Experimental evidence for spatial learning in cuttlefish (Sepia officinalis)

Laboratory mazes were used to study spatial-learning capabilities in cuttlefish (Sepia offcinalis), using escape for reinforcement. In preliminary observations, cuttlefish in an artificial pond moved actively around the environment and appeared to learn about features of their environment. In laboratory experiments, cuttlefish exited a simple alley maze more quickly with experience and retained the learned information. Similar improvement was not found in open-field mazes or T mazes, perhaps because of motor problems. Cuttlefish learned to exit a maze that required them to find openings in a vertical wall. The wall maze was modified to an arena, and simultaneous discrimination learning and reversal learning were demonstrated. These experiments indicate that cuttlefish improve performance over serial reversals of a simultaneous, visual-spatial discrimination problem.     

Conditional same/different concept learning in the short‐beaked echidna (Tachyglossus aculeatus)

Echidnas have evolved separately from other mammalian groups for around 200 million years and incorporate a mixture of reptilian and mammalian features. Because of these attributes, they have historically been considered “primitive” animals. However, they have successfully adapted to a wide variety of ecological niches and their neurophysiology demonstrates a number of unusual and apparently sophisticated characteristics, including a relatively large brain and cerebral cortex and a comparatively massive frontal cortex. Studies of learning in the echidna have thus far been limited to only a handful of experiments which demonstrated relatively basic abilities such as forming a position habit in a T‐maze, successive habit‐reversal learning, and simple visual and instrumental discrimination. This study aimed to expand on these results and test the “primitive” echidna on what are generally considered more advanced cognitive tasks—same/different and conditional same/different concept learning. The results demonstrated that echidnas are able to discriminate on the basis of a relational same/different concept, using simultaneously presented multi‐element stimuli, and transfer that discrimination to novel stimuli. After further training, they were then able to repeat the performance when the correct choice was conditional on the background color of the stimulus panels.     

Orientation in the cuttlefish <Emphasis Type="Italic">Sepia officinalis</Emphasis>: response <Emphasis Type="Italic">versus</Emphasis> place learning

Several studies have demonstrated that mammals, birds and fish use comparable spatial learning strategies. Unfortunately, except in insects, few studies have investigated spatial learning mechanisms in invertebrates. Our study aimed to identify the strategies used by cuttlefish (Sepia officinalis) to solve a spatial task commonly used with vertebrates. A new spatial learning procedure using a T-maze was designed. In this maze, the cuttlefish learned how to enter a dark and sandy compartment. A preliminary test confirmed that individual cuttlefish showed an untrained side-turning preference (preference for turning right or left) in the T-maze. This preference could be reliably detected in a single probe trial. In the following two experiments, each individual was trained to enter the compartment opposite to its side-turning preference. In Experiment 1, distal visual cues were provided around the maze. In Experiment 2, the T-maze was surrounded by curtains and two proximal visual cues were provided above the apparatus. In both experiments, after acquisition, strategies used by cuttlefish to orient in the T-maze were tested by creating a conflict between the formerly rewarded algorithmic behaviour (turn, response learning) and the visual cues identifying the goal (place learning). Most cuttlefish relied on response learning in Experiment 1; the two strategies were used equally often in Experiment 2. In these experiments, the salience of cues provided during the experiment determined whether cuttlefish used response or place learning to solve this spatial task. Our study demonstrates for the first time the presence of multiple spatial strategies in cuttlefish that appear to closely parallel those described in vertebrates.     

Sign tracking in cuttlefish (Sepia officinalis)

Two groups of cuttlefish (Sepia officinalis) were used to demonstrate classical conditioning in this species and to determine whether the resulting approach response would be that of sign tracking or goal tracking. For cuttlefish in the paired condition, a flashing light was presented at one end of a long tank followed by food dropped into the center of the tank. For cuttlefish in the unpaired condition, food was dropped into the center of the tank either before or after the flashing-light stimulus. Paired cuttlefish oriented to the light, positioned themselves within striking distance, and occasionally attacked the light. Unpaired cuttlefish showed no reliable response to either stimulus. The results demonstrate that cuttlefish are capable of signal learning and that, under the conditions tested, cuttlefish sign tracked. This study begins a comparative analysis of learning in cuttlefish and offers a possible ecological advantage for sign-tracking behavior.     

Development and crossmodal transfer of contextual control of emergent stimulus relations

Six normally capable adults first learned three conditional relations in each of two prospective equivalence classes via match-to-sample training with figures as conditional (sample) and discriminative (comparison) stimuli. Then one trained conditional relation in each prospective class was brought under the control of contextual stimuli, two dictated nonsense syllables. Test performances indicated the emergence of untrained conditional relations, and therefore two equivalence classes, that were conditional on the contextual stimuli. These tests involved untrained combinations of contextual stimuli and stimuli in conditional relations, suggesting that the contextual stimuli functioned independently to control conditional relations rather than forming compound stimuli with samples and comparisons in training. Next, two novel figures were made equivalent to each of the original dictated contextual stimuli by match-to-sample training and testing. On subsequent tests, all subjects demonstrated transfer of conditional control of untrained conditional relations from the original auditory contextual stimuli to equivalent visual stimuli. These outcomes further supported the conclusion that the contextual stimuli exerted true conditional control over conditional relations in the equivalence classes and were not merely elements of compound stimuli.     

Contextual conditional discriminations

Three experiments used a discriminated operant procedure to study conditional discrimination learning in rats. The first experiment showed that rats were capable of learning a biconditional discrimination in which two contexts served as conditional cues signalling the reinforcement contingencies associated with two discriminative stimuli. The discrimination was learned equally well when one discriminative stimulus signalled food, the other its absence, and when one stimulus signalled food, the other extinction plus mild footshock.

In Experiment 2 it was shown that prior training on such a conditional discrimination enhanced the subsequent context specificity of simple conditioning relative to control groups of animals for whom the prior training had not been conditional. Experiment 3 showed that a reversal of the significance of one pair of discriminative stimuli produced no spontaneous reversal in performance to a second, target, pair.

The pattern of results is best accounted for by an analysis of contextual conditional discrimination learning in terms of stimulus configurations and offers no support for the notion that rats may learn a general conditional rule or set.     

Experimental evidence for spatial learning on octopuses (octopus bimaculoides)

Octopuses forage far from temporary home dens to which they return for shelter. Spatial tasks may assess learning. Octopuses (Octopus bimaculoides) were placed in a novel arena, and their movements were tracked for 72 hr. Movements around the arena decreased across time, consistent with exploratory learning. Next, octopuses were given 23 hr to move around an arena; after a 24-hr delay, their memory of a burrow location was tested. Most remembered the location of the open burrow, demonstrating learning in 1 day. Finally, octopuses were trained to locate a single open escape burrow among 6 possible locations. Retention was tested after a week and was immediately followed by reversal training (location rotated 180 degrees ). Octopuses learned the original location of the burrow, remembering it for a week. Path lengths increased significantly after reversal, gradually improving and showing relearning. Octopuses show exploratory behavior, learning, and retention of spatial information.     

Transfer of contextual stimulus function via equivalence class development

In a conditional discrimination, 6 college students arranged six Cyrillic letters into groups of three based upon which of two additional Cyrillic letters (contextual stimuli) was present. All subjects demonstrated symmetry and transitivity within each class of equivalent stimuli. In a second conditional discrimination, two more Cyrillic letters were related to each contextual stimulus. Testing of symmetrical and transitive relations between the original contextual stimulus and the two new ones confirmed the development of two three-member classes of contextual stimuli. Subsequent tests demonstrated that the new contextual stimuli controlled the previously trained sample-comparison relations for all subjects.     

Microcomputer-based programmed instruction in identity matching to sample for persons with severe disabilities

Three individuals with mental retardation, who had failed to learn identity matching to sample with standard fading and prompting procedures, were given microcomputer-based programmed instruction. The methods were based on an analysis of two features of typical identity matching procedures: (a) within each trial, the current sample stimulus must control comparison selection, and (b) across trials, specific comparison stimuli must function both as S+ and as S–, depending upon the sample presented (conditional discrimination). During the first phase of training, one-trial acquisition of discriminative stimulus control was established in a nonconditional discrimination context where the S+ or S– functions of specific stimuli did not change from trial to trial. After one-trial learning was established, conditional discrimination was programmed by gradually introducing reversals of S+/S– stimulus functions. All three participants learned to perform conditional identity matching. Avenues for further analysis of the prerequisites for conditional discrimination and continued development of programmed methods are discussed.     

Conditional discrimination in mentally retarded adults: the development of generalized skills.

The development of generalized conditional discrimination skills was examined in adults with retardation. Two subjects with histories of failure to acquire arbitrary matching under trial-and-error procedures were successful under procedures that trained one or more prerequisite skills. The successive discrimination between the sample stimuli was established by training the subjects to name the stimuli. The simultaneous discrimination between the comparison stimuli was established using either (a) standard simple discrimination training with reversals or (b) a procedure in which each of the two sample-comparison relations in the conditional discrimination was presented in blocks of trials, with the size of the blocks decreasing gradually until sample presentation was randomized. The amount of prerequisite training required varied across subjects and across successive conditional discriminations. After acquiring either two or three conditional discriminations with component training, both subjects learned new conditional discriminations under trial-and-error procedures. In general, each successive conditional discrimination was acquired more rapidly. Tests showed that conditional responding had become a generalized skill. Symmetry was shown for almost all trained relations. Symmetry trial samples were ultimately named the same as the stimuli to which they were related in training.     

Derived control by compound and single stimuli in a matching-to-sample task in children

A matching-to-sample procedure was used to investigate whether 9-year-old children would demonstrate the emergence of a derived compound-sample conditional discrimination following training in four interrelated single-sample conditional discriminations and vice versa, as adults did in previous studies. In Experiment 1, three out of three children demonstrated the emergence of a compound-sample conditional discrimination following training in four single-sample conditional discriminations. In Experiment 2, two out of three children acquired a compound-sample conditional discrimination and they demonstrated the emergence of four single-sample conditional discriminations; one of them did so only after being exposed to a remediation training and testing procedure. Training variables that facilitated discrimination emergence in both directions are discussed. In general, results showed that the sophisticated learning skills that are supposedly possessed by adults are not required to demonstrate the two types of derived control under study.     

Simplifying environmental cues in a Morris-type water maze improves place learning in old NMRI mice.

Old virgin female NMRI mice aged 17 months were compared with mice aged 3 months for their spatial learning abilities in two versions of the Morris water maze. The first one was a simplified version with a salient configuration of cues comparable to a black/white discrimination and the second one was the classical version of the Morris test with many distal cues surrounding the maze. In the simplified version, old mice presented a slower rate of acquisition and a transient poorer retention compared to young mice. However, old mice achieved a final level of performance statistically comparable to their young counterparts as assessed by latencies to escape onto the concealed platform and by the spatial bias measured in probe trials at intervals during testing. When subsequently subjected to classical Morris maze learning, the same old animals showed marked learning deficits and were persistently impaired in their latencies to escape onto the platform. They presented no spatial bias for the location of the platform in the different probe trials. When the goal was cued at the end of the experiment, the performances of old mice rapidly improved, showing that motivation, motor disabilities, or fatigue and ability to use proximal cues cannot explain the place learning deficit. Our results were discussed in terms of cognitive versus sensory/perceptual disabilities in aged rats and mice.     

Complex learning and information processing by pigeons: a critical analysis

Three models of conditional discrimination learning by pigeons are described: stimulus configuration learning, the multiple-rule model, and concept learning. A review of the literature reveals that true concept learning is not characteristic of the behavior of pigeons in matching-to-sample, oddity-from-sample, or symbolic matching studies. Instead, pigeons learn a set of sample-specific S^D rules. Transfer of the discrimination to novel stimuli, at least along the hue dimension, is predicted by a “coding hypothesis”, which holds that pigeons make a unique, but usually unobserved response, R₁, to each sample, and that the comparison stimulus chosen depends on which R₁ was emitted in the presence of the sample. Convincing evidence is found that pigeons do code sample hues, but there is little evidence that allows one to infer that the “coding event” must have behavioral properties. Parameters of the conditional discrimination paradigm are identified, and it is shown that by appropriate parametric manipulation, a variety of analogous tasks may be generated for both human and animal subjects. The tasks make possible the comparative study of complex learning, attention, memory, and information processing, with the added advantage that behavior processes may be compared systematically across tasks.     

Equivalence relations and the reinforcement contingency

Where do equivalence relations come from? One possible answer is that they arise directly from the reinforcement contingency. That is to say, a reinforcement contingency produces two types of outcome: (a) 2‐, 3‐, 4‐, 5‐, or n‐term units of analysis that are known, respectively, as operant reinforcement, simple discrimination, conditional discrimination, second‐order conditional discrimination, and so on; and (b) equivalence relations that consist of ordered pairs of all positive elements that participate in the contingency. This conception of the origin of equivalence relations leads to a number of new and verifiable ways of conceptualizing equivalence relations and, more generally, the stimulus control of operant behavior. The theory is also capable of experimental disproof.     

Can cuttlefish learn by observing others?

Observational learning is the ability to learn through observing others’ behavior. The benefit of observational learning is apparent in that individuals can save time and energy without trial-and-error, thus enhance the chance of survival and reproduction. Cephalopods (octopus, squid, and cuttlefish) have the most sophisticated central nervous system among invertebrates, and it is conceivable that cephalopods can develop some forms of cognition. Although it has been suggested that octopuses have the capacity of observational learning, a previous study indicates that cuttlefish do not improve their predation tactics by observing conspecifics. Given that the danger avoidance is important for animals’ survival, we sought to reevaluate whether cuttlefish show some form of observational learning or observational conditioning under threatening conditions. Cuttlefish (Sepia pharaonis) were divided into three groups: the Experiencer group, the Observer group, and the Control group. In the training phase, a toy submarine was remotely controlled to expel the cuttlefish from its initially preferred place to establish the threat-place association in the Experiencer group. In the Observer group, the threat-place association was established by expelling a conspecific demonstrator at the observer’s initially preferred place while the observer watched the whole process from behind a transparent divider. In the Control group, the observer watched a conspecific and a static toy submarine without actual threat. In the testing phase, the choice of safe place in the absence of threat was used to probe the learning/conditioning of cuttlefish. In the Experiencer group, we found that animals chose the safe place more often than their initially preferred place after training, an indication of the association learning/conditioning. However, in the Observer group, only a subset of animals showed this threat-place association by observation, while the place preference was unchanged in the Control group. These results indicate that most cuttlefish did not learn by observing others, but individual differences exist, and some cuttlefish may have the potential of observational learning/conditioning within their cognitive capacities.     

AUDITORY SUCCESSIVE CONDITIONAL DISCRIMINATION AND AUDITORY STIMULUS EQUIVALENCE CLASSES

This paper describes an experimental demonstration of stimulus equivalence classes consisting entirely of auditory stimuli. Stimuli were digitized arbitrary syllables (e.g., “cug,” “vek”) presented via microcomputer. Training and testing were conducted with a two-choice auditory successive conditional discrimination procedure. On each trial, auditory samples and comparisons were presented successively. As each comparison was presented, a response location (a rectangle) appeared on the computer screen. After all stimuli for a trial were presented, subjects selected one of the response locations. Six subjects acquired the conditional discrimination baseline, 4 subjects demonstrated the formation of three-member auditory equivalence classes resulting from sample-S+ relations, and 1 subject demonstrated equivalence classes resulting from sample-S— relations. Four subjects received additional training and subsequently demonstrated expansion of the three-member classes to four members each.     

Effects of ratio reinforcement schedules on discrimination performance by Japanese monkeys

In Experiment 1, Japanese monkeys were trained on three conditional position-discrimination problems with colors as the conditional cues. Within each session, each problem was presented for two blocks of ten reinforcements; correct responses were reinforced under continuous-reinforcement, fixed-ratio 5, and variable-ratio 5 schedules, each assigned to one of the three problems. The assignment of schedules to problems was rotated a total of three times (15 sessions per assignment) after 30 sessions of acquisition training. Accuracy of discrimination increased to a moderate level with fewer trials under CRF than under ratio schedules. In contrast, the two ratio schedules, fixed and variable, were more effective in maintaining accurate discrimination than was CRF. With further training, as asymptotes were reached, accuracy was less affected by the schedule differences. These results demonstrated an interaction between the effects of reinforcement schedules and the level of acquisition. In Experiment 2, ratio sizes were gradually increased to 30. Discrimination accuracy was maintained until the ratio reached 20; ratio 30 strained the performance. Under FR conditions, accuracy increased as correct choice responses cumulated after reinforcement.     

Conditional discrimination in mentally retarded subjects: programming acquisition and learning set.

In Experiment 1, 3 subjects with retardation were exposed to two visual-visual arbitrary matching-to-sample problems each day. One conditional discrimination was presented under trial-and-error conditions, and the other was presented under a component training procedure. The latter began by establishing the comparison discrimination and its rapid reversal. The successive discrimination between the sample stimuli was established through differential naming. Then, sample naming was maintained in conditional discrimination sessions in which the same sample was presented in blocks of consecutive trials. Block size was decreased across sessions until sample presentation was randomized as in trial-and-error training (but with naming maintained). Two subjects initially learned only with component training. The performance of the 3rd subject was inconsistent across conditional discriminations. One of the successful subjects ultimately learned rapidly and consistently with trial-and-error procedures. Experiment 2 sought to demonstrate learning set in the other 2 subjects. Elements of the component training procedure were withdrawn over successive conditional discriminations. Ultimately, 1 subject nearly always learned under trial-and-error conditions, and the other learned under trial-and-error conditions combined with differential sample naming.     

Spatial behavior in male and female crayfish (Orconectes rusticus): learning strategies and memory duration

Previous studies have demonstrated that animals use multiple strategies to solve spatial tasks. We used a T-maze to examine spatial behavior in crayfish, using visual and tactile stimuli as place cues and a food-scented escape tank as reinforcement to leave the maze. In trials on a single day and across multiple days, crayfish learned to exit the maze with significantly reduced latency and with fewer turns. In addition, we examined place memory in 40-min periods with the maze closed and found that crayfish spent longer in the vicinity of a previously open exit compared to a closed exit. Probe tests were conducted using a forced-choice procedure to determine whether crayfish remembered the route out of the maze using primarily place cues or response learning. We found that approximately equal numbers of animals used each strategy, and individuals were able to switch from one strategy to the other on different test days. Males and females did not differ significantly in their performance in the place memory test, maze exit task, or probe tests. Both sexes displayed place memory for the exit location and reduced latency to exit during trials 24 h, 48 h, 72 h, and 1 week after initial training trials, suggesting that spatial memories in crayfish are relatively enduring.     

Conditional discrimination learning: A critique and amplification

Carter and Werner recently reviewed the literature on conditional discrimination learning by pigeons, which consists of studies of matching-to-sample and oddity-from-sample. They also discussed three models of such learning: the “multiple-rule” model (learning of stimulus-specific relations), the “configuration” model, and the “single-rule” model (concept learning). Although their treatment of the multiple-rule model, which seems most applicable to the pigeon data, is generally excellent, their discussion of the other two models is incomplete and sometimes inaccurate. Potential problems of terminology are discussed in the present paper, as are additional lines of research that deserve consideration by those interested in further work in this area. The issue of response versus stimulus selection (configuration versus compound-cue learning) is discussed in connection with the configuration model. Particular attention is given to Carter and Werner's criticism of the application, in studies with other species, of the learning set procedure in testing for single-rule learning. Some of the important related issues are: the bias for improvement on new problems in a series, the adequacy of a multiple-rule model to explain learning set formation, and evidence in favor of the single-rule model, at least in primates. Consideration of these additional contributions to the study of conditional discrimination learning emphasizes the usefulness of this task in the comparative study of cognitive processes.