Inhibition of the startle reflex in the rat by prior tactile stimulation

In Experiment 1, three groups of rats received a tactile prepulse 0.5, 1, or 2 mA electric shock (to feet) .25, .5, 1, 5, 10, or 20 sec prior to an acoustic startle stimulus. The startle response was, maximally inhibited at the .25-sec interval and gradually recovered thereafter. Inhibition was larger with the intense stimuli, and for the .5-mA stimulus occurred reliably only in animals which responded to the prestimulus. In Experiment 2, the intensity of the prepulse was varied within subjects at intervals of .5, 1, and 2 sec. Inhibition was directly related to prestimulus intensity and was greatest at .5 sec. In Experiment 3, an EMG measure of startle reactivity allowed the use of shorter intervals. The maximal inhibitory interval between the prestimulus and startle stimulus was 40 msec compared with either a shorter 10-msec or a longer 250-msec separation.     

Fear potentiation of the acoustic startle reflex using noises of various spectral frequencies as conditioned stimuli

The effectiveness of noise of various intensities and frequencies in modulating the amplitude of the acoustic startle reflex was evaluated, as a preliminary test of the capacity of these noises to produce consistent and reliable fear-potentiated startle in rats. It was determined that bands of noise containing high frequencies (greater than 10 kHz) tend to unconditionally reduce acoustic startle responses, probably by masking the high-frequency startle-eliciting stimulus. Noise containing high frequencies produced reliable fear-potentiated startle only when its estimated unconditioned startle suppression was subtracted from the enhancement obtained after pairing it with footshocks. Noises devoid of high frequencies produced modest-unconditioned startle enhancements and the most robust and reliable fear-potentiated startle when they were paired with footshocks. A nonmonotonic relationship between training shock intensity and the level of fear-potentiated startle was also exhibited when a low-frequency noise was used as a conditioned stimulus, a finding consistent with previous studies in which a visual stimulus was used. Finally, a differential Pavlovian conditioning procedure indicated that rats could readily discriminate between two different low-frequency bands of noise. The outcome of these experiments indicates that it is easier to employ low-frequency bands of noise to obtain auditory fear-potentiated startle with high-frequency startle-eliciting stimuli.     

Immediate shock,passive avoidance,and potentiated startle: Implications for the unconditioned response to shock

Three experiments were performed to study the immediate-shock freezing deficit, a deficit in freezing in rats that results when electric shock is delivered immediately upon exposure to a novel context. This deficit was accompanied by failures to detect evidence of passive avoidance (Experiment 1) or potentiation of the auditory startle response (Experiment 2). The deficit in freezing was attenuated by preexposure to the shocked context (Experiment 3). The results support the view that fear-related behaviors are activated by signals for shock rather than by shock itself. They also suggest that the immediate-shock freezing deficit is due to a failure to process the to-be-conditioned contextual cues (Fanselow, 1986a, 1990).     

The effects of varying the interreinforcement interval on appetitive contextual conditioning

Appetitive contextual conditioning in rats and ringdoves was investigated in six experiments. In Experiment 1, differential contextual training produced greater anticipatory activity in rats in the presence of a context paired with food than it did in rats in the presence of a different context in which food was never presented. Furthermore, the rats showed a preference for the context associated with food when they were given a simultaneous choice test between contexts. In Experiment 2, rats were more active in and preferred a context associated with a variable-time 30-sec (VT30) schedule as opposed to a VT180 schedule. Experiment 3 was a between-subjects replication of the previous experiment. As expected, rats exhibited significantly more anticipatory activity in a context in which food had been presented on a VT30 schedule than they did in a context in which food had been presented on a VT180 schedule. Experiment 4 showed that anticipatory activity was a reflection of context-US associations in ringdoves, and in Experiments 5 and 6, ringdoves also exhibited an inverse relationship between the. amount of anticipatory activity and the length of the interreinforcement interval (IRI). These results reveal a relation between ERI and contextual conditioning opposite from that obtained in studies of aversive conditioning.     

Fear-potentiated startle using three conditioned stimulus modalities

The capacities of three different conditioned stimulus modalities (light, noise, and airflow produced by a fan) to produce fear-potentiated startle were evaluated. Previous experiments have shown that following either light-shock or noise-shock pairings, both the light and noise conditioned stimuli acquire the ability to potentiate the acoustically elicited startle response in rats (the so-calledfear-potentiated startle effect). In Experiment 1, the ability of airflow produced by a fan to act as a conditioned stimulus was investigated. Rats were given either paired or impaired fan-shock training followed by a test for fear-potentiated startle. The fan conditioned stimulus potentiated startle only in the group given explicit fan-shock pairings. In Experiment 2, we evaluated the discriminability of the three conditioned stimulus modalities. Rats were given light, noise, or fan-shock pairings and were subsequently tested for fear-potentiated startle with the trained conditioned stimulus as well as the two remaining novel conditioned stimuli. Only the trained conditioned stimulus potentiated startle. These results show that fear-potentiated startle can be produced with three discriminable conditioned stimulus modalities, allowing the future use of fear-potentiated startle in the investigation of higher order conditioning phenomena.     

Persistent effect of noise on the acoustic startle reflex in the rat

Continuous noise facilitates acoustic startle reflexes in the rat. Rats were exposed to noise for 23 h (Experiment 1) or to 23 h of startle eliciting stimuli at the rate of 1/min (Experiment 2). Facilitation was reduced following habituation in Experiment 2, but was unaffected by prolonged noise exposure in Experiment 1. Reflex inhibition produced by a brief noise was not altered by habituation. Prior experiments show that increases in intensity of continuous noise engage two disparate processes which affect the acoustic startle reflex, one facilitatory (arousal) and one inhibitory (masking). The present data reveal that arousal is not diminished by prolonged noise exposure. The loss of facilitation following reflex habituation may be attributed to its increased susceptibility to masking, or to a direct effect of stimulus repetition on the arousal process normally associated with the noise background.     

Foraging on the radial-arm maze: Effects of altering the reward at a target location

Thirsty rats were trained to collect small water rewards from the end of each arm of an eight-arm radial maze. During these training trials and subsequent testing trials, the subjects were allowed to choose a maximum of eight arms. “Preference” for a target maze location was studied by noting when, in the sequence of eight choices, the target was selected. During testing, when one maze location was consistently devoid of water, rats decreased their preference for this arm over trials (Experiment 1). Similarly, rats that learned a saccharin-lithium association demonstrated lower preferences for a maze location that consistently held the conditioned saccharin solution. This was true for animals that received saccharin-lithium conditioning on the maze (Experiment 3A) and for animals conditioned to saccharin in a separate context (Experiment 3B). An increase in preference for a target maze location consistently containing a sweet chocolate milk solution was observed in animals that were water- and food-deprived (Experiment 2). These studies demonstrate that animals will modify their responses toward (preferences for) maze locations that predictably contain an altered reward.     

Habituation to illness: Effects of prior experience with the US on the formation of learned taste aversions in rats

Experiment 1 investigated the effects of US habituation on the acquisition and extinction of learned taste aversions in rats. Subjects receiving five noncontingent LiCl intubations prior to conditioning failed to develop a conditioned taste aversion, while control subjects experiencing a single saccharin/LiCl pairing displayed a pronounced taste aversion which weakened during subsequent poisonings. Experiment 2 examined whether habituation, defined as a waning of responses to repeated presentation of an illness stimulus, was a possible mechanism for explaining the results of Experiment 1. Subjects showed a decrease in motor activity following an initial LiCl intubation, but less attenuation of activity with successive intubations.     

Outcome-specific conditioned inhibition in Pavlovian backward conditioning

In the present experiments, the outcome specificity of learning was explored in an appetitive Pavlovian backward conditioning procedure with rats. The rats initially were administered Pavlovian backward training with two qualitatively different unconditioned stimulus conditioned-stimulus (US-CS) pairs of stimuli (e.g., pellet --> noise or sucrose --> light), and then the effects of this training were assessed in Pavlovian-to-instrumental transfer (Experiment 1) and retardation-of-learning (Experiment 2) tests. In the transfer test, it was shown that during the last 10-sec interval, the CSs selectively reduced the rate of the instrumental responses with which they shared a US, relative to the instrumental responses with which they did not share a US. The opposite result was obtained when the USs (in the absence of the CSs) were presented noncontingently. In the retardation test, conditioned magazine approach, responding to the CSs was acquired more slowly when the stimulus-outcome combinations in the backward and the forward conditioning phases were the same, as compared with when they were reversed. These results are collectively in accord with the view that Pavlovian backward conditioning can result in the formation of outcome-specific inhibitory associations. Alternative views of backward conditioning are also examined.     

Selective reinstatement of instrumental performance depends on the discriminative stimulus properties of the mediating outcome

We conducted three experiments to investigate the associative structure underlying the reinstatement of instrumental performance after extinction. In each experiment, rats were initially rewarded on two responses with different outcomes. At test, both responses were extinguished in order to assess the impact of a single noncontingent outcome delivery on response selection. Experiment 1 found evidence of outcome-selective reinstatement (i.e., more responses were performed on the lever that was trained with the reinstating outcome than on the other lever). Experiment 2 demonstrated that the outcome’s capacity to reinstate performance was not affected by a reduction in its motivational value. Experiment 3 found evidence that the reinstating outcome selectively retrieved the response it signaled rather than the response it followed during training. Together, these findings are consistent with the view that instrumental reinstatement depends on the discriminative stimulus properties of the reinstating outcome.     

Tests of a principle of reflex modification: Modification of the human eyeblink-reflex is independent of the intensity of the reflex-eliciting stimulus

The human airpuff-elicited reflexive eyeblink, like the startle reflex of rats and pigeons, occurs with either reduced amplitude or latency when a brief auditory stimulus precedes the reflex-eliciting event by an appropriate lead interval. In common with the overt startle reflex of lower animals, the degree of inhibition or latency reduction of an airpuff-elicited eyeblink in human adults proved to be independent of the intensity of the eyeblink-eliciting airpuff. This finding supports the principle that the amount of a given reflex modification effect (whether latency or amplitude reduction) is determined by the parameters and lead time of the modifying stimulus and not by those of the reflex-eliciting event.     

Effects of stress controllability,immunization, and therapy on the subsequent defeat of colony intruders

Three experiments investigated the influence that various stress-controllability manipulations had on the defensive behaviors of rats when they were subsequently tested as intruders in previously established, aggressive colonies of conspecifics. In Experiment 1, naive subjects that had received a session of 80 shocks in a tube showed an enhanced series of defensive responses and received more bites than did a group of restrained nonshocked rats as colony intruders 24 h later. These two measures were also found to be positively correlated within each group. In Experiment 2, a group that was given 80 yoked inescapable shocks, in contrast to a group that had wheel-turn escape training and a restrained nonshocked control group, displayed more defeat and was bitten more frequently when tested as intruders on the following day. In Experiment 3, 60 trials of wheel-turn escape training were given 4 h prior to (i.e., immunization) or after (i.e., therapy) a session of 60 inescapable tube shocks. During resident-intruder testing 24 h later, both of these groups showed less defeat and received fewer bites than did an inescapably preshocked group but did not differ from a restrained nonshocked control group. These findings clearly indicate that stress controllability alters species-typical defensive responses, and their implications concerning other learned helplessness effects and interpretations are discussed.     

Reinstatement of fear to an extinguished conditioned context

Rats were shocked in the black but not the white compartment of a shuttlebox and then exposed to the black compartment in the absence of the shock unconditioned stimulus (US) to extinguish fear responses (passive avoidance). In five experiments, rats were then shocked in a reinstatement context (distinctively different from the shuttlebox) to determine the conditions that reinstate extinguished fear responding to the black compartment. Rats shocked immediately upon exposure to the reinstatement chamber failed to show either reinstatement of avoidance of the black compartment or fear responses (freezing) when tested in the reinstatement chamber. In contrast, rats shocked 30 sec after exposure to the reinstatement chamber exhibited both reinstatement of avoidance of the black compartment and freezing responses in the reinstatement chamber (Experiment 1). Rats shocked after 30 sec of exposure to the reinstatement chamber but then exposed to that chamber in the absence of shock failed to exhibit reinstatement of the avoidance response and did not freeze when tested in the reinstatement chamber (Experiment 2). Rats exposed to a signaled shock in the reinstatement chamber and then exposed to that chamber in the absence of shock also failed to exhibit reinstatement of the avoidance response (Experiment 5). These rats showed fear responses to the signal but not to the reinstatement chamber. Finally, rats exposed for some time (20 min) to the reinstatement chamber before shock exhibited reinstatement of the avoidance response but failed to freeze when tested in the reinstatement chamber (Experiments 3 and 4). These results are discussed in terms of the contextual conditioning (Bouton, 1994) and the US representation (Rescorla, 1979) accounts of postextinction reinstatement.     

Stimuli associated with the cancellation of food and its cues enhance eating but display negative incentive value

Initially neutral conditioned stimuli paired with food often acquire motivating properties, including serving as secondary reinforcers, enhancing instrumental responding in Pavlovian-instrumental transfer procedures, and potentiating food consumption under conditions of food satiation. Interestingly, cues associated with the cancellation of food and food cues may also potentiate food consumption (e.g., Galarce and Holland, 2009), despite their apparent negative correlations with food delivery. In three experiments with rats, we investigated conditions under which potentiation of feeding by such “interruption stimuIi” (ISs) develops, and some aspects of the content of that learning. Although in all three experiments ISs enhanced food consumption beyond control levels, they were found to act as conditioned inhibitors for anticipatory food cup entry (Experiment 1), to serve as conditioned punishers of instrumental responding (Experiment 2), and to suppress instrumental lever press responding in a Pavlovian instrumental transfer procedure (Experiment 3). Furthermore, when given concurrent choice between different foods, an IS enhanced consumption of the food whose interruption it had previously signaled, but when given a choice between performing two instrumental responses, the IS shifted rats’ choice away from the response that had previously yielded the food whose interruption had been signaled by IS (Experiment 3). Thus, the effects of an IS on appetitive responses were opposite to its effects on consummatory responding. Implications for our understanding of learned incentive motivation and the control of overeating are discussed.     

Stimulus control of behavior during the postreinforcement pause of FI schedules

Pigeons were given the opportunity to terminate certain segments of fixed intervals by pecking a control key. When 30-sec segments of negative and positive stimuli alternated across the interreinforcement interval (Experiment 1), most birds terminated a large proportion of negative segments. However, few control-key responses were made during the negative segment immediately following food presentation. Under schedules during which only one negative segment was programmed, during the first 30 sec of 1-min intervals (Experiment 2), control-key responses, when they occurred at all, were made after several seconds of the interval had elapsed. Similar findings were obtained when a peck on the control key merely changed the color on the food key (Experiment 3). These findings suggest that the post-reinforcement extinction state (Schneider, 1969) during fixed-interval schedules consists of two phases: an immediate postreinforcement inhibitory phase, followed by a second phase during which a control-key response may occur. These two phases and their associated behavior may be related to Staddon’s (1977) distinction between interim and facultative activities.     

Effects of contextual cues previously paired with footshock or illness on behavior and pain sensitivity in the rat

Rats were used in four experiments to study the effects on behavior and pain sensitivity of exposure to a context previously paired with footshock or injection of the emetic drug lithium chloride (LiCl). Exposure to a context previously paired with footshock or injection of LiCl provoked the species-typical defense response of freezing (Experiments 1A and 1B). Exposure to a context previously paired with footshock additionally produced hypoalgesia when rats were tested using the tailflick test (Experiment 1A). By contrast, exposure to a context previously paired with injection of LiCl produced hyperalgesia when rats were tested using the tailflick test (Experiment 1B). However, exposure to a context previously paired with injection of LiCl did provoke hypoalgesia when rats were tested for pain sensitivity using either the hotplate or formalin tests (Experiment 2), which was mediated by the release of endogenous opioid peptides (Experiment 3). These results are discussed with reference to the processes governing associative regulation of defensive behavior and pain control.     

The role of experimenter-odor cues in the performance of object-memory tasks by rats

Two experiments assessed whether odors left on stimulus objects by experimenters who handle them might confound the interpretation of ostensibly visually guided object-memory tasks for rats. In Experiment 1, rats were able to discriminate the relative recency with which an experimenter touched two otherwise identical objects (intertouch interval = 4 sec), presumably on the basis of an odorintensity discrimination. However, after the rats mastered the odor discrimination with no delay between when the second of the two stimulus objects was last touched by the experimenter and when the rats were permitted to attempt the discrimination, their performance dropped to chance levels when this delay was increased to 15 sec. In Experiment 2, rats were trained in two slightly different ways to perform a delayed-nonmatching-to-sample (DNMS) task, one that involved systematic differences in the temporal order in which the experimenter handled the sample and novel stimulus objects and one that did not. There were no significant differences in the rate at which rats mastered the DNMS task with these two procedures, and the performance of rats that were trained according to the former procedure was unaffected when they were switched to the latter procedure. Moreover, rats required considerably fewer trials to master the DNMS task than the rats in Experiment 1 required to master the odor discrimination. These findings demonstrate that, under certain circumstances, rats can discriminate the relative recency with which two objects are handled by an experimenter, but that this ability contributes little to their performance of conventional object-based DNMS tasks.     

Reinforced variation and selection

Long-Evans rats were reinforced for generating variable sequences of four left (L) and right (R) leverpress responses. If the current sequence, for example, LLRR, differed from each of the preceding five sequences, then a food pellet was provided. Otherwise, there was a brief time-out. After the rats were generating a variety of sequences, one sequence was concurrently reinforced whenever it occurred, that is, an “always-reinforced” contingency was superimposed. The frequency of that sequence increased significantly from the variable baseline (Experiment 1). The “difficulty” of the always-reinforced sequence influenced the extent to which its frequency increased—“easy” sequences increased greatly, but “difficult” ones increased not at all (Experiment 2, and a replication with pigeons in Experiment 3). However, when reinforcement for baseline variability was systematically decreased while a difficult sequence was always reinforced, that sequence slowly emerged and attained relatively high levels (Experiments 4 and 5). Thus, a technique for training even highly improbable, or difficult-to-learn, behaviors is provided by concurrent reinforcement of variation and selection.     

Second-order conditioned taste aversion in rats: Shared modality is not sufficient to promote an association between S2 and SI

Second-order conditioning (SOC) in pigeons, but not rats, appears to involve an association between the second-order stimulus (S2) and the first-order stimulus (SI). Nairne and Rescorla (1981) suggested it was the use of stimuli from the same modality that promoted an association between S2 and SI in pigeon SOC studies. In support of their hypothesis, they demonstrated that pigeons, like rats, did not form an association between S2 and SI when these stimuli were from different modalities. In this study, we sought to determine whether rats, like pigeons, would associate S2 with SI when these stimuli shared the same modality. Female Lister rats injected with LiCl after consuming .12M saline solution (SI) showed an aversion to a 15% sucrose solution (S2) that was subsequently paired with the saline. This was so regardless of whether S2 and SI had been presented sequentially (Experiment 1) or simultaneously (Experiment 2). Only in Experiment 2, however, did extinction of the aversion to saline diminish the aversion to sucrose; that is, employing stimuli from the same modality was not a sufficient condition, of itself, to allow rats to associate S2 with SI.     

Instrumental responses become associated with reinforcers that differ in one feature

In three experiments, thirsty rats were trained to make several instrumental responses whose outcomes differed in which of two relatively inconsequential flavor features they contained. In Experiment 1, one of the features was subsequently devalued by pairing it with lithium chloride; in Experiment 2, it was enhanced in value by pairing it with sucrose. In both experiments, differences in the value of the features resulted in parallel differences in the likelihood of the responses during a subsequent extinction test. In Experiment 3, the animals chose between these responses in the presence of discriminative stimuli that had signaled the occurrence of these different features following another response. The stimuli selectively augmented the likelihood of the response with which they shared training by the same-flavored consequence. These results indicate that rats can separately encode features that differ along one dimension, both in the association between an instrumental response and its outcome, and in the association between a discriminative stimulus and that outcome.