Does activation of the baroreceptors reinforce differential Pavlovian conditioning of heart rate responses?

High- and low-pitched tones (CS+ and CS?) signalled baroreceptor stimulation or inhibition (US+ and US-) on 6-s conditioning trials (n= 128). Baroreceptor stimulation was induced by the phase-related external suction (PRES) method of Rau et al. (1992) in which a brief pulse of negative external pressure is applied to the neck at systole and one of positive pressure at diastole within each cardiac cycle (the reverse sequence is used for baroreceptor inhibition). Changes in heart period (R-R intervals) confirmed that PRES manipulated the baroreceptors in the presence of CS+ and CS? without habituation over conditioning trials. However, conditioned heart period responses were not observed on test trials (n= 32) in which CS+ and CS? were presented with the baroreceptor manipulation removed. Subjects were unable to state which CS had signalled baroreceptor stimulation and inhibition when given PRES-alone trials after the conditioning phase (differential attention thus controlled). These results (a) confirm that the differential effect of the two PRES stimuli was specific to the baroreceptors and (b) support earlier studies that have found that differential conditioning is impaired when CS?US relations are not processed in attention. We discuss implications regarding when baroreceptor firing might be discriminable and reinforcing.     

Fear potentiated startle at short intervals following conditioned stimulus onset during delay but not trace conditioning

The latency of conditioned fear after delay and trace conditioning was investigated. Some argue that delay conditioning is not dependent on awareness. In contrast, trace conditioning, where there is a gap between the conditioned stimulus (CS) and the unconditioned stimulus (US), is assumed to be dependent on awareness. In the present study, a tone CS signaled a noise US presented 1000 ms after CS onset in the delay conditioning group. In the trace conditioning group, a 200-ms tone CS was followed by an 800-ms gap prior to US presentation. Fear-potentiated startle should be seen at shorter intervals after delay conditioning compared to trace conditioning. Analyses showed increased startle at 30, 50, 100, and 150 ms after CS onset following delay conditioning compared to trace conditioning. This implies that fear-relevant stimuli elicit physiological reactions before extended processing of the stimuli occur, following delay, but not trace conditioning.     

Rats' behavior in the course of aversive conditioning measured by a stabilimeter]

Aversive behaviors of rats to the conditioned stimulus in the course of classical conditioning of a light (CS) and electric-shock (US) were analyzed using a stabilimeter. For the Classical Conditioning (CC) group (n = 5), CS was preceded 5 s to US (l s) using delayed conditioning procedure in the 3 daily sessions each of which was consisted of 30 reinforcing trials. For the US group (n = 5), US (l s) was presented at the same time as CC group without any CS. The results showed that the activity of the CC group during CS increased as the trials progressed, but it was not changed in the US group. Thus, animals made various kinds of activities during the CS, and these were not reflexes to the presentation of the CS but were responses that have long latencies.     

Learning to fear suffocation: a new paradigm for interoceptive fear conditioning

The present study aimed to establish a new interoceptive fear conditioning paradigm. The conditioned stimulus (CS) was a flow resistor that slightly obstructs breathing; the unconditional stimulus (US) was a breathing occlusion. The paired group (N = 21) received 6 acquisition trials with paired CS–US presentations. The unpaired group (N = 19) received 6 trials of unpaired CS–US presentations. In the extinction phase, both groups were administered 6 CS‐only trials. Measurements included startle eyeblink response, electrodermal responses, and self‐reported US expectancy. In the paired group, startle blink responses were larger during CS compared to intertrial interval during acquisition and extinction. Electrodermal and US expectancies were larger for the paired than for the unpaired group during acquisition, but not during extinction. The present paradigm successfully established interoceptive fear conditioning with panic‐relevant stimuli.     

Effects of Conditioned Stimulus Fear-Relevance and Preexposure on Expectancy and Electrodermal Measures of Human Pavlovian Conditioning

The present research investigated the effects of fear-relevance of the conditioned stimulus (CS) and CS preexposure on human electrodermal conditioning and on a continuous measure of expectancy of the unconditioned stimulus (US). Both experiments employed 20 preexposure, 8 acquisition, and 8 extinction trials in a differential Pavlovian conditioning paradigm with shock as the US. In Experiment 1 (N = 48), electrodermal conditioning was retarded by CS preexposure, but was not influenced by fear-relevance of the CS. Expectancy of the US was retarded by preexposure only in the fear-relevant condition. In Experiment 2 (N = 48), the CS/US contingencies was embedded in a visual masking task. Preexposure retarded both electrodermal conditioning and US expectancy. Neither measure was influenced by fear-relevance of the CS. However, fewer subjects in the preexposure condition learned the CS/US relationship and those who did, did so on later trial than those in the no-preexposure condition. Thus, the results indicated clear retardation of conditioning as a result of preexposure, but no reliable effect of fear-relevance.     

Can human autonomic classical conditioning occur without contingency awareness? The critical importance of the trial sequence

Most evidence suggests that awareness of the CS–US contingency is necessary for human autonomic conditioning. However, Schultz and Helmstetter (2010) reported unaware skin conductance conditioning using difficult-to-discriminate visual CSs. We sought to replicate these findings with procedures nearly identical to Schultz and Helmstetter among 66 participants. Results replicated the findings of significantly greater autonomic responding to CS+ than CS−; however, participants also demonstrated greater expectancy of shock to CS+ than CS− despite being classified as unaware. The differential expectancy and conditioning occurred only on trials that followed a CS+/CS− alternating sequence. On non-alternating trials, there was significantly higher expectancy and skin conductance responding to CS− compared to CS+. These results indicate that what initially appeared to be unaware differential conditioning was likely due to differential expectancy arising from a predictable trial sequence. These results underscore the critical importance of controlling for trial sequence effects in the study of learning.     

The Onset of Contingency Awareness and Electrodermal Classical Conditioning: An Analysis of Temporal Relationships during Acquisition and Extinction

The temporal relationship between the onset of contingency awareness and the onset of discrimination classical conditioning of the skin conductance response was evaluated. Awareness of the CS-UCS contingencies and skin conductance responses were measured trial-by-trial from 60 college student subjects during both acquisition and extinction. In addition, the conditioning paradigm was embedded within a masking task in order to delay the onset of awareness so that preaware and postaware trials could be analyzed. Two skin conductance responses were measured, a short latency first interval response (FIR) and a longer latency second interval response (SIR). Results showed that: 1) the onset of FIR discrimination conditioning began only after subjects indicated awareness of both the positive (CS+) and the negative (CS?) contingencies, 2) concurrent with the onset of this awareness, a) FIR discrimination increased suddenly due to increased responding to CS+ while b) SIR discrimination also increased suddenly for some subjects but gradually developed for others, 3) FIR extinction occurred only among subjects who exhibited expectancy extinction, and was due to decreased responding to CS+. The results are consistent with the interpretation that FIR discrimination is related to the cognitive processing of the CSs’significance, and that SIR discrimination is related to an individual difference variable which was reflected in the rate at which subjects became aware.     

Cell analog of the conditioned reflex to cortical electrical stimulation

Conclusion The possibility of obtaining a cellular analog of a CR was investigated on the sensory motor cortex of the unanesthetized rabbit. Single unit activity was analyzed. Stimulation through surface cortical electrodes 2.5–12mm away from the recording microelectrode was used as the conditional stimulus (CS). The unconditional stimulus (US) was stimulation through two closely situated electrodes.With short (1–5 sec) inter-trial intervals, and with a US of sufficient strength and duration, a well-marked augmentation of the excitatory response to CS was obtained in most neurons. However, it was short (less than 30 sec) and, as a rule, it was the analog not of a CR but of a pseudo conditioned reflex, for it did not require pairing of the CS and US, but appeared after one or a few presentations of the US alone.In 9 of the 21 neurons tested with longer intervals between trials (7–120 sec) conditioned-reflex changes were observed. These changes consisted of the appearance (or modification) of a response to the CS during conditioning trials and disappearance during extinction trials, or of the appearance of a response at the time corresponding to the missing US when the US was intermittently omitted. The character of the conditioned-reflex changes (activation or inhibition) was the same as that of the cell's response to the US. Changes appeared after the first 10–20 conditioning trials and recovery after extinction took place more rapidly than initial conditioning, i.e., in 5–10 combinations.     

Conditioned Orienting and Defensive Responses

Physiological responses were recorded while 9 females (Group P) who Feared spiders and 9 who did not (Group N) viewed “neutral” and spider slides in a delayed, differential conditioning procedure. Two different tones were the conditioned stimuli, and 12 neutral and 12 spider slides the unconditioned stimuli. Each CS was 11 sec long. Only Group P showed differential HR conditioning-anticipatory acceleration to the CS preceding the spider slides (CS+). For both groups, cephalic vasoconstriction was greater to the CS+ than to the CS-. However, with repeated trials Group P's response to the CS+ became more prolonged, so that by the last block of trials contraction persisted until the end of the CS period. Group N's response, on the other hand, continued to be constriction followed by rapid recovery to the prestimulus level. Although significant electrodermal conditioning did not occur, Group P tended to give larger anticipatory SC. responses to the CS+ than to the CS-. There was little evidence of somatic-autonomic coupling on a group basis. When considered along with post-experimental reports, the results indicate that at least some of the cardiovascular components of the defensive response (DR) are conditionable.     

Autonomic classical conditioning as a function of awareness of stimulus contingencies

Two groups of 32 college students were presented compound CSs (lights and tones presented simultaneously) during a classical conditioning paradigm. By means of a masking task and verbal instructions, a partially informed group was made aware of only the visual CS's contingency with the UCS, while a fully informed group was made aware of both the visual and auditory contingencies. Autonomic indices of conditioning (electrodermal responses, heart rate, and digital pulse volume) were later measured to the individual component CSs and to various compound CSs. It was found that: (1) the partially informed group exhibited conditioning exclusively to the visual CS+ and to compounds which included the visual CS+, while (2) the fully informed group exhibited conditioning to both visual and auditory CS+s. The results confirm the importance of awareness in human autonomic discrimination classical conditioning. It is suggested that human autonomic conditioning may be usefully conceptualized as an information processing task with the autonomic indices of conditioning reflecting central cognitive processes.     

Short-Interval Classical SCR Conditioning and the Stimulus-Sequence-Change-Elicited OR: The Case of the Empirical Red Herring

Classical conditioning experiments which employ CS-US intervals shorter than the latency of the CR, and which therefore require interspersed CS-alone test trials to assess conditioning, are open to the stimulus-sequence-change-elicited (SSCE) OR argument. The form of the SSCE argument which denies associative status to SCRs elicited by the CS-alone test trials is here termed an “empirical red herring” because: a) the argument cannot be dismissed on purely logical grounds, but requires the assessment of evidence for its examination; b) the argument enjoys empirical plausibility in the minds of the scientific community, as evidenced by published statements in both experimental articles and textbook chapters on autonomic conditioning; c) critical examination of the evidence which apparently supports the argument reveals that while the argument has provided a fascinating byway in the progress of our understanding of SCR conditioning, it is now time to bid farewell to the argument since it lacks any genuine empirical base. In the course of examining this particular argument, both the advantages and disadvantages of such arguments for scientific progress are discussed. Finally, it is emphasized that if one wants to study multiple-response phenomena in SCR conditioning, then a longer CS-US interval is clearly desirable. Our message only is that if the aim is to study SCR conditioning—defined as an increase in responding to a CS relative to some appropriate control condition(s) which is attributable to the contiguity of the CS with the UR to the US—in its most robust form, then the short-interval CS-US arrangement should not be avoided on the basis of the SSCE argument which, on examination, turns out to be an empirical red herring.     

DIFFERENTIATION OF CONDITIONED AND ORIENTING RESPONSE COMPONENTS IN ELECTRODERMAL CONDITIONING

Different criteria for orienting and conditioned responses (ORs and CRs) are discussed, and it is proposed that neither latency nor differences between conditioning and sensitization treatments provide adequate solutions to the problem. An additional criterion is proposed based on differences in the slopes of the generalization gradients, i.e. ORs should show rising and CRs falling generalization gradients with increased stimulus change. This criterion was tested for conditioning and sensitization groups in paradigms involving generalization along pitch and temporal continua. It was found that the response to the onset of the conditional stimulus (the CS response) fulfilled the proposed criteria for an OR, while responses in the interval of the unconditioned response on trials where the unconditional stimulus (US) was omitted (post-US responses) satisfied the criteria for an OR early in training and the criteria for a CR later in training. For the response preceding US (the pre-US response) no definite conclusion was reached, but the evidence could be interpreted to mean that both OR and CR components participated in that response too. The relationships between these response components and stages of sensory integration and response acquisition of conditioning are discussed.     

Eyeblink conditioning indicates cerebellar abnormality in dyslexia

There is increasing evidence that cerebellar deficit may be a causal factor in dyslexia. The cerebellum is considered to be the major structure involved in classical conditioning of the eyeblink response. In a direct test of cerebellar function in learning, 13 dyslexic participants (mean age 19.5 years) and 13 control participants matched for age and IQ undertook an eyeblink conditioning experiment in which for 60 acquisition trials an 800-ms auditory tone (conditioned stimulus, CS) was presented. On 70% of the trials an 80-ms corneal airpuff (unconditioned stimulus, US) was presented 720 ms after the tone onset. The cerebellar deficit hypothesis, uniquely of the causal hypotheses for dyslexia, predicts that the dyslexic participants would show abnormal performance in the incidence and/or timing of the conditioned response (CR) of an eyeblink in response to the tone (and before the US). Three of the dyslexic group showed no conditioning at all. Furthermore, the dyslexic group showed significantly worse "tuning" of the CR timing, together with significantly reduced habituation of the orienting response (OR) to the CS. Individual analyses indicated that 85% of the dyslexic group showed either no conditioning or abnormally poor CR tuning and/or abnormally low OR habituation. It is concluded that the findings provide further converging evidence of cerebellar abnormality in dyslexia and for the first time demonstrate that there are fundamental abnormalities in the way that dyslexic people learn. Equally important, the eye blink conditioning paradigm provides a method of investigating further both homogeneity and heterogeneity in the learning deficits underlying dyslexia and other developmental disorders.     

Fear acquisition requires awareness in trace but not delay conditioning

The present study explored fear acquisition in differential delay versus trace conditioning in regard to the potential role of the acquired contingency awareness. One of two neutral pictures (CS+) either coterminated with (delay group; n=32) or was followed by the aversive unconditioned stimulus (UCS) after CS offset (trace group; n=32), while startle blink and skin conductance responses (SCR) were measured. As expected, the acquisition of conditioned startle potentiation in delay conditioning was independent of contingency awareness. In contrast, fear-potentiated startle in trace conditioning was only observed for those participants who were aware of the CS-UCS contingencies. SCR conditioning was generally only obtained for aware participants. The present results suggest a more implicit learning process in delay fear conditioning, whereas the explicit acquisition of contingency awareness might be a prerequisite for trace fear conditioning.     

The relationship between electrodermal and digital vasomotor responses in aversive classical conditioning

Thirty-two subjects, exposed to a tone CS, shock UCS simple delayed conditioning paradigm with an interstimulus interval of 8 sec, were compared in skin conductance and finger pulse volume responses to a sensitization control group of 32 subjects given unpaired CS—UCS presentations. Magnitude, probability and amplitude of anticipatory and UCS omission responses were measured. Significant conditioning effects for both these types of response were observed using magnitude and probability measures of the two effector systems. Between-subject correlations showed significant positive relationships between vasomotor and electrodermal CS responses in the sensitization group and early in conditioning training. Later in training, however, this relationship disappeared, indicating a learned dissociation of the response systems during classical conditioning. Within-subject correlations showed that the two response systems developed quite independently over trials.     

Learning- and expectation-related changes in the human brain during motor learning

We have studied a simple form of motor learning in the human brain so as to isolate activity related to motor learning and the prediction of sensory events. Whole-brain, event-related functional magnetic resonance imaging (fMRI) was used to record activity during classical discriminative delay eyeblink conditioning. Auditory conditioned stimulus (CS+) trials were presented either with a corneal airpuff unconditioned stimulus (US, paired), or without a US (unpaired). Auditory CS- trials were never reinforced with a US. Trials were presented pseudorandomly, 66 times each. The subjects gradually produced conditioned responses to CS+ trials, while increasingly differentiating between CS+ and CS- trials. The increasing difference between hemodynamic responses for unpaired CS+ and for CS- trials evolved slowly during conditioning in the ipsilateral cerebellar cortex (Crus I/Lobule HVI), contralateral motor cortex and hippocampus. To localize changes that were related to sensory prediction, we compared trials on which the expected airpuff US failed to occur (Unpaired CS+) with trials on which it occurred as expected (Paired CS+). Error-related signals in the contralateral cerebellum and somatosensory cortex were seen to increase during learning as the sensory prediction became stronger. The changes seen in the ipsilateral cerebellar cortex may be due either to the violations of sensory predictions, or to learning-related increases in the excitability of cerebellar neurons to presentations of the CS+.     

INDIVIDUAL DIFFERENCES IN ORIENTING, CONDITIONABILITY, AND SKIN RESISTANCE RESPONSIVITY

Forty-eight college students, after serving as Ss in a SRR discrimination conditioning experiment, were divided into quartiles on magnitude of SRR to both noxious (UCS) and innocuous (CS) stimuli. With both orienting response (OR) measures, i.e. to the CS and to the UCS, it was shown that subjects giving large ORs gave significantly larger responses to both CS+ and CS? (during conditioning) than did Ss giving small ORs. On the basis of the innocuous stimulus split, Ss giving large ORs demonstrated both significantly faster and greater discrimination conditioning than did Ss giving small ORs. Such differences in rate and amount of discrimination conditioning were not demonstrated with the noxious stimulus split. In other words, with the noxious stimulus measure there is only a significant response level effect, but with the innocuous stimulus definition of OR, there is a significant response level effect, and a significant effect on rate and amount of discrimination conditioning. Thus, noxious and innocuous stimulus definitions of OR do not appear to be measuring the same process.     

Differential conditioning to facial emotional expressions: effects of hemispheric asymmetries and CS identification

Previous studies on aversive learning have suggested a right hemispheric advantage for eliciting autonomic reactions to a masked conditioned facial stimulus (CS) depicting anger. The present study investigated the effects of visual field (VF), stimulus awareness, and emotional valence of the CSs on indicators of conditioning (bilateral SCRs, HR) using a differential conditioning paradigm (N = 41). In Group 1, four different negatively valenced facial expressions (CS+) but not four positively valenced CS- were associated with an unconditioned stimulus (US, aversive vocalization, 97 dB, 3 s) during acquisition. Group 2 received a treatment reversal with positive CS+ associated with the US. In a repeated measures design, CSs were presented with or without awareness during extinction (two weeks interval, order counterbalanced). SOAs were adapted for each subject and condition prior to the experiment so that identification performance was approaching chance level. The results revealed that both negative and positive facial expressions could be aversively conditioned providing evidence for a generalization of learning in the valence dimension. During extinction, preattentive negative CS+ presented to the left VF showed a trend towards greater electrodermal and cardiac reactions. However, no such effect emerged under full awareness of the CSs. These results confirm and further specify the nature of hemispheric asymmetries in emotional associative learning.     

Stimulation at a site of auditory-somatosensory convergence in the medial geniculate nucleus is an effective unconditioned stimulus for fear conditioning.

The medial division of the medial geniculate nucleus (MGm) and the posterior intralaminar nucleus (PIN) are necessary for fear conditioning to an auditory conditioned stimulus (CS), receive both auditory and somatosensory input, and project to the amygdala, which is involved in production of fear conditioned responses. If CS-unconditioned stimulus (US) convergence in the MGm-PIN is critical for fear conditioning, then microstimulation of this area should serve as an effective US during classical conditioning, in place of standard footshock. Guinea pigs underwent conditioning (40-60 trials) using a tone as the CS and medial geniculate complex microstimulation as the US. Conditioned bradycardia developed when the US electrodes were in the PIN. However, microstimulation was not an effective US for conditioning in other parts of the medial geniculate or for sensitization training in the PIN or elsewhere. Learning curves were similar to those found previously for footshock US. Thus, the PIN can be a locus of functional CS-US convergence for previously for footshock US. Thus, the PIN can be a locus of functional CS-US convergence for fear conditioning to acoustic stimuli.     

Persistent activity in a cortical-to-subcortical circuit: bridging the temporal gap in trace eyelid conditioning

We have addressed the source and nature of the persistent neural activity that bridges the stimulus-free gap between the conditioned stimulus (CS) and unconditioned stimulus (US) during trace eyelid conditioning. Previous work has demonstrated that this persistent activity is necessary for trace eyelid conditioning: CS-elicited activity in mossy fiber inputs to the cerebellum does not extend into the stimulus-free trace interval, which precludes the cerebellar learning that mediates conditioned response expression. In behaving rabbits we used in vivo recordings from a region of medial prefrontal cortex (mPFC) that is necessary for trace eyelid conditioning to test the hypothesis that neurons there generate activity that persists beyond CS offset. These recordings revealed two patterns of activity during the trace interval that would enable cerebellar learning. Activity in some cells began during the tone CS and persisted to overlap with the US, whereas in other cells, activity began during the stimulus-free trace interval. Injection of anterograde tracers into this same region of mPFC revealed dense labeling in the pontine nuclei, where recordings also revealed tone-evoked persistent activity during trace conditioning. These data suggest a corticopontine pathway that provides an input to the cerebellum during trace conditioning trials that bridges the temporal gap between the CS and US to engage cerebellar learning. As such, trace eyelid conditioning represents a well-characterized and experimentally tractable system that can facilitate mechanistic analyses of cortical persistent activity and how it is used by downstream brain structures to influence behavior.