Pavlovian Second-order Conditioning Research Articles

Effects of ventral striatal lesions on first‐ and second‐order appetitive conditioning

Rats with bilateral lesions of the ventral striatal nucleus accumbens failed to acquire Pavlovian second-order conditioning to auditory stimuli paired with visual stimuli that had previously received first-order pairings with food. This deficit in second-order conditioning was specific to learning driven by incentive properties of the first-order cues, and was observed whether the first-order training had occurred prior to or after lesion surgery. Lesions also produced deficits in the display of conditioned responses to the first-order conditioned stimulus, but only when they were made after first-order training. These results suggest a specific role for the ventral striatum in acquiring and expressing incentive properties of conditioned stimuli through second-order conditioning, as well as a more general role in expressing previously acquired Pavlovian conditioned responses.

Rapid Associative Encoding in Basolateral Amygdala Depends on Connections with Orbitofrontal Cortex

Certain goal-directed behaviors depend upon interactions between basolateral amygdala (ABL) and orbitofrontal cortex (OFC). Here we describe neurophysiological evidence of this cooperative function. We recorded from ABL in intact and OFC-lesioned rats during learning of odor discrimination problems and reversals. During learning, rats with ipsilateral OFC lesions exhibited a marked decline in the proportion of ABL neurons that fired differentially during cue sampling both before and after reversal and in the proportion of neurons that reversed odor preference when the odor-outcome associations were reversed. This decline appeared to reflect a loss of rapid flexibility in cue selectivity that characterized activity in intact rats. In addition, lesioned rats had fewer neurons that fired in anticipation of the predicted outcome during a delay period after responding but before outcome delivery. These findings support a role for OFC in facilitating the encoding of information about expected outcomes in ABL.

Lesions of basolateral amygdala impair extinction of CS motivational value, but not of explicit conditioned responses, in Pavlovian appetitive second-order conditioning.

The basolateral amygdala (BLA) is important for the modification of the motivational significance of events through associative learning. In previous work, we found that BLA was critical for the acquisition of conditioned reinforcement value to a visual conditioned stimulus (CS) paired with food. Unlike normal rats, rats with neurotoxic lesions of the BLA failed to acquire Pavlovian second-order conditioning to an auditory stimulus paired with the first-order visual CS in the absence of food. In this experiment, we examined the role of BLA in the extinction of the previously acquired conditioned reinforcement value of a Pavlovian CS. Rats received first-order visual CS-food pairings prior to either BLA- or sham-lesions. Subsequent CS-alone extinction training reduced the ability of the visual CS to reinforce second-order conditioning of an auditory stimulus in the sham-lesioned rats, but not in the BLA-lesioned rats. Despite this persistence of the conditioned reinforcement value of the visual first-order CS in the BLA-lesioned rats, no effects of the lesions were observed on extinction of the explicit behavioural conditioned responses elicited by that CS.

The basolateral complex of the amygdala is necessary for acquisition but not expression of CS motivational value in appetitive Pavlovian second-order conditioning.

The basolateral complex of the amygdala (ABL) is involved in processing information about stimulus motivational value. However, it is not clear whether the ABL is critical for acquisition, maintenance, or expression of this information. Our previous work has shown that ABL lesions made prior to training, block acquisition of an appetitive Pavlovian second-order conditioning task, in which performance is thought to depend on the acquisition of motivational (conditioned reinforcement) value by the first-order conditioned stimulus (CS). The present experiments examined the effects of ABL lesions made after first-order conditioning, when the CS acquires motivational value, but before second-order conditioning, the test for acquired value of that CS. Rats received pairings of a visual CS with a food reinforcer. They then received bilateral sham or excitotoxic lesions of the ABL. After recovery, they received pairings of a second-order auditory CS with the previously conditioned visual CS. In two experiments, both sham and lesioned rats acquired normal second-order conditioned behaviours. Some of the same rats were then given another round of second-order conditioning with novel CSs. In this case, when first-order training occurred after surgery, some second-order conditioned behaviours were impaired in lesioned rats. Tests of the associative underpinnings of second-order conditioned behaviours showed that those behaviours impaired by ABL lesions were based on stimulus-response associations. The results show that although the ABL is critical for second-order conditioning, this role is limited to acquisition of information about the motivational value of the first-order CS, and it is not critical for maintenance of this information or for its use in forming second-order associations.

Disconnection of the basolateral amygdala complex and nucleus accumbens impairs appetitive pavlovian second-order conditioned responses.

There is considerable evidence that the basolateral complex of the amygdala (ABL) is involved in learning about the motivational value of otherwise neutral stimuli. The authors examined the role in this function of the ABL and one of its major efferent structures. the nucleus accumbens. Male Long-Evans rats received either sham, ipsilaterally, or contralaterally placed unilateral lesions of the ABL and accumbens and were trained in an appetitive Pavlovian second-order conditioning task. Sham-lesioned and ipsilaterally lesioned rats acquired the task normally, but contralaterally lesioned rats, in which the ABL and accumbens were functionally disconnected, failed to acquire second-order conditioned responses (although they did acquire second-order conditioned orienting responses). The results suggest that the ABL and accumbens are part of a system critical for processing information about learned motivational value.

Transfer of Value from S+ to S- in Simultaneous Discriminations in Humans

When animals learn a simultaneous discrimination, some of the value of the positive stimulus (S+) appears to transfer to the negative stimulus (S-). The present experiments demonstrate that such value transfer can also be found in humans. In Experiment 1 humans were trained on 2 simple simultaneous discriminations, the first between a highly positive stimulus, A (1,000 points); and a negative stimulus, B (0 points); and the second between a less positive stimulus, C (100 points); and a negative stimulus, D (0 points). On test trials, most participants preferred B over D. In Experiments 2 and 3 the value of the 2 original discriminations was equated in training (A[100]B[0] and C[100]D[0]). In Experiment 2 the values of the positive stimuli were then altered (A[1,000]C[0]); again, most participants preferred B over D. In Experiment 3, however, when the values of B and D were altered (B[1,000]D[0]), participants were indifferent to A and C. Thus, the mechanism that underlies value transfer in humans appears to be related to Pavlovian second-order conditioning. Similar mechanisms may be involved in assimilation processes in social contexts.

Pavlovian second-order conditioned analgesia.

Three experiments with rat subjects assessed conditioned analgesia in a Pavlovian second-order conditioning procedure by using inhibition of responding to thermal stimulation as an index of pain sensitivity. In Experiment 1, rats receiving second-order conditioning showed longer response latencies during a test of pain sensitivity in the presence of the second-order conditioned stimulus (CS) than rats receiving appropriate control procedures. Experiment 2 found that extinction of the first-order CS had no effect on established second-order conditioned analgesia. Experiment 3 evaluated the effects of post second-order conditioning pairings of morphine and the shock unconditioned stimulus (US). Rats receiving paired morphine-shock presentations showed significantly shorter response latencies during a hot-plate test of pain sensitivity in the presence of the second-order CS than did groups of rats receiving various control procedures; second-order analgesia was attenuated. These data extend the associative account of conditioned analgesia to second-order conditioning situations and are discussed in terms of the mediation of both first- and second-order analgesia by an association between the CS and a representation or expectancy of the US, which may directly activate endogenous pain inhibition systems.

Pavlovian second-order conditioned analgesia.

Three experiments with rat subjects assessed conditioned analgesia in a Pavlovian second-order conditioning procedure by using inhibition of responding to thermal stimulation as an index of pain sensitivity. In Experiment 1, rats receiving second-order conditioning showed longer response latencies during a test of pain sensitivity in the presence of the second-order conditioned stimulus (CS) than rats receiving appropriate control procedures. Experiment 2 found that extinction of the first-order CS had no effect on established second-order conditioned analgesia. Experiment 3 evaluated the effects of post second-order conditioning pairings of morphine and the shock unconditioned stimulus (US). Rats receiving paired morphine-shock presentations showed significantly shorter response latencies during a hot-plate test of pain sensitivity in the presence of the second-order CS than did groups of rats receiving various control procedures; second-order analgesia was attenuated. These data extend the associative account of conditioned analgesia to second-order conditioning situations and are discussed in terms of the mediation of both first- and second-order analgesia by an association between the CS and a representation or expectancy of the US, which may directly activate endogenous pain inhibition systems.

Associative influence on the foraging behavior of pigeons (Columba livia).

In a laboratory simulation of foraging conditions, pigeons maintained ad lib weight by treadle pressing for lengthy periods of access to grain in a 24-hr live-in environment. Localized visual signals produced by treadle pressing evoked approach and pecking behavior if they signaled impending food presentation (Pavlovian first-order conditioning) or the presentation of an established signal for food (Pavlovian second-order conditioning). These findings imply a role for associative mechanisms in the control of foraging.

Pavlovian Second-Order Conditioning: Studies in Associative Learning

Pavlovian Second-Order Conditioning: Studies in Associative Learning

Spatial contiguity facilitates Pavlovian second-order conditioning.

Two experiments investigated the effects of spatial contiguity upon the formation of second-order conditioning in pigeon subjects. Experiment 1 used an autoshaping procedure to pair two visual stimuli, S2 and S1, after S1 had previously been paired with food. The resulting second-order conditioning of S2 was superior when both stimuli appeared on the same response key within a trial, compared with their appearing on different keys. Experiment 2 found a similar importance of spatial contiguity between S2 and S1 in a conditioned suppression paradigm. In addition, consistently presenting S2 and S1 in the same spatial location produced superior conditioning compared with varying their spatial relation from trial to trial. The design of these experiments was such as to imply that spatial contiguity facilitates performance by improving the formation of association rather than by promoting stimulus generalization or pseudoconditioning. Moreover, the observation of a facilitative effect of spatial contiguity between S1 and S2 in two different paradigms that use qualitatively different unconditioned stimuli and evoke different responses implies some generality for these findings. Consequently, these results suggest that spatially contiguous stimuli are especially associable in Pavlovian conditioning paradigms.

Spatial contiguity facilitates Pavlovian second-order conditioning.

Two experiments investigated the effects of spatial contiguity upon the formation of second-order conditioning in pigeon subjects. Experiment 1 used an autoshaping procedure to pair two visual stimuli, S2 and S1, after S1 had previously been paired with food. The resulting second-order conditioning of S2 was superior when both stimuli appeared on the same response key within a trial, compared with their appearing on different keys. Experiment 2 found a similar importance of spatial contiguity between S2 and S1 in a conditioned suppression paradigm. In addition, consistently presenting S2 and S1 in the same spatial location produced superior conditioning compared with varying their spatial relation from trial to trial. The design of these experiments was such as to imply that spatial contiguity facilitates performance by improving the formation of association rather than by promoting stimulus generalization or pseudoconditioning. Moreover, the observation of a facilitative effect of spatial contiguity between S1 and S2 in two different paradigms that use qualitatively different unconditioned stimuli and evoke different responses implies some generality for these findings. Consequently, these results suggest that spatially contiguous stimuli are especially associable in Pavlovian conditioning paradigms.