Studies Of Classical Conditioning Research Articles

A mini-review of the pathophysiology of task-specific tremor: insights from electrophysiological and neuroimaging findings

Task-specific tremor (TST) is a specific type of tremor that occurs when performing or attempting to perform a specific task, such as writing or playing a musical instrument. The clinical entity of TST remains heterogeneous. Some TSTs can only be induced by conducting a specific task, while others can be elicited when adopting a particular position simulating a task. The pathophysiology of TST is controversial. Whether TST is an isolated tremor syndrome, a spectrum of dystonic tremor syndrome (DTS), or essential tremor (ET) is not yet clear. Evidence from electrophysiological studies suggests that TST patients have normal reciprocal inhibition responses but abnormal motor cortical excitability, especially relating to the maladaptive long-interval intracortical inhibitory circuitry. The blink recovery study and eyeblink classical conditioning studies demonstrated possible hyperexcitability of the brainstem circuits and cerebellar dysfunction in patients with TST. Functional MRI studies have further shown that patients with TST have reduced functional connectivity in the cerebellum, similar to patients with DTS and ET. Due to variable methodologies and the sparsity of functional MRI studies in TST, it remains uncertain if patients with TST share the connectivity abnormalities between the cortical or subcortical areas that have been demonstrated in patients with DTS. Comprehensive electrophysiological and functional neuroimaging studies may help to elucidate the pathophysiology of TST.

The mushroom body output encodes behavioral decision during sensory-motor transformation

Animals form a behavioral decision by evaluating sensory evidence on the background of past experiences and the momentary motivational state. In insects, we still lack understanding of how and at which stage of the recurrent sensory-motor pathway behavioral decisions are formed. The mushroom body (MB), a central brain structure in insects1 and crustaceans,2,3 integrates sensory input of different modalities4,5,6 with the internal state, the behavioral state, and external sensory context7,8,9,10 through a large number of recurrent, mostly neuromodulatory inputs,11,12 implicating a functional role for MBs in state-dependent sensory-motor transformation.13,14 A number of classical conditioning studies in honeybees15,16 and fruit flies17,18,19 have provided accumulated evidence that at its output, the MB encodes the valence of a sensory stimulus with respect to its behavioral relevance. Recent work has extended this notion of valence encoding to the context of innate behaviors.8,20,21,22 Here, we co-analyzed a defined feeding behavior and simultaneous extracellular single-unit recordings from MB output neurons (MBONs) in the cockroach in response to timed sensory stimulation with odors. We show that clear neuronal responses occurred almost exclusively during behaviorally responded trials. Early MBON responses to the sensory stimulus preceded the feeding behavior and predicted its occurrence or non-occurrence from the single-trial population activity. Our results therefore suggest that at its output, the MB does not merely encode sensory stimulus valence. We hypothesize instead that the MB output represents an integrated signal of internal state, momentary environmental conditions, and experience-dependent memory to encode a behavioral decision.

Increased early and late neuronal responses to aversively conditioned faces across different attentional conditions

Faces with emotional information–by virtue of their expression or their history of affective learning–are prioritized during neuronal processing as compared to neutral faces. Classical conditioning studies have shown that aversively conditioned (CS+) faces potentiate different face processing stages as evidenced by increased early and late event-related potential (ERPs) components. However, it is unknown whether and how ERP modulations depend on certain attentional conditions. To examine this question, this preregistered study investigated ERPs to faces paired with aversive screams or neutral sounds under three tasks with increasing attention to CS + relevant features of the face: Participants (N = 40) had to discriminate either the orientation of superimposed lines, perceived gender, or the CS association. We found potentiation of the N170, the Early Posterior Negativity (EPN), and, most remarkably, the Late Positive Potential (LPP) to CS + faces regardless of task condition. This finding suggests that, in contrast to other types of emotional information and learning, classical conditioning boosts early and late processing stages, even if no explicit attention to the face information or the CS association is required.

A Review of the Effects of Valenced Odors on Face Perception and Evaluation.

How do valenced odors affect the perception and evaluation of facial expressions? We reviewed 25 studies published from 1989 to 2020 on cross-modal behavioral effects of odors on the perception of faces. The results indicate that odors may influence facial evaluations and classifications in several ways. Faces are rated as more arousing during simultaneous odor exposure, and the rated valence of faces is affected in the direction of the odor valence. For facial classification tasks, in general, valenced odors, whether pleasant or unpleasant, decrease facial emotion classification speed. The evidence for valence congruency effects was inconsistent. Some studies found that exposure to a valenced odor facilitates the processing of a similarly valenced facial expression. The results for facial evaluation were mirrored in classical conditioning studies, as faces conditioned with valenced odors were rated in the direction of the odor valence. However, the evidence of odor effects was inconsistent when the task was to classify faces. Furthermore, using a z-curve analysis, we found clear evidence for publication bias. Our recommendations for future research include greater consideration of individual differences in sensation and cognition, individual differences (e.g., differences in odor sensitivity related to age, gender, or culture), establishing standardized experimental assessments and stimuli, larger study samples, and embracing open research practices.

Amygdala Adaptation and Temporal Dynamics of the Salience Network in Conditioned Fear: A Single-Trial fMRI Study.

Research in rodents has established the role of the amygdaloid complex in defensive responses to conditioned threat. In human imaging studies, however, activation of the amygdala by conditioned threat cues is often not observed. One hypothesis states that this finding reflects adaptation of amygdaloid responses over time. We tested this hypothesis by estimating single-trial neural responses over a large number of conditioning trials. Functional MRI (fMRI) was recorded from 18 participants during classical differential fear conditioning: Participants viewed oriented grayscale grating stimuli (45° or 135°) presented centrally in random order. In the acquisition block, one grating (the CS+) was paired with a noxious noise, the unconditioned stimulus (US), on 25% of trials. The other grating, denoted CS–, was never paired with the US. Consistent with previous reports, BOLD in dorsal anterior cingulate cortex (dACC) and insula, but not the amygdala, was heightened when viewing CS+ stimuli that were not paired with US compared to CS– stimuli. Trial-by-trial analysis showed that over the course of acquisition, activity in the amygdala attenuated. Interestingly, activity in the dACC and insula also declined. Representational similarity analysis (RSA) corroborated these results, indicating that the voxel patterns evoked by CS+ and CS– in these brain regions became less distinguishable over time. Together, the present findings support the hypothesis that the lack of BOLD differences in the amygdaloid complex in many studies of classical conditioning is due to adaptation, and the adaptation effects may reflect changes in large-scale networks mediating aversive conditioning, particularly the salience network.

Operant Conditioning in Honey Bees (Apis mellifera L.): The Cap Pushing Response.

The honey bee has been an important model organism for studying learning and memory. More recently, the honey bee has become a valuable model to understand perception and cognition. However, the techniques used to explore psychological phenomena in honey bees have been limited to only a few primary methodologies such as the proboscis extension reflex, sting extension reflex, and free flying target discrimination-tasks. Methods to explore operant conditioning in bees and other invertebrates are not as varied as with vertebrates. This may be due to the availability of a suitable response requirement. In this manuscript we offer a new method to explore operant conditioning in honey bees: the cap pushing response (CPR). We used the CPR to test for difference in learning curves between novel auto-shaping and more traditional explicit-shaping. The CPR protocol requires bees to exhibit a novel behavior by pushing a cap to uncover a food source. Using the CPR protocol we tested the effects of both explicit-shaping and auto-shaping techniques on operant conditioning. The goodness of fit and lack of fit of these data to the Rescorla-Wagner learning-curve model, widely used in classical conditioning studies, was tested. The model fit well to both control and explicit-shaping results, but only for a limited number of trials. Learning ceased rather than continuing to asymptotically approach the physiological most accurate possible. Rate of learning differed between shaped and control bee treatments. Learning rate was about 3 times faster for shaped bees, but for all measures of proficiency control and shaped bees reached the same level. Auto-shaped bees showed one-trial learning rather than the asymptotic approach to a maximal efficiency. However, in terms of return-time, the auto-shaped bees’ learning did not carry over to the covered-well test treatments.

When touch predicts pain: predictive tactile cues modulate perceived intensity of painful stimulation independent of expectancy

AimsNon-nociceptive somatosensory input, such as tactile or proprioceptive information, always precedes nociceptive input during a painful event. This relationship provides clear opportunities for predictive associative learning, which may shape future painful experiences. In this differential classical conditioning study we tested whether pain-associated tactile cues (conditioned stimuli; CS) could alter the perceived intensity of painful stimulation, and whether this depends on duration of the CS—seeing that CS duration might allow or prevent conscious expectation. MethodsSubjects underwent a classical differential conditioning task in which a tactile cue at location A (CS+) preceded painful electrical stimulation at location B (UShigh), whereas a tactile cue at location C (CS−) preceded non-painful electrical stimulation at location B (USlow). At test, we compared the pain evoked by a moderately painful stimulus (USmed) when preceded by either the CS+ or CS−. CS duration was manipulated between subjects. Participants were assigned to one of three groups: Long CS (4s, allowing conscious expectation), Short CS (110ms) and CS-US indistinguishable (20ms), preventing conscious expectation). We hypothesised that more pain would be evoked by the US when preceded by the CS+ relative to the CS-, and that the effect would be independent of CS duration. ResultsFifty-four healthy participants (31 females, age=26, SD=9) were included in the analysis. The hypotheses were supported in that more intense pain was evoked by the USmed when paired with the tactile CS+, than when paired with the tactile CS-; mean difference 3mm on a 150mm VAS (CI 0.4–4.8mm). CS duration did not moderate the effect. The effect was greater in those participants where calibration was optimal, as indicated by a relatively more painful UShigh. ConclusionWe conclude that pain-associated tactile cues can influence pain, and that this effect is not dependent on stimulus duration. This suggests that explicit expectation is not a requirement for predictive cues to modulate pain. That the presence of the CS+ resulted in only a 5.3% higher intensity rating compared with the CS− may reflect a limitation of laboratory studies, where a limited number of trials, an artificial context and the use of experimental pain are likely to reveal only glimpses of what is clinically possible. ImplicationsPain-associated visual and auditory cues have been shown to enhance pain in laboratory and clinical scenarios, supposedly by influencing expectation of impending harm. We show that pain-associated somatosensory cues can also modulate pain and that this can occur independently of expectation. This points to a larger potential role for associative learning in the development and treatment of pain than has previously been considered. We suggest that research into associative mechanisms underpinning pain, as distinct from those that link pain to pain-related fear and avoidance, is worthwhile.

Spike-coding mechanisms of cerebellar temporal processing in classical conditioning and voluntary movements.

Time is a fundamental and critical factor in daily life. Millisecond timing, which is the underlying temporal processing for speaking, dancing, and other activities, is reported to rely on the cerebellum. In this review, we discuss the cerebellar spike-coding mechanisms for temporal processing. Although the contribution of the cerebellum to both classical conditioning and voluntary movements is well known, the difference of the mechanisms for temporal processing between classical conditioning and voluntary movements is not clear. Therefore, we review the evidence of cerebellar temporal processing in studies of classical conditioning and voluntary movements and report the similarities and differences between them. From some studies, which used tasks that can change some of the temporal properties (e.g., the duration of interstimulus intervals) with keeping identical movements, we concluded that classical conditioning and voluntary movements may share a common spike-coding mechanism because simple spikes in Purkinje cells decrease at predicted times for responses regardless of the intervals between responses or stimulation.

Selections on the Empirical and Theoretical Investigations of Behavioral Variability: An Introduction to the Special Issue

A. Blaisdell & W. D. Stahlman Special Issue Introduction Selections on the Empirical and Theoretical Investigations of Behavioral Variability: An Introduction to the Special Issue W. David Stahlman University of Mary Washington, U.S.A. Aaron P. Blaisdell University of California, Los Angeles, U.S.A. This special issue of the International Journal of Comparative Psychology is dedicated in memory of Seth Roberts who passed away before its publication. The ideas contained herein are in part the result of, and greatly inspired by, his innovative and important work on behavioral variability . “Under carefully controlled experimental circumstances, an animal will behave as it damned well pleases.” -The Harvard Law of Animal Behavior Though the Harvard Law is much a tongue-in-cheek, wry statement for researchers to evoke when their investigations do not go as planned, it holds a critical reminder for those who would set out to forecast the behavior of organisms. Namely, it suggests an important role for the unpredictability inherent to behavior. The Law subtly indicates that this unpredictability is neither due to measurement error, nor due to an incomplete understanding of the factors that control behavior, nor owing to improper control of the relevant observational parameters. Instead, due to intrinsic stochasticity, behavior retains a degree of necessary unpredictability. In other words, while researchers can readily make accurate predictions regarding typical behavior when collecting many data, they must necessarily struggle to accurately predict a single organism’s behavior at a given instant in time. Behavior appears to be probabilistic in nature, not determined. The experimental investigation of behavioral variability as an important phenomenon, rather than a nuisance, has really only entered the scientific literature in very recent decades. Certainly, there were investigations that predate the so-called cognitive revolution (e.g., Antonitis, 1951; Dashiell, 1930); however, the systematic investigation of behavior has traditionally focused on the strength of discrete response classes, rather than the examination of the control of the form of behavior. Much of this focus may be attributable to the giant intellectual forebears in the studies of classical conditioning and instrumental learning. Thorndike’s (1911) law of effect focused on the lawfulness of how Stimulus-Response (S-R) learning follows from Correspondence concerning this article should be addressed to W. David Stahlman, UMW Department of Psychology, 1301 College Ave., Fredericksburg, VA 22401. (Email: wdstahlm@umw.edu)

Spatial memory extinction: A c-Fos protein mapping study

While the neuronal basis of spatial memory consolidation has been thoroughly studied, the substrates mediating the process of extinction remain largely unknown. This study aimed to evaluate the functional contribution of selected brain regions during the extinction of a previously acquired spatial memory task in the Morris water maze. For that purpose, we used adult male Wistar rats trained in a spatial reference memory task. Learning-related changes in c-Fos inmunoreactive cells after training were evaluated in cortical and subcortical regions. Results show that removal of the hidden platform in the water maze induced extinction of the previously reinforced escape behavior after 16 trials, without spontaneous recovery 24h later. Extinction was related with significantly higher numbers of c-Fos positive nuclei in amygdala nuclei and prefrontal cortex. On the other hand, the lateral mammillary bodies showed higher number of c-Fos positive cells than the control group. Therefore, in contrast with the results obtained in studies of classical conditioning, we show the involvement of diencephalic structures mediating this kind of learning. In summary, our findings suggest that medial prefrontal cortex, the amygdala complex and diencephalic structures like the lateral mammillary nuclei are relevant for the extinction of spatial memory.

The placebo in practice

Recent placebo literature provides the scientific basis for the different psychological factors that influence the outcome of a medical treatment. The aim of the present review is to summarize the recent findings of placebo research offering useful tools for everyday medical routine. Treatment efficacy is influenced by the patient's expectations of therapeutic benefit. Indeed, positive or negative expectations may lead to symptom improvement or worsening, respectively. Therefore, in clinical practice, patients' expectations and beliefs need to be considered and controlled appropriately. In addition, previous experience influences the healing process, as shown by classical conditioning studies. This knowledge can be used to increase the effect of pharmacological or procedural treatments, to reduce drug intake, and to minimize psychological adverse events. Overall, a significant enhancement of the therapeutic outcome can be obtained by potentiating empathic communication and establishing a cooperative patient-provider relationship. Placebo research provides solid scientific ground for all those psychological aspects that characterize every medical treatment. It also gives us information on the functioning of the human brain, with the possibility to exploit some of these mechanisms in routine medical practice.

Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

The honeybee Apis mellifera has emerged as a robust and influential model for the study of classical conditioning, thanks to the existence of a powerful Pavlovian conditioning protocol, the olfactory conditioning of the proboscis extension response (PER). In 2011, the olfactory PER conditioning protocol celebrates 50 years since it was first introduced by Kimihisa Takeda in 1961. Here, we review its origins, developments, and perspectives in order to define future research avenues and necessary methodological and conceptual evolutions. We show that olfactory PER conditioning has become a versatile tool for the study of questions in extremely diverse fields in addition to the study of learning and memory and that it has allowed behavioral characterizations, not only of honeybees, but also of other insect species, for which the protocol was adapted. We celebrate, therefore, Takeda's original work and prompt colleagues to conceive and establish further robust behavioral tools for an accurate characterization of insect learning and memory at multiple levels of analysis.

Learning in a simple biological system: a pilot study of classical conditioning of human macrophages in vitro

Recent advances in cell biology and gene regulation suggest mechanisms whereby associative learning could be performed by single cells. Therefore, we explored a model of classical conditioning in human macrophages in vitro. In macrophage cultures, bacterial lipopolysaccharide (LPS; unconditioned stimulus) was paired once with streptomycin (conditioned stimulus). Secretion of interleukin-6 (IL-6) was used as response measure. At evocation, conditioning was not observed. Levels of IL-6 were higher only in those cultures that had been exposed to LPS in the learning phase (p's < .05), regardless whether they received the conditioned stimulus or not at evocation.However, habituation was evident, with a 62% loss of the IL-6 response after three LPS presentations (p < .001). If further experiments confirm that simple learning can occur in immune cells, this may have bearings not only on immune regulation, but also on the brain response to molecular signals detected in the periphery. Importantly, whether capacities for simple learning in single cells extend beyond habituation, and how this would be demonstrated, remain open questions.

Olfactory Conditioning in the Third Instar Larvae of Drosophila melanogaster Using Heat Shock Reinforcement

Adult Drosophila melanogaster has long been a popular model for learning and memory studies. Now the larval stage of the fruit fly is also being used in an increasing number of classical conditioning studies. In this study, we employed heat shock as a novel negative reinforcement for larvae and obtained high learning scores following just one training trial. We demonstrated heat-shock conditioning in both reciprocal and non-reciprocal paradigms and observed that the time window of association for the odor and heat shock reinforcement is on the order of a few minutes. This is slightly wider than the time window for electroshock conditioning reported in previous studies, possibly due to lingering effects of the high temperature. To test the utility of this simplified assay for the identification of new mutations that disrupt learning, we examined flies carrying mutations in the dnc gene. While the sensitivity to heat shock, as tested by writhing, was similar for wild type and dnc homozygotes, dnc mutations strongly diminished learning. We confirmed that the learning defect in dnc flies was indeed due to mutation in the dnc gene using non-complementation analysis. Given that heat shock has not been employed as a reinforcement for larvae in the past, we explored learning as a function of heat shock intensity and found that optimal learning occurred around 41 °C, with higher and lower temperatures both resulting in lower learning scores. In summary, we have developed a very simple, robust paradigm of learning in fruit fly larvae using heat shock reinforcement.

Pour une approche cognitive du conditionnement pavlovien

Over the past 30 years, classical conditioning studies have been examined within a cognitive perspective. This paper introduces the main studies that have emerged through models that refer to cognitive concepts. After a brief review concerning the basic models of Pavlovian conditioning, (e.g. Rescorla-Wagner, 1972), we present more recent models based on the concepts of memory and representation (e.g. Miller & Matzel, 1988). These models, which rely on the cognitive distinction between learning and performance, present another vision of the relationship between the representations of stimuli in memory.

Study of classical conditioning in Aplysia through the implementation of computational models of its learning circuit

The learning phenomenon can be analysed at various levels, but in this paper we treat a specific paradigm of artificial intelligence, i.e. artificial neural networks (ANNs), whose main virtue is their capacity to seek unified and mutually satisfactory solutions which are relevant to biological and psychological models. Many of the procedures and methods proposed previously have used biological and/or psychological principles, models, and data; here, we focus on models which look for a greater degree of coherence. Therefore we analyse and compare all aspects of the Gluck–Thompson and Hawkins ANN models. A multithread computer model is developed for analysis of these models in order to study simple learning phenomena in a marine invertebrate (Aplysia californica) and to check their applicability to research in psychology and neurobiology. The predictive capacities of the models differs significantly: the Hawkins model provides a better analysis of the behavioural repertory of Aplysia on both the associative and the non-associative learning level. The scope of the ANN modelling technique is broadened by integration with neurobiological and behavioural models of associative learning, allowing enhancement of some architectures and procedures that are currently being used.

A learned response to sperm competition in the field cricket, Gryllus bimaculatus (de Geer)

While, historically, studies of classical conditioning have been concerned mainly with the rules and mechanisms of stimulus association, more recent work is providing evidence of its adaptive value to the animal. Much of this has focused on reproductive advantages, such as learning to predict the availability of a potential mate or competitor. We looked at classically conditioned stimulus association in the novel context of sperm competition. Using field crickets, Gryllus bimaculatus, we looked at the ability of adult males to associate topographical features of the environment (configurations of toy bricks) or olfactory cues (artificial odours) with the presence or absence of an apparent competitor (another male on the other side of a clear partition). Males were able to learn associations between apparent competition and one of two spatial configurations or odours, in that they transferred larger spermatophores to a female in the conditions associated with another male, both during training (when another male was present) and during testing (when it was not). Males thus appeared to modulate sperm transfer in relation to learned environmental predictors of sperm competition. However, while males began stridulating sooner after the introduction of a female, stridulated more often and were quicker to transfer a spermatophore in some conditions associated with the presence of another male, these differences were apparent only during training, and not during testing.

Dissociating basal forebrain and medial temporal amnesic syndromes: insights from classical conditioning.

In humans, anterograde amnesia can result from damage to the medial temporal (MT) lobes (including hippocampus), as well as to other brain areas such as basal forebrain. Results from animal classical conditioning studies suggest that there may be qualitative differences in the memory impairment following MT vs. basal forebrain damage. Specifically, delay eyeblink conditioning is spared after MT damage in animals and humans, but impaired in animals with basal forebrain damage. Recently, we have likewise shown delay eyeblink conditioning impairment in humans with amnesia following anterior communicating artery (ACoA) aneurysm rupture, which damages the basal forebrain. Another associative learning task, a computer-based concurrent visual discrimination, also appears to be spared in MT amnesia while ACoA amnesics are slower to learn the discriminations. Conversely, animal and computational models suggest that, even though MT amnesics may learn quickly, they may learn qualitatively differently from controls, and these differences may result in impaired transfer when familiar information is presented in novel combinations. Our initial data suggests such a two-phase learning and transfer task may provide a double dissociation between MT amnesics (spared initial learning but impaired transfer) and ACoA amnesics (slow initial learning but spared transfer). Together, these emerging data suggest that there are subtle but dissociable differences in the amnesic syndrome following damage to the MT lobes vs. basal forebrain, and that these differences may be most visible in non-declarative tasks such as eyeblink classical conditioning and simple associative learning.

An Automated Apparatus for Conditioning Proboscis Extension in Honey Bees, Apis mellifera L.

An apparatus is described for the study of classical conditioning of proboscis extension in harnessed honey bees, Apis mellifera L., that permits automatic programming of events and recording of data. The apparatus is easy to use, accommodates a wide range of stimuli and can be used to study both associative and nonassociative learning. The technique was evaluated in a series of experiments in which the performance of bees was compared under automated and traditional methods of conditioning. The results indicated that the automated apparatus can successfully be used to study Pavlovian conditioning, discrimination learning, and habituation. A unique finding was that the odor of honeycomb can serve as an unconditioned stimulus to support Pavlovian conditioning.

Emotional modulation of attention orienting: A classical conditioning study

Emotional modulation of attention shifting was investigated in Posner’s (1980) spatial orienting task by conditioning the attention cue to an aversive white noise. Prior to the attention task, the Conditioning group received a 90dB white noise unconditioned stimulus (UCS) contingent upon the frame‐lit rectangle attention cue, while the Control group received non‐contingent presentations. The Conditioning group evidenced greater skin conductance responses to the frame‐lit rectangle in the conditioning phase, reflecting an electrodermal conditioned response. In the attention phase, the frame‐lit rectangle served as the attention cue in the spatial orienting task. The Conditioning group showed equally fast reaction times (RTs) to targets presented outside the location of the cue as to targets at the same location as the cue, reflecting elimination of the cognitive cost usually involved in shifting attention. The Control group evidenced the regular cost of shifting attention away from the location of the cue. The Conditioning group also evidenced a larger N1‐component with a parietal distribution of the event‐related brain potentials to the cue and a larger N1‐component at the frontal regions to targets presented outside the cued location. This suggests that both visual orienting to the cue and attention shifting from cue to target on invalid trials were amplified by the emotional salience attached to the cue through the classical conditioning procedure.