Genetic factors determine the asymmetrical position of vertebrate embryos allowing asymmetric environmental stimulation to shape cerebral lateralization. In birds, late-light stimulation, just before hatching, on the right optic nerve triggers anatomical and functional cerebral asymmetries. However, some brain asymmetries develop in absence of embryonic light stimulation. Furthermore, early-light action affects lateralization in the transparent zebrafish embryos before their visual system is functional. Here we investigated whether another pathway intervenes in establishing brain specialization. We exposed chicks' embryos to light before their visual system was formed. We observed that such early stimulation modulates cerebral lateralization in a comparable vein of late-light stimulation on active retinal cells. Our results show that, in a higher vertebrate brain, a second route, likely affecting the genetic expression of photosensitive regions, acts before the development of a functional visual system. More than one sensitive period seems thus available to light stimulation to trigger brain lateralization.
Sophisticated cognitive abilities have been documented in honeybees, possibly an aspect of their complex sociality. In vertebrates brain asymmetry enhances cognition and directional biases of brain function are a putative adaptation to social behaviour. Here we show that honeybees display a strong lateral preference to use their right antenna in social interactions. Dyads of bees tested using only their right antennae (RA) contacted after shorter latency and were significantly more likely to interact positively (proboscis extension) than were dyads of bees using only their left antennae (LA). The latter were more likely to interact negatively (C-responses) even though they were from the same hive. In dyads from different hives C-responses were higher in RA than LA dyads. Hence, RA controls social behaviour appropriate to context. Therefore, in invertebrates, as well as vertebrates, lateral biases in behaviour appear to be associated with requirements of social life.
In a variety of circumstances animals can represent numerical values per se, although it is unclear how salient numbers are relative to non-numerical properties. The question is then: are numbers intrinsically distinguished or are they processed as a last resort only when no other properties differentiate stimuli? The last resort hypothesis is supported by findings pertaining to animal studies characterized by extensive training procedures. Animals may, nevertheless, spontaneously and routinely discriminate numerical attributes in their natural habitat, but data available on spontaneous numerical competence usually emerge from studies not disentangling numerical from quantitative cues. In the study being outlined here, we tested animals' discrimination of a large number of elements utilizing a paradigm that did not require any training procedures. During rearing, newborn chicks were presented with two stimuli, each characterized by a different number of heterogeneous (for colour, size and shape) elements and food was found in proximity of one of the two stimuli. At testing 3 day-old chicks were presented with stimuli depicting novel elements (for colour, size and shape) representing either the numerosity associated or not associated with food. The chicks approached the number associated with food in the 5vs.10 and 10vs.20 comparisons both when quantitative cues were unavailable (stimuli were of random sizes) or being controlled. The findings emerging from the study support the hypothesis that numbers are salient information promptly processed even by very young animals.
The macroscopic, three-dimensional surface layout geometry of an enclosure apparently provides a different contribution for spatial reorientation than the geometric cues associated with freestanding objects arranged in arrays with similar geometric shape. Here, we showed that a unitary spatial representation can account for the capability of animals to reorient both by extended surfaces and discrete objects in a small-scale spatial task. We trained domestic chicks to locate a food-reward from an opening on isolated cylinders arranged either in a geometrically uninformative (square-shaped) or informative (rectangular-shaped) arrays. The arrays were located centrally within a rectangular-shaped enclosure. Chicks trained to access the reward from a fixed position of openings proved able to reorient according to the geometric cues specified by the shape of the enclosure in all conditions. Chicks trained in a fixed position of opening with geometric cues provided both by the arena and the array proved able to reorient according to each shape separately. However, chicks trained to access the reward from a variable position of openings failed to reorient. The results suggest that the physical constrains associated with the presence of obstacles in a scene, rather than their apparent visual extension, are crucial for spatial reorientation.
spatial reorientation; geometric module; view-based navigation; environmental axis; array of freestanding objects
Bilateral symmetry is visually salient to diverse animals including birds, but whereas experimental studies typically use bilaterally symmetrical two-dimensional patterns that are viewed approximately fronto-parallel; in nature, animals observe three-dimensional objects from all angles. Many animals and plant structures have a plane of bilateral symmetry. Here, we first (experiment I) give evidence that young poultry chicks readily generalize bilateral symmetry as a feature of two-dimensional patterns in fronto-parallel view. We then test the ability of chicks to recognize symmetry in images that would be produced by the transformed view produced by a 40° horizontal combined with a 20° vertical rotation of a pattern on a spherical surface. Experiment II gives evidence that chicks trained to distinguish symmetrical from asymmetrical patterns treat rotated views of symmetrical ‘objects’ as symmetrical. Experiment III gives evidence that chicks trained to discriminate rotated views of symmetrical ‘objects’ from asymmetrical patterns generalize to novel symmetrical objects either in fronto-parallel or rotated view. These findings emphasize the importance of bilateral symmetry for three-dimensional object recognition and raise questions about the underlying mechanisms of symmetry perception.
symmetry; vision; object recognition; domestic chick; categorization
Four-month-old infants can integrate local cues provided by two-dimensional pictures and interpret global inconsistencies in structural information to discriminate between possible and impossible objects. This leaves unanswered the issue of the relative contribution of maturation of biologically predisposed mechanisms and of experience with real objects, to the development of this capability. Here we show that, after exposure to objects in which junctions providing cues to global structure were occluded, day-old chicks selectively approach the two-dimensional image that depicted the possible rather than the impossible version of a three-dimensional object, after restoration of the junctions. Even more impressively, completely naive newly hatched chicks showed spontaneous preferences towards approaching two-dimensional depictions of structurally possible rather than impossible objects. These findings suggest that the vertebrate brain can be biologically predisposed towards approaching a two-dimensional image representing a view of a structurally possible three-dimensional object.
impossible objects; early predispositions; object perception; domestic chick
Questions concerning the role of nature and nurture in higher cognition appear to be intractable if one restricts one's attention to development in humans. However, in other domains, such as sensory development, much information has been gained from controlled rearing studies with animals. Here, we used a similar experimental strategy to investigate intuitive reasoning about occluded objects. Newborn domestic chicks (Gallus gallus) were reared singly with a small object that became their social partner. They were then accustomed to rejoin such an imprinting object when it was made to move and disappear behind either one of two identical opaque screens. After disappearance of the imprinting object, chicks were faced with two screens of different slants, or of different height or different width, which may or may not have been compatible with the presence of the imprinting object hidden beneath/behind them. Chicks consistently chose the screen of slant/height/width compatible with the presence of the object beneath/behind it. Preventing chicks from touching and pecking at the imprinting object before testing did not affect the results, suggesting that intuitive reasoning about physical objects is largely independent of specific experience of interaction with objects and of objects' occluding events.
naive physics; filial imprinting; object permanence; experience; biological predispositions
The honeybee, Apis mellifera L. (Hymenoptera: Apidae), has recently become a model for studying brain asymmetry among invertebrates. A strong lateralization favouring the right antenna was discovered in odour learning and short-term memory recall experiments, and a lateral shift favouring the left antenna for long-term memory recall. Corresponding morphological asymmetries have been found in the distribution of olfactory sensilla between the antennae and confirmed by electrophysiological odour response measurements in isolated right and left antennae. The aim of this study was to investigate whether a morphological asymmetry can be observed in the volume of the primary olfactory centres of the central nervous system, the antennal lobes (ALs). Precise volume measurements of a subset of their functional units, the glomeruli, were performed in both sides of the brain, exploiting the advantages of two-photon microscopy. This novel method allowed minimal invasive acquisition of volume images of the ALs, avoiding artefacts from brain extraction and dehydration. The study was completed by a series of behavioural experiments in which response asymmetry in odour recall following proboscis extension reflex conditioning was assessed for odours, chosen to stimulate strong activity in the same glomeruli as in the morphological study. The volumetric measurements found no evidence of lateralization in the investigated glomeruli within the experimental limits. Instead, in the behavioural experiments, a striking odour dependence of the lateralization was observed. The results are discussed on the basis of recent neurophysiological and ethological experiments in A. mellifera.
Apis mellifera; brain asymmetry; olfactory learning; antennal lobes; two-photon microscopy
Recent studies have revealed asymmetries between the left and right sides of the brain in invertebrate species. Here we present a review of a series of recent studies from our laboratories, aimed at tracing asymmetries at different stages along the honeybee’s (Apis mellifera) olfactory pathway. These include estimates of the number of sensilla present on the two antennae, obtained by scanning electron microscopy, as well as electroantennography recordings of the left and right antennal responses to odorants. We describe investigative studies of the antennal lobes, where multi-photon microscopy was used to search for possible morphological asymmetries between the two brain sides. Moreover, we report on recently published results obtained by two-photon calcium imaging for functional mapping of the antennal lobe aimed at comparing patterns of activity evoked by different odours. Finally, possible links to the results of behavioural tests, measuring asymmetries in single-sided olfactory memory recall, are discussed.
Apis mellifera; Antennal lobe; Olfactory learning; Brain asymmetry; PER; SEM; EAG; Two-photon microscopy
Human and non-human animals are capable of using basic geometric information to reorient in an environment. Geometric information includes metric properties associated with spatial surfaces (e.g., short vs. long wall) and left-right directionality or ‘sense’ (e.g. a long wall to the left of a short wall). However, it remains unclear whether geometric information is encoded by explicitly computing the layout of surface geometry or by matching images of the environment. View-based spatial encoding is generally thought to hold for insect navigation and, very recently, evidence for navigation by geometry has been reported in ants but only in a condition which does not allow the animals to use features located far from the goal. In this study we tested the spatial reorientation abilities of bumblebees (Bombus terrestris). After spatial disorientation, by passive rotation both clockwise and anticlockwise, bumblebees had to find one of the four exit holes located in the corners of a rectangular enclosure. Bumblebees systematically confused geometrically equivalent exit corners (i.e. corners with the same geometric arrangement of metric properties and sense, for example a short wall to the left of a long wall). However, when one wall of the enclosure was a different colour, bumblebees appeared to combine this featural information (either near or far from the goal) with geometric information to find the correct exit corner. Our results show that bumblebees are able to use both geometric and featural information to reorient themselves, even when features are located far from the goal.
Spatial reorientation by layout geometry occurs in numerous species, but its underlying mechanisms are debated. While some argue that navigating animals' sense of place is based on geometric computations over three-dimensional representations, others claim it depends on panoramic image-matching processes. Because children reorient by subtle three-dimensional perturbations of the terrain and not by salient two-dimensional brightness contours on surfaces or freestanding columns, children's sense of place cannot be explained by image matching. To test image-matching theories in a different species, the present experiment investigates the reorientation performance of domestic chicks (Gallus gallus) in environments similar to those used with children. Chicks, like children, spontaneously reoriented by geometric relationships of subtle three-dimensional terrains, and not by salient two-dimensional brightness contours on surfaces or columns. These findings add to the evidence for homologous navigation systems in humans and other vertebrates, and they cast doubt on image-matching theories of reorientation in these species.
navigation; reorientation; geometry; image matching
Newly hatched domestic chicks, reared with identical objects, when presented with sets of 3 vs. 2 objects disappearing one-by-one behind separate screens, spontaneously inspected the screen occluding the larger set; even when the continuous variables (area or perimeter) were controlled for (Rugani et al., 2009). Here, using a similar paradigm, we investigated the ability of chicks to perform addition on larger sets of objects. Chicks imprinted on five identical objects, were presented at test with 6 vs. 9 objects which disappeared one-by-one (Exp. 1). In Exp. 2, the same overall number of objects (15) was used, but employing an increased ratio, i.e., 5 vs. 10. In both experiments, when continuous variables were not made equal, chicks spontaneously inspected the screen occluding the larger set. However, when the size of the objects was adjusted so as to make the total surface area or perimeter equal for the two sets, chicks did not exhibit any preference. Lack of choice in the control conditions could be due to a combination of preferences; to rejoin the larger numerousness as well as the bigger objects (Rugani et al., 2010a). In Exp. 3, chicks were familiarized, during imprinting, with objects of various dimensions, in an attempt to reduce or suppress their tendency to approach objects larger than the familiar ones. Again chicks failed to choose at test between 5 vs. 10 objects when continuous variables were made equal. Results showed that chicks, after a one-by-one presentation of a large number of objects, rejoined the larger set. In order to choose the larger set, chicks estimated the objects in the two sets and then compared the outcomes. However, differently to what has been described for small numerousness, chicks succeeded only if non-numerical cues as well as numerical cues were available. This study suggests that continuous variables are computed by chicks for sets of objects that are not present at the same time and that are no longer visible at the time of choice.
number cognition; counting; number sense; arithmetic; domestic chick; human infant; large numeracy; continuous variables
Following spatial disorientation, animals can reorient themselves by relying on geometric cues (metric and sense) specified both by the macroscopic surface layout of an enclosed space and prominent visual landmarks in arrays. Whether spatial reorientation in arrays of landmarks is based on explicit representation of the geometric cues is a matter of debate. Here we trained homing pigeons (Columba livia) to locate a food-reward in a rectangular array of four identical or differently coloured pipes provided with four openings, only one of which allowed the birds to have access to the reward. Pigeons were trained either with a stable or a variable position of the opening on pipes, so that they could view the array either from the same or a variable perspective. Explicit mapping of configural geometry would predict successful reorientation irrespective of access condition. In contrast, we found that a stable view of the array facilitated spatial learning in homing pigeons, likely through the formation of snapshot-like memories.
Brain and behavioural lateralization at the population level has been recently hypothesized to have evolved under social selective pressures as a strategy to optimize coordination among asymmetrical individuals. Evidence for this hypothesis have been collected in Hymenoptera: eusocial honey bees showed olfactory lateralization at the population level, whereas solitary mason bees only showed individual-level olfactory lateralization. Here we investigated lateralization of odour detection and learning in the bumble bee, Bombus terrestris L., an annual eusocial species of Hymenoptera. By training bumble bees on the proboscis extension reflex paradigm with only one antenna in use, we provided the very first evidence of asymmetrical performance favouring the right antenna in responding to learned odours in this species. Electroantennographic responses did not reveal significant antennal asymmetries in odour detection, whereas morphological counting of olfactory sensilla showed a predominance in the number of olfactory sensilla trichodea type A in the right antenna. The occurrence of a population level asymmetry in olfactory learning of bumble bee provides new information on the relationship between social behaviour and the evolution of population-level asymmetries in animals.
Converging evidence from different species indicates that some newborn vertebrates, including humans, have visual predispositions to attend to the head region of animate creatures. It has been claimed that newborn preferences for faces are domain-relevant and similar in different species. One of the most common criticisms of the work supporting domain-relevant face biases in human newborns is that in most studies they already have several hours of visual experience when tested. This issue can be addressed by testing newly hatched face-naïve chicks (Gallus gallus) whose preferences can be assessed prior to any other visual experience with faces.
In the present study, for the first time, we test the prediction that both newly hatched chicks and human newborns will demonstrate similar preferences for face stimuli over spatial frequency matched structured noise. Chicks and babies were tested using identical stimuli for the two species. Chicks underwent a spontaneous preference task, in which they have to approach one of two stimuli simultaneously presented at the ends of a runway. Human newborns participated in a preferential looking task.
Results and Significance
We observed a significant preference for orienting toward the face stimulus in both species. Further, human newborns spent more time looking at the face stimulus, and chicks preferentially approached and stood near the face-stimulus. These results confirm the view that widely diverging vertebrates possess similar domain-relevant biases toward faces shortly after hatching or birth and provide a behavioural basis for a comparison with neuroimaging studies using similar stimuli.
Due to the honey bee’s importance as a simple neural model, there is a great need for new functional imaging modalities. Herein we report on the development and new findings of a combined two-photon microscope with a synchronized odor stimulus platform for in-vivo functional and morphological imaging of the honey bee’s olfactory system focusing on its primary centers, the antennal lobes (ALs). Our imaging platform allows for simultaneously obtaining both morphological measurements of the AL’s functional units, the glomeruli, and in-vivo calcium recording of their neural activities. By applying external odor stimuli to the bee’s antennae, we were able to record the characteristic glomerular odor response maps. Compared to previous works where conventional fluorescence microscopy was used, our approach has been demonstrated to offer all the advantages of multi-photon imaging, providing substantial enhancement in both spatial and temporal resolutions while minimizing photo-damages. In addition, compared to previous full-field microscopy calcium recordings, a four-fold improvement in the functional signal has been achieved. Finally, the multi-photon associated extended penetration depth allows for functional imaging of profound glomeruli.
(170.3880) Medical and biological imaging; (170.2655) Functional monitoring and imaging; (180.4315) Nonlinear microscopy
Here we compare whether birds encode surface geometry using principal axes, medial axes or local geometry. Birds were trained to locate hidden food in two geometrically identical corners of a rectangular arena and subsequently tested in an L-shaped arena. The chicks showed a primary local geometry strategy, and a secondary medial axes strategy, whereas the pigeons showed a medial axes strategy. Neither species showed behaviour supportive of the use of principal axes. This is, to our knowledge, the first study to directly examine these three current theories of geometric encoding.
orientation; geometric encoding; domestic chick; racing pigeon
Newly hatched domestic chicks were reared with five identical objects. On days 3 or 4, chicks underwent free-choice tests in which sets of three and two of the five original objects disappeared (either simultaneously or one by one), each behind one of two opaque identical screens. Chicks spontaneously inspected the screen occluding the larger set (experiment 1). Results were confirmed under conditions controlling for continuous variables (total surface area or contour length; experiment 2). In the third experiment, after the initial disappearance of the two sets (first event, FE), some of the objects were visibly transferred, one by one, from one screen to the other (second event, SE). Thus, computation of a series of subsequent additions or subtractions of elements that appeared and disappeared, one by one, was needed in order to perform the task successfully. Chicks spontaneously chose the screen, hiding the larger number of elements at the end of the SE, irrespective of the directional cues provided by the initial (FE) and final (SE) displacements. Results suggest impressive proto-arithmetic capacities in the young and relatively inexperienced chicks of this precocial species.
number cognition; counting; number sense; arithmetic; addition; subtraction
Recent studies have revealed a variety of left–right asymmetries among vertebrates and invertebrates. In many species, left- and right-lateralized individuals coexist, but in unequal numbers (‘population-level’ lateralization). It has been argued that brain lateralization increases individual efficiency (e.g. avoiding unnecessary duplication of neural circuitry and reducing interference between functions), thus counteracting the ecological disadvantages of lateral biases in behaviour (making individual behaviour more predictable to other organisms). However, individual efficiency does not require a definite proportion of left- and right-lateralized individuals. Thus, such arguments do not explain population-level lateralization. We have previously shown that, in the context of prey–predator interactions, population-level lateralization can arise as an evolutionarily stable strategy when individually asymmetrical organisms must coordinate their behaviour with that of other asymmetrical organisms. Here, we extend our model showing that populations consisting of left- and right-lateralized individuals in unequal numbers can be evolutionarily stable, based solely on strategic factors arising from the balance between antagonistic (competitive) and synergistic (cooperative) interactions.
asymmetry; brain evolution; brain lateralization; evolutionarily stable strategy; laterality; lateralization of behaviour
We report that adult nutcrackers (Nucifraga columbiana) and newborn domestic chicks (Gallus gallus) show a leftward bias when required to locate an object in a series of identical ones on the basis of its ordinal position. Birds were trained to peck at either the fourth or sixth element in a series of 16 identical and aligned positions. These were placed in front of the bird, sagittally with respect to its starting position. When, at test, the series was rotated by 90° lying frontoparallel to the bird's starting position, both species showed a bias for identifying selectively the correct position from the left but not from the right end. The similarity with the well-known phenomenon of the left-to-right spatially oriented number line in humans is considered.
avian brain; mental number line; domestic chick; Clark's nutcracker
Honeybees, Apis mellifera, readily learn to associate odours with sugar rewards and we show here that recall of the olfactory memory, as demonstrated by the bee extending its proboscis when presented with the trained odour, involves first the right and then the left antenna. At 1–2 hour after training using both antennae, recall is possible mainly when the bee uses its right antenna but by 6 hours after training a lateral shift has occurred and the memory can now be recalled mainly when the left antenna is in use. Long-term memory one day after training is also accessed mainly via the left antenna. This time-dependent shift from right to left antenna is also seen as side biases in responding to odour presented to the bee's left or right side. Hence, not only are the cellular events of memory formation similar in bees and vertebrate species but also the lateralized networks involved may be similar. These findings therefore seem to call for remarkable parallel evolution and suggest that the proper functioning of memory formation in a bilateral animal, either vertebrate or invertebrate, requires lateralization of processing.
Do animals have privileged access to lower level sensory information before it is packaged into concepts, as it has been argued for autistic savants?
The EUROPEAN BRAIN AND BEHAVIOUR SOCIETY has held its 39th Annual General Meeting in Trieste, in the campus next to
the Miramare castle and its park, co-hosted by SISSA, the International School for Advanced Studies, and ICTP, the Abdus Salam
International Centre for Theoretical Physics. Alessandro Treves (SISSA) was the head and inspiration of the Local Organizing
committee, supported by P. Battaglini, L. Chelazzi, M. Diamond and G. Vallortigara. All approaches relating brain and behaviour
were represented at the meeting, which aimed to further expand the wide spectrum of previous EBBS AGMs, and to bring together
integrative, system, cognitive, computational neuroscientists.
See also the societies home page: http://www.ebbs-science.org/.
Brain lateralization is common among vertebrates. However, despite its implications for higher-order cognitive functions, almost no empirical evidence has been provided to show that it may confer any advantage to the functioning of the brain. Here, we show in the domestic chick (Gallus gallus domesticus) that cerebral lateralization is associated with an enhanced ability to perform two tasks simultaneously: finding food and being vigilant for predators. This finding suggests that cerebral lateralization enhances brain efficiency in cognitive tasks that demand the simultaneous but different use of both hemispheres.
In recent years, it has become apparent that behavioural and brain lateralization at the population level is the rule rather than the exception among vertebrates. The study of these phenomena has so far been the province of neurology and neuropsychology. Here, we show how such research can be integrated with evolutionary biology to understand lateralization more fully. In particular, we address the fact that, within a species, left- and right-type individuals often occur in proportions different from one-half (e.g. hand use in humans). The traditional explanations offered for lateralization of brain function (that it may avoid unnecessary duplication of neural circuitry and reduce interference between functions) cannot account for this fact, because increased individual efficiency is unrelated to the alignment of lateralization at the population level. A further puzzle is that such an alignment may even be disadvantageous, as it makes individual behaviour more predictable to other organisms. Here, we show that alignment of the direction of behavioural asymmetries in a population can arise as an evolutionarily stable strategy when individual asymmetrical organisms must coordinate their behaviour with that of other asymmetrical organisms. Brain and behavioural lateralization, as we know it in humans and other vertebrates, may have evolved under basically 'social' selection pressures.