Stimulus factors in aversive controls: conditioned suppression after equal training to two stimuli

Pigeons trained to peck a key for food were periodically presented with tones ending with electrical shock until tone presentation consistently suppressed ongoing pecks. Shock was then discontinued and gradients of stimulus generalization were assessed by presenting tones with frequencies above, below, and at the frequencies of those used to develop conditioned suppression. When the training tones had frequencies at 670 and 1500 cps, resulting gradients were bi-modal with peak suppression at 670 and 1500 cps. Of the other test tones, 1000 cps produced the most suppression. When the training tones had frequencies at 450 and 2250 cps, bi-modal gradients were again obtained with peak suppression to the 450 and 2250 cps tones. Of the other test tones, 1000 cps produced the least suppression. These results support the hypothesis that generalized response tendencies summate.     

Techniques for establishing schedules with wheel running as reinforcement in rats.

In three experiments, access to wheel running was contingent on lever pressing. In each experiment, the duration of access to running was reduced gradually to 4, 5, or 6 s, and the schedule parameters were expanded gradually. The sessions lasted 2 hr. In Experiment 1, a fixed-ratio 20 schedule controlled a typical break-and-run pattern of lever pressing that was maintained throughout the session for 3 rats. In Experiment 2, a fixed-interval schedule of 6 min maintained lever pressing throughout the session for 3 rats, and for 1 rat, the rate of lever pressing was positively accelerated between reinforcements. In Experiment 3, a variable-ratio schedule of 20 or 35 was in effect and maintained lever pressing at a very stable pace throughout the session for 2 of 3 rats; for 1 rat, lever pressing was maintained at an irregular rate. When the session duration was extended to successive 24-hr periods, with food and water accessible in Experiment 3, lever pressing settled into a periodic pattern occurring at a high rate at approximately the same time each day. In each experiment, the rats that developed the highest local rates of running during wheel access also maintained the most stable and highest rates of lever pressing.     

Extinction of responding maintained by timeout from avoidance

The resistance to extinction of lever pressing maintained by timeout from avoidance was examined. Rats were trained under a concurrent schedule in which responses on one lever postponed shock on a free-operant avoidance (Sidman) schedule (response-shock interval = 30 s) and responses on another lever produced 2 min of signaled timeout from avoidance on a variable-ratio 15 schedule. Following extended training (106 to 363 2-hr sessions), two experiments were conducted. In Experiment 1 two different methods of extinction were compared. In one session, all shocks were omitted, and there was some weakening of avoidance but little change in timeout responding. In another session, responding on the timeout lever was ineffective, and under these conditions timeout responding showed rapid extinction. The within-session patterns produced by extinction manipulations were different than the effects of drugs such as morphine, which also reduces timeout responding. In Experiment 2 shock was omitted for many consecutive sessions. Response rates on the avoidance lever declined relatively rapidly, with noticeable reductions within 5 to 10 sessions. Extinction of the timeout lever response was much slower than extinction of avoidance in all 4 rats, and 2 rats continued responding at baseline levels for more than 20 extinction sessions. These results show that lever pressing maintained by negative reinforcement can be highly resistant to extinction. The persistence of responding on the timeout lever after avoidance extinction is not readily explained by current theories.     

Response acquisition and fixed-ratio escalation based on interresponse times in rats

The effectiveness of a fixed‐ratio (FR) escalation procedure, developed by Pinkston and Branch (2004) and based on interresponse times (IRTs), was assessed during lever‐press acquisition. Forty‐nine experimentally naïve adult male Long Evans rats were deprived of food for 24 hr prior to an extended acquisition session. Before the start of the session, three food pellets were placed in the magazine. Otherwise, no magazine training, shaping, nor autoshaping procedure was employed. The first 20 presses each resulted in the delivery of a 45‐mg food pellet. Then, the FR increased (2, 4, 8, 11, 16, 20, 25, 30) when each IRT in the ratio was less than 2 s during three consecutive ratios. Sessions lasted 13 hr or until 500 pellets were earned. On average, rats reached a terminal ratio of 11 (mean) or 16 (median) during the first session. Seven rats reached the maximum value of FR 30 and only one rat did not acquire the response. In most rats, a break‐and‐run pattern of responding characteristic of FR schedules began to develop in this acquisition session. Subsequently, the ratio‐escalation procedure continued during daily 2‐hr sessions. In these sessions, the starting ratio requirement was set at the terminal ratio reached in the previous session. Using this procedure, over half (26) of the rats reached the FR 30 requirement by the fourth session. These data demonstrate that a ratio‐escalation procedure based on IRTs provides a time‐efficient way of establishing ratio responding.     

Some experiments relating to the perception of complex tones

Pattern recognition models for the perception of complex tones assume that the pitch of a complex tone is derived from more primary sensations, such as the pitches of the individual partials. Thus a complex tone will only have a well-defined pitch when at least one partial in the complex is separately perceptible. Models based on time-interval measurements, on the other hand, require an interaction of the original components, so that the periodicity of the input waveform is preserved. In Experiment I the relative intensity of a “target” tone, necessary for its identification in the presence of either one or two “masking” tones, was determined, over a range of frequencies. This intensity changes abruptly at around 5 kHz, a result consistent with the idea that the pitches of pure tones are determined by temporal mechanisms for frequencies up to 5 kHz, and by place mechanisms for frequencies above this. In Experiments II and III the audibility of the partials in a multi-tone complex was measured as a function of their frequency separation and compared with the range of conditions over which a complex stimulus produced a clear pitch sensation, using the same set of subjects in each experiment. It was found that under some conditions the complex had a well-defined pitch when none of the individual partials was separately audible. This is contrary to the predictions from the pattern recognition models. The effects of masking noise in the frequency region below the complex, and the results of individual subjects, also did not conform with the predictions from these models. Such models are not ruled out, however, for low harmonic numbers, or for stimuli containing only a small number of partials.     

Blockade of GABAA receptors in the interpositus nucleus modulates expression of conditioned excitation but not conditioned inhibition of the eyeblink response

The cerebellum and related brainstem structures are essential for excitatory eyeblink conditioning. Recent evidence indicates that the cerebellar interpositus and lateral pontine nuclei may also play critical roles in conditioned inhibition (CI) of the eyeblink response. The current study examined the role of GABAergic inhibition of the interpositus nucleus in retention of CI. Male Long-Evans rats were implanted with a cannula positioned just above or in the anterior interpositus nucleus before training. The rats were trained with two different tones and a light as conditioned stimuli, and a periorbital shock as the unconditioned stimulus. CI training consisted of four phases: 1) excitatory conditioning (8 kHz tone paired with shock); 2) feature-negative discrimination (2 kHz tone paired with shock or 2 kHz tone concurrent with light); 3) summation test (8 kHz tone or 8 kHz tone concurrent with light); and 4) retardation test (light paired with shock) After reaching a criterion level of performance on the feature-negative discrimination (40% discrimination), 0.5 μl picrotoxin (a GABA_A receptor antagonist) was infused at one of four concentrations, each concentration infused during separte test sessions. Picrotoxin transiently impaired conditioned responses during trials with the excitatory stimulus (tone) in a dose-dependent manner, but did not significantly impact responding to the inhibitory compound stimulus (tone-light). The results suggest that expression of conditioned inhibition of the eyeblink conditioned response does not require GABAergic inhibition of neurons in the anterior interpositus nucleus.     

Blockade of GABAA Receptors in the Interpositus Nucleus Modulates Expression of Conditioned Excitation but not Conditioned Inhibition of the Eyeblink Response

The cerebellum and related brainstem structures are essential for excitatory eyeblink conditioning. Recent evidence indicates that the cerebellar interpositus and lateral pontine nuclei may also play critical roles in conditioned inhibition (CI) of the eyeblink response. The current study examined the role of GABAergic inhibition of the interpositus nucleus in retention of CI. Male Long-Evans rats were implanted with a cannula positioned just above or in the anterior interpositus nucleus before training. The rats were trained with two different tones and a light as conditioned stimuli, and a periorbital shock as the unconditioned stimulus. CI training consisted of four phases: 1) excitatory conditioning (8 kHz tone paired with shock); 2) feature-negative discrimination (2 kHz tone paired with shock or 2 kHz tone concurrent with light); 3) summation test (8 kHz tone or 8 kHz tone concurrent with light); and 4) retardation test (light paired with shock). After reaching a criterion level of performance on the feature-negative discrimination (40% discrimination), 0.5 microl picrotoxin (a GABAA receptor antagonist) was infused at one of four concentrations, each concentration infused during separate test sessions. Picrotoxin transiently impaired conditioned responses during trials with the excitatory stimulus (tone) in a dose-dependent manner, but did not significantly impact responding to the inhibitory compound stimulus (tone-light). The results suggest that expression of conditioned inhibition of the eyeblink conditioned response does not require GABAergic inhibition of neurons in the anterior interpositus nucleus.     

Temporal course of perceived auditory duration

A series of experiments explored the temporal course of the perceived duration of an auditory stimulus. A backward recognition masking paradigm was utilized, in which the subject was to determine which of two target durations was presented on a given trial. The target tone was followed, after a variable silent intertone interval, by a masking tone which could assume one of three possible durations. Identification of the long target was found to improve consistently with increases in the intertone interval. In contrast, identification of the short target was as accurate at the short as at the long intertone intervals. Blocking the intertone interval across experimental sessions eliminated these differences between the two target tones. Performance on both the long and the short target tones improved monotonically with increases in the intertone interval. When masking tone duration was randomized within an experimental session, identification of the long (short) target was most accurate with the longer (shorter) masking tone. Blocking the duration of the masking tone across experimental sessions eliminated the effect of the duration of the mask, but did not alter any of the other results. A model, proposed to account for the results, assumes that the percept of target duration grows over time, and can be terminated by the onset of the masking tone. The masking tone also acts to lengthen the perceived duration of the target tone, and this lengthening is a direct function of the duration of the masking tone.     

Induced loudness reduction as a function of frequency difference between test tone and inducer

When a high-intensity tone (inducer) is followed by a moderate-intensity tone (test tone), the loudness of the latter is reduced. This phenomenon, called induced loudness reduction (ILR), depends on the frequency separation of the two tones; as the difference in frequency increases, the amount of ILR decreases. However, the precise course of this decrease is not well known. This article presents two experiments that address this question. In the first experiment, the amount of loudness reduction produced by a 2.5-kHz 80-dB-SPL inducer was measured with the frequency of the test tone swept from 800 Hz to 6 kHz. In the second experiment, the amount of ILR was measured with the same inducer and with test tones set at 2, 2.5, 3, and 4 kHz. Both experiments show that some ILR occurs at frequency separations as wide as four critical bands.     

The effects of 100 dB 1‐kHz and 22‐kHz tones as punishers on lever pressing in rats

Aversive control is an important yet understudied process of learning. One reason aversive control may be relatively understudied is ethical concerns about painful stimuli (e.g., electric shock). High decibel broad‐band noise and 22‐kHz vocalizations both demonstrably affect rodent behavior while not necessarily being painful. The goal of this study was to determine if 100‐dB 22‐kHz‐pure tones were differentially more effective in reducing operant response rates in rats. We examined whether 22‐kHz pure tones would function as aversive stimuli, specifically as positive punishers. The effects of response‐dependent as well as continuously presented 22‐kHz and 1‐kHz tones on rate of response maintained by variable interval 30‐s food deliveries were assessed across several conditions. We found that response rates were lower when tones were presented response dependently than when tones were presented continuously throughout a session. We also found that the lower response rates obtained with response‐dependent 22‐kHz tones were not significantly different from response rates obtained with response‐dependent 1‐kHz tones. The primary conclusion of this experiment is that both 1‐kHz and 22‐kHz tones functioned as punishers, but that the 22‐kHz tones were not differentially more effective in reducing response rate.     

Stimulus aspects of aversive controls: the retention of conditioned suppression

Three years ago a tone ending in unavoidable electrical shock was periodically presented to pigeons while they pecked a key for food. When pecking was disrupted by tone, shock was disconnected and the training tone as well as tones of different frequencies were presented. At first, all tones caused a reduction in the rate of pecking, but as testing proceeded, suppression began to extinguish and the gradient narrowed. In the present work, testing was resumed after a 2½-yr interruption. Analysis of the gradients obtained just before and just after the interruption yielded no evidence of changes with the passage of time. As testing proceeded, however, extinction of suppression continued and the gradient all but disappeared. In subsequent experiments with these subjects (Ss) it was found that the presentation of free shocks caused a reappearance of the gradient and that this effect persisted in reduced amount for several sessions after the shock condition was terminated.     

Perceptual grouping in audition

The present experiments evaluated the effect of relative frequency as a determinant of the figure-ground organization of sequences of auditory tones. Observers counted sequences of 20 ms tones that were presented at the same frequency or that alternated between two different frequencies. The alternating tones differed in frequency by one whole tone, seven tones, or nineteen tones. Counting accuracy increased with increases in the silent interval between the tones. When the alternating tones differed by seven or nineteen tones, counting was disrupted at rates of presentation of eight tones per second or slower. In contrast to this decrement in the counting of tones that alternated by over an octave, very little decrement was observed when the tones alternated by just one whole tone. The best subjects counted these alternating tones more accurately than the tones presented at the same frequency. The poorest subjects showed a small decrement even when the tones alternated by just one whole tone. The results were discussed in terms of determinants of figure-ground organization in auditory information processing.     

Drug discrimination in rats under concurrent variable-interval variable-interval schedules

Eight rats were trained to discriminate pentobarbital from saline under a concurrent variable-interval (VI) VI schedule, on which responses on the pentobarbital-biased lever after pentobarbital were reinforced under VI 20 s and responses on the saline-biased lever were reinforced under VI 80 s. After saline, the reinforcement contingencies programmed on the two levers were reversed. The rats made 62.3% of their responses on the pentobarbital-biased lever after pentobarbital and 72.2% on the saline-biased lever after saline, both of which are lower than predicted by the matching law. When the schedule was changed to concurrent VI 50 s VI 50 s for test sessions with saline and the training dose of pentobarbital, responding on the pentobarbital-biased lever after the training dose of pentobarbital and on the saline-biased lever after saline became nearly equal, even during the first 2 min of the session, suggesting that the presence or absence of the training drug was exerting minimal control over responding and making the determination of dose-effect relations of drugs difficult to interpret. When the pentobarbital dose-response curve was determined under the concurrent VI 50-s VI 50-s schedule, responding was fairly evenly distributed on both levers for most rats. Therefore, 6 additional rats were trained to respond under a concurrent VI 60-s VI 240-s schedule. Under this schedule, the rats made 62.6% of their responses on the pentobarbital-biased lever after pentobarbital and 73.5% of their responses on the saline-biased lever after saline, which also is lower than the percentages predicted by perfect matching. When the schedule was changed to a concurrent VI 150-s VI 150-s schedule for 5-min test sessions with additional drugs, the presence or absence of pentobarbital continued to control responding in most rats, and it was possible to generate graded dose-response curves for pentobarbital and other drugs using the data from these 5-min sessions. The dose-response curves generated under these conditions were similar to the dose-response curves generated using other reinforcement schedules and other species.     

Pure-tone perception and ear advantages in dichotic listening

A same-different matching task was used to investigate how subjects perceived a dichotic pair of pure tones. Pairs of stimulus tones in four frequency ranges (center frequencies of 400–1,700 Hz), with separations between 40 and 400 Hzt were tested. Five types of test tones were matched to the stimulus pair: the stimulus pair presented again (control) or crossed over (same tones, different ears), the geometric mean of the two tones, or a binaural tone of the low or high tone of the pair. In the lowest frequency range and the highest with maximum separation, the crossed-over test tones were perceived as different from the same stimulus tones. A bias for perceiving the higher tone of a pair was evident in the frequency ranges with separations of 40-200 Hz. In the lowest frequency range, the bias was for perceiving the higher tone in the right ear. This restricted ear advantage in the perception of pure tones was not significantly related to the right-ear advantage in dichotic word monitoring.     

Rapid induction of specific associative behavioral memory by stimulation of the nucleus basalis in the rat

Hypothesized circuitry enabling behavioral memory formation can be tested by its direct activation in the absence of normal experience. Neuromodulation via the cortical release of acetylcholine by the nucleus basalis (NB) is hypothesized to be sufficient to induce specific, associative behavioral memory. Previously, we found that tone paired with stimulation of the nucleus basalis (NBs) for 3000 trials over 15 days induced such memory, supporting the hypothesis. However, as standard associative memory can be established much more rapidly, we asked whether NB-induced memory develops rapidly. Adult male Sprague-Dawley rats, trained and tested in the same calm, waking state, were divided into Paired (n=5) and control (n=4) groups, each of which received a single session of 200 trials of an 8.0 kHz conditioned stimulus (CS) either paired with NBs or with unpaired presentation of NBs. Respiration, cardiac activity, and evoked potentials in the primary auditory cortex (ACx) were recorded. Memory and its degree of specificity were assessed 24 h later by presenting tones of various frequencies (1-15 kHz) in the absence of NBs to yield behavioral frequency generalization gradients. Behavioral responses to test tones consisted of interruption of ongoing respiration and changes in heart rate. Post-training behavioral generalization gradients exhibited response peaks centered on the CS frequency for the Paired group alone. Tone evoked potentials from the ACx also developed CS-specific plasticity. The findings indicate that NB induction of specific behavioral associative memory, like normal memory, can develop rapidly and is accompanied by specific cortical plasticity, supporting the view that NB engagement during normal learning produces memory.     

Classical Delay Eyeblink Conditioning in in 4- and 5-Month-Old Human Infants

Abstract-Simple delay classical eyeblink conditioning, using a tone conditioned stimulus (CS) and airpuff unconditioned stimulus (US), was studied in cross-sectional samples of 4- and 5-month-old healthy, full-term infants. Infants received two identical training sessions, 1 week apart. At both ages, infants experiencing paired tones and air-puffs demonstrated successful conditioning over two sessions, relative to control subjects who had unpaired training. Conditioning was not evident, however, during the first session. Two additional groups of 5-month-olds received varied experiences during Session 1, either unpaired presentations of the CS and US or no stimulus exposure, fol-lowed by paired conditioning during Session 2. Results from these groups suggest that the higher level of conditioning observed following two sessions of paired conditioning was not the result of familiarity with the testing environment or the stimuli involved but, rather, the result of retention of associative learning not expressed during the first conditioning session.     

Duration-reduction of avoidance sessions as negative reinforcement

Five rats were exposed to a shock-postponement procedure in which responses on each of two levers initially had equivalent effects. After an initial training sequence that ensured at least some responding on each lever, an additional consequence was made conjointly operative on the previously less-preferred lever for each animal. Each response on this lever continued to postpone shock, but also reduced the session duration by one minute. The conjoint contingencies were operative until, through session-shortening responses and the passage of time, the session was scheduled to end in two minutes; during the final two minutes the session-shortening contingency was disabled while the shock-postponement contingency continued to be operative on both levers. When responding shifted to a predominance on the session-shortening lever, the conjoint contingency was shifted to the other lever; for four of the five rats this reversal was followed by two additional reversals. Two of the rats' responding showed clear, strong, and unambiguous sensitivity to the session-shortening contingency. The responding of two others was also systematically controlled by that contingency, but the effects were less clearcut. The fifth animal showed an initial shift when session-shortening was introduced, but its subsequent behavior proved insensitive to reversals of procedure. The results clearly indicate a sensitivity of behavior to events on a time scale quite distinct from that of immediate consequences. They also support an interpretation of avoidance sessions, considered in their entirety, as events whose contingent relationship to behavior can affect that behavior—even in the absence of stimuli that delineate those relationships. Finally, these results support an interpretation of aversively based conditioning within a broader context, analogous to the “open versus closed economy” interpretation of appetitively controlled behavior.     

Conditioned suppression by a stimulus associated with nalorphine in morphine-dependent monkeys

Three rhesus monkeys, physically dependent on morphine, were trained to press a lever for food on a fixed ratio of 10 responses. A tone, initially a neutral stimulus, was aperiodically presented every third or fourth session, 5 min before and after the intravenous injection of nalorphine, a morphine antagonist which produces an immediate withdrawal syndrome in morphine-dependent monkeys. After several sessions, conditioned suppression of food-lever response rate was observed. Conditioned bradycardia, emesis, and excessive salivation also occurred. In 40 to 45 sessions the conditioned suppression of food-lever response rate and the conditioned autonomic changes were extinguished by presenting pairings of a tone and saline injection. The monkeys were then reconditioned by presenting the tone aperiodically, every third or fourth session, 5 min before and after the intravenous injection of nalorphine. Results were similar to the initial conditioning sessions. Two rhesus monkeys not dependent on morphine were stabilized on a food schedule similar to that used for the first three monkeys. These monkeys showed no change in food-lever response rate during or after nalorphine injections.     

Evaluation of a novel translational task for assessing emotional biases in different species

Changes in the processing of emotional information are key features of affective disorders. Neuropsychological tests based on emotional faces or words are used to detect emotional/affective biases in humans, but these tests are not applicable to animal species. In the present study, we investigated whether a novel affective tone discrimination task (ATDT), developed to study emotion-related behaviour in rats, could also be used to quantify changes in affective states in humans. To date, the methods used in human neuropsychology have not been applicable to animal experiments. Participants completed a training session in which they learnt to discriminate specific tone frequencies and to correctly respond in order to gain emotionally valenced outcomes, to obtain rewards (money), or to avoid punishment (an aversive sound clip). During a subsequent test session, additional ambiguous probe tones were presented at frequencies intermediate between the reward and avoidance paired tones. At the end of the task, participants completed self-report questionnaires. All participants made more avoidance responses to the most ambiguous tone cues, suggesting a bias towards avoidance of punishment. Individual differences in the degrees of bias observed were correlated with anxiety measures, suggesting the task’s sensitivity to differences in state anxiety within a healthy population. Further studies in clinical populations will be necessary to assess the task’s sensitivity to pathological anxiety states. These data suggest that this affective tone discrimination task provides a novel method to study cognitive affective biases in different species, including humans, and offers a novel assessment to study anxiety.     

Rats (Rattus norvegicus) find occupancy of a restraint tube rewarding

Two experiments evaluated whether rats' occupancy of a restraint tube is reinforcing. In Experiment 1, each rat in the 0-min group moved freely in a chamber where a wall blocked access to a restraint tube. After 10 min the wall was removed, permitting 15 min of chamber access and tube entry. The other 2 groups were locked in the tube for 10 and 20 min respectively before release into the chamber for 15 min. Across sessions, rats locked up for 10 and 20 min entered the tube more frequently than rats in the 0-min group, and during the first 2 sessions rats in the 20-min group stayed in the tube longer than the other groups. Over sessions this difference disappeared. However, for all groups and sessions the mean percentage of session time in the tube exceeded chance expectations. This result suggests tube occupation was reinforcing. In Experiment 2’s Phase 1, rats could enter an open tube. On exiting, the tube door closed. A lever press opened the door for the rest of the 1-hr session. In Phase 2, these rats were locked in the tube for 10 min before the door opened. Upon exiting, the door closed. As in Phase 1, a lever press opened the door for the rest of the session. The latency between pressing and tube entry decreased over sessions, indicating that tube entry reinforced lever pressing. These results are difficult to reconcile with accounts of rat empathy based on the thesis that tube restraint distresses occupants.