
The Journal of Neuroscience : the... Feb 2022Despite numerous studies examining the mechanisms of operant conditioning (OC), the diversity of OC plasticity loci and their synergism have not been examined...
Despite numerous studies examining the mechanisms of operant conditioning (OC), the diversity of OC plasticity loci and their synergism have not been examined sufficiently. In the well-characterized feeding neural circuit of , and appetitive OC increases neuronal excitability and electrical coupling among several neurons leading to an increase in expression of ingestive behavior. Here, we used the analog of OC to investigate whether OC reduces the excitability of a neuron, B4, whose inhibitory connections decrease expression of ingestive behavior. We found OC decreased the excitability of B4. This change appeared intrinsic to B4 because it could be replicated with an analog of OC in isolated cultures of B4 neurons. In addition to changes in B4 excitability, OC decreased the strength of B4's inhibitory connection to a key decision-making neuron, B51. The OC-induced changes were specific without affecting the excitability of another neuron critical for feeding behavior, B8, or the B4-to-B8 inhibitory connection. A conductance-based circuit model indicated that reducing the B4-to-B51 synapse, or increasing B51 excitability, mediated the OC phenotype more effectively than did decreasing B4 excitability. We combined these modifications to examine whether they could act synergistically. Combinations including B51 synergistically enhanced feeding. Taken together, these results suggest modifications of diverse loci work synergistically to mediate OC and that some neurons are well suited to work synergistically with plasticity in other loci. The ways in which synergism of diverse plasticity loci mediate the change in motor patterns in operant conditioning (OC) are poorly understood. Here, we found that OC was in part mediated by decreasing the intrinsic excitability of a critical neuron of feeding behavior, and specifically reducing the strength of one of its inhibitory connections that targets a key decision-making neuron. A conductance-based computational model indicated that the known plasticity loci showed a surprising level of synergism to mediate the behavioral changes associated with OC. These results highlight the importance of understanding the diversity, specificity and synergy among different types of plasticity that encode memory. Also, because OC in is mediated by dopamine (DA), the present study provides insights into specific and synergistic mechanisms of DA-mediated reinforcement of behaviors.
Topics: Animals; Aplysia; Computer Simulation; Conditioning, Operant; Models, Neurological; Neuronal Plasticity; Neurons
PubMed: 34992131
DOI: 10.1523/JNEUROSCI.1722-21.2021 -
Neuroscience and Biobehavioral Reviews Jul 2022Sensory preconditioned and second-order conditioned responding are each well-documented. The former occurs in subjects (typically rats) exposed to pairings of two... (Review)
Review
Sensory preconditioned and second-order conditioned responding are each well-documented. The former occurs in subjects (typically rats) exposed to pairings of two relatively neutral stimuli, S2 and S1, and then to pairings of S1 and a motivationally significant event [an unconditioned stimulus (US)]; the latter occurs when the order of these experiences is reversed with rats being exposed to S1-US pairings and then to S2-S1 pairings. In both cases, rats respond when tested with S2 in a manner appropriate to the affective nature of the US, e.g., approach when the US is appetitive and withdrawal when it is aversive. This paper reviews the neural substrates of sensory preconditioning and second-order conditioning. It identifies commonalities and differences in the substrates of these so-called higher-order conditioning protocols and discusses these commonalities/differences in relation to what is learned. In so doing, the review highlights ways in which these types of conditioning enhance our understanding of how the brain encodes and retrieves different types of information to generate appropriate behavior.
Topics: Animals; Conditioning, Classical; Conditioning, Operant; Conditioning, Psychological; Humans; Learning; Rats
PubMed: 35561894
DOI: 10.1016/j.neubiorev.2022.104687