Classical aversive conditioning of catecholamine and corticosterone responses

Some earlier work, not rigorously controlled, suggested that conditional increases in sympathoadrenal stress hormones could occur. The purpose of this experiment was to test this idea further using an appropriately controlled design. To do this, we subjected rats living in a tether-type apparatus to differential fear conditioning. Chronic catheterization allowed us to sample blood before and after conditional stimulus probes without having to touch the rats. No evidence for conditional changes in norepinephrine and corticosterone was found. In contrast, differential conditioning of epinephrine responses was found. The conditional response, however, was not a simple one in that conditional increases in epinephrine following CS+ probes were not always seen. These data support the idea that learned changes in hormonal stress respondents can occur. But they leave open the question of why clear cut conditional changes in these visceral systems are so difficult to obtain.     

Reinstatement of fear responses in human aversive conditioning

The treatment of choice for a number of anxiety disorders is exposure therapy. However, successful reduction of fear through exposure is sometimes followed by a (partial) return of symptoms of fear (return of fear, ROF; Clin. Psychol. Rev. 9 (1989) 147). Several possible learning mechanisms have been suggested to explain ROF (e.g. mechanisms related to spontaneous recovery, renewal, reacquisition and reinstatement). The present study focuses on reinstatement, which refers to the observation that mere US-only presentations can 'reinstate' previously extinguished fear responses. Although animal research has repeatedly demonstrated this phenomenon, little is known about fear reinstatement in humans. The present study employed a differential aversive conditioning procedure: after acquisition and a subsequent extinction procedure, a series of four unpredicted US-only trials was scheduled in the reinstatement group. The control group did not receive additional US presentations. A significant reinstatement effect was observed for US-expectancy ratings and fear ratings in the reinstatement group, but not in the control group. No differences were observed in a reaction time measure of resource allocation to the conditioned stimuli. These findings constitute a first demonstration of reinstatement of conditioned fear responses in humans. Implications for exposure treatment and suggestions for future research are discussed.     

Classical conditioning of beginning reading responses

The present study describes the first demonstration that laboratory-controlled experimental procedures can lead to the successful acquisition and subsequent retention of classically conditioned beginning reading responses (CCBRRs) in children of both sexes and mean age of 4 yr. Anticipatory instructions combined with higher-order classical conditioning temporally arranged into a trace conditioning paradigm presented for 10 trials for each response to be learned led to beginning reading responses being successfully acquired by 20 children during 95% of the 2,220 total acquisition learning trials and subsequently correctly recalled on 114 of the 222 retention test trials. Findings support the view that perhaps the relatively sudden and sustained acquisition learning curves for reading responses on the second-signalling-system level of behavior in the present study may be quite different from the relatively slow and incremental learning curves usually obtained in classical conditioning of the autonomic type which occur on the first-signalling-system level.     

Differential preparatory cardiovascular responses to aversive and appetitive behavioral conditioning

Dogs were required to press a response panel either to avoid shock or obtain food. During a one-hour interval immediatelypreceding performance on the avoidance task, blood pressure increased while heart rate decreased. In contrast, both blood pressure and heart rate increased during the one-hour interval immediatelypreceding performance on the food task. During both the shock-avoidance and food performancesper se, however, elevations in heart rate and blood pressure were observed, though the avoidance task produced less consistent heart rate changes. These effects were observed (1) with different individual dogs on each of the two training procedures, and (2) with the same dogs exposed successively to both aversive and appetitive behavioral conditioning.     

Classical aversive conditioning of heart rate in curarized rats at different blood gas levels

In an effort to examine whether normal blood gas tensions were essential for conditioning, paralyzed rats received a classical aversive heart rate (HR) conditioning session while respirated at different peak expired CO₃ values. After the session, arterial blood was drawn for analysis. That peak expired CO₂ was effective in manipulating Pco₂ was indicated by a significant correlation (r = 0.594, df = 17, P < 0.05). In addition, only rats with blood gas values similar to those of anesthetized controls displayed a discriminated HR CR. These animals also had lower baseline HRs and greater HR variability. Further, 7 of the 9 rats with normal blood gas values were respirated at peak expired CO₂ values from 5.0–5.1 per cent, and no animal ventilated within this range displayed abnormal values. These findings suggest that previous difficulties in obtaining classical and operant conditioning in paralyzed animals may, in part, be attributable to inadequate ventilation.     

Sign-tracking in aversive conditioning

Two experiments were conducted to determine if rats tend to avoid contact with a stimulus that signals the occurrence of shock and contact a stimulus that signals the nonoccurrence of shock. The conditioned stimulus was a 60-sec platform presentation, and the unconditioned stimulus was a 2-sec inescapable shock. In each experiment, the emphasis was on two types of Pavlovian pairings: forward pairing in which each platform presentation was followed by shock, and backward pairing in which each platform presentation was preceded by shock and followed by a lengthy shock-free interval. Experiment 1 showed that in comparison with Random and CS-only procedures, the backward procedure produced a significant increase in approach and contact with the platform, but the forward procedure failed to produce a significant decrease in contact with the platform. Experiment 2, in which all groups were roughly equated for baseline levels of platform preference, demonstrated strong effects of both forward and backward conditioning. The experiments provide evidence for an aversive sign-tracking system in which animals' tendencies to withdraw from or approach and contact a platform CS are determined by the Pavlovian contingencies which render it a reliable signal for the occurrence or nonoccurrence of shock.     

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.     

Classical conditioning of eyelid and mystacial vibrissae responses in conscious mice

The murine vibrissae sensorimotor system has been scrutinized as a target of motor learning through trace classical conditioning. Conditioned eyelid responses were acquired by using weak electrical whisker-pad stimulation as conditioned stimulus (CS) and strong electrical periorbital stimulation as unconditioned stimulus (US). In addition, conditioned vibrissal protraction was obtained pairing either weak electrical whisker-pad stimulation or a tone as CS, with a strong electric shock delivered in the whisker-pad as US. This finding suggests that evolutionary pressure has selected a sensorimotor system capable of constructing conditioned responses on the basis of temporal relationships of stimuli, independently of any putative functional purpose.     

Classical conditioning of autonomic fear responses is independent of contingency awareness

The role of contingency awareness in classical conditioning experiments using human subjects is currently under debate. This study took a novel approach to manipulating contingency awareness in a differential Pavlovian conditioning paradigm. Complex sine wave gratings were used as visual conditional stimuli (CS). By manipulating the fundamental spatial frequency of the displays, we were able to construct pairs of stimuli that varied in discriminability. One group of subjects was given an "easy" discrimination, and another was exposed to a "difficult" CS+ and CS-. A 3rd group was exposed to a stimulus that was paired with the unconditional stimulus (UCS) 50% of the time and served as a control. Skin conductance response (SCR) and continuous UCS expectancy data were measured concurrently throughout the experiment. Differential UCS expectancy was found only in the easy discrimination group. Differential SCRs were found in the easy discrimination group as well as in the difficult discrimination group, but not in the 50% contingency control. The difficult discrimination group did not exhibit differential UCS expectancy but did show clear differential SCR. These observations support a dual process interpretation of classical conditioning whereby conditioning on an implicit level can occur without explicit knowledge about the contingencies. The role of contingency awareness in classical conditioning experiments using human subjects is currently under debate. This study took a novel approach to manipulating contingency awareness in a differential Pavlovian conditioning paradigm. Complex sine wave gratings were used as visual conditional stimuli (CS). By manipulating the fundamental spatial frequency of the displays, we were able to construct pairs of stimuli that varied in discriminability. One group of subjects was given an "easy" discrimination, and another was exposed to a "difficult" CS+ and CS-. A 3rd group was exposed to a stimulus that was paired with the unconditional stimulus (UCS) 50% of the time and served as a control. Skin conductance response (SCR) and continuous UCS expectancy data were measured concurrently throughout the experiment. Differential UCS expectancy was found only in the easy discrimination group. Differential SCRs were found in the easy discrimination group as well as in the difficult discrimination group, but not in the 50% contingency control. The difficult discrimination group did not exhibit differential UCS expectancy but did show clear differential SCR. These observations support a dual process interpretation of classical conditioning whereby conditioning on an implicit level can occur without explicit knowledge about the contingencies.     

Classical conditioning of human ‘evaluative’ responses

Human behaviour includes an important component which may conveniently be called evaluative. Using postcard reproductions as stimulus materials, 10 volunteer subjects selected the two pictures most liked and the two most disliked. These were then used as UCSs with appropriate controls from the neutral category. The conditioning hypothesis—that a neutral stimulus followed by a positively or negatively valued stimulus will acquire the evaluative weight of the second stimulus—was supported at a highly statistically significant level. The effect of negative evaluation was demonstrably stronger than that for positive evaluation, a result consistent with our knowledge of aversive conditioning. The possibility is discussed that evaluation of the UCS by the subject, shown to be a sufficient condition for learning, may also be the only necessary condition. This would imply a model of conditioning based on affective evaluation rather than on response production.     

Hedonic and nucleus accumbens neural responses to a natural reward are regulated by aversive conditioning

The nucleus accumbens (NAc) plays a role in hedonic reactivity to taste stimuli. Learning can alter the hedonic valence of a given stimulus, and it remains unclear how the NAc encodes this shift. The present study examined whether the population response of NAc neurons to a taste stimulus is plastic using a conditioned taste aversion (CTA) paradigm. Electrophysiological and electromyographic (EMG) responses to intraoral infusions of a sucrose (0.3 M) solution were made in naïve rats (Day 1). Immediately following the session, half of the rats (n = 6; Paired) received an injection of lithium chloride (0.15 M; i.p.) to induce malaise and establish a CTA while the other half (n = 6; Unpaired) received a saline injection. Days later (Day 5), NAc recordings during infusions of sucrose were again made. Electrophysiological and EMG responses to sucrose did not differ between groups on Day 1. For both groups, the majority of sucrose responsive neurons exhibited a decrease in firing rate (77% and 71% for Paired and Unpaired, respectively). Following conditioning, in Paired rats, EMG responses were indicative of aversion. Moreover, the majority of responsive NAc neurons now exhibited an increase in firing rate (69%). Responses in Unpaired rats were unchanged by the experience. Thus, the NAc differentially encodes the hedonic value of the same stimulus based on learned associations.Our search for sustenance and pleasurable stimuli is often balanced by our desire to avoid punishment and harm. Similarly, neural systems responsible for generating approach behavior must be countered by signals that suppress approach behavior under contexts where approach is dangerous or maladaptive (Hoebel et al. 2007). The nucleus accumbens (NAc) is acutely involved in food intake and goal-directed, approach behavior. Pharmacological manipulations of the NAc promote food intake even in sated rats (Maldonado-Irizarry and Kelley 1995; Stratford and Kelley 1997). Lesions or inactivation of the NAc impair conditioned approach behavior (Cardinal et al. 2002; Blaiss and Janak 2009). Interestingly, drugs that lead to inhibition of select regions of the NAc increase positive hedonic responses to palatable taste solutions (Pecina and Berridge 2005). Recordings from individual NAc neurons have mirrored these findings. We and others have shown that consumption of palatable food stimuli is associated with decreases in the firing rate of the majority of responsive NAc neurons (Nicola et al. 2004b; Roitman et al. 2005; Taha and Fields 2005; Wheeler et al. 2008). In addition, decreases in NAc neural activity are associated with bouts of licking behavior for palatable stimuli (Taha and Fields 2006), and disruption of these decreases halt feeding bouts (Krause et al. 2010). Finally, decreases in NAc neural activity are associated with preferred locations previously paired with drug reward (German and Fields 2007). Thus, decreases in NAc activity appear to be closely linked to positive hedonic stimuli, stimuli that have been explicitly paired with them and behavioral approach.The NAc is also responsive to aversive stimuli (Carlezon and Thomas 2009; Levita et al. 2009). The delivery of aversive taste stimuli to rats is associated with increases in the firing rate of the majority of responsive NAc neurons (Roitman et al. 2005; Wheeler et al. 2008). In addition to responding to primary appetitive and aversive taste stimuli, NAc neurons develop responses to predictors of reward and aversion. Individual NAc neurons selectively encode cues that predict either appetitive (Roitman et al. 2005; Day et al. 2006) or aversive (Roitman et al. 2005) stimuli following purely Pavlovian conditioning or a combination of instrumental and Pavlovian conditioning (Setlow et al. 2003; Nicola et al. 2004a). NAc neurons come to encode departure from locations not associated with reward with the majority response being that of excitation (German and Fields 2007). Thus, NAc neurons appear to encode aversive stimuli and withdrawal behavior with increases in activity. These and other findings have led to the recent postulation that reward and aversion are differentially encoded by the activity of NAc neurons (Carlezon and Thomas 2009).Data supportive of the activity hypothesis (Carlezon and Thomas 2009) have been generated by the use of different stimuli to serve as appetitive or aversive primary or predictive stimuli. Thus, selective encoding could be biased by the sensory properties of each stimulus rather than their hedonic valence. When a novel, palatable taste is paired with visceral malaise, a Pavlovian association is made and a conditioned taste aversion (CTA) is established. Subsequent exposure to the once palatable stimulus is met with avoidance or aversion and rejection (Garcia et al. 1974; Schafe et al. 1995). Thus, the same taste stimulus can either be appetitive or aversive, depending on Pavlovian associations. Here, individual NAc neurons were recorded in rats (Paired) before (Day 1) and after a CTA (Day 5) was established and compared with rats that received equal exposure to the same stimuli but in an unpaired manner (Unpaired), and hence no CTA developed. Simultaneously, oro-motor behavior was characterized to provide an index of the associative strength of the taste stimulus. Using this paradigm, we determined that the population response of the NAc does indeed encode hedonic valence.     

An aversive conditioning unit for ants

An apparatus is described for studying aversive conditioning in ants. The aversive stimulus is mechanically produced vibration. Responses are recorded automatically by an infrared photocell system.