Food approach conditioning and discrimination learning using sound cues in benthic sharks

The marine environment is filled with biotic and abiotic sounds. Some of these sounds predict important events that influence fitness while others are unimportant. Individuals can learn specific sound cues and ‘soundscapes’ and use them for vital activities such as foraging, predator avoidance, communication and orientation. Most research with sounds in elasmobranchs has focused on hearing thresholds and attractiveness to sound sources, but very little is known about their abilities to learn about sounds, especially in benthic species. Here we investigated if juvenile Port Jackson sharks could learn to associate a musical stimulus with a food reward, discriminate between two distinct musical stimuli, and whether individual personality traits were linked to cognitive performance. Five out of eight sharks were successfully conditioned to associate a jazz song with a food reward delivered in a specific corner of the tank. We observed repeatable individual differences in activity and boldness in all eight sharks, but these personality traits were not linked to the learning performance assays we examined. These sharks were later trained in a discrimination task, where they had to distinguish between the same jazz and a novel classical music song, and swim to opposite corners of the tank according to the stimulus played. The sharks’ performance to the jazz stimulus declined to chance levels in the discrimination task. Interestingly, some sharks developed a strong side bias to the right, which in some cases was not the correct side for the jazz stimulus.     

Sex differences in discrimination reversal learning in the guppy

In several mammalian and avian species, females show a higher performance than males in tasks requiring cognitive flexibility such as the discrimination reversal learning. A recent study showed that female guppies are twice as efficient as males in a reversal learning task involving yellow–red discrimination, suggesting a higher cognitive flexibility in female guppies. However, the possibility exists that the superior performance exhibited by females does not reflect a general sex difference in cognitive abilities, but instead, is confined to colour discrimination tasks. To address this issue, we compared male and female guppies in two different discrimination reversal learning tasks and we performed a meta-analysis of these experiments and the previous one involving colour discrimination. In the first experiment of this study, guppies were tested in a task requiring them to learn to select the correct arm of a T-maze in order to rejoin a group of conspecifics. In experiment 2, guppies were observed in a numerical task requiring them to discriminate between 5 and 10 dots in order to obtain a food reward. Although females outperformed males in one condition of the T-maze, we did not find any clear evidence of females’ greater reversal learning performance in either experiment. However, the meta-analysis of the three experiments supported the hypothesis of females’ greater reversal learning ability. Our data do not completely exclude the idea that female guppies have a generally higher cognitive flexibility than males; however, they suggest that the size of this sex difference might depend on the task.     

Numerical acuity of fish is improved in the presence of moving targets,but only in the subitizing range

There is controversy in comparative psychology about whether on the one hand non-symbolic number estimation of small (≤4) and large numbers involves a single mechanism (an approximate number system), or whether on the other hand enumeration of the numbers 1–4 is accomplished by a separate mechanism, an object tracking system. To date, support for the latter hypothesis has come only from the different ratio-dependency of performance seen in the two numerical ranges, a reading that has been criticized on several grounds. In humans, the two-system hypothesis is supported by evidence showing that manipulation of the physical properties of the stimuli (e.g., the motion of the items) has dissimilar effects on small- and large-number discrimination. In this research, we studied this effect on guppies. Initially, fish were trained to simultaneously discriminate two numerical contrasts having the same easy ratio (0.50): one in the small-number (2 vs. 4) range and one in the large-number (6 vs. 12) range. Half of the fish were presented with moving items; the other half were shown the same stimuli without motion. Fish were then subjected to non-reinforced probe trials in the presence of a more difficult ratio (0.75: 3 vs. 4 and 9 vs. 12). Under both static and moving conditions, the fish significantly discriminated 6 versus 12, but not 9 versus 12 items. As regards small numbers, both groups learned to discriminate a 0.50 ratio, but only fish tested with moving stimuli also discriminated 3 and 4 items. This differential effect suggests that fish may possess two separate systems for small- and large-number discrimination.     

Involvement of the rat anterior cingulate cortex in control of instrumental responses guided by reward expectancy

The anterior cingulate cortex (ACC) plays a critical role in stimulus-reinforcement learning and reward-guided selection of actions. Here we conducted a series of experiments to further elucidate the role of the ACC in instrumental behavior involving effort-based decision-making and instrumental learning guided by reward-predictive stimuli. In Experiment 1, rats were trained on a cost-benefit T-maze task in which they could either choose to climb a barrier to obtain a high reward (four pellets) in one arm or a low reward (two pellets) in the other with no barrier present. In line with previous studies, our data reveal that rats with quinolinic acid lesions of the ACC selected the response involving less work and smaller reward. Experiment 2 demonstrates that breaking points of instrumental performance under a progressive ratio schedule were similar in sham-lesioned and ACC-lesioned rats. Thus, lesions of the ACC did not interfere with the effort a rat is willing to expend to obtain a specific reward in this test. In a subsequent task, we examined effort-based decision-making in a lever-press task where rats had the choice between pressing a lever to receive preferred food pellets under a progressive ratio schedule, or free feeding on a less preferred food, i.e. lab chow. Results show that sham- and ACC-lesioned animals had similar breaking points and ingested comparable amounts of less-preferred food. Together, the results of Experiment 1 and 2 suggest that the ACC plays a role in evaluating how much effort to expend for reward; however, the ACC is not necessary in all situations requiring an assessment of costs and benefits. In Experiment 3 we investigated learning and reversal learning of instrumental responses guided by reward predictive stimuli. A reaction time (RT) task demanding conditioned lever release was used in which the upcoming reward magnitude (five vs. one food pellet) was signalled in advance by discriminative visual stimuli. Results revealed that rats with ACC lesions were able to discriminate reward magnitude-predictive stimuli and to adapt instrumental behavior to reversed stimulus-reward magnitude contingencies. Thus, in a simple discrimination task as used here, the ACC appears not to be required to discriminate reward magnitude-predictive stimuli and to use the learned significance of the stimuli to guide instrumental behavior.     

Extensive training extends numerical abilities of guppies

Recent studies on animal mathematical abilities suggest that all vertebrates show comparable abilities when they are given spontaneous preference tests, such as selecting the larger number of food items, but that mammals and birds generally achieve much better performance than fish when tested with training procedures. At least part of these differences might be due to the fact that fish are usually trained with only one or two dozen trials while extensive training, sometimes with thousands of trials, is normally performed in studies of mammals and birds. To test this hypothesis, female guppies were trained on four consecutive numerical discriminations of increasing difficulty (from 2 vs. 3 to 5 vs. 6 items), with up to 120 trials with each discrimination. Five out of eight subjects discriminated all contrasts up to 4 versus 5 objects at levels significantly better than chance, a much higher limit than the 2 versus 3 limit previously reported in studies that provided fish with only short training sequences. Our findings indicate that the difference in numerical cognition between teleosts and warm-blooded vertebrates might be smaller than previously supposed.     

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.     

Colour versus quantity as cues in reverse-reward-competent squirrel monkeys (Saimiri sciureus)

To assess the relative salience of colour and quantity cues, squirrel monkeys previously trained to reach for the smaller of two quantities of food in a reverse-reward contingency task received colour discrimination training. After initial failure to discriminate between two colours of dots under a differential reinforcement regime, they learned the task when the S- colour was associated with zero reward. The monkeys then showed good retention on the original reverse-reward task of 1 versus 4 with pairs of dots presented in S+ or S- colours. However, on "mismatch" trials of 1S- versus 4S+ , only 2 of 4 monkeys tested showed a preference--1 monkey chose based on quantity, the other based on colour. Individual differences and the possible roles of overshadowing and blocking are discussed.     

Colour versus quantity as cues in reverse-reward-competent squirrel monkeys (Saimiri sciureus)

To assess the relative salience of colour and quantity cues, squirrel monkeys previously trained to reach for the smaller of two quantities of food in a reverse-reward contingency task received colour discrimination training. After initial failure to discriminate between two colours of dots under a differential reinforcement regime, they learned the task when the S? colour was associated with zero reward. The monkeys then showed good retention on the original reverse-reward task of 1 versus 4 with pairs of dots presented in S + or S? colours. However, on “mismatch” trials of 1S? versus 4S + , only 2 of 4 monkeys tested showed a preference—1 monkey chose based on quantity, the other based on colour. Individual differences and the possible roles of overshadowing and blocking are discussed.     

Shape discrimination and concept formation in the jungle crow (Corvus macrorhynchos)

We investigated whether jungle crows can learn concepts by using printouts of shapes in a simultaneous two-alternative task. Jungle crows were first trained with a red triangle and red square until they reached the discrimination criterion (80 % of correct choices in two blocks of 10 trials each). Then, we tested crows with successive transfer tests to investigate both the discrimination cues being used and concept formation ability, by using novel triangular and non-triangular stimuli. All of the jungle crows learnt to discriminate between the triangle and square during training. The discrimination performance was generally not affected either by changes in the colour of the stimuli or when both shape and colour cues conflicted, with the previously non-rewarded shape but matching colour (red square) versus rewarded shape but non-matching colour (green triangle). The use of only outlines of the familiar stimuli also did not affect discrimination behaviour of crows. In addition, crows significantly discriminated novel triangular shapes during the limited trials given, suggesting their ability to form the concept of triangularity. However, failure to discriminate when the novel stimuli size deviated from the original suggests that there is a limit to shape concept formation in a familiar–novel context in the jungle crow.     

Reconsolidation after remembering an odor-reward association requires NMDA receptors

A rapidly learned odor discrimination task based on spontaneous foraging behavior of the rat was used to evaluate the role of N-methyl-D-aspartate (NMDA) receptors (NMDARs) in ongoing memory consolidation. Rats were trained in a single session to discriminate among three odors, one of which was associated with palatable food reward. Previous experiments showed that the NMDAR antagonist DL-APV induced amnesia for this task when injected immediately after training. In the present study, memory was reactivated 24 h after training by exposure to the rewarded odor within the experimental context after which rats received an intracerebroventricular injection of APV. Combined reactivation-drug treatment induced profound amnesia when tested 48 h later. Animals receiving drug alone, in absence of reactivation, showed perfect retention. It is concluded that NMDARs support a consolidation process taking place after memory reactivation.     

Orbital prefrontal cortex and guidance of instrumental behavior of rats by visuospatial stimuli predicting reward magnitude

The orbital prefrontal cortex (OPFC) is part of a circuitry mediating the perception of reward and the initiation of adaptive behavioral responses. We investigated whether the OPFC is involved in guidance of the speed of instrumental behavior by visuospatial stimuli predictive of different reward magnitudes. Unoperated rats, sham-lesioned rats, and rats with bilateral lesions of the OPFC by N-methyl-D-aspartate (NMDA) were trained in a visuospatial discrimination task. The task required a lever press on the illuminated lever of two available to obtain a food reward. Different reward magnitudes were permanently assigned to lever presses to respective sides of the operant chamber; that is, responses to one lever (e.g., the left one) were always rewarded with one pellet and responses to the other lever with five pellets. On each trial, the position of the illuminated lever was pseudorandomly determined in advance. Results revealed that OPFC lesions did not impair acquisition of the task, as the speed of conditioned responses was significantly shorter with expectancy of a high reward magnitude. In addition, during reversal, shift and reshift of lever position–reward magnitude contingencies and under extinction conditions, performance of the OPFC-lesioned and control groups did not differ. It is concluded that the OPFC in rats might not be critical for adapting behavioral responses to changes of stimulus–reward magnitude contingencies signaled by visuospatial cues.     

When quantity trumps number: discrimination experiments in cotton-top tamarins (<Emphasis Type="Italic">Saguinus oedipus</Emphasis>) and common marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>)

The capacity for non-linguistic, numerical discrimination has been well characterized in non-human animals, with recent studies providing careful controls for non-numerical confounds such as continuous extent, density, and quantity. More poorly understood are the conditions under which animals use numerical versus non-numerical quantification, and the nature of the relation between these two systems. Here we test whether cotton-top tamarins and common marmosets can discriminate between two quantities on the basis of the amount of food rather than on number. In three experiments, we show that when choosing between arrays containing different numbers and sizes of food objects, both species based their decisions on the amount of food with only minor influences of numerical information. Further, we find that subjects successfully discriminated between two quantities differing by a 2:3 or greater ratio, which is consistent with the ratio limits found for numerical discrimination with this species. These studies demonstrate that non-human primates possess mechanisms that enable quantification of total amount, in addition to the numerical representations demonstrated in previous studies, with both types of quantification subject to similar processing limits.     

Valuable orientations capture attention

Visual attention has long been known to be drawn to stimuli that are physically salient or congruent with task-specific goals. Several recent studies have shown that attention is also captured by stimuli that are neither salient nor task relevant, but that are rendered in a colour that has previously been associated with reward. We investigated whether another feature dimension—orientation—can be associated with reward via learning and thereby elicit value-driven attentional capture. In a training phase, participants received a monetary reward for identifying the colour of Gabor patches exhibiting one of two target orientations. A subsequent test phase in which no reward was delivered required participants to search for Gabor patches exhibiting one of two spatial frequencies (orientation was now irrelevant to the task). Previously rewarded orientations robustly captured attention. We conclude that reward learning can imbue features other than colour—in this case, specific orientations—with persistent value.     

Stereotyping starlings are more ‘pessimistic’

Negative affect in humans and animals is known to cause individuals to interpret ambiguous stimuli pessimistically, a phenomenon termed ‘cognitive bias’. Here, we used captive European starlings (Sturnus vulgaris) to test the hypothesis that a reduction in environmental conditions, from enriched to non-enriched cages, would engender negative affect, and hence ‘pessimistic’ biases. We also explored whether individual differences in stereotypic behaviour (repetitive somersaulting) predicted ‘pessimism’. Eight birds were trained on a novel conditional discrimination task with differential rewards, in which background shade (light or dark) determined which of two covered dishes contained a food reward. The reward was small when the background was light, but large when the background was dark. We then presented background shades intermediate between those trained to assess the birds’ bias to choose the dish associated with the smaller food reward (a ‘pessimistic’ judgement) when the discriminative stimulus was ambiguous. Contrary to predictions, changes in the level of cage enrichment had no effect on ‘pessimism’. However, changes in the latency to choose and probability of expressing a choice suggested that birds learnt rapidly that trials with ambiguous stimuli were unreinforced. Individual differences in performance of stereotypies did predict ‘pessimism’. Specifically, birds that somersaulted were more likely to choose the dish associated with the smaller food reward in the presence of the most ambiguous discriminative stimulus. We propose that somersaulting is part of a wider suite of behavioural traits indicative of a stress response to captive conditions that is symptomatic of a negative affective state.     

Associative memory or algorithmic search: a comparative study on learning strategies of bats and shrews

Two common strategies for successful foraging are learning to associate specific sensory cues with patches of prey ("associative learning") and using set decision-making rules to systematically scan for prey ("algorithmic search"). We investigated whether an animal's life history affects which of these two foraging strategies it is likely to use. Natterer's bats (Myotis nattereri) have slow life-history traits and we predicted they would be more likely to use associative learning. Common shrews (Sorex araneus) have fast life-history traits and we predicted that they would rely more heavily on routine-based search. Apart from their marked differences in life-history traits, these two mammals are similar in body size, brain weight, habitat, and diet. We assessed foraging strategy, associative learning ability, and retention time with a four-arm maze; one arm contained a food reward and was marked with four sensory stimuli. Bats and shrews differed significantly in their foraging strategies. Most bats learned to associate the sensory stimuli with the reward and remembered this association over time. Most shrews searched the maze using consistent decision-making rules, but did not learn or remember the association. We discuss these results in terms of life-history traits and other key differences between these species. Our results suggest a link between an animal's life-history strategy and its use of associative learning.     

Food and token quantity discrimination in capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Quantity discrimination is adaptive in a variety of ecological contexts and different taxa discriminate stimuli differing in numerousness, both in the wild and in laboratory settings. Quantity discrimination between object arrays has been suggested to be more demanding than between food arrays but, to our knowledge, the same paradigm has never been used to directly compare them. We investigated to what extent capuchin monkeys’ relative numerousness judgments (RNJs) with food and token are alike. Tokens are inherently non-valuable objects that acquire an associative value upon exchange with the experimenter. Our aims were (1) to assess capuchins’ RNJs with food (Experiment 1) and with tokens (Experiment 2) by presenting all the possible pair-wise choices between one to five items, and (2) to evaluate on which of the two proposed non-verbal mechanisms underlying quantity discrimination (analogue magnitude and object file system) capuchins relied upon. In both conditions capuchins reliably selected the larger amount of items, although their performance was higher with food than with tokens. The influence of the ratio between arrays on performance indicates that capuchins relied on the same system for numerical representation, namely analogue magnitude, regardless of the type of stimuli (food or tokens) and across both the small and large number ranges.     

Great apes’ performance in discriminating weight and achromatic color

Much work has been done on visual discrimination in primates over the past decade. In contrast, very little is known about the relevance of non-visual information in discrimination learning. We investigated weight and achromatic color (color, henceforth) discrimination in bonobos, gorillas and orangutans, using the exchange paradigm in which subjects have to give objects to the experimenter in order to receive a reward. Unlike previous studies, subjects were not trained to lift objects because lifting the objects was an integral part of the exchange procedure. This methodology also allowed us a direct comparison between visual and weight discrimination. We presented 12 subjects (5 bonobos, 2 gorillas and 5 orangutans) with two sets of objects corresponding to two conditions. The objects in the color condition (white/black) differed only in color and those in the weight condition (light/heavy) differed only in weight. Five apes learned to discriminate weight and six to discriminate color. Subjects learned color discrimination faster than weight discrimination. Our results suggest that bonobos and orangutans are sensitive to differences in weight and able to learn discriminating objects that differ in this property.     

Pigeons can discriminate “good” and “bad” paintings by children

Humans have the unique ability to create art, but non-human animals may be able to discriminate “good” art from “bad” art. In this study, I investigated whether pigeons could be trained to discriminate between paintings that had been judged by humans as either “bad” or “good”. To do this, adult human observers first classified several children’s paintings as either “good” (beautiful) or “bad” (ugly). Using operant conditioning procedures, pigeons were then reinforced for pecking at “good” paintings. After the pigeons learned the discrimination task, they were presented with novel pictures of both “good” and “bad” children’s paintings to test whether they had successfully learned to discriminate between these two stimulus categories. The results showed that pigeons could discriminate novel “good” and “bad” paintings. Then, to determine which cues the subjects used for the discrimination, I conducted tests of the stimuli when the paintings were of reduced size or grayscale. In addition, I tested their ability to discriminate when the painting stimuli were mosaic and partial occluded. The pigeons maintained discrimination performance when the paintings were reduced in size. However, discrimination performance decreased when stimuli were presented as grayscale images or when a mosaic effect was applied to the original stimuli in order to disrupt spatial frequency. Thus, the pigeons used both color and pattern cues for their discrimination. The partial occlusion did not disrupt the discriminative behavior suggesting that the pigeons did not attend to particular parts, namely upper, lower, left or right half, of the paintings. These results suggest that the pigeons are capable of learning the concept of a stimulus class that humans name “good” pictures. The second experiment showed that pigeons learned to discriminate watercolor paintings from pastel paintings. The subjects showed generalization to novel paintings. Then, as the first experiment, size reduction test, grayscale test, mosaic processing test and partial occlusion test were carried out. The results suggest that the pigeons used both color and pattern cues for the discrimination and show that non-human animals, such as pigeons, can be trained to discriminate abstract visual stimuli, such as pictures and may also have the ability to learn the concept of “beauty” as defined by humans.     

Visual discrimination by heifers (Bos taurus) of their own species

Species discrimination has been described in several taxa but rarely in domestic animals. In contrast to wild species, domestic species present a great phenotypic variety. This study investigated whether 10 Prim'Holstein heifers (Bos taurus) could discriminate images of cows from images of other domestic animals. The experiment was based on simultaneous discrimination. Responses were obtained through instrumental conditioning using a food reward. In Experiment 1, the reward was associated with a cow face and, in the reversal learning task, with faces of other domestic species. The results showed that in both tasks, cows were able to reach the criterion in few sessions. Therefore, despite great phenotypic variety (a cognitive challenge) cows were able to visually discriminate their own species from other domestic species.