Studies on the aversive classical conditioning. 1. Acquisition and differentiation of motor and cardiac conditioned classical defensive reflexes in dog.
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Classical conditioning provides a rich and powerful method for studying basic learning, memory, and emotion processes in animals. However, it is important to recognize that an animal's performance in a conditioning experiment provides only an indirect indication of what it has learned. Various remembering and forgetting processes, in addition to other psychological processes, may intervene and complicate what investigators can infer about learning from performance. This article reviews the role of context, interference, and retrieval in a number of classical conditioning phenomena (e.g. extinction), and provides an overview of how long-term and short-term memory processes influence behavior as it is studied in classical conditioning.
Classical conditioning of the marine snail Hermissenda can be produced in a single session of 50 pairings of light and rotation stimuli. Voltage clamp measurements of two outward K+ currents, IA and ICa2(+)-K+ were obtained from medial Type B photoreceptors that were isolated from the nervous system 1 day after animals were exposed to paired light and rotation stimuli or control procedures (Unpaired, or no exposure to light and rotation), ICa2(+)-K+ was found to be unchanged 18-30 h after 50 training trials. This result is consistent with a previous study where ICa2(+)-K+ was found to be unchanged after 50 light and rotation trials, although significantly reduced by 100 trials. In the present study 50 pairings of light and rotation produced a significant reduction in IA, suggesting an important role for this current in the earliest stages of classical conditioning.
Two groups of Ss received either two or 16 paired classical conditioning trails beyond the peak CR. A third group received the same stimuli as the 16 postpeak condition but in an unpaired and random order. The stimuli in all three groups were delivered directly to S. Subsequently, all three groups, including a fourth which was not given any prior direct classical conditioning, were exposed to vicariously instigated classical conditioning. This consisted of having S observe someone (model) employed by E who received the same CS as was delivered during direct conditioning. The CS was paired with the feigned arm movement of the model, simulating a reaction to shock. This vicarious classical conditioning procedure when compared to direct classical conditioning resulted in smaller GSR magnitudes for both the CRs and UCRs. Previous experience with direct classical conditional seems to have had an attenuating effect on GSR magnitude during the vicarious situation. A postexperimental questionnaire tended to support the results, and the relationship between the present study and current classical conditioning theory is discussed.
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Previous attempts to condition classically the pupillary response have resulted in mixed outcome. Studies using light as the UCS have generally been unsuccessful while those studies using shock as the UCS have been more successful. In the present study six subjects were visually presented 15 CVC trigrams while their pupil sizes were monitored. Five of the CVCs had been previously presented, five had been previously presented while paired with shock, and five had not been previously presented. Analysis indicated that more pupillary constriction occurred to the five CVCs paired with shock than those presented without shock or those not previously presented. The resulting classically conditioned pupillary constriction is discussed in terms of the development of meaning through classical conditioning.
Exposure to restraint and brief intermittent tailshocks facilitates associative learning of the classical conditioned eyeblink response in male rats. Based on evidence of sex differences in learning and responses to stressful events, we investigated sexually dimorphic effects of a stressor of restraint and intermittent tailshock on classical eyeblink conditioning 24 h after stressor cessation. Our results indicate that exposure to the acute stressor had diametrically opposed effects on the rate of acquisition of the conditioned response in male vs. female rats. Exposure to the stressor facilitated acquisition of the conditioned response in males, whereas exposure to the same stressful event dramatically impaired acquisition in females. We further demonstrate that the stress-induced impairment in female conditioning is dependent on the presence of ovarian hormones. Conditioning of stressed sham-ovariectomized females was significantly impaired relative to the unstressed controls, whereas conditioning in stressed ovariectomized females was not impaired. We present additional evidence that estrogen mediates the stress-induced impairment in female acquisition. Females administered sesame oil vehicle and then stressed were significantly impaired relative to their unstressed controls, whereas females administered the estrogen antagonist tamoxifen prior to stress were not impaired. In summary, these results indicate that exposure to the same aversive event can induce opposite behavioral responses in males vs. females. These effects underscore sex differences in associative learning and emotional responding, and implicate estrogen in the underlying neuronal mechanism.
During classical conditioning of the rabbit blink reflex, a large fraction of the hippocampal pyramidal neurons are recruited to respond to the conditioned stimulus. The summed response of these neurons comes to match the whole time-amplitude profile of nictitating membrane movement, whereas some individual neurons respond only to part of this profile. A model is described which accounts for these data. The model proposes a learning rule to explain neuron recruitment and uses a tapped delay line to account for the temporal learning properties of the system and the spectrum of individual unit responses.
Classical conditioning of sexual arousal has previously been demonstrated in human males but not in females. This study explored the role of classical (Pavlovian) conditioning in the activation of genital sexual arousal in both women and men, and assessed the effects of varying conditioned stimulus (CS) duration (subliminal/conscious) and relevance (sexually relevant/irrelevant). Twenty-seven female and 29 male participants received either subliminal or conscious presentations of a photograph of either a sexually relevant (abdomen of the opposite sex) or irrelevant (gun) CS+, which was followed by the unconditioned stimulus (US-erotic film clip). A CS-, a stimulus not paired with the US, was also included in the 11 conditioning trials. Ten participants were assigned to a control group that received unpaired presentations of the CS+, CS-, and the US. Both women and men showed more evidence of conditioning to the abdomen than to the gun when the CS was presented subliminally. When consciously perceived CSs were used, however, gender differences emerged. Men again showed the expected cue-to-consequence specificity but women showed the opposite effect, that is, conditioned arousal to the sexually irrelevant rather than to the relevant CS. The latter finding may be due to increased autonomic nervous system arousal associated with the irrelevant CS (gun). Skin conductance responses indicated more general arousal to the gun than to the male abdomen in women. This is the first study to compare the effects of a subliminal and conscious CS and to find classical conditioning of sexual arousal in women.
Eyeblink classical conditioning (EBCC) is a useful paradigm for studying the neurobiology of learning and memory. EBCC shows large age effects and has been shown to be sensitive to Alzheimer-like neuropathology. The EBCC data of 241 participants, including young, middle-aged, and elderly normal adults, adults with Down's syndrome, and patients with probable Alzheimer's disease, were analyzed to identify a minimum number of trials for reliable assessment. Results indicate that EBCC performance can be as reliably assessed in 63 trials as in 90 trials. Using fewer conditioning trials reduces administration time, making EBCC more practical for both research and potential diagnostic purposes.
A classical conditioning method was used to alter in acute fashion a discrete portion of the activity rhythm of squirrel monkeys living in social groups. Time of day was considered the unconditioned stimulus, while a previously neutral flashing light was used as the conditioned stimulus. When the CS was associated with an active period, its subsequent presentation during a quiet time of day resulted in significant increases in activity in conditioned subjects. This demonstration of the conditionability of daily activity patterns has important implications in both clinical and experimental settings.
Classical conditioning of the eyelid response in the rabbit was used to investigate the neuronal structures mediating basic associative learning of discrete, adaptive responses. Lesions of the ipsilateral dentate-interpositus nuclei, but not of the cerebellar cortex, abolished the learned eyeblink response. Recordings from these nuclei have revealed neuronal responses related to the learning of the response. Stimulating these recording sites produced the eyelid response. The dentate-interpositus nuclei were concluded to be critically involved in the learning and production of classically conditioned responses.
Rabbits received classical conditioning of the nictitating membrane response (NMR) in a trace conditioning paradigm. In this paradigm, a 250-ms tone conditioned stimulus (CS) occurs, after which there is a 500-ms period of time in which no stimuli occur (the trace interval), followed by a 100-ms air puff unconditioned stimulus (UCS). In Experiment 1, lesions of the hippocampus or cingulate/retrosplenial cortex disrupted acquisition of the long-latency or adaptive conditioned response relative to unoperated controls and animals that received neocortical lesions that spared the cingulate/retrosplenial areas. When animals with hippocampal or cingulate/retrosplenial lesions were switched to a standard delay paradigm in which the CS and UCS were contiguous in time, they acquired in about the same number of trials as naive rabbits. In a second experiment multiple-unit activity in area CA1 of the hippocampus was examined during acquisition of the trace conditioned response (CR). Three groups of animals were tested: animals that had a 500-ms trace interval (Group T-500), animals that received explicitly unpaired presentations of the CS and UCS (Group UP), and animals that underwent conditioning with a 2,000-ms trace interval (Group T-2000). Animals in Group T-500 acquired the CR in about 500 trials. Early in training, and well before any CRs occurred, there was a substantial increase in neuronal activity in the hippocampus that began during the CS and persisted through the trace interval. There was also an increase in the UCS period that modeled the amplitude-time course of the behavioral unconditioned response. Later in conditioning as CRs emerged, there was no longer neuronal bursting throughout the CS + trace period. Rather, the activity shifted to later in the trace interval and formed a model of the amplitude-time course of the behavioral CR. Activity during the UCS period was similar to that seen earlier in conditioning. Animals in Group UP showed no behavioral conditioning and no increase in neuronal activity. Animals in Group T-2000 showed no long-latency behavioral conditioning and no increase in neuronal activity. The data are discussed in terms of the role of the hippocampus in conditioning during situations in which the CS and UCS are not contiguous in time.
This paper contains a critical review of the claim that evaluative conditioning (EC) represents a theoretically distinct form of classical conditioning. A review of the evidence suggests that: (i) while it is claimed that EC can occur without awareness, EC studies have either adopted inappropriate statistical comparisons to demonstrate this or have failed to use the control conditions necessary to indicate that what is being measured is associative conditioning; (ii) there is no theoretical reason why conditioning without awareness might be observed in any conditioning paradigm if a relatively complex covariation assessment procedure such as that adopted in EC studies is used; and (iii) there are a variety of possible explanations for the relative resistance to extinction reported with EC, some of which allude to failure to use appropriate control conditions and others which point to specific details unique to the EC extinction procedure. Until these appropriate procedural and statistical comparisons are made, it is concluded that it is premature to assume that EC represents a form of conditioning that is theoretically distinct from other types of classical conditioning.
A classical conditioning procedure, in which tones of different intensities and frequencies constituted the conditioned stimuli and an air puff on the corner of the infants' eye represented the unconditioned stimulus, proved to be an effective device for evaluating the hearing ability of young babies. The 45 infants participating in the present study were able to start responding to the presentation of the tones (i.e. complete and prolonged closure of their eye before the onset of the air puff or independent of the puff) in a relatively short period of time. The presence of responding could be regarded as a reliable sign of the infants' hearing functioning across frequencies and intensities.
Hippocampal participation in classical conditioning in terms of Grossberg's (1975) attentional theory is described. According to the present rendition of this theory, pairing of a conditioned stimulus (CS) with an unconditioned stimulus (US) causes both an association of the sensory representation of the CS with the US (conditioned reinforcement learning) and an association of the sensory representation of the CS with the drive representation of the US (incentive motivation learning). Sensory representations compete among themselves for a limited-capacity short-term memory (STM) that is reflected in a long-term memory storage. The STM regulation hypothesis, which proposes that the hippocampus controls incentive motivation, self-excitation, and competition among sensory representations thereby regulating the contents of a limited capacity STM, is introduced. Under the STM regulation hypothesis, nodes and connections in Grossberg's neural network are mapped onto regional hippocampal-cerebellar circuits. The resulting neural model provides (a) a framework for understanding the dynamics of information processing and storage in the hippocampus and cerebellum during classical conditioning of the rabbit's nictitating membrane, (b) principles for understanding the effect of different hippocampal manipulations on classical conditioning, and (c) numerous novel and testable predictions.
We have recorded the firing activities of hippocampal pyramidal cells throughout the classical conditioning of eyelid responses in alert cats. Pyramidal cells (n = 220) were identified by their antidromic activation from the ipsilateral fornix and according to their spike properties. Upper eyelid movements were recorded with the search coil in a magnetic field technique. Latencies and firing profiles of recorded pyramidal cells following the paired presentation of conditioned (CS) and unconditioned (US) stimuli were similar, regardless of the different sensory modalities used as CS (tones, air puffs), the different conditioning paradigms (trace, delay), or the different latency and topography of the evoked eyelid conditioned responses. However, for the three paradigms used here, evoked neuronal firing to CS presentation increased across conditioning, but remained unchanged for US presentation. Contrarily, pyramidal cell firing was not modified when the same stimuli used here as CS and US were presented unpaired, during pseudoconditioning sessions. Pyramidal cell firing did not seem to encode eyelid position, velocity, or acceleration for either reflex or conditioned eyelid responses. Evoked pyramidal cell responses were always in coincidence with a beta oscillatory activity in hippocampal extracellular field potentials. In this regard, the beta rhythm represents a facilitation, or permissive time window, for timed pyramidal cell firing. It is concluded that pyramidal cells encode CS-US associative strength or CS predictive value.
This study examined the temporal characteristics and behavioral correlates of the conditioned response (CR) following classical conditioning of the embryonic Day 20 (E20 rat fetus). The conditioning procedure involved pairing of an artificial nipple (the CS) with an infusion of milk (the US) to establish classical conditioning. The test for classical conditioning involved measurement of a stimulus-evoked facial wiping response in a classical conditioning test. Experiment 1 compared the effectiveness of one- and three-trial procedures to establish classical conditioning. Experiment 2, 3, and 4 described the time course for the CR following one- and three-trial conditioning procedures. Experiments 3b and 4b describe the behavioral responses to (a) presentation of the CS at the time of conditioning, (b) infusion of the milk US at the time of conditioning, and (c) reexposure to the CS before the test for classical conditioning. Experiments 5 and 6 exposed the fetus to manipulations that either increased or decreased stretching (a behavior found to be associated with the CR). The results are discussed in terms of the temporal characteristics and behavioral correlates of conditioned and unconditioned responses and their mediation by activity in endogenous mu and kappa opioid systems.