Response rates track the history of reinforcement times

When conditioning involves a consistent temporal relationship between the conditioned stimulus (CS) and unconditioned stimulus (US), the expression of conditioned responses within a trial peaks at the usual time of the US relative to the CS. Here we examine the temporal profile of responses during conditioning with variable CS-US intervals. We conditioned stimuli with either uniformly distributed or exponentially distributed random CS-US intervals. In the former case, the frequency of each CS-US interval within a specified range is uniform but the momentary probability of the US (the hazard function) increases as time elapses during the trial; with the latter distribution, short CS-US intervals are more frequent than longer intervals, but the momentary probability of the US is constant across time within the trial. We report that, in a magazine approach paradigm, rats' response rates remained stable as time elapses during the CS when the CS-US intervals were uniformly distributed, whereas their response rates declined when the CS-US intervals were exponentially distributed. In other words, the profile of responding during the CS matched the frequency distribution of the US times, not the momentary probability of the US during the CS. These results are inconsistent with real-time associative models, which predict that associative strength tracks the momentary probability of the US, but may provide support for timing models of conditioning in which conditioned responding is tied to remembered times of reinforcement.     

Purkinje cell activity in the cerebellar anterior lobe after rabbit eyeblink conditioning

The cerebellar anterior lobe may play a critical role in the execution and proper timing of learned responses. The current study was designed to monitor Purkinje cell activity in the rabbit cerebellar anterior lobe after eyeblink conditioning, and to assess whether Purkinje cells in recording locations may project to the interpositus nucleus. Rabbits were trained in an interstimulus interval discrimination procedure in which one tone signaled a 250-msec conditioned stimulus-unconditioned stimulus (CS-US) interval and a second tone signaled a 750-msec CS-US interval. All rabbits showed conditioned responses to each CS with mean onset and peak latencies that coincided with the CS-US interval. Many anterior lobe Purkinje cells showed significant learning-related activity after eyeblink conditioning to one or both of the CSs. More Purkinje cells responded with inhibition than with excitation to CS presentation. In addition, when the firing patterns of all conditioning-related Purkinje cells were pooled, it appeared that the population showed a pattern of excitation followed by inhibition during the CS-US interval. Using cholera toxin-conjugated horseradish peroxidase, Purkinje cells in recording areas were found to project to the interpositus nucleus. These data support previous studies that have suggested a role for the anterior cerebellar cortex in eyeblink conditioning as well as models of cerebellar-mediated CR timing that postulate that Purkinje cell activity inhibits conditioned response (CR) generation during the early portion of a trial by inhibiting the deep cerebellar nuclei and permits CR generation during the later portion of a trial through disinhibition of the cerebellar nuclei.     

Form and characteristics of the cardiovascular conditional response in Rhesus monkeys

Three Rhesus monkeys restrained in primate chairs were exposed to several Pavlovian control procedures, followed by 13 sessions of cardiac conditioning under a delay paradigm. The conditional stimulus (CS) was a vertical line and the unconditional stimulus (US) was electric foot shock. Heart rate (HR) was analyzed in successive fivesecond intervals beginning five seconds before CS onset. The major finding was that the conditional response was consistently biphasic and consisted of an initial acceleration followed by deceleration toward the baseline, but rarely reaching it before onset of US. The subjects differed in magnitude of acceleration and subsequent deceleration as well as the location of the maximum rate in the CS-US interval. A breakdown of trials on the basis of the pre-CS HR revealed that the magnitude of effect was inversely related to the pre-CS rate.     

Postnatal development of respiratory and vocal responses during aversive classical conditioning in cats

Respiratory rate, respiration amplitude, and vocal responses were recorded in cats of different ages during classic conditioning. Vocal responses to the conditional stimulus (CS) appeared first in 8-week-old kittens, and became prominent at older ages. An increase in respiration rate occurred after the onset of the CS in cats of all ages. Similarly, the decrease of respiration amplitude was observed at all ages, but only in 8-week-old and older subjects did this response resemble an adult pattern. In 4-week-old kittens the response was characterized by an early and brief peak, suggesting an alpha conditional response (CR). Clear and significant discrimination between a warning and a safety signal was present in both respiratory and vocal responses after the age of 8 weeks.     

Fear develops to the conditioned stimulus and to the context during classical eyeblink conditioning in rats

In classical eyeblink conditioning, non-specific emotional responses to the aversive shock unconditioned stimulus (US), which are presumed to coincide with the development of fear, occur early in conditioning and precede the emergence of eyeblink responses. This twoprocess learning model was examined by concurrently measuring fear and eyeblink conditioning in the freely moving rat. Freezing served as an index of fear in animals and was measured during the inter-trial intervals in the training context and during a tone conditioned stimulus (CS) presented in a novel context. Animals that received CS-US pairings exhibited elevated levels of fear to the context and CS early in training that decreased over sessions, while eyeblink conditioned responses (CRs) developed gradually during acquisition and decreased during extinction. Random CS-US presentations produced a similar pattern of fear responses to the context and CS as paired presentations despite low eyeblink CR percentages, indicating that fear responding was decreased independent of high levels of learned eyeblink responding The results of paired training were consistent with two-process models of conditioning that postulate that early emotional responding facilitates subsequent motor learning, but measures from random control animals demonstrate that partial CS-US contingencies produce decrements in fear despite low levels of eyeblink CRs. These findings suggest, a relationship between CS-US contingency and fear levels during eyeblink conditioning, and may serve to clarify further the role that fear conditioning plays in this simple paradigm.     

Fear Develops to the Conditioned Stimulus and to the Context during Classical Eyeblink Conditioning in Rats

In classical eyeblink conditioning, non-specific emotional responses to the aversive shock unconditioned stimulus (US), which are presumed to coincide with the development of fear, occur early in conditioning and precede the emergence of eyeblink responses. This two-process learning model was examined by concurrently measuring fear and eyeblink conditioning in the freely moving rat. Freezing served as an index of fear in animals and was measured during the inter-trial intervals in the training context and during a tone conditioned stimulus (CS) presented in a novel context. Animals that received CS-US pairings exhibited elevated levels of fear to the context and CS early in training that decreased over sessions, while eyeblink conditioned responses (CRs) developed gradually during acquisition and decreased during extinction. Random CS-US presentations produced a similar pattern of fear responses to the context and CS as paired presentations despite low eyeblink CR percentages, indicating that fear responding was decreased independent of high levels of learned eyeblink responding. The results of paired training were consistent with two-process models of conditioning that postulate that early emotional responding facilitates subsequent motor learning, but measures from random control animals demonstrate that partial CS-US contingencies produce decrements in fear despite low levels of eyeblink CRs. These findings suggest a relationship between CS-US contingency and fear levels during eyeblink conditioning, and may serve to clarify further the role that fear conditioning plays in this simple paradigm.     

Timing of conditioned responses utilizing electrical stimulation in the region of the interpositus nucleus as a CS

A large body of evidence indicates that the cerebellum is essential for the acquisition, retention, and expression of the standard delay conditioned eyeblink response and that the basic memory trace appears to be established in the anterior interpositus nucleus (IP). Adaptive timing of the conditioned response (CR) is a prominent feature of classical conditioning—the CR peaks at the time of onset of the unconditioned stimulus (US) over a wide range of CS-US interstimulus intervals (ISI). A key issue is whether this timing is established by the cerebellar circuitry or prior to the cerebellum. In this study timing of conditioned eyeblink responses established via electrical stimulation of the interpositus nucleus as a conditioned stimulus (CS) was analyzed prior to and following modification of the CS-US interval in well-trained rabbits. Consistent with previous results, learning under these conditions is very rapid and robust. The CR peak eyeblink latencies are initially timed to the US onset and adjust accordingly to lengthening or shortening of the CS-US interval, just as with peripheral CSs. The acquisition of conditioned eyeblink responses by direct electrical stimulation of the IP as a CS thus retains temporal flexibility following shifts in the CS-US delay, as found in standard classical eyeblink conditioning procedures.     

Timing of Conditioned Responses Utilizing Electrical Stimulation in the Region of the Interpositus Nucleus as a CS

A large body of evidence indicates that the cerebellum is essential for the acquisition, retention, and expression of the standard delay conditioned eyeblink response and that the basic memory trace appears to be established in the anterior interpositus nucleus (IP). Adaptive timing of the conditioned response (CR) is a prominent feature of classical conditioning-the CR peaks at the time of onset of the unconditioned stimulus (US) over a wide range of CS-US interstimulus intervals (ISI). A key issue is whether this timing is established by the cerebellar circuitry or prior to the cerebellum. In this study timing of conditioned eyeblink responses established via electrical stimulation of the interpositus nucleus as a conditioned stimulus (CS) was analyzed prior to and following modification of the CS-US interval in well-trained rabbits. Consistent with previous results, learning under these conditions is very rapid and robust. The CR peak eyeblink latencies are initially timed to the US onset and adjust accordingly to lengthening or shortening of the CS-US interval, just as with peripheral CSs. The acquisition of conditioned eyeblink responses by direct electrical stimulation of the IP as a CS thus retains temporal flexibility following shifts in the CS-US delay, as found in standard classical eyeblink conditioning procedures.     

The incubation theory of fear/anxiety: experimental investigation in a human laboratory model of Pavlovian conditioning

The aim of this work was to test Eysenck's incubation theory of fear/anxiety in human Pavlovian B conditioning of heart rate (HR) responses. The conditioned stimuli (CSs) were phobia-relevant slides (snakes and spiders) and the unconditioned stimuli (UCSs) were aversive noises. The subjects were presented with two levels of noise intensity during acquisition and three levels of nonreinforced CS presentation (CS-only) in a delay differential (CS+/CS-) conditioning paradigm (2 x 3 x 2). Consistent with the incubation theory, conditioned HR acceleratory responses were sustained (resistance to extinction) for high-noise intensity and short-presentations of CS-only subjects. During the extinction phase, HR acceleratory responses quickly extinguished in low-noise intensity groups after the first presentations of CS-only. These findings were interpreted as support for the incubation theory of phobic fear.     

Classical conditioning of the eyeblink response in the delay paradigm in adults aged 18-83 years

To determine if age differences in classical conditioning of the eyelid response begin to appear in middle age in humans as they do in animals, adult subjects aged 18-83 years were trained in the delay conditioning paradigm. Large age effects occurred. Statistically significant differences first appeared in the decade of the 40s. Within-age-group variability was large. To reduce variability, subjects were classified by the magnitude of their unconditioned response (UR). Regardless of age, subjects with low amplitude URs conditioned poorly. In the normal UR amplitude group, the correlation between age and total percentage conditioned responses (CRs) was -.58. Eyeblink rate and voluntary responding did not account for age differences in conditioning, and it was unlikely that hearing acuity or corneal sensitivity caused the differences. Parallels between human and animal eyelid conditioning are considered, and it is suggested that age changes in the cerebellum may affect conditioning in aging mammals, including humans.     

Blocking of inhibitory conditioning within a serial conditioned stimulus-conditioned inhibitor compound: Maintenance of acquired behavior without an unconditioned stimulus

Well-trained classically conditioned stimuli, presented unreinforced, were protected from extinction when they were followed by a signal of the omission of the reinforcer (conditioned inhibitor Konorskian type) in eight cats. An aversive classical conditioning paradigm with shock as the reinforcer was used. Of several behavioral (leg flexion, vocalization) and organismic arousal (heart rate, respiration rate, respiration amplitude) measures of conditioned responses, the respiration amplitude changes were found to be most informative for the continuous assessment of elicited arousal of low and medium intensity. In all subjects conditioned stimuli presented during extinction in serial compound with the conditioned inhibitor elicited larger responses than did conditioned stimuli presented alone during extinction. The mechanism of protection from extinction in a paradigm in which the elicitor of learned behavior occurs prior to the conditioned inhibitor provides the organism with the mechanism for the maintenance of learned behavior in the absence of a reinforcer.     

Conditioned stimulus informativeness governs conditioned stimulus-unconditioned stimulus associability

In a conditioning protocol, the onset of the conditioned stimulus ([CS]) provides information about when to expect reinforcement (unconditioned stimulus [US]). There are two sources of information from the CS in a delay conditioning paradigm in which the CS-US interval is fixed. The first depends on the informativeness, the degree to which CS onset reduces the average expected time to onset of the next US. The second depends only on how precisely a subject can represent a fixed-duration interval (the temporal Weber fraction). In three experiments with mice, we tested the differential impact of these two sources of information on rate of acquisition of conditioned responding (CS-US associability). In Experiment 1, we showed that associability (the inverse of trials to acquisition) increased in proportion to informativeness. In Experiment 2, we showed that fixing the duration of the US-US interval or the CS-US interval or both had no effect on associability. In Experiment 3, we equated the increase in information produced by varying the C/T ratio with the increase produced by fixing the duration of the CS-US interval. Associability increased with increased informativeness, but, as in Experiment 2, fixing the CS-US duration had no effect on associability. These results are consistent with the view that CS-US associability depends on the increased rate of reward signaled by CS onset. The results also provide further evidence that conditioned responding is temporally controlled when it emerges.     

Reaction time task as unconditional stimulus

The present study was conducted to demonstrate classic conditioning in electrodermal (ED) and heart rate (HR) responses by using a nonaversive reaction time (RT) task as unconditional stimulus (US). Three groups of 12 subjects each were studied to test the efficacy of this US procedure by varying the essential components of the RT task-US between groups. Eight seconds differential delay conditioning was applied in each group. Simple geometric features (square, cross) displayed on a TV screen were used as CS+ and CS−. RT task consisted of a nonaversive tone (72 dBA, 1000 or 1200 Hz) and a motor response (pressing a button with the left index finger). Subjects were asked to respond as soon as the tone stimulus was presented. The three groups received different stimulus sequences during the 16-trial acquisition phase only. In one group (Group C1), CS+ was followed by a tone to which subjects were to respond, whereas CS− was not followed by a tone. Similarly, in a second group (Group H), CS+ was followed by a tone, whereas CS− was not; however, subjects of Group H (habituation group) were not required to respond to the tone. In a third group, (Group C2) CS+ was followed by a tone to which subjects were to respond, while CS− was followed by a different tone requiring no response. According to analysis of Group C1 data, differential conditioning was obtained in each response measure. Group H displayed habituation in each response measure obtained. In Group C2, differential conditioning was obtained in the second latency window of ED responses only. In all trials, first-interval anticipatory ED responses and HR responses did occur during acquisition, but were not differentiated with respect to the CS conditions. Although the results of Group C2 need further exploration, differential conditioning of HR and in all latency windows of ED responses was demonstrated by the use of a nonaversive RT task as US.     

Neuromuscular blocking drugs and heart rate changes after direct nerve stimulation and during classical conditioning in cats.

Two experiments investigated cardiovascular responses to several common neuromuscular blocking compounds. Experiment 1, employing 16 cats, assessed ganglionic transmission in sympathetic and parasympathetic systems controlling heart rate and blood pressure after d-tubocurarine chloride (d-T.C.), dimethyl d-tubocurarine iodide (D. d-T.I.), succinylcholine chloride (SC), or saline. Cardiovascular responses to sympathetic stimulation were essentially unaffected at drug levels that blocked evoked electromyograms; however, vagally evoked bradycardia and corresponding blood pressure decrease were blocked by d-T.C. and redduced by D. d-T.I. and SC. Experiment 2 compared heart responses of 12 cats under the same blocking compounds during differential classical aversive conditioning. Differential conditioned responses and unconditioned responses occurred under D. d-T.I., less under SC, but not under d-T.C. However, animals trained under d-T.C. and tested under D. D-T.I. showed differential conditioned responses.     

A pitfall for the expectancy theory of human eyelid conditioning

Two simple eyeblink conditioning experiments with random intermittent reinforcement schedules were performed. In Experiment 1, subjects had to rate their expectancy for an unconditioned stimulus (US) on a seven-level scale prior to each trial. As anticipated, expectancy for US increased with a successive conditioned stimulus (CS) alone, and decreased with successive CS-US pairings. However, Experiments 1 and 2 showed that the frequency of eyeblink conditioned responses (CRs) evolved in a direction opposite to that of expectancy changes: CRs increased, whereas expectancy for US decreased, and vice versa. The possible effect of sensitization on eyeblink response was ruled out by the lack of a run effect in an unpaired control group in Experiment 2. These results tend to disconfirm the expectancy theory of conditioning. Although they were explicitly predicted by the conventional “strength” theory of conditioning, an alternative interpretation is proposed within a cognitive framework.     

Heart rate conditioning in the newborn infant

In an attempt to condition heart rate in newborns, 21 infants were assigned to Conditioning, Random Control, and Backward Conditioning Groups. During training trials, the Conditioning Group received an eight-second tone (CS), a six-second ISI, and a ten-second presentation of glucose via nipple (UCS) that overlapped the last two seconds of tone. The Random Control Group received tones at the same intertrial intervals as the Conditioning Group, but glucose varied randomly. The Backward Conditioning Group received glucose during the ten seconds immediately preceding tone onset. The response to both CS and UCS during base trials was HR acceleration. The response to tone habituated in all groups, but the acceleration to glucose was maintained throughout conditioning. Although no conditioned response to the tone developed over trials, a large HR deceleration appeared during extinction to the absence of the UCS in the Conditioning Group only. This deceleration was interpreted as an orienting response to the absence of an expected event.     

Trace fear conditioning is reduced in the aging rat

Auditory trace fear conditioning is a hippocampus-dependent learning task that requires animals to associate an auditory conditioned stimulus (CS) and a fear-producing shock-unconditioned stimulus (US) that are separated by an empty 20-s trace interval. Previous studies have shown that aging impairs learning performance on hippocampus-dependent tasks. This study measured heart rate (HR) and freezing fear responses to determine if aging impairs hippocampus-dependent auditory trace fear conditioning in freely moving rats. Aging and Young rats received one long-trace fear conditioning session (10 trials). Each trial consisted of a tone-CS (5 s) and a shock-US separated by an empty 20-s trace interval. The next day rats received CS-alone retention trials. Young rats showed significantly larger HR and freezing responses on the initial CS-alone retention trials compared to the Aging rats. A control group of aging rats received fear conditioning trials with a short 1-s trace interval separating the CS and US. The Aging Short-Trace Group showed HR and freezing responses on the initial CS alone retention trials that were similar to the Young Long-Trace Group, but greater than the Aging Long-Trace Group. A second aging control group received unpaired CSs and USs, and showed no HR or freezing responses on CS-alone retention trials. These data show that HR and freezing are effective measures for detecting aging-related deficits in trace fear conditioning.     

Decelerative cardiac responsiveness to acoustical stimulation in the near term fetus.

Human fetal cardiac responses (36-39 weeks gestational age) to brief, repeated vocal stimuli (male or female voice uttering the same sentence), given at 90-95 dB SPL ex utero (around 20-30 dB less in utero) during a state of low fetal heart rate (FHR) variability, were examined using highly conservative statistical criteria taking into account each subject's prestimulus FHR variability. Subjects exposed to either of the two stimuli displayed significantly more decelerative heart rate (HR) changes compared to control subjects receiving no stimulation. The decelerative changes started during the first seconds following the onset of stimulation and reached their amplitude peak within 10 or 20 sec, depending on the subject. The direction--HR acceleration or deceleration--and the amplitude of the response depended on prestimulus HR variability only, not on prestimulus level. No major difference was found between the effects of the two voices. The data are compared to previous studies demonstrating fetal decelerative changes to acoustic stimuli of less than 105 dB SPL. The choice of an objective criterion to define an HR response and the possible orienting response nature of the decelerative change are discussed.     

Varying temporal location of a conditioned stimulus in heart rate conditioning ofMacaca mulatta

The several functions that a stimulus can assume were investigated in a Pavlovian conditioning procedure. The subjects were six rhesus monkeys; the response under observation was heart rate. The conditioning began with a temporal separation of zero between a signal and a regularly repeating electric shock; the signal was then moved to a series of earlier locations in the inter-shock interval. After six sessions at each location, two sessions followed in which only the shock was delivered periodically. The findings included: (1) A two-phased conditioned cardiac rate response seen at the first location became more multiphasic and irregular during longer intervals between signal and shock; (2) the location where the conditioned response peaked became increasingly variable as the signal was moved back, but this variability maintained a constant proportion to the signal-shock interval; and, (3) heart rate during a presignal period, and during a comparable period in shock only sessions, was generally deceleratory early in training and acceleratory thereafter. Sessions with the signal showed heart rate in the presignal period to have become acceleratory earlier in training than sessions with shock only. The data pertain to stimulus control over heart rate as a function of: (A) the temporal proximity of a signal to an aversive stimulus; and, (B) the presence or absence of the signal. The use of appropriate response units in cardiac conditioning is also discussed.     

Decelerative cardiac responsiveness to acoustical stimulation in the near term fetus

Human fetal cardiac responses (36-39 weeks gestational age) to brief, repeated vocal stimuli (male or female voice uttering the same sentence), given at 90-95 dB SPL ex utero (around 20-30 dB less in utero) during a state of low fetal heart rate (FHR) variability, were examined using highly conservative statistical criteria taking into account each subject's prestimulus FHR variability. Subjects exposed to either of the two stimuli displayed significantly more decelerative heart rate (HR) changes compared to control subjects receiving no stimulation. The decelerative changes started during the first seconds following the onset of stimulation and reached their amplitude peak within 10 or 20 sec, depending on the subject. The directions—HR acceleration or deceleration—and the amplitude of the response depended on prestimulus HR variability only, not on prestimulus level. No major difference was found between the effects of the two voices. The data are compared to previous studies demonstrating fetal decelerative changes to acoustic stimuli of less than 105 dB SPL. The choice of an objective criterion to define an HR response and the possible orienting response nature of the decelerative change are discussed.