Learning strategies during fear conditioning

This paper describes a model of fear learning, in which subjects have an option of behavioral responses to impending social defeat. The model generates two types of learning: social avoidance and classical conditioning, dependent upon (1) escape from or (2) social subordination to an aggressor. We hypothesized that social stress provides the impetus as well as the necessary information to stimulate dichotomous goal-oriented learning. Specialized tanks were constructed to subject rainbow trout to a conditioning paradigm where the conditioned stimulus (CS) is cessation of tank water flow (water off) and the unconditioned stimulus (US) is social aggression from a larger conspecific. Following seven daily CS/US pairings, approximately half of the test fish learned to consistently escape the aggression to a neutral chamber through a small escape hole available only during the interaction. The learning curve for escaping fish was dramatic, with an 1100% improvement in escape time over 7 days. Fish that did not escape exhibited a 400% increase in plasma cortisol and altered brain monoamine response to presentation of the CS alone. Elevated plasma cortisol levels represent classical fear conditioning in non-escaping fish, while a lack of fear conditioning and a decreased latency to escape over the training period in escapers indicates learned escape.     

A reappraisal of successive negative contrast in two populations of domestic dogs

When an anticipated food reward is unexpectedly reduced in quality or quantity, many mammals show a successive negative contrast (SNC) effect, i.e. a reduction in instrumental or consummatory responses below the level shown by control animals that have only ever received the lower-value reward. SNC effects are believed to reflect an aversive emotional state, caused by the discrepancy between the expected and the actual reward. Furthermore, how animals respond to such discrepancy has been suggested to be a sign of animals’ background mood state. However, the occurrence and interpretation of SNC effects are not unequivocal, and there is a relative lack of studies conducted outside of laboratory conditions. Here, we tested two populations of domestic dogs (24 owned pet dogs and 21 dogs from rescue kennels) in a SNC paradigm following the methodology by Bentosela et al. (J Comp Psychol 123:125–130, 2009), using a design that allowed a within-, as well as a between-, subjects analysis. We found no evidence of a SNC effect in either population using a within- or between-subjects design. Indeed, the within-subjects analysis revealed a reverse SNC effect, with subjects in the shifted condition showing a significantly higher level of response, even after they received an unexpected reduction in reward quality. Using a within-, rather than a between-, subjects design may be beneficial in studies of SNC due to higher sensitivity and statistical power; however, order effects on subject performance need to be considered. These results suggest that this particular SNC paradigm may not be sufficiently robust to replicate easily in a range of environmental contexts and populations.     

Learning in cod (Gadus morhua): long trace interval retention

Basic knowledge about learning capacities and awareness in fish is lacking. In this study we investigated which temporal gaps Atlantic cod could tolerate between two associated events, using an appetitive trace-conditioning paradigm with blinking light as conditioned stimulus (CS) and dry fish food as unconditioned stimulus (US). CS–US presentations were either temporally overlapping (delay conditioning, CS duration 24 s, interstimulus interval 12 s) or separated by 20, 60, or 120 s (trace conditioning, CS duration 12 s) or 2 h (control, CS duration 12 s). The percentage of fish in the feeding area increased strongly during CS presentation in all delay, 20 s, and 60 s trace groups and in one out of two 120 s trace groups, but not in the control groups. In the 20 and 60 s trace procedures, the fish crowded together in the small feeding area during the trace interval, showing strong anticipatory behaviour. In all the conditioned groups, the fish responded to the CS within eight trials, demonstrating rapid learning. At 88 and 70 days after the end of the conditioning experiments, the delay and 20 s trace groups, respectively, were presented the CS six times at 2-h intervals without reward. All groups responded to the light signal, demonstrating memory retention after at least 3 months. This study demonstrates that Atlantic cod has an impressively good ability to associate two time-separated events and long time retention of learnt associations.     

Learning and memory in the Port Jackson shark,Heterodontus portusjacksoni

Basic understanding of the fundamental principles and mechanisms involved in learning is lacking for elasmobranch fishes. Our aim in this study was to experimentally investigate the learning and memory capacity of juvenile Port Jackson sharks, Heterodontus portusjacksoni. Sharks (N = 30) were conditioned over a 19-day period to associate an underwater LED light or stream of air-bubbles [conditioned stimulus (CS)] with a food reward [unconditioned stimulus (US)], using three procedures (delay, trace and control). During experiments, the CS signalled at a random time between 180 and 300 s for 30 s (six times per day). For the delay the US overlapped in time with the CS, for the trace the US delivered 10 s after the CS and for our control the US was delivered at random time between 180 and 300 s after the CS. H. portusjacksoni sharks trained in all procedures improved consistently in their time to obtain food, indicative of Pavlovian learning. Importantly, the number of sharks in the feeding area 5 s prior to CS onset did not change over time for any procedures. However, significantly more sharks were present 5 s after CS onset for delay for both air-bubble and light CS. Sharks trained in the delay and trace procedures using air-bubbles as the CS also displayed significantly more anticipatory behaviours, such as turning towards the CS and biting. Sharks trained with the light CS did not exhibit such behaviours; however, trace procedural sharks did show a significant improvement in moving towards the CS at its onset. At 20 and 40 days after the end of the conditioning experiments, some sharks were presented the CS without reward. Two sharks trained in the delay procedure using air-bubbles as the CS exhibited biting behaviours: one at 20 and the other at 40 days. This study demonstrates that H. portusjacksoni have the capacity to learn a classical conditioning procedure relatively quickly (30 trials during 5 days) and associate two time-separated events and retention of learnt associations for at least 24 h and possibly up to 40 days.     

The impact of non‐aggressive behaviour early in aggressive interactions: Sex differences in direct and indirect aggression in response to provocation

Using an adapted form of the Taylor competitive reaction time task (TCRT: Taylor, 1967), we examined the effect of initially non‐aggressive behaviour during aggressive encounters. Specifically, if a person is initially non‐aggressive, but becomes more aggressive later, does an opponent respond more or less aggressively in response? Participants (N = 148) played a competitive reaction time task against a bogus partner, who was either initially non‐aggressive, or initially moderately aggressive, and then delivered increasingly loud noise blasts to participants on trials when the participant lost. Both direct (noise blasts delivered to the partner) and indirect aggression (damage to partner's reputation) were assessed. The impact of whether or not participants expected to meet the partner on direct and indirect aggression was also examined. All participants reduced their direct aggression towards an initially non‐aggressive partner and a partner they expected to meet. However, for females, the switch from initial non‐aggression to later aggression generated a negative evaluation of the partner, exhibited by indirect but not direct aggression.     

Heart rate reactivity in attention deficit disorder subgroups.

Beat-to-beat heart rate (HR) was analyzed for 9 contiguous seconds in a warned reaction time (RT) paradigm. Imperative stimuli were tones of three intensity levels (55, 78, and 100 db); a visual warning signal occurred 5 sec before tone onset. Baseline and reward conditions were run. Normal controls were contrasted with three Attention Deficit Disorder (ADD) subgroups: ADD-only, ADD with hyperactivity (ADDH), ADD with hyperactivity and aggression (ADDHA). The ADD subgroups were predicted to show less deceleration in HR because of their problem sustaining readiness to respond. Significant sex x group differences in HR levels and change scores were found. Overall, girls had higher HR levels than boys and the ADD-only group (boys and girls) had lower HRs than the other ADD groups. But, the ADD-only boys had more marked deceleration to the warning signal and acceleration to the tones than the other ADD boys, whereas the ADD-only girls were no more reactive than the ADDH and ADDHA girls. Control girls had the highest HR levels and were the most reactive to stimuli. Control boys and ADD-only boys had similar HR levels and reaction patterns. ADD-only girls appear to be underaroused, whereas ADD-only boys do not. Results suggest that cardiac measures can provide external validation of disruptive and nondisruptive ADD subtypes.     

Heart rate reactivity in attention deficit disorder subgroups

Beat-to-beat heart rate (HR) was analyzed for 9 contiguous seconds in a warned reaction time (RT) paradigm. Imperative stimuli were tones of three intensity levels (55, 78, and 100 db); a visual warning signal occurred 5 sec before tone onset. Baseline and reward conditions were run. Normal controls were contrasted with three Attention Deficit Disorder (ADD) subgroups: ADD-only, ADD with hyperactivity (ADDH), ADD with hyperactivity and aggression (ADDHA). The ADD subgroups were predicted to show less deceleration in HR because of their problem sustaining readiness to respond. Significant sex x group differences in HR levels and change scores were found. Overall, girls had higher HR levels than boys and the ADD-only group (boys and girls) had lower HRs than the other ADD groups. But, the ADD-only boys had more marked deceleration to the warning signal and acceleration to the tones than the other ADD boys, whereas the ADD-only girls were no more reactive than the ADDH and ADDHA girls. Control girls had the highest HR levels and were the most reactive to stimuli. Control boys and ADD-only boys had similar HR levels and reaction patterns. ADD-only girls appear to be underaroused, whereas ADD-only boys do not. Results suggest that cardiac measures can provide external validation of disruptive and nondisruptive ADD subtypes.     

Autonomic conditioning to monetary and social stimuli and aggression in children

Poor conditioning to punishment, such as loud tones or electric shock, has been proposed as an important factor involved in the etiology of aggressive and psychopathic behavior. However, it is not known whether the association holds when monetary or social stimulus is used as the unconditioned stimulus, and if aggressive individuals also have impaired conditioning to rewards. In this study, skin conductance responses in a conditioning task involving both monetary/social reward and punishment as unconditioned stimuli were assessed in 340 male and female 8‐ to 9‐year‐old children from the community. Children reported their reactive and proactive aggression using the Reactive and Proactive Aggression Questionnaire (RPQ; Raine et al., 2006). Results showed that monetary/social reward and punishment were effective in eliciting physiological classical conditioning in children, and that reduced reward conditioning was associated with high levels of proactive aggression in particular. Findings highlight the importance of distinguishing between reactive and proactive aggression when examining antisocial behavior in children, and suggest that reward‐oriented treatment programs may not be effective for children with more proactive, instrumental aggressive behavior.

     

When congruence breeds preference: the influence of selective attention processes on evaluative conditioning

We investigated in two experiments whether selective attention processes modulate evaluative conditioning (EC). Based on the fact that the typical stimuli in an EC paradigm involve an affect-laden unconditioned stimulus (US) and a neutral conditioned stimulus (CS), we started from the assumption that learning might depend in part upon selective attention to the US. Attention to the US was manipulated by including a variant of the Eriksen flanker task in the EC paradigm. Similarly to the original Flanker paradigm, we implemented a target-distracter logic by introducing the CS as the task-relevant stimulus (i.e. the target) to which the participants had to respond and the US as a task-irrelevant distracter. Experiment 1 showed that CS–US congruence modulated EC if the CS had to be selected against the US. Specifically, EC was more pronounced for congruent CS–US pairs as compared to incongruent CS–US pairs. Experiment 2 disentangled CS–US congruence and CS–US compatibility and suggested that it is indeed CS–US stimulus congruence rather than CS–US response compatibility that modulates EC.     

Regulatory interactions of stress and reward on rat forebrain opioidergic and GABAergic circuitry

Palatable food intake reduces stress responses, suggesting that individuals may consume such ?comfort? food as self-medication for stress relief. The mechanism by which palatable foods provide stress relief is not known, but likely lies at the intersection of forebrain reward and stress regulatory circuits. Forebrain opioidergic and gamma-aminobutyric acid ergic signaling is critical for both reward and stress regulation, suggesting that these systems are prime candidates for mediating stress relief by palatable foods. Thus, the present study (1) determines how palatable ?comfort? food alters stress-induced changes in the mRNA expression of inhibitory neurotransmitters in reward and stress neurocircuitry and (2) identifies candidate brain regions that may underlie comfort food-mediated stress reduction. We used a model of palatable ?snacking? in combination with a model of chronic variable stress followed by in situ hybridization to determine forebrain levels of pro-opioid and glutamic acid decarboxylase (GAD) mRNA. The data identify regions within the extended amygdala, striatum, and hypothalamus as potential regions for mediating hypothalamic-pituitary-adrenal axis buffering following palatable snacking. Specifically, palatable snacking alone decreased pro-enkephalin-A (ENK) mRNA expression in the anterior bed nucleus of the stria terminalis (BST) and the nucleus accumbens, and decreased GAD65 mRNA in the posterior BST. Chronic stress alone increased ENK mRNA in the hypothalamus, nucleus accumbens, amygdala, and hippocampus; increased dynorphin mRNA in the nucleus accumbens; increased GAD65 mRNA in the anterior hypothalamus and BST; and decreased GAD65 mRNA in the dorsal hypothalamus. Importantly, palatable food intake prevented stress-induced gene expression changes in subregions of the hypothalamus, BST, and nucleus accumbens. Overall, these data suggest that complex interactions exist between brain reward and stress pathways and that palatable snacking can mitigate many of the neurochemical alterations induced by chronic stress.     

Gender differences in emotional and overt/covert aggressive responses to stress

We examined the role of stress exposure on gender differences in hostile (emotional and behavioral) reactions within the context of a laboratory paradigm. Aggressive behavior was indexed via the intensity (overt) and the duration (covert) of putative shocks delivered to a confederate. Half of the participants were exposed to a chronic stressor (high stress) and half were not (low stress). Participants' emotional responses were measured via self-report mood ratings before and after the experiment. Men displayed higher aggression in both stress conditions, which corresponded to their ratings of state hostility. On the other hand, women in high stress delivered lower intensity shocks, and this decreased overt aggression was positively correlated with sadness ratings. However, women did not decrease their levels of shock duration (covert aggression) under high stress and showed equivalent shock duration compared with men in high stress. These findings are discussed in terms of differential overt manifestations of distress between men and women.     

The effects of negative reinforcement for irritable aggression on resident-intruder behavior

This experiment demonstrated that rats trained to display elevated levels of shock-induced aggression in a negative reinforcement paradigm displayed more boxing behavior than yoked control groups in a later test in which intruder rats were placed in the home cage of resident rats. Resident or intruder status did not affect the influence of the negative reinforcement procedure on the observed resident-intruder behavior of trained animals; however, naive intruders paired with trained residents displayed increased defensive behavior, suggesting that negative reinforcement for shock-induced aggression affected the behavior of these residents.     

Correlation between Changes in Stress-Induced Corticosterone Secretion and GR mRNA Levels

The current study was conducted to determine the potential relationship between stress-induced corticosterone secretion and corticosteroid receptor mRNA levels after 5 days of intermittent stress. In particular, we were interested in the rate at which animals terminate a stress response, and how this termination may be altered by repeated stress. Adult male Sprague-Dawley rats were subjected to either 5 days of restraint stress or 5 days of an unpredictable stress paradigm. Restraint-stress induced corticosterone secretion was measured on Days 1 and 5 in both groups, and animals were killed on Day 6. Glucocorticoid receptor (GR), and mineralocorticoid (MR) mRNA levels were determined using in-situ hybridization techniques. Five days of restraint stress caused an habituation of the plasma corticosterone response to stress measured 60 and 90 min post-stress initiation; this pattern of corticosterone secretion was not observed in the animals subjected to unpredictable stress. Five days of either stress paradigm did not alter MR mRNA levels measured within the hippocampus or GR mRNA levels within the hippocampus or the medial parvocellular division of the paraventricular nucleus of the hypothalamus (mpPVN). However, an individual's GR mRNA levels measured within the CA1/2 region of the hippocampus and the mpPVN were significantly correlated with the degree of habituation of the corticosterone response to stress measured on Day 5. This suggests that an increase in the rate of termination of the stress response and levels of GR within the hippocampus and mpPVN may be functionally related.     

A new approach to explain aggression

Two separate experiments are reported. They show the methodological difficulties and subsequent conceptual complications in Berkowitz's modified frustration-aggression theory and Zillman's theory of aggression. There was a marginally significant difference in the verbal measure of aggression favouring subjects aroused by frustration over subjects aroused by exercise, but not on the behavioral measure of aggression. Exp. II was conducted to test an alternative hypothesis, deduced from Fraisse's theory of emotion, which states that subjects respond more aggressively when confronted with unexpected than with expected annoyance. All six measures of aggression confirmed the hypothesis. The results of these two experiments indicate conceptual and methodological difficulties inherent in Berkowitz's modified frustration-aggression theory and Zillman's theory of aggression; they also suggest that Fraisse's theory of emotion presents a better model of aggression.     

Psychopharmacologic strategies for the treatment of aggression in juveniles

Maladaptive aggression in youth is one of the most common and troublesome reasons for referrals to child psychiatrists. It has a complex relationship with psychopathology. There are several syndromes, which are primary disturbances of clustered maladaptive aggression, most notably oppositional defiant disorder and conduct disorder. However, problems with aggression also appear in a wide range of other disturbances, such as bipolar disorder, posttraumatic stress disorder, and mood disorders. Additionally, aggression is normative, serves an adaptive purpose and can be situationally induced. These complexities need to be carefully addressed before targeting maladaptive aggression psychopharmacologically. We summarize the literature on the psychopharmacology of maladaptive aggression in youth, focusing on disorders without cognitive impairment. We delineate the subtypes of aggression which are most likely to respond to medication (reactive-affective-defensive-impulsive in their acute and chronic form) and conclude with a discussion of specific medication strategies which are supported by controlled clinical trials and clinical experience.     

Learning of a T-maze by rat pups when contact with the mother is either permitted or denied

Mother–pup interactions constitute an important component of environmental stimulation of the offspring during the neonatal period. Employing maternal contact as either a positive reinforcer or, its denial, as a frustrative, non-rewarding stimulus, we developed a novel experimental paradigm involving learning by rat neonates of a T-maze. When trained under the reward of maternal contact during postnatal days 10–13 Wistar rat pups learned the choice leading to the mother in a T-maze. When tested 2 h later, in the absence of the mother, pups showed a clear preference for the arm of the T-maze leading to the position of the mother during training. Furthermore, pups receiving the expected reward of maternal contact had higher numbers of c-Fos immunopositive cells in the dorsal striatum compared to either naïve or pups denied the expected reward. The above behavioral and cellular results indicate that pups receiving the expected reward developed a procedural-like memory. When trained under frustrative non-reward pups learned to make the correct choice in the T-maze, albeit less efficiently than pups receiving the expected reward. Following this training condition c-Fos immunohistochemistry revealed increased activation of the CA1 area of the hippocampus and the orbitofrontal cortex. Expression of the information learned by the pups denied the expected reward was contingent upon the presence of the mother in the experimental setup in exactly the same configuration as during the training.     

Children’s competitive peer aggression during reward and punishment

Behavior‐disordered children (N = 65) competed with a presumed unknown peer on consecutive administrations of an analogue aggression task of instrumental aggression (blocking the opponent’s game) and hostile aggression (sending the opponent a noise). The first administration as a reward‐only, nonpunishment condition. The second administration contained both reward and punishment conditions. Results indicated clear differences on aggressive responding during conditions of reward and punishment. Significant correlations were found between instrumental aggression during reward across the two administrations, whereas correlations between aggression during reward and aggression during punishment were nonsignificant. Teacher ratings of Covert‐Proactive Aggression correlated with analogue task instrumental aggression but not with hostile aggression on both administrations. Aggression during punishment was significantly correlated with Continuous Performance Test inattention and impulsivity scores, suggesting that impulsivity and inattention may play an important role in children’s ability to inhibit aggression during cues for punishment. These data indicate the utility of a laboratory analogue procedure to assess conditions associated with childhood aggression and to further our understanding of childhood aggression subtypes. Aggr. Behav. 27:1–13, 2001. © 2001 Wiley‐Liss, Inc.     

P300 to emotionally relevant stimuli as an indicator of aggression levels

Severe acts of aggression have been associated with prefrontal dysfunction. Less severe aggression may be associated with more subtle abnormalities. P300 event‐related potentials were recorded from 32 healthy volunteers during a novel modified oddball task. The task required participants to respond only to rare, food words (targets), which occurred randomly among neutral words. Aggressive words appeared randomly with the same frequency as the target words. A median split divided subjects into high‐ and low‐aggression groups based on their scores on the Buss–Durkee Hostility Inventory. The groups did not differ in their responses to the target words. Participants with higher aggression scores had lowered responses to the aggressive words at the frontal relative to the other electrode sites. Cognitive processing of aggressive stimuli was less efficient at frontal sites in individuals who reported higher levels of aggression. This result extends work showing frontal P300 decrements in more severe aggressive groups, using simple oddball tasks. Aggr. Behav. 32:1–8, 2006. © 2006 Wiley‐Liss, Inc.     

Cues produced by reward and nonreward and temporal cues influence responding in the intertrial interval and to the conditioned stimulus

Rats in a Pavlovian situation were trained under three different reward schedules, at either a 30 s or a 90 s intertrial interval (ITI): Consistent reward (C), 50% irregular reward (I), and single alternation of reward and nonrewarded trials (SA). Activity was recorded to the conditioned stimulus (CS) and in all 10 s bins in each ITI except the first 10 s bin. Responding increased progressively over the bins of the 90 s ITI indicating a role for temporal cues in the ITI. Single alternation patterning (SAP), more vigorous responding on rewarded than on nonrewarded trials, occurred in the ITI as well as to the CS and differed little at the 30 s and 90 s ITI. The occurrence of SAP to the CS and, as shown here for the first time, in the ITI along with the findings for the C and I schedules, indicate three matters of importance. First, along with other cues such as temporal cues, behavior is influenced by cues associated with reward and nonreward both in the ITI and when the CS is presented. Second, as the percentage of reward associated with these cues increases so too does vigor of responding. Finally, if the cues produced by reward events are memories the retrieval cues for such memories are present in the ITI as well as when the CS is presented. Considerations are advanced indicating that reward produced cues may influence responding in the Pavlovian situation not only under regular schedules such as the SA schedule, but under all schedules. Indeed, such cues may more validly signal reward and nonreward than the CS itself.     

Group vs individual equity judgments: Is there a polarization effect?

Two-hundred male undergraduates, individually and in groups of five, divided a fixed reward between two performers with unequal inputs under conditions in which they either expected or did not expect future interaction with recipients. Individuals who anticipated future interaction with recipients divided the reward equally, while groups divided the reward equitably. When interaction was not expected, individuals divided the reward equitably by discriminating between recipients, while groups made more extreme discriminations (the group polarization effect). Experiencing group discussions made individuals more confident in the fairness of their subsequent allocations. The results are discussed in terms of the social and informational influences of groups on allocation decisions.