Aggressive behavior of pigeons: Suppression by archistriatal lesions

The agonistic responses of pigeons to the introduction of a stick and the experimenter's hand into their home cages is described. The effects of lesions of the archistriatum, a presumed homologue of the mammalian amygdala, of lesions of the overlying neostriatum and of control sham operations on this behavior in selected aggressive pigeons are reported. Only archistriatal lesions lead to a persistent depression of the aggressive and a converse increment of the avoidance components of the pigeon's response to both test stimuli. The results are discussed in relation to other evidence on the role of the avian archistriatum and this structure's correspondence with the amygdala.     

Avoidance responding in pigeons

Four pigeons were trained in a one-way shuttle box avoidance situation. Three of the birds met the criterion of 90% avoidances; the fourth, although frequently avoiding successfully, was too erratic to meet the criterion. Avoidance responding in two of the birds was subsequently extinguished, showing that the response was true avoidance, and not escape from the buzzer warning stimulus. In Experiment 2, the three birds that had met criterion in Experiment 1 were trained in a two-way avoidance task, and all three met the criterion of 90% avoidances. The shuttle box therefore provides a rapid and reliable method of obtaining avoidance performance in pigeons.     

Pavlovian processes and response competition as determinants of avoidance response-prevention effects

Two experiments investigated the facilitation of avoidance extinction by exposure to lengthy (5-sec) shock during avoidance response prevention. In Experiment 1, animals exposed to light only or to light-shock pairings during response prevention showed equal facilitation of extinction relative to shock-only animals or to animals receiving no response prevention. Preshock rearing, directly antagonistic to the avoidance response, developed for shocked animals during response prevention and persisted during extinction for light-shock animals. Immediately before extinction, half of each group was permitted a single escape from a light-shock compound by means of the response previously required for avoidance. The only effect was upon the extinction performance of light-shock animals. Rearing was eliminated and extinction responding increased to a level far above that for any of the other animals. Experiment 2 demonstrated that the shock-only treatment affected the extinction performance and rearing of nonescape and escape animals in a manner entirely equivalent to the effects of the light-shock treatment of Experiment 1, provided stimulus conditions (light absent) were the same for all experimental phases. Thus, lengthy shock during avoidance response prevention simultaneously leads to the acquisition of competing behavior and enhances control by a warning signal or contextual stimuli over the avoidance response. Implications for the CS-only response-prevention treatment and the transfer of aversive control are discussed.     

Paleostriatal lesions and instrumental learning in the pigeon

In three experiments, pigeons with lesions of the paleostriatum (experimental subjects) and unoperated control birds were trained on tasks designed to assess their instrumental learning abilities. In Experiment 1, using an orthodox Skinner box, training was given on a variable interval (VI) followed by a fixed interval (FI) schedule of reinforcement and only non-significant differences between the groups emerged. Experiment 2 examined the performance of the same subjects on a VI schedule in which a response-contingent signal accompanied reinforcement. For control subjects the presence of the signal resulted in a low rate of response compared with that found in equivalent conditions with the signal omitted. Experimental subjects showed the same response rate when the signal was present as when it was absent. Experiment 3 employed naive subjects, and a Skinner box modified to facilitate key-pecking in total darkness. In this apparatus, experimental subjects showed a lowered response rate on a VI schedule. These tasks were analyzed in terms of the classical (stimulus-reinforcer) and instrumental (response-reinforcer) learning they involve. The results suggest that pigeons with paleostriatal lesions show a deficit in forming response-reinforcer associations, perhaps because the lesions reduce the salience of response-produced cues.     

Extinction effects following interpolation of instrumental trials among response prevention periods

Two experiments evaluated the effectiveness of response prevention when prevention periods were interpolated with instrumental trials which permitted performance of the originally trained instrumental behavior. In Experiment 1, interpolation of instrumental escape trials under shock and nonshock procedures reliably reduced prevention's influence on performance and yielded extinction responding similar to that of pseudo-prevention controls. In Experiment 2 interpolation of instrumental escape trials under nonshock conditions yielded passive avoidance performance similar to that of pseudo-prevention controls but reliably different from that of a regular prevention group.     

Prior exposure to inescapable electric shock in rats affects extinction behavior after the successful acquisition of an escape response

In Expt 1, rats exposed to 64 inescapable electric shocks in a restrainer or merely restrained were later given either 0, 5, 15 or 30 escape/avoidance training trials with a two-way shuttlebox procedure that does not lead to interference with escape acquisition due to prior exposure to inescapable shock. After escape training all rats were given an escape/avoidance extinction procedure in which shock was inescapable. The rats which had received prior exposure to inescapable shock responded less often and with longer latencies in extinction than did the restrained rats. Experiment 2 demonstrated that this effect is caused by the inescapability of the initial shock treatment. These results were explained in terms of (a) associative interference which minimized the effect of shuttlebox escape training for the preshocked subjects, and (b) a stronger tendency to recognize the presence of an inescapable shock situation during extinction for the preshocked subjects. The relationship between these results and previous work demonstrating that exposure to the escape contingency mitigates the effects of inescapable shock exposure was also discussed.     

Representation of serial order in pigeons (Columba livia)

In Experiment 1, 2 groups of pigeons were trained to respond to either a 4-item (A→B→C→D) or 5-item (A→B→C→D→E) list. After learning their respective list, half of the subjects were trained on a positive pair with reinforcement provided when pairs were responded to in the order true to that of the original sequence (4-item: B→C; 5-item: B→D). The remaining subjects were trained on a negative pair with reinforcement provided for responding to the pairs in the order opposite to that learned in the original sequence (4-item: C→B; 5-item: D→B). Subjects in the positive pair condition learned their respective pair faster than did subjects in the negative pair condition. In Experiment 2, after reaching criterion on a 4-item list, subjects received 16 BC probe trials spread across 4 sessions of training. Subjects performed significantly above chance on the probe trials. The performance of our subjects in Experiments 1 and 2 demonstrates that, similar to monkeys, pigeons form a representation of the lists that they learn.     

Immobility as an avoidance response, and its disruption by drugs

Much of the available literature on avoidance behavior is based on responses which require the animal to run, lever-press, or to make some active response to avoid noxious stimulation. The purpose of Experiment I reported in this paper was to determine whether animals can learn to sit or stand motionless in order to escape or avoid electric shock. Five experimental rats were given escape-avoidance training, while five yoked control animals received electric shocks without any response-related contingency. It was shown that an immobility avoidance response, as distinct from the unconditioned “freezing” response to shock, can be trained. The results of Experiment II (30 rats) revealed that this response is more readily acquired at higher shock intensities than at lower ones, provided escape by jumping is prevented at the high shock intensities. The effects of six doses of each of three drugs on the immobility avoidance response were studied in Experiment III (13 rats). Methylphenidate, chlorpromazine, and imipramine all produced a decrement in the immobility response, but the pattern and amount of the effects of the three drugs were quite different, one from the other. The implications of these findings for a general theory of avoidance behavior and for drug screening are discussed.     

Measurement of fear of the conditioned stimulus and of situational cues at several stages of two-way avoidance learning

In Experiment 1, subjects were trained in a signaled two-way avoidance task to a criterion of either 2, 10, or 20 consecutive avoidance responses. Subsequently, they were allowed to escape, in the absence of shock, from one compartment of the avoidance apparatus to an adjacent safe box. For one group at each criterion level, the conditioned stimulus (CS) was presented during these trials; for another group, it was not (NCS). The rate and level of learning of the escape response were taken to reflect the amount of fear of the CS and situational cues present at the end of avoidance training for the CS groups and the amount of fear of the situational cues alone for the NCS groups. Under the CS condition, all groups learned equally well; under the NCS condition, learning occurred only in the two-criterion group. This pattern of results suggests that, as avoidance training continued, differential reinforcement led to the formation of a discrimination so that a substantial amount of fear was elicited by the CS plus situational cues but only a minimal amount by the situational cues alone. Such a loss of fear of situational cues would, according to effective reinforcement theory, serve to maintain or even increase reinforcement as avoidance training progressed. The results of Experiment 2, by ruling out some alternative explanations, supported the interpretation that the learning of the instrumental escape response in the first experiment was based on prior fear conditioning.     

The Effects of Hippocampal and Area Parahippocampalis Lesions in Pigeons: I. Delayed Matching to Sample

Four experiments were conducted to determine the effects of bilateral damage to the hippocampus and area parahippocampalis (Hp-APH) on visual memory in pigeons using the delayed matching-to-sample (DMS) procedure. In Experiment 1, we generated visual retention gradients with delays of 0, 1.5, 3, 6, and 12 sec both preoperatively and postoperatively in three pigeons with considerable preoperative visual DMS experience. Bilateral Hp-APH lesions had no effect whatsoever on visual retention. In Experiment 2, we examined the effects of Hp-APH lesions on both the acquisition of a visual DMS task with a 0-sec delay, and the subsequent retention performance with delays of 0, 3, 6, 12, and 24 sec. There was no difference between unoperated control pigeons and Hp-APH pigeons either in terms of the number of sessions required to learn the visual DMS task or in terms of their subsequent visual retention performance levels. In Experiments 3 and 4, we examined whether Hp-APH pigeons might be more sensitive than control pigeons to the effects of proactive interference (by reducing the duration of the intertrial interval) and retroactive interference (by introducing delay-interval illumination). Although reducing the duration of the intertrial interval and increasing the level of delay-interval illumination both resulted in lower performance levels on the visual DMS task, there was no indication that the Hp-APH pigeons were any more affected by the changes in interference levels than were unoperated control pigeons. These findings support the view that the Hp-APH in pigeons plays little role in the processing and retention of purely visual information.     

Predictability,controllability, and inoculation against learned helplessness

Nondepressed human subjects were divided into seven groups. On a series of discrimination problems, a helplessness group received insoluble problems, a solvable group received contingent feedback, and a no treatment control group received no feedback. For two other groups insoluble problems were preceded by success feedback on a different task presented according to a fixed ratio (FR) or variable ratio (VR) schedule of reinforcement. Two control groups received either FR or VR schedules of success but were not examined on the discrimination problems. All groups were tested for escape/avoidance performance on a human shuttle box. Both FR and VR schedules produced an inoculation against learned helplessness; escape performance by the helplessness group was significantly worse than that of FR and VR inoculation groups. These latter groups performed similar to the solvable and three control groups. Significantly worse than that of FR and VR inoculation groups. These latter groups performed similar to the solvable and three control groups. Significantly fewer subjects in the VR inoculation group exhibited avoidance responses than their counterparts in the FR inoculation group. despite similar escape performance. The findings indicate that learned helplessness can be prevented in humans and suggest different sources of interference produced by unpredictable and uncontrollable events.     

Hyperstriatal function in the pigeon: response inhibition or response shift?

Experiment 1 showed that pigeons with lesions of the anterior or posterior hyperstriatum were impaired relative to unoperated controls and to control operates having neostriatal lesions on both acquisition and reversal of a simultaneous position discrimination. The observation that hyperstriatal birds showed more tendency than controls to halt responding altogether in this situation cast doubt on the notion that the reversal deficit was due to a loss of response inhibition. A second experiment supported an alternative hypothesis, that hyperstriatal birds have a deficit in the ability to shift responding to an alternative stimulus as a consequence of nonreinforcement.     

The differentiation of response numerosities in the pigeon

Two experiments examined how pigeons differentiate response patterns along the dimension of number. In Experiment 1, 5 pigeons received food after pecking the left key at least N times and then switching to the right key (Mechner's Fixed Consecutive Number schedule). Parameter N varied across conditions from 4 to 32. Results showed that run length on the left key followed a normal distribution whose mean and standard deviation increased linearly with N; the coefficient of variation approached a constant value (the scalar property). In Experiment 2, 4 pigeons received food with probability p for pecking the left key exactly four times and then switching. If that did not happen, the pigeons still could receive food by returning to the left key and pecking it for a total of at least 16 times and then switching. Parameter p varied across conditions from 1.0 to .25. Results showed that when p= 1.0 or p=.5, pigeons learned two response numerosities within the same condition. When p=.25, each pigeon adapted to the schedule differently. Two of them emitted first runs well described by a mixture of two normal distributions, one with mean close to 4 and the other with mean close to 16 pecks. A mathematical model for the differentiation of response numerosity in Fixed Consecutive Number schedules is proposed.     

Glucose effects on memory: behavioral and pharmacological characteristics

Recent findings indicate that post-training glucose injections can modulate memory storage for inhibitory (passive) avoidance training. Experiment I extended these findings to determine whether glucose, like other memory modulating treatments, enhances memory storage when administered after training with low footshock and impairs memory storage after high footshock training. In Experiment I, male Sprague-Dawley rats were trained in a one-trial inhibitory avoidance task using either a brief footshock (0.5 mA, 0.7 s) or slightly more intense footshock kept on until escape (0.7 mA, mean escape latency = 3.4 s). Immediately after training, each rat received a subcutaneous injection of glucose (100 mg/kg). When tested for retention performance 24 h later, the glucose-injected animals exhibited enhanced retention performance for low footshock training and impaired retention for high footshock training. Experiment II determined whether pretreatment with adrenergic antagonists blocked the effects of glucose on memory. Pretreatment with the alpha- or beta-adrenergic receptor antagonists, phenoxybenzamine, or propranolol, respectively, had no effect on acquisition or retention in animals trained with the brief footshock and did not affect glucose facilitation of that memory. In animals trained to escape footshock, phenoxybenzamine did not attenuate the amnesia produced by glucose. Propranolol-pretreated animals had impaired retention whether or not they received post-training amnestic injections of glucose; glucose had no effect on retention in these amnestic animals. These findings add further support to the view that glucose release after training and treatment may represent a physiological response subsequent to epinephrine release in modulating memory storage processing.     

Preference for signalled reinforcement

Key pecking was reinforced on a two-component multiple schedule. A variable-interval schedule controlled reinforcement in both components. During one component, access to reinforcement was preceded by a tone; in the other component, a standard unsignalled schedule was in effect. After performance stabilized, subjects were given a choice between the signalled and unsignalled schedules. They were placed in the chamber with the unsignalled schedule in effect on the right key. A single response on the left, or changeover, key produced the signalled schedule for 1 min. Both pigeons in Experiment I pecked the changeover key at a rate sufficient to remain under the signalled schedule for over 90% of the session. Removing and reintroducing the tone demonstrated that the changeover-key responses were due to the occurrence of the tone. In Experiment II, when pecking the changeover key produced the unsignalled schedule, pecking the changeover key declined. The results may be explained either in terms of Hendry's information hypothesis or as escape from an intermittent positive reinforcement schedule.     

Medial prefrontal cortex lesions abolish contextual control of competing responses

There is much debate as to the extent and nature of functional specialization within the different subregions of the prefrontal cortex. The current study was undertaken to investigate the effect of damage to medial prefrontal cortex subregions in the rat. Rats were trained on two biconditional discrimination tasks, one auditory and one visual, in two different contexts. At test, they received presentations of audiovisual compounds of these training stimuli in extinction. These compounds had dictated either the same (congruent trials) or different (incongruent trials) responses during training. In sham-operated controls, contextual cues came to control responding to conflicting information provided by incongruent stimulus compounds. Experiment 1 demonstrated that this contextual control of responding was not evident in individual rats with large amounts of damage that included the prelimbic and cingulate subregions of the prefrontal cortex. Experiment 2 further dissociated the result of Experiment 1, demonstrating that lesions specific to the anterior cingulate cortex were sufficient to produce a deficit early on during presentation of an incongruent stimulus compound but that performance was unimpaired as presentation progressed. This early deficit suggests a role for the anterior cingulate cortex in the detection of response conflict, and for the medial prefrontal cortex in the contextual control of competing responses, providing evidence for functional specialization within the rat prefrontal cortex.     

Overcoming unlearned response biases: delayed escape following errors facilitates acquisition of win-stay and win-shift working memory water-escape tasks in rats

Previous research has demonstrated that perseveration in escape situations is an unlearned response bias of rats and mice which is difficult to overcome. In Experiment I, Sprague-Dawley rats were trained to a criterion of nine correct choices in 10 consecutive trials in a win-stay working memory water-escape task wherein an escape platform was hidden in one of two compartments. Subjects were given a forced choice on an Information Trial followed by a free choice on a Test Trial 5 min later. Subjects who were given a 30-s forced swim in the incorrect section following errors on the Test Trial showed faster acquisition and less use of response perseveration than control subjects. In Experiment II, the delayed escape procedure was used to compare acquisition of win-stay and win-shift strategies. Contrary to previous research both groups learned the tasks, although the win-stay group showed better performance. It is concluded that unlearned response biases of perseverating and returning to previous escape sites can be overcome if experimental conditions are appropriately arranged.     

Effects of response-shock interval and shock intensity on free-operant avoidance responding in the pigeon

Two experiments investigated free-operant avoidance responding with pigeons using a treadle-pressing response. In Experiment I, pigeons were initially trained on a free-operant avoidance schedule with a response-shock interval of 32 sec and a shock-shock interval of 10 sec, and were subsequently exposed to 10 values of the response-shock parameter ranging from 2.5 to 150 sec. The functions relating response rate to response-shock interval were similar to the ones reported by Sidman in his 1953 studies employing rats, and were independent of the order of presentation of the response-shock values. Shock rates decreased as response-shock duration increased. In Experiment II, a free-operant avoidance schedule with a response-shock interval of 20 sec and a shock-shock interval of 5 sec was used, and shock intensities were varied over five values ranging from 2 to 32 mA. Response rates increased markedly as shock intensity increased from 2 to 8 mA, but rates changed little with further increases in shock intensity. Shock rates decreased as intensity increased from 2 to 8 mA, and showed little change as intensity increased from 8 to 32 mA.     

Plasma corticosterone and renin activity during two-way active avoidance learning in spontaneously hypertensive and Wistar-Kyoto rats

The spontaneously hypertensive rat (SHR) exhibits increased sympathetic and behavioral responses to several types of environmental stress compared to its normotensive progenitor, the Wistar-Kyoto rat (WKY). The aim of the present study was to investigate response-dampening mechanisms in the SHR. This study examines whether learning to control a stressful environment reduces behavioral and neuroendocrine activation in the SHR. Twelve SHR and 12 WKY were subjected to daily sessions (S) of 20 trials of signaled two-way active avoidance. Another 12 SHR served as maturation controls. Blood samples were collected immediately after S 1, S 5, and S 14 and plasma level of corticosterone (p-CS) and plasma renin activity (PRA) were measured. There was an insignificant tendency for the SHR to exhibit larger increases in p-CS in response to stress than the WKY did. By S 5 both groups had attained the avoidance task. However, the level of p-CS was the same as after S 1, showing that activation is independent of the number of shock pulses received and performance. Postsession p-CS decreased between S 5 and 14, slightly more so in the SHR than in the WKY. The SHR exhibited lower PRA than the WKY, but there were no significant effects of exposure to the avoidance schedule. Behaviorally, the SHR exhibited shorter latency to escape in the first trial than the WKY did. The SHRs were hyperactive compared to the WKY, showing more ambulation and rearing behavior. The maturation control SHR reached the same mean arterial pressure as the SHRs which were tested. After S 14, signal duration was shortened from 10 to 3 s for six additional sessions. Both p-CS and PRA increased, while at the same time ambulation and rearing behavior decreased. These data show that the relationship between behavioral control and adrenocortical activation is normal in the SHR in spite of differences in behavior. The present results also confirm previous data on hyperreactivity to footshocks in two-way active avoidance tasks in the SHR.     

Deficient passive and one-way active avoidance acquisition following medial forebrain bundle lesions in rats.

Cathodal electrolytic lesions of the medial forebrain bundle (MFB) at posterior hypothalamic levels in male hooded rats produced a mild, transient hypodipsia and lowered jump thresholds to footshock. The lesions produced marked deficits in passive avoidance performance in a paradigm that paired discrete, linearly incrementing footshock intensities with contact of a water spout following 48 hr of water deprivation. Intraperitoneal injections of DL-5-hydroxytryptophan (75 mg/kg), the immediate metabolic precursor of serotonin, had no effect on the passive avoidance performance of either experimental or operated control subjects. Lesions of the MFB also resulted in deficient acquisition in a one-trial step-through passive avoidance paradigm not using motivation to drink and caused a severe acquisition deficit in a one-way active avoidance task. Lesions of the septal nuclei produced lowered jump thresholds but did not affect acquisition in the first passive avoidance task. The results are interpreted as indicating a lesion-induced deficiency in fear learning, independent of the serotonergic functions of the MFB.