Dissociation between conditioned emotional response and extended avoidance performance

The present experiments examined the dissociation between the strength of a shuttlebox avoidance response (AR) and one index of fear of the avoidance CS. Avoidance response strength was indexed by resistance to extinction of the AR and by changes in response latency, and fear of the CS was indexed by the conditioned emotional response (CER) technique. Experiments 1, 2A, and 3A all found that rats trained to a criterion of 27 consecutive avoidance responses (CARs) showed response strength comparable or superior to rats trained to a criterion of 9 CARs. Experiments 2B and 3A demonstrated that rats trained to 27 CARs showed less suppression of bar pressing during the avoidance CS (less CER) than rats trained to 9 CARs. Experiment 3A also found that, when extinguished in the shuttlebox to a moderate criterion (5 consecutive trials without a response) before CER testing, rats trained to 9 CARs showed some, although not complete, loss of CER, whereas rats trained to 27 CARs showed no loss of CER. In Experiment 3B rats that took 1 vs 2 days to reach a criterion of 27 CARs were compared for their AR strength and for their CER. Although rats taking 2 days to reach criterion showed somewhat greater resistance to extinction of the AR than rats reaching criterion in 1 day, this variable had no apparent effect on the CER. Implications of the present results for current theories of avoidance learning are discussed.     

Acquisition and discrimination of appetitively and aversively conditioned heart rate responses in rhesus monkeys

This report describes the acquisition of a conditional heart rate response to both classical aversive and appetitive conditioning in eight rhesus monkeys(Macaca mulatta). The behavioral paradigm consisted of two discrete one minute tones followed by the corresponding unconditional stimuli,i.e., electric shock or Purina monkey chow. A third tone followed by neither food nor shock served as a discriminative stimulus (DS). The conditional heart rate responses developed in two phases. The first phase was characterized by similar responses to both conditional stimuli and the DS. Control heart rate rose during this period. During the second phase, control heart rate decreased (five animals), the DS response disappeared, and different conditional heart rate patterns to food and shock emerged. The existence of distinct conditional response patterns indicates probable differences in the autonomic nervous regulation of the heart during aversive and appetitive conditioning.     

Similarity of cardiac CR forms in the rhesus monkey during several experimental procedures

Cardiac rates of rhesus monkeys were observed in a variety of different conditioning procedures, each of which involved a visual stimulus (CS) followed by an electric shock (US). With a 30-sec CS, cardiac rate accelerated rapidly after CS onset, reached a maximum in the middle of CS, and decelerated thereafter, with a terminal CS rate often at the level of, or below, pre-CS levels. A similar biphasic cardiac rate response in CS was also observed under subsequent exposure to intermittent pairings of CS and US, avoidance of US, response-produced termination of US, and when CS-US pairings were superimposed upon an avoidance baseline, even when CS duration was varied from 12 to 60 seconds. The unusual regularity of cardiac rate responses in several different procedures may result from one or more of these factors: (a) characteristics of the rhesus monkey, (b) initial exposure to Pavlovian conditioning, or (c) the uniformity of measurement of cardiac rate employed in this study.     

Effect of posttrial episodes on conditioning in compound conditioned stimuli

The effect of signaled and nonsignaled posttrial episodes (PTEs) on conditioning to the target CS of a preceding compound CS-US trial was examined in two conditioned emotional response (CER) experiments with rats. Experiment 1 revealed that a nonsignaled PTE, a second shock US, interfered with conditioning to the preceding target CS and that the interference effect of the PTE was greater when it occurred 5 sec as opposed to 1,800 sec after the preceding compound CS-US trial. Experiment 2 revealed that if the shock PTE was signaled by a CS, its ability to interfere with conditioning was reduced. This second study also revealed that omission of an "expected" US interfered with conditioning to the target CS. The implications of these data for information processing models of Pavlovian conditioning are discussed.     

Transfer of conditioned appetitive stimuli to conditioned aversive excitatory and inhibitory stimuli

The transfer of Pavlovian appetitive stimuli to Pavlovian aversive stimuli was examined in three experiments. In Experiment 1, rats received appetitive (Ap) conditioning designed to establish a flashing-light stimulus as either a CS+, CSo, or CS? for food, or to maintain it as a novel stimulus for US-alone subjects. Then, the stimulus was employed as a signal for weak shock in conditioned-emotional-response (CER) training. Both acquisition and extinction results showed that the ApCS+ facilitated and the ApCS? retarded aversive excitatory conditioning relative to the ApCSo and US-alone controls. Experiment 2 replicated the findings of Experiment 1 with both a moderate and a severe shock in CER training. In Experiment 3, different groups received the same appetitive conditioning as before, but to a flashing-light stimulus which was then employed as a signal for no shock in CER training. The ApCS? facilitated and the ApCS+ retarded aversive inhibitory conditioning relative to ApCSo and US-alone controls. Collectively, these findings establish that, in Pavlovian conditioning, transfer of an appetitive CS to an aversive excitor or inhibitor is facilitated by maintaining the initial conditioning contingency.     

Reevaluation of things past

The ability of rats to reevaluate previously presented information in light of subsequently provided information was evaluated using a CER (conditioned emotional response) procedure. In Experiment 1, rats suppressed responding to a compound light + tone stimulus that was repeatedly paired with shock. Groups of rats were then presented with only one element of the compound (the tone), either presented alone or paired with shock, for 15 days. During this 15-day period, two control groups received trials with the shock alone or neither stimulus nor shock. All of the rats were then tested with the other element of the compound (the light). Rats that had received the tone paired with shock during the intervening training continued to suppress to the light, whereas rats that had received the tone alone showed rapid extinction of the CER to light. The control groups showed that this effect was not due to the number of shock presentations received. A subsequent experiment also demonstrated that these results were not due to nonspecific stimulus effects. Apparently, a subsequent change in the associative strength of one element results in a similar change to the other element of a previously established compound stimulus.     

Cardiac pacing and the law of initial value in rhesus monkeys

A cardiac pacemaker was used to produce a wide range of pre-CS heart rates in Pavlovian conditioning, and correlations were computed between pre-CS and CS heart rates. Two rhesus monkeys were presented trials in which 30 sec of light (CS) was followed by a brief electric shock (UCS). Pacing rates during the inter-trial intervals were varied from 150 to 350 bpm. Pacing was discontinued during CS. Unpaced control sessions showed that the maximum heart rate in CS on each trial was proportional to the pre-CS heart rate. Following pacing, however, heart rate in CS did not depend on the pacing rate; rather, the rates were not different from those of the unpaced control sessions. Pacing at high rates shifted the maximum heart rate toward the end of CS.     

The heart rate component of the social reflex in dogs: The conditional effects of petting and person

Five dogs were given a 480-cps tone followed by shock for more than 200 trials. A 200-cps tone was then introduced followed by a person petting the dog at the end of the conditional signal (CS) for 50 trials. Finally, the 480-cps tone-shock (T-S) sequence was reintroduced for five trials, after which the person entered the experimental room and stood beside the dog during one additional T-S sequence. It was observed that both the heart rate (HR) increase to shock, and the HR decrease to petting could be conditioned rapidly (1–5 trials). These findings are discussed in terms of the theory of stimulus substitution in classical HR conditioning. After the person had been made part of a CS for petting, and the T-S sequence reintroduced, the HR increase during the CS was reduced. The HR response to the shock, however, was greater than the response to this US when the dog was alone. A control group, given the same T-S sequence with a person present who had not been a CS for petting, did not show any significant HR changes from the usual response given to the T-S sequence. It is emphasized that these findings, in conjunction with earlier reports, indicate that the cardiovascular system may be a valuable index in studying the psychophysiology of socialization processes.     

Preconditioning exposure to the unconditined stimulus affects the acquisition of a conditioned emotional response

Four experiments examined the UCS preexposure phenomenon using conditioned suppression of food-reinforced responding as a measure of excitatory conditioning, and electric shock as a UCS. In Experiment 1, groups of rats were preexposed to unsignaled 0.8-mA electric shocks for 0, 1, 3, 5, or 10 days, and then conditioned with a 0.8-mA electric shock. Preexposure to electric shock 1 day prior to conditioning enhanced the acquisition of a CER, whereas preexposure to electric shock for 3, 5, or 10 days prior to conditioning attenuated the acquisition of a CER as a direct function of the number of days of preexposure. In Experiments 2 and 2A, groups of rats were preexposed to unsignaled electric shocks of 0.3, 0.5, 0.8, or 1.3 mA for 10 days, and then conditioned with a 0.8-mA electric shocl. All groups preexposed to electric shock acquired the CER at a slower rate than a group not preexposed to electric shock. The greatest attenuation of CER conditioning occurred when the same intensity electric shock was used during both the preexposure and conditioning phases. In Experiment 3, groups of rats were preexposed to signaled electric shocks of either 0.5, 0.8, or 1.3 mA, and then conditioned with a 0.8-mA electric shock. All groups preexposed to electric shock acquired the CER at a slower rate than a group not preexposed to electric shock. As in Experiments 2 and 2A, the greatest attenuation of CER conditioning occurred when the same intensity electric shock was used during both the preexposure and conditioning phases. In Experiment 4, groups of rats were preexposed to series of 0.5, 0.8, or 1.3-mA electric shocks which they could escape by performing a chain-pull response. Rats in each of these groups had yoked partners which received the same number, intensity, and temporal pattern of electric shocks, but could not perform a response to escape shock. All groups were then conditioned with a 0.8-mA electric shock. Rats preexposed to escapable electric shocks showed equal or greater attenuation of CER conditioning than rats which could not escape shock during the preexposure phase. These results are discussed in terms of nonassociative and associative explanations of the UCS preexposure phenomenon.     

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.     

Localized intracaudate dopamine D2 receptor activation during the post-training period improves memory for visual or olfactory conditioned emotional responses in rats.

Rats with cannulas aimed at the posteroventral (PV) or ventrolateral (VL) areas of the caudate nucleus were trained on a conditioned emotional response (CER) task. Post-training microinjections of the indirect catecholamine agonist, d-amphetamine (5 micrograms), or of the dopamine D2 receptor agonist, LY171555 (1 microgram), into the PV area improved retention of a CER with a visual CS, but had no effect on a CER with an olfactory CS. Post-training injections of the same two drugs into the VL area improved retention of a CER with an olfactory CS, but had no effect on a CER with a visual CS. Post-training injections of the dopamine D1 receptor agonist, SKF38393 (0.5, 1.0, 2.0 micrograms), into either site had no effects on either CER. These findings suggest that different areas of the caudate nucleus mediate acquisition of CERs with different CSs, possibly implicating the topographically organized corticostriatal innervation in the acquisition of certain types of memories in the caudate nucleus. The findings also suggest that dopamine D2 receptors in the caudate nucleus are involved in the acquisition of these CERs.     

Hippocampal associative cellular responses: dissociation with behavioral responses revealed by a transfer-of-control technique

Multiunit activity was recorded in the CA3 field of the dorsal hippocampus in freely moving rats during classical conditioning and subsequent presentation of the CS on operant baselines for food reward as well as shock avoidance. Rats were first trained in a nonsignaled bar-pressing-dependent shock omission task and in a food-motivated lever-pressing task (60-s VI). Five sessions with presentations of a previously habituated tone as a CS paired with footshock as a US were then given. Testing was carried out by presenting the CS alone while behavioral responses were maintained by reinforcement in both instrumental tasks on alternate sessions. As expected, the CS induced a marked suppression of lever pressing for food reward and a marked enhancement of bar-pressing for shock avoidance. The analysis of the frequency of multiunit discharges to the CS revealed that the hippocampal cellular responses established during classical conditioning were maintained while two different behavioral responses were exhibited to the CS. The results showed that the associative response of hippocampal neurons may be dissociated from the Pavlovian conditioned responses the CS elicits. They support the hypothesis that hippocampal cellular responses represent a neural index of the acquired CS-US associative representation.     

Mechanisms of blocking by contextual stimuli

The influence of contextual stimuli on the conditioning and performance of responding to a discrete stimulus was examined in the US preexposure paradigm using both context shift manipulations and a measure of context conditioning. Four groups of rats received both repeated exposure to an electric shock US in one context (Context 1), and repeated nonshocked exposure to a second context (Context 2). Two additional groups of rats received exposure to these contexts, but never received shock presentations. Rats exposed to shock learned to escape from the stimuli of Context 1, but did not escape from the stimuli provided by Context 2. Rats not exposed to shock failed to escape from either context. All rats then received a single CER conditioning session in which four pairings of a 3-min noise CS and shock US were presented. Half the rats received those CS-US pairings in the excitatory Context 1, while the remaining rats received those pairings in the neutral Context 2. Finally, half the rats in each of the CER conditioning treatments received extinction test trials of the noise CS in Context 1, while the remaining rats received those test trials in Context 2. Thus, this design factorially manipulated the presence of excitatory or neutral contextual stimuli during both conditioning and testing of a discrete CS. In comparison with the two groups of rats never preexposed to shock alone, attenuation in acquisition of conditioned suppression observed during test trials occurred only when CER conditioning had been administered in the excitatory Context 1, and this effect was manifested when testing occurred in either the excitatory Context 1 or the neutral Context 2. These results support the model of R. A. Rescorla and A. R. Wagner (1972) (in A. H. Black & W. F. Prokasy (Eds.) Classical Conditioning II, pp. 64–99, New York: Appleton-Century-Crofts) which asserts that contextual stimuli and sicrete CSs compete for limited associative strength supportable by a given US.     

Dissociative effects of different types and amounts of nonreinforced CS exposure on avoidance extinction and the CER

Two experiments examined the effectiveness of two amounts of flooding or response-prevention on hastening avoidance response extinction and on reducing CS-produced suppression of bar-pressing for food. In Experiment 1, 20 and 30 flooding trials were both shown to be effective in hastening the extinction of a well-learned shuttlebox avoidance response. In Experiment 2, rats trained under comparable conditions to those in Experiment 1 were tested following flooding for the CER in a different apparatus. The results indicated that 30, but not 20, flooding trials were sufficient to reduce the CER. In each experiment the results of additional control groups equated with the flooded groups for nonreinforced CS exposure also revealed a dissociation between the effectiveness of this CS time control procedure in hastening avoidance response extinction and in reducing the CER. Further comparisons showed that although 30 flooding trials did reduce the CER, the same total duration of nonreinforced CS Exposure in the form of avoidance extinction trials did not. Thus the context in which CS exposure occurs may affect the dynamics of extinction of the CER. The experiments are discussed in the broader context of dissociation of various indices of fear in humans.     

The discriminative control of free-operant avoidance despite exposure to shock during the stimulus correlated with nonreinforcement

Four rats were trained in darkness on a free-operant avoidance procedure in which shocks occurred randomly, but lever presses could reduce their frequency. Discrimination training followed, during which responses in light continued to reduce shock frequency, but responses in darkness had no effect. During each cycle, the light period was 4 min, while darkness lasted only until a 20-sec interval had elapsed without a response. This no-response requirement was increased to 40 sec for three animals and eventually to 60 sec for two of them. Discriminative control developed, despite a greater shock density in the dark, with response rate and number of responses per shock maintained or increasing during light and decreasing to very low values in darkness. Two animals were later exposed to a procedure in which shock density was unaffected by responding either in light or darkness. A 60-sec no-response requirement was continued in the dark. Discriminative control persisted through 42 sessions for one animal and required 45 sessions to approach extinction for the other animal. The role of the light as a potential conditioned reinforcer of other behavior in the dark was implicated in the development and persistence of discriminative control. These data support shock-frequency reduction as reinforcement for avoidance behavior.     

Medial auditory thalamic input to the lateral pontine nuclei is necessary for auditory eyeblink conditioning

Auditory and visual conditioned stimulus (CS) pathways for eyeblink conditioning were investigated with reversible inactivation of the medial (MPN) or lateral (LPN) pontine nuclei. In Experiment 1, Long-Evans rats were given three phases of eyeblink conditioning. Phase 1 consisted of three training sessions with electrical stimulation of the medial auditory thalamic nuclei (MATN) paired with a periorbital shock unconditioned stimulus (US). An additional session was given with a muscimol (0.5 μL, 10 mM) or saline infusion targeting the LPN followed by a recovery session with no infusions. The same training and testing sequence was then repeated with either a tone or light CS in phases 2 and 3 (counterbalanced). Experiment 2 consisted of the same training as Experiment 1 except that muscimol or saline was infused in the MPN during the retention tests. Muscimol infusions targeting the LPN severely impaired retention of eyeblink conditioned responses (CRs) to the MATN stimulation and tone CSs but only partially reduced CR percentage to the light CS. Muscimol infusions that targeted the MPN had a larger effect on CR retention to the light CS relative to MATN stimulation or tone CSs. The results provide evidence that the auditory CS pathway necessary for delay eyeblink conditioning includes the MATN-LPN projection and the visual CS pathway includes the MPN.     

Learned fear of "unseen" faces after Pavlovian, observational, and instructed fear

This study compared fear learning acquired through direct experience (Pavlovian conditioning) and fear learning acquired without direct experience via either observation or verbal instruction. We examined whether these three types of learning yielded differential responses to conditioned stimuli (CS+) that were presented unmasked (available to explicit awareness) or masked (not available to explicit awareness). In the Pavlovian group, the CS+ was paired with a mild shock, whereas the observational-learning group learned through observing the emotional expression of a confederate receiving shocks paired with the CS+. The instructed-learning group was told that the CS+ predicted a shock. The three groups demonstrated similar levels of learning as measured by the skin conductance response to unmasked stimuli. As in previous studies, participants also displayed a significant learning response to masked stimuli following Pavlovian conditioning. However, whereas the observational-learning group also showed this effect, the instructed-learning group did not.     

Counterconditioning of appetitive and defensive CRs in rabbits

Two experiments examined interactions between conditioned appetitive and defensive responses in the rabbit. In Experiment I, a conditioned jaw-movement response was established by following presentations of a clicker CS with intra-oral sucrose delivery on 50% of trials. The jaw-movement response was then maintained on this partial reinforcement schedule during a counterconditioning phase. A group which received para-orbital shock paired with the CS on non-sucrose trials showed acquisition of eyeblink responding and suppression of jaw-movement responding to the CS, in comparison to control groups which received either no shock or unpaired presentations of the CS and shock. Experiment II was identical in design to Experiment I except that the roles of the sucrose and shock reinforcers were reversed. The paired group acquired a conditioned jaw-movement response when sucrose was added in the counterconditioning phase, but in contrast to Experiment I showed a slight enhancement of the previously established eyeblink response. The asymmetry of appetitive and defensive counterconditioning was discussed in relation to opponent-process theories of motivation and reinforcement.     

Brain Indices of Nonconscious Associative Learning

Using a classical conditioning technique, this study investigated whether nonconscious associative learning could be indexed by event-related brain activity (ERP). There were three phases. In a preconditioning baseline phase, pleasant and unpleasant facial schematics were presented in awareness (suprathreshold). A conditioning phase followed, in which stimuli were presented outside awareness (subthreshold, via energy masking), with an unpleasant face (CS+) linked to an aversive shock and a pleasant face (CS−) not linked to a shock. The third, postconditioning phase, involved stimulus presentations in awareness (suprathreshold). Evidence for acquisition of a conditional response was sought by comparing suprathreshold pre- and postconditioning phases, as well as in the subthreshold conditioning phase itself. For the pre-postconditioning phase analyses, significant ERP component differences differentiating CS+ and CS− were observed for N1, P2, and especially P3. For the conditioning phase, significant differences were observed in the 100–400 ms. post-stimulus region reflecting a CS+ processing negativity. Brain activity does indeed index the acquisition of a conditional response to subthreshold stimuli. Associative learning can occur outside awareness.     

Pavlovian conditioning of distinct components of Hermissenda's responses to rotation

In two experiments with the nudibranch mollusk Hermissenda, distinct characteristics of conditioned and unconditioned responses to high-speed orbital rotation were examined. In Experiment 1, two principle unconditioned responses to rotation were identified, namely, reduced rate of locomotion and contraction of the foot. The magnitude of the foot contraction increased throughout a 20-s period of rotation, whereas locomotion was reduced immediately after the onset of the rotation and was maintained at this constant low rate throughout the stimulus presentation. These divergent response patterns suggest that the two responses emerge independently. In Experiment 2, a classical conditioning procedure was employed in which a light (CS) was paired with the rotation (US) employed in Experiment 1. In a subsequent test, it was found that the light had acquired the capability to evoke both foot contraction and decreased locomotion. Although the magnitude of these conditioned responses was reduced relative to the corresponding unconditioned response, the patterns of responding were virtually identical; that is, foot contraction developed gradually whereas locomotion decreased immediately. In contrast, animals that received unpaired presentations of the light and rotation, light alone, or no prior exposure to those stimuli exhibited foot extension in response to the light. These results illustrate a transfer of some of the response-evoking properties of the US to the CS as a result of conditioning, as well as the emergence of two independent conditioned responses. Moreover, these results suggest modulation of at least two distinct motor pathways as a function of learning.