Differential recruitment of ventral pallidal e-types by behaviorally salient stimuli during Pavlovian conditioning.
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ABSTRACT:
SUBMITTER: Hegedus P
PROVIDER: S-EPMC8066429 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Pavlovian aversive conditioning is a fundamental form of learning helping organisms survive in their environment. Previous research has suggested that organisms are prepared to preferentially learn to fear stimuli that have posed threats to survival across evolution. Here, we examined whether enhanced Pavlovian aversive conditioning can occur to stimuli that are relevant to the organism's concerns beyond biological and evolutionary considerations, and whether such preferential learning is modulated by inter-individual differences in affect and motivation. Seventy-two human participants performed a spatial cueing task where the goal-relevance of initially neutral stimuli was experimentally manipulated. They subsequently underwent a differential Pavlovian aversive conditioning paradigm, in which the goal-relevant and goal-irrelevant stimuli served as conditioned stimuli. Skin conductance response was recorded as an index of the conditioned response and participants' achievement motivation was measured to examine its impact thereon. Results show that achievement motivation modulated Pavlovian aversive learning to goal-relevant vs. goal-irrelevant stimuli. Participants with high achievement motivation more readily acquired a conditioned response to goal-relevant compared with goal-irrelevant stimuli than did participants with lower achievement motivation. However, no difference was found between goal-relevant and goal-irrelevant stimuli during extinction. These findings suggest that stimuli that are detected as relevant to the organism can induce facilitated Pavlovian aversive conditioning even though they hold no inherent threat value and no biological evolutionary significance, and that the occurrence of such learning bias is critically dependent on inter-individual differences in the organism's concerns, such as achievement motivation.
| S-EPMC6482202 | biostudies-literature
Project description:A critical area of inquiry in the neurobiology of alcohol abuse is the mechanism by which cues gain the ability to elicit alcohol use. Previously, we found that cue-evoked activity in rat ventral pallidum robustly encodes the value of sucrose cues trained under both Pavlovian and instrumental contingencies, despite a stronger relationship between cue-evoked activity and behavioral latency after instrumental training (Richard et al., 2018, Elife, 7, e33107). Here, we assessed: (a) ventral pallidal representations of Pavlovian versus instrumental cues trained with alcohol reward, and (b) the impact of non-associative alcohol exposure on ventral pallidal representations of sucrose cues. Decoding of cue identity based on ventral pallidum firing was blunted for the Pavlovian alcohol cue in comparison to both the instrumental cue trained with alcohol and either cue type trained with sucrose. Further, non-associative alcohol exposure had opposing effects on ventral pallidal encoding of sucrose cues trained on instrumental versus Pavlovian associations, enhancing decoding accuracy for an instrumental discriminative stimulus and reducing decoding accuracy for a Pavlovian conditioned stimulus. These findings suggest that alcohol exposure can drive biased engagement of specific reward-related signals in the ventral pallidum.
| S-EPMC6848750 | biostudies-literature
Project description:The ventral pallidum (VP) mediates motivated behaviors largely via the action of VP GABA and glutamatergic neurons. In addition to these neuronal subtypes, there is a population of cholinergic projection neurons in the VP, whose functional significance remains unclear. To understand the functional role of VP cholinergic neurons, we first examined behavioral responses to an appetitive (APP) odor that elicited approach, and an aversive (AV) odor that led to avoidance. To examine how VP cholinergic neurons were engaged in APP vs. AV responses, we used an immediate early gene marker and in-vivo fiber photometry, examining the activation profile of VP cholinergic neurons in response to each odor. Exposure to each odor led to an increase in the number of cFos counts and increased calcium signaling of VP cholinergic neurons. Activity and cre-dependent viral vectors were designed to label engaged VP cholinergic neurons in two distinct contexts: (1) exposure to the APP odor, (2) followed by subsequent exposure to the AV odor, and vice versa. These studies revealed two distinct, non-overlapping subpopulations of VP cholinergic neurons: one activated in response to the APP odor, and a second distinct population activated in response to the AV odor. These two subpopulations of VP cholinergic neurons are spatially intermingled within the VP, but show differences in electrophysiological properties, neuronal morphology, and projections to the basolateral amygdala. Although VP cholinergic neurons are engaged in behavioral responses to each odor, VP cholinergic signaling is only required for approach behavior. Indeed, inhibition of VP cholinergic neurons not only blocks approach to the APP odor, but reverses the behavior, leading to active avoidance. Our results highlight the functional heterogeneity of cholinergic projection neurons within the VP. These two subpopulations of VP cholinergic neurons differentially encode valence of olfactory stimuli and play unique roles in approach and avoidance behaviors.
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Project description:Associative learning can enable environmental cues to signal food and stimulate feeding, independent of physiological hunger. Two forebrain regions necessary in cue driven feeding, the basolateral area of the amygdala and the medial prefrontal cortex, communicate via extensive, topographically organized connections. The basolateral nucleus (BLA) sends extensive projections to the prelimbic cortex (PL), and our aim here was to determine if this pathway was selectively recruited during cue-food associative learning. The anterior and posterior basolateral nuclei are recruited during different phases of cue-food learning, and thus we examined whether distinct pathways that originate in these nuclei and project to the PL are differently recruited during early and late stages of learning. To accomplish this we used neuroanatomical tract tracing combined with the detection of Fos induction. To identify projecting neurons within the BLA, prior to training, rats received a retrograde tracer, Fluoro-Gold (FG) into the PL. Rats were given either one or ten sessions of tone-food presentations (Paired group) or tone-only presentations (Control group). The Paired group learned the tone-food association quickly and robustly and had greater Fos induction within the anterior and posterior BLA during early and late learning compared to the Control group. Notably, the Paired group had more double-labeled neurons (FG + Fos) during late training compared to the Control group, specifically in the anterior BLA. This demonstrates selective recruitment of the anterior BLA-PL pathway by late cue-food learning. These findings indicate plasticity and specificity in the BLA-PL pathways across cue-food associative learning.
| S-EPMC5494146 | biostudies-literature
Project description:Until half a century ago, associative learning played a fundamental role in theories of perceptual appearance [Berkeley, G. (1709) An Essay Towards a New Theory of Vision (Dublin), 1st Ed.]. But starting in 1955 [Gibson, J. J. & Gibson, E. J. (1955) Psychol. Rev. 62, 32-41], most studies of perceptual learning have not been concerned with association or appearance but rather with improvements in discrimination ability. Here we describe a "cue recruitment" experiment, which is a straightforward adaptation of Pavlov's classical conditioning experiment, that we used to measure changes in visual appearance caused by exposure to novel pairings of signals in visual stimuli. Trainees viewed movies of a rotating wire-frame (Necker) cube. This stimulus is perceptually bistable. On training trials, depth cues (stereo and occlusion) were added to force the perceived direction of rotation. Critically, an additional signal was also added, contingent on rotation direction. Stimuli on test trials contained the new signal but not the depth cues. Over 45 min, two of the three new signals that we tested acquired the ability to bias perceived rotation direction on their own. Results were consistent across the eight trainees in each experiment, and the new cue's effectiveness was long lasting. Whereas most adaptation aftereffects on appearance are opposite in direction to the training stimuli, these effects were positive. An individual new signal can be recruited by the visual system as a cue for the construction of visual appearance. Cue recruitment experiments may prove useful for reexamining of the role of experience in perception.
| S-EPMC1326158 | biostudies-literature
Project description:We used a differential Pavlovian conditioning paradigm to measure tilt aftereffect (TAE) strength. Gabor patches, rotated clockwise and anticlockwise, were used as conditioned stimuli (CSs), one of which (CS+) was followed by the unconditioned stimulus (UCS), whereas the other (CS-) appeared alone. The UCS was an air puff delivered to the left eye. In addition to the CS+ and CS-, the vertical test patch was also presented for the clockwise and anticlockwise adapters. The vertical patch was not followed by the UCS. After participants acquired differential conditioning, eyeblink conditioned responses (CRs) were observed for the vertical patch when it appeared to be tilted in the same direction as the CS+ owing to the TAE. The effect was observed not only when the adapter and test stimuli were presented in the same retinotopic position but also when they were presented in the same spatiotopic position, although spatiotopic TAE was weak-it occurred approximately half as often as the full effect. Furthermore, spatiotopic TAE decayed as the time after saccades increased, but did not decay as the time before saccades increased. These results suggest that the time before the performance of saccadic eye movements is needed to compute the spatiotopic representation.
| S-EPMC5240094 | biostudies-literature
Project description:The interconnected nuclei of the ventral basal ganglia have long been identified as key regulators of motivated behavior, and dysfunction of this circuit is strongly implicated in mood and substance use disorders. The ventral pallidum (VP) is a central node of the ventral basal ganglia, and recent studies have revealed complex VP cellular heterogeneity and cell- and circuit-specific regulation of reward, aversion, motivation, and drug-seeking behaviors. Although the VP is canonically considered a relay and output structure for this circuit, emerging data indicate that the VP is a central hub in an extensive network for reward processing and the regulation of motivation that extends beyond classically defined basal ganglia borders. VP neurons respond temporally faster and show more advanced reward coding and prediction error processing than neurons in the upstream nucleus accumbens, and regulate the activity of the ventral mesencephalon dopamine system. This review will summarize recent findings in the literature and provide an update on the complex cellular heterogeneity and cell- and circuit-specific regulation of motivated behaviors and reinforcement by the VP with a specific focus on mood and substance use disorders. In addition, we will discuss mechanisms by which stress and drug exposure alter the functioning of the VP and produce susceptibility to neuropsychiatric disorders. Lastly, we will outline unanswered questions and identify future directions for studies necessary to further clarify the central role of VP neurons in the regulation of motivated behaviors. Significance: Research in the last decade has revealed a complex cell- and circuit-specific role for the VP in reward processing and the regulation of motivated behaviors. Novel insights obtained using cell- and circuit-specific interrogation strategies have led to a major shift in our understanding of this region. Here, we provide a comprehensive review of the VP in which we integrate novel findings with the existing literature and highlight the emerging role of the VP as a linchpin of the neural systems that regulate motivation, reward, and aversion. In addition, we discuss the dysfunction of the VP in animal models of neuropsychiatric disorders.
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Project description:The hedonic value of a sweet food reward, or how much a taste is 'liked', has been suggested to be encoded by neuronal firing in the posterior ventral pallidum (VP). Hedonic impact can be altered by psychological manipulations, such as taste aversion conditioning, which can make an initially pleasant sweet taste become perceived as disgusting. Pairing nausea-inducing LiCl injection as a Pavlovian unconditioned stimulus (UCS) with a novel taste that is normally palatable as the predictive conditioned stimulus (CS+) suffices to induce a learned taste aversion that changes orofacial 'liking' responses to that sweet taste (e.g., lateral tongue protrusions) to 'disgust' reactions (e.g., gapes) in rats. We used two different sweet tastes of similar initial palatability (a sucrose solution and a polycose/saccharin solution, CS ± assignment was counterbalanced across groups) to produce a discriminative conditioned aversion. Only one of those tastes (arbitrarily assigned and designated as CS+) was associatively paired with LiCl injections as UCS to form a conditioned aversion. The other taste (CS-) was paired with mere vehicle injections to remain relatively palatable as a control sweet taste. We recorded the neural activity in VP in response to each taste, before and after aversion training. We found that the safe and positively hedonic taste always elicited excitatory increases in firing rate of VP neurons. By contrast, aversion learning reversed the VP response to the 'disgusting' CS+ taste from initial excitation into a conditioned decrease in neuronal firing rate after training. Such neuronal coding of hedonic impact by VP circuitry may contribute both to normal pleasure and disgust, and disruptions of VP coding could result in affective disorders, addictions and eating disorders.
| S-EPMC4724492 | biostudies-literature
Project description:Threat conditioning is a common associative learning model with translational relevance. How threat-conditioned cues impact on formally unrelated instrumental behavior in humans is not well known. Such an effect is known as Pavlovian-to-instrumental transfer (PIT). While PIT with aversive primary Pavlovian reinforcers is established in nonhuman animals, this is less clear in humans, where secondary reinforcers or instructed instrumental responses are most often investigated. We modified an existing human PIT procedure to include primary reinforcers. Participants first learned to obtain (or avoid losing) appetitive instrumental reinforcement (chocolate) by appropriate approach or avoidance actions. They either had to act (Go) or to withhold an action (NoGo), and in the Go condition either to approach a reward target to collect it or to withdraw from the reward target to avoid losing it. Then they learned to associate screen color (CS) with aversive Pavlovian reinforcement (electric shock US). In the transfer phase, we conducted the instrumental task during the presence of Pavlovian CS. In a first experiment, we show that the aversive Pavlovian CS+, compared to CS-, increased response rate in Go-Withdraw trials, i.e., induce conditioned facilitation of avoidance responses. This finding was confirmed in a second and independent experiment with an increased number of Go-Withdraw trials. Notably, we observed no appreciable conditioned suppression of approach responses. Effect size to distinguish CS+/CS- in Go-Withdraw trials was d = 0.42 in the confirmation sample. This would require n = 37 participants to demonstrate threat learning with 80% power. Thus, the effect size is on a practically useful scale although smaller than for model-based analysis of autonomic measures. In summary, our results indicate conditioned facilitation of formally unrelated instrumental avoidance behavior in humans and provide a novel behavioral threat learning measure that requires only key presses.
| S-EPMC6478249 | biostudies-literature
Project description:Pavlovian fear conditioning, which offers the advantage of simplicity in both the control of conditional and unconditional stimuli (CS, US) presentation and the analysis of specific conditional and unconditional responses (CR, UR) in a controlled laboratory setting, has been the standard model in basic and translational fear research. Despite 100 years of experiments, the utility of fear conditioning has not been trans-situationally validated in real-life contexts. We thus investigated whether fear conditioning readily occurs and guides the animal's future behavior in an ecologically-relevant environment. To do so, Long-Evans rats foraging for food in an open arena were presented with a tone CS paired with electric shock US to their dorsal neck/body that instinctively elicited escape UR to the safe nest. On subsequent test days, the tone-shock paired animals failed to exhibit fear CR to the CS. In contrast, animals that encountered a realistic agent of danger (a looming artificial owl) paired with a shock, simulating a plausible predatory strike, instantly fled to the nest when presented with a tone for the first time. These results highlight the possibility of a nonassociative, rather than standard associative, fear process providing survival function in life-threatening situations that animals are likely to encounter in nature.
| S-EPMC9388582 | biostudies-literature