Differential effects of inactivation of the orbitofrontal cortex on strategy set-shifting and reversal learning

Different subregions of the rodent prefrontal cortex (PFC) mediate dissociable types of behavioral flexibility. For example, lesions of the medial or orbitofrontal (OFC) regions of the PFC impair extradimensional shifts and reversal learning, respectively, when novel stimuli are used during different phases of the task. In the present study, we assessed the effects of inactivation of the OFC on strategy set-shifting and reversal learning, using a maze based set-shifting task mediated by the medial PFC. Long–Evans rats were trained initially on a visual-cue discrimination to obtain food. On the subsequent day, rats had to shift to using a response strategy (e.g., always turn left). On Day 3 (reversal), rats were required to reverse the direction of their turn (e.g., always turn right). Infusions of the local anesthetic bupivacaine into the OFC did not impair initial visual discrimination learning, nor did it impair performance on the set-shift. In contrast, inactivation of the OFC did impair reversal learning; yet, these rats ceased using the previously acquired response rule as readily as controls. Instead, rats receiving OFC inactivations made a disproportionate number of erroneous arm entries towards the visual-cue, suggested that these animals reverted back to using the original visual-cue based strategy. These findings, in addition to previous data, further support the notion that the OFC and medial PFC play dissociable roles in reversal learning and set-shifting. Furthermore, the lack of effect of OFC inactivations on the set-shift indicates that this type of behavioral flexibility does not require cognitive operations related to reversal learning.     

Olfactory discrimination, reversal learning, and stimulus control in rats.

Rats were trained to discriminate lights, tones, or odors and then given a series of discrimination reversals. Only rats trained with odors showed positive transfer on the first reversal and acquisition of a reversal set. Other experiments demonstrated that rats preferentially attend to odors when presented in compound with lights or tones; that odors exert more discriminative control than tones in tests using compound stimuli of competing sign; and that after pretraining on the positive stimulus, acquisition of an odor but not a light discrimination occurs with virtually no errors. These results demonstrate the importance of stimulus modality in the establishment of stimulus control and the need for more careful analysis of stimulus factors in cross-species comparisons of learning ability.     

Successive olfactory reversal learning in honeybees

Honeybees Apis mellifera can associate an originally neutral odor with a reinforcement of sucrose solution. Forward pairings of odor and reinforcement enable the odor to release the proboscis extension reflex in consecutive tests. Bees can also be conditioned differentially: They learn to respond to a reinforced odor and not to a nonreinforced one. They can also learn to reverse their choice. Here we ask whether honeybees can learn successive olfactory differential conditioning tasks involving different overlapping pairs of odors. The conditioning schedules were established in order to train the animals with 3, 2, 1, or 0 reversals previous to a last differential conditioning phase in which two additional reversals were present. We studied whether or not successive reversal learning is possible and whether or not learning olfactory discrimination reversals affects the solving of subsequent discrimination reversals. Therefore we compared the responses of bees that had experienced reversals with those of bees that had not experienced such reversals when both are confronted with a new reversal situation. In experiment 1 we showed that bees that had experienced three previous reversals were better in solving the final reversal task than bees with no previous reversal experience. In experiment 2, we showed that one reversal learning is enough for bees to perform better in the final reversal task. The successive different reversals trained in our experiments resemble the natural foraging situation in which a honeybee forager has to switch successively from an initial floral species to different ones. The fact that experiencing such changes seems to improve a bee's performance in dealing with further new exploited food sources has therefore an adaptive impact for the individual and for the colony as a whole.     

Context specificity of operant discrimination performance in pigeons

In an experiment designed to investigate odors as potential retrieval cues in pigeons' memory (i.e., as conditional stimuli), 8 pigeons first learned to peck a red keylight (S+, reinforced) and not a blue one (S−, extinguished) in the presence of either a eucalyptus oil or isoamyl acetate odor. They were repeatedly switched between two chambers with the same odor to habituate any reaction to the switching that would be required for eventual testing for conditional control by the odors. Next, the birds learned the reversal (blue S+, red S−) in the presence of the alternative odor in one of these chambers. When the birds were then switched to the alternative chamber for additional training, although the odor was still appropriate to the reversal problem, behavior appropriate to the original training condition recurred. Testing indicated that reversal performance was specific to the one chamber in which it had been trained.     

Discrimination learning with and without “errors”

Responses to S− (“errors”) are not a necessary condition for the formation of an operant discrimination of color. Errors do not occur if discrimination training begins early in conditioning and if S+ and S− initially differ with respect to brightness, duration and wavelength. After training starts, S−'s duration and brightness is progressively increased until S+ and S− differ only with respect to wavelength. Errors do occur if training starts after much conditioning in the presence of S+ has occurred or if S+ and S− differ only with respect to wavelength throughout training. Performance following discrimination learning without errors lacks three characteristics that are found following learning with errors. Only those birds that learned the discrimination with errors showed (1) “emotional” responses in the presence of S−, (2) an increase in the rate (or a decrease in the latency) of its response to S+, and (3) occasional bursts of responses to S−.     

Context specificity of operant discriminative performance in pigeons: II. Necessary and sufficient conditions

Six experiments were performed to explore the necessary and sufficient conditions for producing context specificity of discriminative operant performance in pigeons. In Experiment 1, pigeons learned a successive discrimination (red S+/blue S−) in two chambers that had a particular odor present and between which they were frequently switched. The birds subsequently learned the reversal (blue S+/ red S−) in one of these chambers with a different odor present. When switched to the alternative chamber, although the odor and the reinforcement contingency were still appropriate to the reversal, performance appropriate to the original discrimination recurred in subjects for which the houselights were on during training and testing but not for those for which the houselights were off. This indicated the importance of visual contextual cues in producing context specificity. Experiment 2 showed that the frequent switching between boxes in initial training was of no consequence, presumably because the apparatus cues were highly salient to the subjects. Experiment 3 showed significantly less context specificity when odor cues were omitted. Experiment 4 showed that simply using a different reinforced stimulus in each phase of training was ineffective in producing context specificity. Experiment 5 showed that the generalization test procedure used in Experiment 4 was sensitive to context specificity when discrimination-reversal training was used with different odors in the two training phases. Experiment 6 replicated the results of Experiment 4, but then showed that when different odors accompanied the two training phases, context specificity was obtained with the single-stimulus paradigm. Thus in both single-stimulus and discrimination-reversal paradigms, redundant odor cues potentiated learning about apparatus cues.     

Interactive effects of training condition and septal lesions on perseverative responding in the rat.

Rats that had received septal lesions either prior to acquisition of a position habit (Group SAR) or immediately after position habit acquisition (Group SR) were tested on two reversals of the task. Compared with control-operated rats, both groups of rats with septal lesions exhibited position-habit reversal deficits. The two groups with septal lesions could not be distinguished in terms of the total number of errors made during reversal learning, but could be distinguished on the basis of the type of error committed. Compared with Group SR, Group SAR made significantly more perservative errors on the first reversal and significantly fewer perserverative errors on the second reversal. Group SR made significantly more nonperservative errors than Group SAR on both reversals.     

Interocular generalization: a study of mirror-image reversal following monocular discrimination training in the pigeon

Generalization gradients along a continuum of angular orientation were obtained from four pigeons, following monocular training on a discrimination between a 45° oblique line (S+) and a 135° oblique line (S−). All pigeons were trained on a chain DRO VI 1 schedule of reinforcement. Generalization gradients obtained with the trained and untrained eye were compared. All pigeons responded maximally to the 45° line (S+) when tested with only the trained eye open. During generalization tests of interocular transfer with only the untrained eye open, three pigeons responded maximally to S− (135°), the mirror-image of the stimulus associated with reinforcement during training (45°). The other pigeon failed to show interocular transfer of the discrimination. Interocular reversal of left-right mirror-image stimuli has not been reported for any other species.     

SUCCESSIVE REVERSALS OF A CLASSICALLY CONDITIONED HEART-RATE DISCRIMINATION1

Rats were trained to criterion in successive reversals of a classically conditioned heart-rate discrimination. Criterion was attained more rapidly in the later reversals in the series than in the early reversals and the inter-problem learning curve was of the same general form as that found with successive instrumental discrimination reversal in the same species.     

The involvement of the orbitofrontal cortex in learning under changing task contingencies

Previous investigations examining the rat prefrontal cortex subregions in attentional-set shifting have commonly employed two-choice discriminations. To better understand how varying levels of difficulty influence the contribution of the prefrontal cortex to learning, the present studies examined the effects of orbitofrontal cortex inactivation in a two- or four-choice odor reversal learning test. Long-Evans rats were trained to dig in cups that contained distinct odors. In the two-choice odor discrimination, one odor cup was always associated with a cereal reinforcement in acquisition while the opposite odor cup was associated with a cereal reinforcement in reversal learning. In the four-choice odor discrimination, an additional two cups containing distinct odors were used that were never associated with reinforcement in acquisition or reversal learning. Bilateral infusions of the GABA-A agonist, muscimol (0.5 microg) into the orbitofrontal cortex did not impair acquisition of either the two- or four-choice discrimination task. However, muscimol infusions into the orbitofrontal cortex impaired two- and four-choice reversal learning. In the two-choice odor reversal, muscimol treatment selectively increased perseverative errors. In the four-choice odor reversal, muscimol treatment increased perseverative, regressive, as well as irrelevant errors. These findings suggest that the orbital prefrontal cortex not only enables task switching by supporting the initial inhibition of a previously relevant choice pattern, but under increasing task demands also enables the reliable execution of a new choice pattern and reduction of interference to irrelevant stimuli.     

Serial reversal learning in bumblebees (Bombus impatiens)

Bumblebees are capable of rapidly learning discriminations, but flexibility in bumblebee learning is less well understood. We tested bumblebees (Bombus impatiens) on a serial reversal learning task. A serial reversal task requires learning of an initial discrimination between two differentially rewarded stimuli, followed by multiple reversals of the reward contingency between stimuli. A reduction in errors with repeated reversals in a serial reversal task is an indicator of behavioural flexibility. Bees were housed in a large indoor environment and tested during foraging flights. Testing free-flying bees allowed for large numbers of trials and reversals. All bees were trained to perform a simultaneous discrimination between two colours for a nectar reward, followed by nine reversals of this discrimination. Results showed that bumblebees reduced errors and improved their performance across successive reversals. A reduction in perseverative errors was the major cause of the improvement in performance. Bees showed a slight increase in error rate in their final trials, perhaps as a consequence of increasing proactive interference, but proactive interference may also have contributed to the overall improvement in performance across reversals. Bumblebees are thus capable of behavioural flexibility comparable to that of other animals and may use proactive interference as a mechanism of behavioural flexibility in varying environments.     

Discrimination and Reversal Learning by Toddlers Aged 15-23 Months

Few studies have investigated simple discrimination and discrimination reversal learning by children younger than 2 years. Extant research has shown that teaching discrimination reversals may be challenging with this population. We used social reinforcement and correction procedures to teach simple simultaneous discrimination and discrimination reversal tasks involving three pairs of animal pictures displayed in a paper notebook. Participants were eight typically developing toddlers aged 15-23 months. All learned at least one simple discrimination/discrimination reversal problem. Four children learned all problems and showed evidence of learning set formation. Perhaps surprisingly, discrimination reversals were sometimes learned more rapidly than original discriminations. The procedures suggest a potentially efficient methodology for investigating more complex aspects of relational learning in toddlers.

     

An olfactory discrimination procedure for mice

This paper describes an olfactory discrimination procedure for mice that is inexpensively implemented and leads to rapid discrimination learning. Mice were first trained to dig in small containers of sand to retrieve bits of buried chocolate. For discrimination training, two containers were presented simultaneously for eight trials per session. One container held sand mixed with cinnamon, and the other held sand mixed with nutmeg. Both containers were baited with chocolate buried in the sand. One odor was designated S+, and mice were allowed to dig and retrieve the chocolate from this container. The other odor was S-, and both containers were removed immediately if subjects began to dig in an S- container. After meeting a two-session acquisition criterion, subjects were given a series of discrimination reversals. In Experiment 1, 12 Swiss-Webster mice (6 male and 6 female) acquired the olfactory discrimination in three to five sessions and completed 3 to 10 successive discrimination reversals within a 50-session testing limit. In Experiment 2, subjects were 14 Pah(enu2) mice, the mouse mutant for phenylketonuria; 7 were homozygotes in which the disorder was expressed (PKU), and 7 were heterozygotes with normal metabolism (non-PKU). Thirteen mice completed pretraining in four to seven sessions, acquisition required 3 to 12 sessions, and all mice completed at least three reversals. Learning rates were similar in PKU and non-PKU mice. We discuss issues related to implementation and several potentially useful procedural variations.     

Successive reversals involving two cues

Rats were trained on a visual discrimination problem with two relevant cues—brightness and orientation. They were then given eight reversals in succession on the same problem. After reversals 7 and 8 they were tested with each cue presented on its own to see how much they had learned about each. Individual animals tended to reverse the cue about which they learned more from reversals 7 to 8, so that animals that had learned reversal 7 mainly in terms of the brightness cue learned reversal 8 mainly in terms of the orientation cue and vice versa. The result provides further confirmation for a two-process model of discrimination learning in which one process is that of selective attention     

An investigation of reversal learning in octopus vulgaris lamarck

Eighteen octopuses were trained by a method of successive discrimination training to discriminate between a vertical and a horizontal rectangle. They were then overtrained for either 20 or 60 trials, after which they learnt the reverse discrimination. At the beginning of each reversal they were given 20 trials pretraining on the new positive stimulus. The subjects completed from two to nine reversals.

It was found that the amount of overtraining had no effect on the rate of learning the subsequent reversal. The first four reversals all took significantly longer to learn than the original problem, but did not differ significantly from one another. However, examination of the raw data suggests that later reversals do take longer to learn. The performance when learnt (i.e. on the first day of overtraining) was as good after reversal learning as after the learning of the original problem.

The results do not show definite signs that could be interpreted as an exhaustion of a limited supply of neurones available for learning.     

Cycloheximide produces amnesia for extinction and reconsolidation in an appetitive odor discrimination task in rats

A considerable literature has shown deficits in memory resulting from the administration of protein synthesis inhibitors; however, most of the past literature in this field has focused on acquisition of new memory using aversively-motivated tasks. The effect of protein synthesis inhibition on appetitive learning and memory as well as extinction is less clear. The present study employed an appetitive odor discrimination paradigm to examine the effects of acute cycloheximide administration (1 mg/kg) on reconsolidation and extinction.Male, Long-Evans adult rats were trained to discriminate between two odors (i.e., cocoa and cinnamon) and then received extinction trials following an intraperitoneal injection of cycloheximide or vehicle. Twenty-four hours later, rats were tested via one non-reinforced test trial. Results showed amnesia for extinction as well as original training (i.e., correct odor choice) in cycloheximide-injected rats in this appetitive task, while vehicle-injected controls showed good memory for extinction. These data add to a growing literature showing the importance of protein synthesis inhibition for extinction and reconsolidation in appetitive learning and memory.     

The intercalated reinforcement technique: Learning without differential total reinforcement between groups

An intercalated reinforcement technique is described. The method equates number of trials, response topography, sensory exposure, and frequency of reinforcement between reversal Ss overtrained on a discrimination and then trained on reversals and nonreversal Ss similarly overtrained but continued on the same discrimination. In extending previous successful work in the rat, monkeys were trained on spatial discrimination and reversal tasks in the WGTA at 50%, 75%, and 100% reinforcement in order to test the efficacy of learning by this procedure, and to compare the method with learning obtained by a more classical procedure. Learning rates were the same by both procedures. This technique, therefore, appears useful for investigating neurochemical (or other) correlates of learning unconfounded by performance or sensory effects.     

Strain and sex differences on olfactory discrimination learning in C57BL/6J and DBA/2J inbred mice (Mus musculus)

In this study, the authors explored potential strain and sex differences in nonspatial cognitive ability. Beginning around 90 days of age, male and female C57BL/6J (C57) and DBA/2J (DBA) inbred mice (Mus musculus) were tested on a task of simple odor discrimination learning with 3 repeated reversals. Males learned the task more readily than females, and DBA mice learned the task more readily than C57 mice. All differences became evident after repeated testing. Similarity of perseveration measures indicated the differences were not due to inhibitory deficits. Instead, a phase analysis localized differences to a transitional period of reversal learning. Females increased transitional errors that more likely indicated adaptive sampling strategies than memory failures. C57 females used this strategy indiscriminately, but DBA females sampled as a function of environmental uncertainty.     

Visual discrimination and reversal learning in rough-necked monitor lizards (Varanus rudicollis)

Reptile learning has been studied with a variety of methods and has included numerous species. However, research on learning in lizards has generally focused on spatial memory and has been studied in only a few species. This study explored visual discrimination in two rough-necked monitors (Varanus rudicollis). Subjects were trained to discriminate between black and white stimuli. Both subjects learned an initial discrimination task as well as two reversals, with the second reversal requiring fewer sessions than the first. This reduction in trials required for reversal acquisition provides evidence for behavioral flexibility in the monitor lizard genus.     

Chickadees discriminate contingency reversals presented consistently,but not frequently

Chickadees are high-metabolism, non-migratory birds, and thus an especially interesting model for studying how animals follow patterns of food availability over time. Here, we studied whether black-capped chickadees (Poecile atricapillus) could learn to reverse their behavior and/or to anticipate changes in reinforcement when the reinforcer contingencies for each stimulus were not stably fixed in time. In Experiment 1, we examined the responses of chickadees on an auditory go/no-go task, with constant reversals in reinforcement contingencies every 120 trials across daily testing intervals. Chickadees did not produce above-chance discrimination; however, when trained with a procedure that only reversed after successful discrimination, chickadees were able to discriminate and reverse their behavior successfully. In Experiment 2, we examined the responses of chickadees when reversals were structured to occur at the same time once per day, and chickadees were again able to discriminate and reverse their behavior over time, though they showed no reliable evidence of reversal anticipation. The frequency of reversals throughout the day thus appears to be an important determinant for these animals’ performance in reversal procedures.