Mauricio R. Papini

Comparative Psychology of Surprising Nonreward

The surprising or unexpected omission of an appetitive reinforcer has at least two effects: An allocentric effect according to which the organism updates knowledge about the environment, and an egocentric effect that allows the organism to learn about its own emotional reaction to the change. This egocentric effect (traditionally called frustration) is correlated to activation of the hypothalamic-pituitary-adrenal axis, can be modulated by treatment with anxiolytics, and is expressed in terms of behavioral changes that have an emotional component (e.g., agonistic behavior). It is hypothesized that all vertebrates share the mechanisms underlying the allocentric effect, but only mammals possess the mechanisms underlying the egocentric effect. It is further argued that frustrative mechanisms evolved in early mammals from those underlying fear conditioning.

Opioid receptors modulate recovery from consummatory successive negative contrast.

Three experiments explored the role of the opioid system in consummatory successive negative contrast. In Experiment 1, rats treated with the nonspecific opioid-receptor antagonist naloxone (2mg/kg) exhibited increased suppression after a shift from 32% to 6% sucrose solution (32-->6), relative to 6-->6 unshifted controls. A similar but shorter effect was observed with the delta-opioid receptor antagonist naltrindole (1mg/kg). In Experiment 2, naloxone increased suppression after a more conventional 32-->4 sucrose shift. In Experiment 3, rats classified as expressing slow recovery from contrast (after a 32-->4 sucrose downshift) were more sensitive to naloxone in an activity test than fast-recovery rats. Whereas it was previously known that contrast was reduced by the extrinsic administration of opioid agonists, the effects reported here with antagonists provide the first evidence that the opioid system is intrinsically engaged by situations involving surprising reward loss.

Instrumental learning in toads (Bufo arenarum): reinforcer magnitude and the medial pallium.

Two experiments studied the effects of shifts in the amount of water reinforcement on the instrumental performance of toads (Bufo arenarum) using one trial per day. In the first experiment, a shift from a large to a small reward magnitude led to a gradual change in performance without evidence of negative contrast. A shift from large or small reward magnitude to extinction led to similar extinction rates and provided no indication of the magnitude of reinforcement extinction effect. In the second experiment, the gradual change in performance (with no contrast) after a shift from a large to a small reward magnitude was completely eliminated by ablation of the medial pallium. These results provide support for the hypothesis that the medial pallium in amphibians is homologous to the hippocampal formation in mammals and also indicate that species differences in these learning phenomena may be related to the differential development and differentiation of the hippocampal formation.

Lesions of the medial pallium, but not of the lateral pallium, disrupt spaced-trial avoidance learning in goldfish (Carassius auratus)

The effects of telencephalic lesions of the medial pallium (MP) and lateral pallium (LP) of goldfish on avoidance learning were studied in a two-way, shuttle response, spaced-trial avoidance conditioning situation. Animals received one trial per day, a training regime that permits the assessment of avoidance learning in the absence of stimulus carry-over effects from prior trials. Control and LP-lesioned goldfish exhibited significantly faster avoidance learning than MP-lesioned animals. These results suggest that the MP, but not the LP, is responsible for the widely described deficits in avoidance learning after lesions of the entire telencephalon. The proposal of a functional similarity between the fish MP and the mammalian amygdala, known to be involved in fear conditioning, suggests a conservative phylogenetic role of this area in avoidance learning.

Selective Effects of the δ-Opioid Receptor Agonist DPDPE on Consummatory Successive Negative Contrast.

Two experiments explored the role of the opioid system in a situation involving a surprising reduction in reward magnitude: consummatory successive negative contrast. Rats received access to 32% sucrose solution (preshift Trials 1-10) followed by 4% solution (postshift Trials 11-15). Independent groups received an injection of either the vehicle or the delta-receptor agonist [D-Ala2-,N-Me-Phe4,Gly-ol] enkephalin (DPDPE; 24 microg/kg). DPDPE attenuated the contrast effect when injected before Trial 11 but not when injected before Trial 12. An additional experiment showed that the attenuating effect of partial reinforcement on the recovery from contrast was reduced by DPDPE injections administered before nonreinforced preshift trials.

Involvement of the telencephalon in spaced-trial avoidance learning in the goldfish (Carassius auratus)

Goldfish (Carassius auratus) received escape-avoidance training in a shuttle-response situation at a rate of a single trial per day. Widely spaced training evaluates the ability of a discriminative stimulus to control an avoidance response in the absence of stimulus carry-over effects from prior recent trials. In Experiment 1, master goldfish exhibited significantly faster avoidance learning than yoked controls. The results suggest that the shuttle response was instrumentally acquired. Experiment 2 demonstrated a significant deficit in the acquisition of avoidance behavior following ablation of the telencephalon. The implications of spaced-trial, telencephalon-dependent avoidance learning, as demonstrated in these experiments for the first time, are discussed in the context of comparative research on instrumental learning in goldfish. These results provide further support for the hypothesis that the fish telencephalon contains an emotional system that is critical for fear conditioning.

Successive negative contrast in the consummatory responding of didelphid marsupials

In a consummatory experiment patterned after previous work with rats and goldfish, successive negative incentive contrast was sought in didelphid marsupials of two species (Lutreolina crassicaudata andDidelphis albiventris). Half of the subjects of each species were trained from the outset with a 32% sucrose solution and shifted occasionally to a 4% sucrose solution; the rest, which served as controls, were trained only with the 4% solution. The positive results obtained (less response to the 4% solution in the shifted subjects than in the controls) fit the hypothesis, based on comparative work with descendants of older vertebrate lines, that the mechanism of successive negative incentive contrast evolved in a common reptilian ancestor of birds and mammals.

Administration of corticosterone after the first downshift trial enhances consummatory successive negative contrast

Rats given access to a 32% sucrose solution and then downshifted to a 4% solution exhibit less contact with the sipper tube than unshifted controls always given access to 4% solution. This phenomenon, called consummatory successive negative contrast, was facilitated in Experiment 1 by a post-trial injection of corticosterone (3 mg/kg) administered immediately after the first downshift trial. Experiment 2 demonstrated that this facilitatory effect of post-trial corticosterone does not occur when administered 3 hr after the first downshift trial. These results support the hypothesis that corticosterone strengthens an aversive emotional component elicited by the surprising downshift in reward magnitude during the initial downshift trial.

The Two-Test Strategy in the Study of Inhibitory Conditioning

It is commonly believed that both a summation test and a retardation test should be used to determine whether a stimulus becomes inhibitory in consequence of some specified treatment, because the 2 tests together rule out alternative interpretations. Depending, however, on the choice of control treatments, a single test may provide credible evidence of inhibition or both together may not. A comprehensive review of the 2-test literature shows that suitable controls have been used only rarely and that compelling evidence of inhibition is correspondingly rare. The only such evidence now available is provided by retardation tests in experiments with some variation of A+/AB- training as the putatively inhibitory treatment.

Incentive Contrast in Domestic Dogs (Canis familiaris)

Dogs (Canis familiaris) trained to receive a preferred food (dry beef liver) from an experimenter learned to maintain a longer gaze on the experimenter than dogs receiving a less preferred food (dog pellets). Dogs downshifted from dry liver to pellets rejected food more frequently than nonshifted controls. Gaze duration also decreased in downshifted dogs below the level of a group always reinforced with pellets. In addition, downshifted dogs tended to move away from the experimenter, adopting a lying down posture. This phenomenon, called successive negative contrast, has been described in analogous experiments with a variety of mammalian species, but has failed to occur in similar experiments with nonmammalian vertebrates. Unlike similar previous observations, the present data were obtained in an environment involving interspecific communication.