Reevaluation of things past

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

The strength of the orienting response during blocking

In two experiments rats initially received appetitive Pavlovian conditioning with an auditory conditioned stimulus (CS). Subsequently this stimulus was presented in compound with a novel light and paired with the same appetitive reinforcer. In keeping with the outcome of many such experiments on blocking, there was very little evidence of appetitive conditioning during subsequent independent presentations of the light. Of main concern in the present experiments, however, was the influence of this training on the strength of the orienting response directed towards the light. When the light was first presented it elicited a strong orienting response. The strength of this response declined rapidly when the light was presented in compound with the previously trained auditory CS but more slowly when it was paired with the reinforcer either by itself or in conjunction with an initially neutral auditory stimulus. It is suggested that the extent to which the events following the light are accurately predicted determines the strength of orientation towards this stimulus.     

Second-order autoshaped key pecking based on an auditory stimulus.

In Experiment 1, pigeons were exposed either to paired or to unpaired presentations of a tone and grain, and then to paired presentations of a keylight with the tone. Substantial second-order conditioned pecking to the keylight was produced in the birds that had received paired presentations of tone and grain. In Experiment 2, second-order pecking to the keylight increased in probability across four groups that had received, respectively, 20, 80, 140, or 200 paired presentations of tone and grain. In Experiment 3, the amount of pecking directed towards a keylight which predicted the first-order, tone CS was as substantial in birds without a prior history of key pecking as in birds with such a history. A further experiment failed to discover any significant differences in the levels of second-order pecking to a keylight paired with a first-order tone CS or with a first-order keylight CS. Thus, an auditory signal that does not itself support pecking may enable a localized visual stimulus to evoke key pecking.     

Representation-mediated extinction of conditioned flavor aversions

Conditioned flavor aversions were extinguished by presenting without consequence auditory stimuli that had been previously paired with the aversive flavor. In Experiment 1, rats that received tone-sucrose pairings, then sucrose-lithium chloride (LiCl) pairings, and finally repeated tone-alone presentations showed greater sucrose consumption in subsequent testing than rats that received similar sucrose-LiCl pairings and tone-alone presentations but no initial tone-sucrose pairings. Experiment 2 demonstrated the stimulus specificity of the mediated extinction observed in Experiment 1. In Experiment 3, rats that received first-order light-food and second-order tone-light pairings prior to sucrose-LiCl pairings did not show greater subsequent sucrose consumption when extinction of the second-order tone intervened. These results suggest that conditioned stimulus (CS)-evoked representations of events can substitute for those events themselves in the extinction of previously established associations.     

Contextually Based Conditional Discrimination of the Rabbit Eyeblink Response

Rabbits received conditional discrimination training using contextual stimuli to set the occasion for stimulus pairings during eyelid conditioning. Specifically, animals were exposed to either the presence or the absence of an oscillating chamber light throughout the intertrial interval (50 ± 10 s). For half the animals, this light signaled paired presentations of a discrete tone conditioned stimulus (CS) and air puff unconditioned stimulus (US) while darkness signaled presentations of only the tone CS. The remaining animals experienced the opposite contextual relationship to the conditioning stimuli. These trial types occurred pseudo-randomly across a session, with all transitions between contextual settings (i.e., light or dark) taking place immediately at the CS–US offset. Under these conditions, animals successfully utilized the contextual stimuli as conditional cues for differential responding to the shared CS. Moreover, both light and dark were equally effective as discriminative stimuli. A subset of animals received further training in which the contextual contingency was removed by restricting all conditioning to the CS-alone context. Without the contingency in place, subsequent CS presentations (paired and CS-alone) evoked equivalent conditioned responding across three sessions of training. Following the reinstatement of the contextual contingencies, discriminatory responding was immediately observed and returned to previous levels within three sessions. Finally, animals appeared to use the static representation of the conditional cue, rather than the phasic transition between cues, for discriminatory responding. These findings are discussed in terms of current neurobiological models of eyelid conditioning.     

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.     

Appetitive-aversive interactions: Superconditioning of fear by an appetitive cs

Four groups of rats received conditioned suppression training in which a tone and light compound was reinforced with shock. If the light had been previously paired with free food, enhanced fear conditioning accrued to the tone during compound training relative to control groups pre-exposed to the light alone, the light semi-randomly associated with food, or the light unpaired with food. The second experiment replicated the difference in aversive conditioning for the groups receiving the light either paired or unpaired with food. The results are discussed in terms of the functional similarity of a conditioned excitor for food and a conditioned inhibitor for shock.     

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

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

Bilateral Ablation of Auditory Cortex in Mongolian Gerbil Affects Discrimination of Frequency Modulated Tones but not of Pure Tones

This study examines the role of auditory cortex in the Mongolian gerbil in differential conditioning to pure tones and to linearly frequency-modulated (FM) tones by analyzing the effects of bilateral auditory cortex ablation. Learning behavior and performance were studied in a GO/NO-GO task aiming at avoidance of a mild foot shock by crossing a hurdle in a two-way shuttle box. Hurdle crossing as the conditioned response to the reinforced stimulus (CR+), as false alarm in response to the unreinforced stimulus (CR−), intertrial activity, and reaction times were monitored. The analysis revealed no effects of lesion on pure tone discrimination but impairment of FM tone discrimination. In the latter case lesion effects were dependent on timing of lesion relative to FM tone discrimination training. Lesions before training in naive animals led to a reduced CR+ rate and had no effect on CR− rate. Lesions in pretrained animals led to an increased CR− rate without effects on the CR+ rate. The results suggest that auditory cortex plays a more critical role in discrimination of FM tones than in discrimination of pure tones. The different lesion effects on FM tone discrimination before and after training are compatible with both the hypothesis of a purely sensory deficit in FM tone processing and the hypothesis of a differential involvement of auditory cortex in acquisition and retention, respectively.     

Posttraining prefrontal lesions impair jaw movement conditioning performance,but have no effect on accompanying heart rate changes

This experiment examined the role of the medial prefrontal cortex (mPFC) in regulating learned autonomic and somatomotor responses in rabbits using appetitive Pavlovian conditioning. Interstimulus interval (ISI) duration [i.e., the time between the onset of the conditioned stimulus (CS) and unconditioned stimulus (US)] was manipulated in order to determine whether ISI duration was related to the heart rate (HR) responses obtained during conditioning. Two groups received either a 1- or a 4-s ISI, with a tone as the CS and an intraoral pulse of water as the US. Another two groups received explicitly unpaired presentations of either the 1- or 4-s tone CS and water US. Few conditioned jaw movement (JM) or HR conditioned responses (CRs) were observed in the unpaired conditions. Significant JM conditioning was, however, elicited by the paired conditions, especially to the 4-s ISI. Consistent CS-evoked HR accelerations were observed in both ISI conditions. After five sessions of training, the mPFC was lesioned in half the animals. A separate group of paired animals received sham lesions. After surgical recovery, all animals received 3 days of postoperative training. During the first postoperative training session, JM CRs significantly declined in both groups with mPFC lesions in comparison to the groups with sham lesions. The mPFC lesions, however, did not affect the CS-evoked cardiac accelerations, which again occurred during postoperative training.     

Brief flight to a familiar enclosure in response to a conditional stimulus in rats

The authors observed brief, directed movement to a familiar enclosure in rats to determine whether this behavior is part of a rat's defensive repertoire when exposed to a conditional-fear stimulus. In Experiment 1, upon exposure to the compound conditional-fear stimulus of tone and light, only rats that received paired presentations of the conditional stimuli and shock fled into a small, familiar enclosure where they then froze. Rats that had received unpaired presentations did not enter the enclosure in significant amounts when later tested. In Experiment 2, the authors observed rats' freezing and use of either a familiar or an unfamiliar enclosure when tested with a conditional-fear stimulus. Rats tested with a familiar enclosure entered it more quickly than did rats without prior exposure to the enclosure. Freezing was greatest when both training and testing environments were similar with respect to access to the enclosure. The results of these 2 experiments support the idea that brief, directed flight in rats is a component of the postencounter stage of predatory imminence (M. S. Fanselow & L. S. Lester, 1988) and is compatible with freezing.     

Overshadowing in operant conditioning as a function of discriminability

Pigeons were trained in an operant, go/no-go, discrimination by successive presentations of discrete, positive and negative trials. In separate groups, the rate of discriminaion learning based on an auditory cue, on visual cues of different discriminability, and on combined auditory and visual cues was determined. The auditory cue was tone/no-tone, the visual cue was a difference in brightness level on the key. Following discrimination training, stimulus control was tested in extinction by presenting tone or notone at each of four key-brightness levels.Learning was more rapid with two cues than with either cue singly, demonstrating summation. The contribution made by the tone cue to the learning of the discrimination decreased with increasing discriminability of the light cue. The control exerted by the tone cue also decreased (i.e., the tone cue was overshadowed) with increasing discriminability of the light cue. In certain cases, the tone cue decreased control by brightness, showing that in two-cue discriminations each cue may reduce the control exerted by the other.     

Combined-stimulus control as a function of the response rate controlled by the absence of the single stimuli

Rat's bar-press responses were maintained at moderate rates during separate presentations of light and tone by separate but concurrent variable-interval schedules of food and shock presentation. The relative response rate maintained during light-out-no-tone was alternated in four successive phases: in Phases 1 and 3 responding was maintained at a higher rate than that during light and tone alone by a variable-interval food schedule, while in Phases 2 and 4 responding was reduced to a lower rate by a differential-reinforcement-of-other-behavior food schedule. In test presentations of light, tone and a light-plus-tone combination, administered at the end of each phase, the proportion of responses emitted during light-plus-tone was an inverse function of the relative response rate controlled by light-out-no-tone, indicating that the relative training response rate controlled by the absence of the single stimuli determined the control exerted by the combined stimuli. Different relative response rates maintained in training may also be partly responsible for previously observed differences in the form of generalization gradients following the establishment of multi-stimulus control.     

Reversibility of single-incentive selective associations.

Rats were trained to press a lever in the presence of a tone-light compound stimulus and not to press in its absence. In each of two experiments, schedules were designed to make the compound a conditioned punisher for one group and a conditioned reinforcer for the other. In Experiment 1, one group's responding produced food in the presence of the compound but not in its absence. The other group's responding terminated the compound stimulus, and food was presented only in its absence. When tone and light were later presented separately, light controlled more responding than did tone in the former group, but tone gained substantial control in the latter. The same effects were also observed within subjects when the training schedules were switched over groups. In Experiment 2, two groups avoided shock in the presence of the compound stimulus. In the absence of the compound, one group was not shocked, and the other received both response-independent and response-produced shock. When tone and light were presented separately, the former group's responding was mainly controlled by tone, but the latter group's responding was almost exclusively controlled by light. These effects were also observed within subjects when the training schedules were switched over groups. Thus, these single-incentive selective association effects (appetitive in Experiment 1 and aversive in Experiment 2) were completely reversible. The schedules in which the compound should have been a conditioned reinforcer consistently produced visual control, and auditory control increased when the compound should have become a conditioned punisher. Currently accepted accounts of selective associations based on affinities between shock and auditory stimuli and between food and visual stimuli (i.e., stimulus-reinforcer interactions) do not adequately address these results. The contingencies of reinforcement most recently associated with the compound and with its absence, rather than the nature of the reinforcer, determined whether auditory or visual stimulus control developed.     

Avoidance learning facilitates temporal processing in the primary auditory cortex

The primary auditory cortex is now known to be involved in learning and memory, as well as auditory perception. For example, spectral tuning often shifts toward or to the frequency of the conditioned stimulus during associative learning. As previous research has focused on tonal frequency, less is known about how learning might alter temporal parameters of response in the auditory cortex. This study addressed the effects of learning on the fidelity of temporal processing. Adult male rats were trained to avoid shock that was signaled by an 8.0 kHz tone. A novel control group received non-contingent tone and shock with shock probability decreasing over days to match the reduced number of shocks received by the avoidance group as they mastered the task. An untrained (nai ve) group served as a baseline. Following training, neuronal responses to white noise and a broad spectrum of tones were determined across the primary auditory cortex in a terminal experiment with subjects under general anesthesia. Avoidance conditioning significantly improved the precision of spike-timing: the coefficient of variation of 1st spike latency was significantly reduced in avoidance animals compared to controls and nai ves, both for tones and for noise. Additionally, avoidance learning was accompanied by a reduction of the latency of peak response, by 2.0-2.5 ms relative to nai ves and approximately 1.0 ms relative to controls. The shock-matched controls also exhibited significantly shorter peak latency of response than nai ves, demonstrating the importance of this non-avoidance control. Plasticity of temporal processing showed no evidence of frequency specificity and developed independently of the non-temporal parameters magnitude of response, frequency tuning and neural threshold, none of which were facilitated. The facilitation of temporal processing suggests that avoidance learning may increase synaptic strength either within the auditory cortex, in the subcortical auditory system, or both.     

Second-order schedules with paired auditory brief stimuli

Pigeons were exposed to multiple second-order schedules of paired and unpaired brief stimuli in which responding on the main key was reinforced according to a fixed-interval thirty-second schedule by a brief stimulus (a tone in the paired schedule) and advancement to the next segment of the second-order schedule. In Experiment 1, a response on the second key was required during the tone in its fourth and final presentation to produce food. Responses during earlier brief stimuli indicated the extent to which the final brief stimulus was discriminated from preceding ones. Responding was comparable during all tones, extending prior findings with visual paired brief stimuli and weakening explanations of subjects' failure to discriminate between brief-stimulus presentations in terms of elicited responding. In Experiment 2 the number of fixed-interval segments comprising the second-order schedules varied from one through eight. Although main-key response rates increased across segments in both experiments, they increased much less sharply with a variable number of segments. These results suggest that the increase in main-key response rates across segments is due primarily to a degree of temporal discrimination not reflected on the second key. Main-key response rates were higher on paired auditory brief-stimulus schedules than on unpaired visual brief-stimulus schedules, especially in Experiment 2, thus further extending findings with visual brief stimuli to second-order schedules with auditory brief stimuli.     

Recovery of an overshadowed association achieved by extinction of the overshadowing stimulus

Three experiments are reported in which conditioned lick suppression by water-deprived rats was used as an index of associative strength. In Experiment 1, overshadowing of a light by a tone was observed when the light-tone compound stimulus was paired with foot shock. After initial compound pairings, the tone-shock association was extinguished in one group of subjects. Subsequently, these animals demonstrated significantly higher levels of suppression to the light relative to a control group in which the tone had not been extinguished. Experiment 2 replicated this effect while failing to find evidence to support the possibilities that extinction presentations of the overshadowing tone act as retrieval cues for the light-shock association, or that, via second-order conditioning, the light-shock association is actually formed during extinction of the tone. Experiment 3 determined that the recovery from overshadowing observed in Experiments 1 and 2 was specific to the extinction of the overshadowing stimulus rather than the extinction of any excitatory cue. Collectively, these results suggest that the debilitated response to an overshadowed stimulus does not represent an acquisition failure, but rather the failure of an acquired association to be manifest in behavior.     

Stimulus generalization of conditioned eyelid responses produced without cerebellar cortex: implications for plasticity in the cerebellar nuclei

In Pavlovian eyelid conditioning and adaptation of the vestibulo-ocular reflex, cerebellar cortex lesions fail to completely abolish previously acquired learning, indicating an additional site of plasticity in the deep cerebellar or vestibular nucleus. Three forms of plasticity are known to occur in the deep cerebellar nuclei: formation of new synapses, plasticity at existing synapses, and changes in intrinsic excitability. Only a cell-wide increase in excitability predicts that learning should generalize broadly from a training stimulus to other stimuli capable of supporting learning, whereas the alternatives predict that learning should be relatively specific to the training stimulus. Here we show that deep nucleus plasticity, as assessed by conditioned eyelid responses produced without input from the cerebellar cortex, is relatively specific to the training conditioned stimulus (CS). We trained rabbits to a tone or light CS with periorbital stimulation as the unconditioned stimulus (US), and pharmacologically disconnected the cerebellar cortex during a posttraining generalization test. The short-latency conditioned responses unmasked by this treatment showed strong decrement along the dimension of auditory frequency and did not generalize across stimulus modalities. These results cannot be explained solely by a cell-wide increase in the excitability of deep nucleus neurons, and imply that an input-specific mechanism in the deep cerebellar nucleus operates as well.     

Selective attention and stimulus-reinforcer interactions in the pigeon

The study supplies further evidence that non-associative effects and temporal-spatial similarities between certain combinations of cue and consequence cannot explain all instances of stimulus-reinforcer interactions. Pigeons were trained to press a treadle in the presence of a discriminative compound stimulus either to avoid shock or to obtain a food reinforcer. The compound stimulus was composed of diffuse tone and light cues which had identical temporal patterns of onset, duration and offset. With the avoidance schedule the auditory cue acquired more control than the visual cue; however, when food was the reinforcer, the visual cue exerted more control. This pattern of stimulus control on the appetitive schedule did not change if random shocks were also added, even though these shocks were equal in density to the food presentations and equal in magnitude to those used for the avoidance schedule. Other changes in the appetitive procedure, such as making the tone spatially contiguous with food and removing the light in the food hopper, also failed to alter the relative control by the different cues. Prior training with a food reinforcer did not produce any change in the relative control by the two cues when the birds were retrained on the shock-avoidance schedule. The results suggest that some frequently stated alternatives to selective associability are not adequate explanations of this instance of a stimulus-reinforcer interaction.     

SELECTIVE ASSOCIATIONS PRODUCED SOLELY WITH APPETITIVE CONTINGENCIES: THE STIMULUS-REINFORCER INTERACTION REVISITED

In studies reporting stimulus-reinforcer interactions in traditional conditioning paradigms, when a tone-light compound was associated with food the light gained stimulus control, but when the compound was paired with shock avoidance the tone gained control. However, the physical nature of the reinforcerrelated events (food vs. shock) presented in the presence of the tone-light compound was always confounded with the conditioned hedonic value of the compound's presence relative to its absence. When the compound was paired with shock, its presence was negative relative to its absence (which was shock-free). In contrast, when the compound was paired with food, its presence was positive relative to its absence (which was food-free). The present experiment dealt with this confounding effect by conditioning a tone-light compound to be positive or negative, relative to its absence, solely with food reinforcement. One group of rats received food for responding in the presence of the tone-light compound and no food in its absence. The other group also responded in the presence of the compound, but received food only in its absence. These rats were trained on a chained schedule in which responding in the presence of the tone-light compound produced a terminal link signaled by the absence of the compound; responding ceased in the terminal link because it delayed food delivery. In a test session to assess stimulus control by the elements of the compound, tone and light were presented separately under extinction conditions. Rats that had been exposed to a positive correlation between food and the compound emitted almost double the responses in the presence of the light as in the presence of the tone. In comparison, rats that had been exposed to a negative correlation emitted only two thirds as many responses in the presence of the light as in the presence of the tone. Because this selective association was produced using only food, it appears that the contingencies under which a reinforcer is presented, rather than (or as well as) its physical properties, can generate the selective associations previously attributed to “stimulus-reinforcer interactions.” This could mean that regardless of the class of reinforcer that ultimately maintains responding (appetitive or aversive), the contingency-generated hedonic value of the compound stimulus may influence the dominant modality of stimulus control.