Defining Natural Categories in Acoustic Signals: Comparison of Three Methods Applied to ‘Chick-a-dee’ Call Notes

Chicks were trained to discriminate between two identical boxes on the basis of their position. Subsequently, the colour of parts of the positive (reinforced) box was changed and chicks were retrained. Results showed that chicks were more or less impaired during retraining depending on the spatial distribution of the changed stimuli. Chicks behaved as if a figure (a disc or a spot of dots) painted on a box was irrelevant to them, whereas they did respond to changes in the colour of a uniformly coloured box or of scattered dots painted on a box. Similar results were obtained in simultaneous discrimination learning tasks involving addition of cues (e.g. colour plus position). Addition of cues facilitated learning using boxes the same colour all over or with painted scattered dots, but not using boxes with a disc or a spot of dots. Furthermore, addition of shape and position information had different outcomes depending on the use of three-dimensional objects or of painted figures: learning facilitation occurred only using three-dimensional objects. Results are interpreted in terms of an “object hypothesis”, and the validity and usefulness of traditional terms such as cues is questioned.     

Simultaneous Discrimination Learning in Chicks: Spatial Representations and Object Characteristics

Chicks were trained to discriminate (1) between two boxes of the same colour on the basis of their positions; (2) between two boxes of different colours on the basis of their positions or on the basis of their colours. No significant differences between these tasks appeared. Addition of colour and position improved learning when the boxes were entirely coloured but not when differently coloured discs were placed over the lids of two identical boxes. It is argued that in simultaneous discrimination learning chicks rely primarily on the “relative” position of the goal objects (i. e. in relation to each other) and utilize featural information (colour) to segregate the goal objects as distinct perceptual units. Results also stressed the role of “object characteristics” as opposed to the traditional notion of “cues”.     

Contrast versus colour in aposematic signals

Conspicuousness is an important feature of warning coloration. One hypothesis for its function is that it increases signal efficacy by facilitating avoidance learning. An alternative, based on the handicap hypothesis, suggests that the degree of conspicuousness holds information directly about the quality of the prey, and that predators associate and learn about the conspicuousness of the coloration, and not the actual colour pattern. We studied the relative importance of signal contrast and the colours of signals for predator attention during discrimination. We used young chicks, Gallus gallus domesticus, as predators and small blue or red paper cones on either matching or contrasting paper backgrounds as stimuli associated with palatable or unpalatable chick crumbs. In four treatment groups, birds could use either cone and/or background colour, cone colour only, background colour only or cone-to-background contrast as cues for discrimination. Only birds in the contrast treatment failed to learn their discrimination task. Birds that had a choice between cone and background colour as cues used the cone colour and they learned the task faster than did birds that had to use background colour as a cue. The results suggest that birds primarily attend to the colours of signals and disregard contrast in discrimination tasks; they thus fail to support a handicap function of conspicuous aposematic coloration. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Goffin's cockatoos discriminate objects based on weight alone

Paying attention to weight is important when deciding upon an object''s efficacy or value in various contexts (e.g. tool use, foraging). Proprioceptive discrimination learning, with objects that differ only in weight, has so far been investigated almost exclusively in primate species. Here, we show that while Goffin''s cockatoos learn faster when additional colour cues are used, they can also quickly learn to discriminate between objects on the basis of their weight alone. Ultimately, the birds learned to discriminate between visually identical objects on the basis of weight much faster than primates, although methodological differences between tasks should be considered.     

Blue colour preference in honeybees distracts visual attention for learning closed shapes

Spatial vision is an important cue for how honeybees (Apis mellifera) find flowers, and previous work has suggested that spatial learning in free-flying bees is exclusively mediated by achromatic input to the green photoreceptor channel. However, some data suggested that bees may be able to use alternative channels for shape processing, and recent work shows conditioning type and training length can significantly influence bee learning and cue use. We thus tested the honeybees’ ability to discriminate between two closed shapes considering either absolute or differential conditioning, and using eight stimuli differing in their spectral characteristics. Consistent with previous work, green contrast enabled reliable shape learning for both types of conditioning, but surprisingly, we found that bees trained with appetitive-aversive differential conditioning could additionally use colour and/or UV contrast to enable shape discrimination. Interestingly, we found that a high blue contrast initially interferes with bee shape learning, probably due to the bees innate preference for blue colours, but with increasing experience bees can learn a variety of spectral and/or colour cues to facilitate spatial learning. Thus, the relationship between bee pollinators and the spatial and spectral cues that they use to find rewarding flowers appears to be a more rich visual environment than previously thought.     

Pattern discrimination by the honeybee: disruption as a cue

The discrimination of pattern disruption in freely flying honeybees (Apis mellifera) was examined. Bees were trained to discriminate at a fixed distance between a regularly repeated black/white pattern and the same pattern at a different magnification in targets of the same angular size. The locations of areas of black were regularly shuffled to make them useless as cues. The results of the experiments indicate that the bees discriminate the disruption of the pattern as a whole, irrespective of the actual pattern. Bees trained to prefer a larger period transfer to an even larger period, when given a forced choice with a pair of patterns of differing disruption from those they were trained on, as if their spontaneous preference has not been overcome. Bees trained to prefer a smaller period, however, prefer the former negative pattern rather than transfer to an even smaller period. These results show that the bees do not rely solely on learning the absolute period of a pattern nor the relative disruption of two patterns, and they are confused when these two cues conflict in tests with unfamiliar targets. Bees can discriminate between fields of view that differ in average disruption as a generalized cue, irrespective of pattern. Accepted: 7 April 1997     

Interaction between positional but not between non-positional cues in human predictive learning

Four experiments with human subjects examined the cue-interaction effects using a computer-controlled predictive learning task. In Phase 1, subjects learned that cue P was consistently associated with the occurrence of an outcome (P+), whereas cue N was never followed by the outcome (N−). In Phase 2, two neutral cues, R and I, were compounded with P and N, respectively. Each compound was followed by the outcome (PR+ and NI+). Thus, cue R was compounded with the already predictive cue P, whereas cue I was compounded with the non-predictive cue N. In each phase, subjects rated the contingency between the different cues and the outcome. In experiments 1 and 2, the spatial position of the cues was fixed, whereas it was variable in experiments 3, 4a and 4b. Verbal cues were used in experiments 1–3, whereas the cues consisted of geometrical figures in experiments 4a and 4b. Evidence for cue interaction, as indicated by giving cue I a higher contingency rating than cue R after or during Phase 2, was only found under the conditions of experiments 1 and 2. The results indicate that the use of positional cues facilitates the occurrence of cue-interaction effects. Possible reasons for this finding are discussed.     

Position learning in chicks

Chicks were trained to discriminate between two similar boxes according to their “relative” (i.e. in relation to each other) or “absolute” (i.e. in relation to the cage or other features of the environment) position. Results showed: (a) when the boxes were placed close together, learning on the basis of their relative position was much more rapid than on the basis of their absolute position; (b) when the boxes were placed further apart, learning required more trials but differences between the two training methods were reduced.     

Modulation of synaptic plasticity in the hippocampus and piriform cortex by physiologically meaningful olfactory cues in an olfactory association task

Animals were trained to discriminate two natural odors while another group was trained to discriminate between a patterned electrical stimulation distributed on the lateral olfactory tract (LOT), labelled olfaco-mimetic stimulation (OMS), used as an olfactory cue versus a natural odor. No statistically significant difference was observed in behavioral data between these two groups. The animals trained to learn the meaning of the OMS exhibited a gradual long-term potentiation (LTP) phenomenon in the piriform cortex. When a group of naive animals was pseudo-conditioned, giving the OMS for the same number of sessions but without any olfactory training, no LTP was recorded. These results indicate that the process of learning olfactory association gradually potentiates cortical synapses in a defined cortical terminal field, and may explain why LTP in the piriform cortex is not elicited by the patterned stimulation itself, but only in an associative context. As olfactory and hippocampus regions are connected via the lateral entorhinal cortex, the olfactomimetic model was used to study the dynamic of involvement of the dentate gyrus (DG) in learning and memory of this associative olfactory task. Polysynaptic field potentials, evoked by the LOT stimulation, were recorded in the molecular layer of the ipsilateral DG. An early and rapid (2nd session) potentiation was observed when a significant discrimination of the two cues began to be observed. The onset latency of the potentiated response was 30–40 ms. When a group of naive animals was pseudoconditioned, no change was observed. Taken together, these results support the hypothesis that early activation of the DG during the learning of olfactory cue allows the progressive storage of olfactory information in a defined set of potentiated cortical synapses. The onset latency of the polysynaptic potentiated responses suggests the existence of a reactivating hippocampal loops during the processing of olfactory information.     

Sound improves visual discrimination learning in avian predators

Aposematic insects use warning colours to deter predators, but many also produce odours or sounds when attacked by a predator. One possible role for these additional components is that they promote the association between the warning colour and the non-profitability it signals, thus reducing the chance of future attacks from visually hunting predators. This experiment explicitly tests this idea by looking at the effects of sound on a visual discrimination task. Young domestic chicks were trained to look for food rewards under coloured paper cones scattered in an experimental arena. In a subsequent visual discrimination task, they learned to discriminate between rewarded and non-rewarded hats on the basis of colour. Half the chicks performed this task in silence, whilst the other half had a tone played when they attacked non-rewarded hats. The presence of the tone improved the speed of colour discrimination learning. This demonstrates that there could be a selective advantage for aposematic coloured insects to emit sounds when attacked, since avian predators will learn to avoid their coloration more quickly. The role of psychological interactions between signal components in receivers is discussed in relation to the evolution of multimodal displays.     

Guppies learn faster to discriminate between red and yellow than between two shapes

Animal species are expected to evolve specialised cognitive abilities to solve the tasks that are critical for their fitness. The literature contains several examples of specialised cognitive abilities, but few regard fish. The guppy, Poecilia reticulata, is a freshwater fish in which females choose their mates based on colouration, and orange‐coloured fruits are important diet enrichments for both sexes. For these reasons, we expect that this species has evolved enhanced learning abilities in colour discrimination compared to other types of discrimination. The comparison between studies in which guppies were tested for colour discrimination and studies in which guppies were tested for shape discrimination seems to support this hypothesis, but direct testing is still lacking. We experimentally compared the learning performance of guppies trained in a red–yellow colour discrimination learning task and that of guppies trained in a shape discrimination learning task using the same, automated conditioning procedure. Guppies trained in the colour discrimination showed greater learning performance, which provides support to the hypothesis that guppies possess enhanced colour discrimination abilities. Moreover, we found that male guppies performed better than females in both shape and colour discrimination learning.     

Trichromatic colour vision in the hummingbird hawkmoth, Macroglossum stellatarum L.

Hymenopterans have long been shown to choose colours by means of the spectral distribution and independently of the intensity (true colour vision). The same ability has only very recently been proven for two butterfly species. We present evidence for the existence of true colour vision in the European hummingbird hawkmoth, Macroglossum stellatarum. Moths were trained in dual-choice situations to spectral lights of a rewarding and an unrewarding wavelength. After training, unrewarded tests were performed during which the intensities of the lights were changed. The results confirm that the species has three spectral receptor types and uses true colour vision when learning the colour of a food source. If colour vision is not possible since only one receptor type is receiving input from both stimuli, the moths learn to associate some achromatic cue correlated to the receptor quantum catch, with the reward. The moths learn spectral cues rapidly and choose correctly after one to several rewarded visits even when trained to different colours in sequence. Accepted: 24 February 1999     

Colour processing in complex environments: insights from the visual system of bees

Colour vision enables animals to detect and discriminate differences in chromatic cues independent of brightness. How the bee visual system manages this task is of interest for understanding information processing in miniaturized systems, as well as the relationship between bee pollinators and flowering plants. Bees can quickly discriminate dissimilar colours, but can also slowly learn to discriminate very similar colours, raising the question as to how the visual system can support this, or whether it is simply a learning and memory operation. We discuss the detailed neuroanatomical layout of the brain, identify probable brain areas for colour processing, and suggest that there may be multiple systems in the bee brain that mediate either coarse or fine colour discrimination ability in a manner dependent upon individual experience. These multiple colour pathways have been identified along both functional and anatomical lines in the bee brain, providing us with some insights into how the brain may operate to support complex colour discrimination behaviours.     

Use of water flow direction to provide spatial information in a small-scale orientation task

Experiments were designed to investigate whether three-spined sticklebacks Gasterosteus aculeatus can use direction of water flow as an orientation cue. The fish had to learn the location of a food patch in a channel where water flow direction was the only reliable indicator of the food patch position. Fish from two ponds and two rivers were trained and tested in the spatial task to determine whether river three-spined sticklebacks are more adept at using water flow as a spatial cue than fish from ponds. All fish were able to use water flow to locate the food patch but one of the two river groups was significantly faster at learning the patch location. When the task was reversed so that fish that had formerly been trained to swim downstream now had to learn to swim upstream and vice versa both river groups learned the reversed task faster than the two pond groups. In a second experiment, to investigate whether fish from ponds or rivers vary in the type of spatial cue that they prefer to use, fish from one pond and one river were given a choice between two different types of spatial cue: flow direction or visual landmarks. A test trial in which these two cues were put into conflict revealed that the river population showed a strong preference for flow direction whilst the pond population preferred to use visual landmarks.     

Recall of sequences based on the position of the first cue stimulus in rats

We investigated the ability of rats to recall sequences of nose-poke holes with a modified serial reaction time task. In each trial, a sequence was randomly selected and the position of the first illuminated hole, which functioned as a cue stimulus, informed the rats whether the following sequence was a predictable one or not, based on prior training. The rats responded predictively only when the cues of the predictable sequences were presented. They did not show predictive responses when the cues of unpredictable sequences were presented, even though the unpredictable sequences partially had the same order of holes as the predictable sequences. These results indicate that the rats can recall sequences on the basis of presentation of the first cue stimulus informing predictable or unpredictable sequences. Recording neuronal activity while rats perform this behavioral task would be useful to elucidate neuronal mechanisms that mediate sequence recall.     

Navigational ability in the domestic fowl (Gallus gallus domesticus)

Little is known about the navigational abilities of domestic fowl. The question of how chickens represent and orient in space becomes relevant when they are kept in non-cage systems. Since the sun is known to be the dominant spatial organiser in other diurnal bird species, we started our investigation of the chicken’s spatial abilities by subjecting them to a food-searching task with the sun as the only consistent visual cue. In an additional experiment we tried to rule out the use of auditory cues in finding a food reward.

Eight ISA Brown chicks were housed in outdoor pens. A separate test arena comprised an open-topped, opaque-sided wooden octagon (2 m wide and 1.5 m high). Eight goal boxes with food pots were attached to each of the arena sides; a wooden barrier inside each goal box prevented the birds from seeing the food pot before entering. After habituation we tested during five daily 5 min trials whether the chicks were able to find food in a systematically allocated goal direction. Food residue in every foot pot controlled for the use of olfactory cues and no external landmark cues were visible. Every day each box was unpredictably moved to a randomly assigned side of the arena and the side to face north was also randomly allocated, to prevent the chicks from using cues other than the sun’s position. Circular statistics were used to determine whether birds moved in a non-random direction and if so, if they significantly oriented goalwards. The results showed that seven of the eight birds moved significantly in the goal direction. It seems likely that the chicks used the sun to orient. Due to weather constraints only four chicks received the same treatment on a new location, to rule out the use of auditory cues. Two of these four chicks significantly moved in the goal direction.

The results from our experiments show that domestic chicks use spatial memory to orient towards a hidden goal. Moreover, their orientation is most likely to be based on sun cues opening up the possibility that the sun compass may dominate even in this ancestrally predominantly ground-living forest bird.     

Colour preferences and colour vision in poultry chicks

The dramatic colours of biological communication signals raise questions about how animals perceive suprathreshold colour differences, and there are long-standing questions about colour preferences and colour categorization by non-human species. This study investigates preferences of foraging poultry chicks (Gallus gallus) as they peck at coloured objects. Work on colour recognition often deals with responses to monochromatic lights and how animals divide the spectrum. We used complementary colours, where the intermediate is grey, and related the chicks' choices to three models of the factors that may affect the attractiveness. Two models assume that attractiveness is determined by a metric based on the colour discrimination threshold either (i) by chromatic contrast against the background or (ii) relative to an internal standard. An alternative third model is that categorization is important. We tested newly hatched and 9-day-old chicks with four pairs of (avian) complementary colours, which were orange, blue, red and green for humans. Chromatic contrast was more relevant to newly hatched chicks than to 9-day-old birds, but in neither case could contrast alone account for preferences; especially for orange over blue. For older chicks, there is evidence for categorization of complementary colours, with a boundary at grey.     

When to approach novel prey cues? Social learning strategies in frog-eating bats

Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.     

Vision of the honeybee Apis mellifera for patterns with one pair of equal orthogonal bars

The visual discrimination of patterns of two equal orthogonal black bars by honeybees has been studied in a Y-choice apparatus with the patterns presented vertically at a fixed range. Previous work shows that bees can discriminate the locations of one, or possibly more, contrasts in targets that are in the same position throughout the training. Therefore, in critical experiments, the locations of areas of black were regularly shuffled to make them useless as cues. The bees discriminate consistent radial and tangential cues irrespective of their location on the target during learning and testing. Orientation cues, to be discriminated, must be presented on corresponding sides of the two targets. When orientation, radial and tangential cues are omitted or made useless by alternating them, discrimination is impossible, although the patterns may look quite different to us. The shape or the layout of local cues is not re-assembled from the locations of the bars, even when there are only two bars in the pattern, as if the bees cannot locate the individual bars within the large spatial fields of their global filters.     

Tactile learning by a whip spider, <Emphasis Type="Italic">Phrynus marginemaculatus</Emphasis> C.L. Koch (Arachnida,Amblypygi)

The ability of animals to learn and remember underpins many behavioural actions and can be crucial for survival in certain contexts, for example in finding and recognising a habitual refuge. The sensory cues that an animal learns in such situations are to an extent determined by its own sensory specialisations. Whip spiders (Arachnida, Amblypygi) are nocturnal and possess uniquely specialised sensory systems that include elongated ‘antenniform’ forelegs specialised for use as chemo- and mechanosensory feelers. We tested the tactile learning abilities of the whip spider Phrynus marginemaculatus in a maze learning task with two tactile cues of different texture—one associated with an accessible refuge, and the other with an inaccessible refuge. Over ten training trials, whip spiders got faster and more accurate at finding the accessible refuge. During a subsequent test trial where both refuges were inaccessible, whip spiders searched for significantly longer at the tactile cue previously associated with the accessible refuge. Using high-speed cinematography, we describe three distinct antenniform leg movements used by whip spiders during tactile examination. We discuss the potential importance of tactile learning in whip spider behaviour and a possible role for their unique giant sensory neurons in accessing tactile information.