Angelo Bisazza

Possible evolutionary origins of cognitive brain lateralization

Despite the substantial literature on the functional architecture of the asymmetries of the human brain, which has been accumulating for more than 130 years since Dax and Brocas early reports, the biological foundations of cerebral asymmetries are still poorly understood. Recent advances in comparative cognitive neurosciences have made available new animal models that have started to provide unexpected insights into the evolutionary origins and neuronal mechanisms of cerebral asymmetries. Animal model-systems, particularly those provided by the avian brain, highlight the interrelations of genetic, hormonal and environmental events to produce neural and behavioural asymmetries. Novel evidences showing that functional and structural lateralization of the brain is widespread among vertebrates (including fish, reptiles and amphibians) have accumulated rapidly. Perceptual asymmetries, in particular, seem to be ubiquitous in everyday behaviour of most species of animals with laterally placed eyes; in organisms with wider binocular overlap (e.g., amphibians), they appear to be retained for initial detection of stimuli in the extreme lateral fields. We speculate that adjustment of head position and eye movements may play a similar role in mammals with frontal vision as does the choice for right or left lateral visual fields in animals with laterally placed eyes. A first attempt to trace back the origins of brain asymmetry to early vertebrates is presented, based on the hypothesis that functional incompatibility between the logical demands associated with very basic cognitive functions is central to the phenomenon of cerebral lateralization.

Modularity and spatial reorientation in a simple mind: encoding of geometric and nongeometric properties of a spatial environment by fish

When disoriented in environments with distinctive geometry, such as a closed rectangular arena, human infants and adult rats reorient in accord with the large-scale shape of the environment, but not in accord with nongeometric properties such as the colour of a wall. Human adults, however, conjoined geometric and nongeometric information to reorient themselves, which has led to the suggestion that spatial processing tends to become more flexible over development and evolution. We here show that fish tested in the same tasks perform like human adults and surpass rats and human infants. These findings suggest that the ability to make use of geometry for spatial reorientation is an ancient evolutionary tract and that flexibility and accessibility to multiple sources of information to reorient in space is more a matter of ecological adaptations than phylogenetic distance from humans.

Population lateralisation and social behaviour: A study with 16 species of fish

We investigated turning responses in 16 species of fish faced with a vertical-bar barrier through which a learned dummy predator was visible. Ten of these species showed a consistent lateral bias to turn preferentially to the right or to the left. Species belonging to the same family showed similar directions of lateral biases. We performed an independent test of shoaling tendency and found that all gregarious species showed population lateralisation, whereas only 40% of the nongregarious species did so. The results provide some support to the Rogers (1989) hypothesis that population lateralisation might have been developed in relation to the need to maintain coordination among individuals in behaviours associated with social life.

Modularity as a Fish (Xenotoca eiseni) Views It: Conjoining Geometric and Nongeometric Information for Spatial Reorientation

When disoriented in a closed rectangular tank, fish (Xenotoca eiseni) reoriented in accord with the large-scale shape of the environment, but they were also able to conjoin geometric information with nongeometric properties such as the color of a wall or the features provided by panels located at the corners of the tank. Fish encoded geometric information even when featural information sufficed to solve the spatial task. When tested after transformations that altered the original arrangement of the panels, fish were more affected by those transformations that modified the geometric relationship between the target and the shape of the environment. Finally, fish appeared unable to use nongeometric information provided by distant panels. These findings show that a reorientation mechanism based on geometry is widespread among vertebrates, though the joint use of geometric and nongeometric cues by fish suggest that the degree of information encapsulation of the mechanism varies considerably between species.

Insemination efficiency of two alternative male mating tactics in the guppy Poecilia reticulata

In this study we compared the insemination efficiency of two alternative mating tactics (courtship and sneak mating) in the guppy Poecilia reticulata by quantifying the number of sperm delivered during a copulation. During a single copulation, guppies delivered between zero and 92% of the sperm available, as determined by mechanically stripping the males sperm reserve at rest. The absolute number of sperm delivered after courtship was three times larger than that delivered through sneak mating; nonetheless, the variance was large with both tactics and the two distributions largely overlapped. The number of sperm available at rest increased with male size. With both tactics, the number of sperm delivered was positively correlated with the sperm available. Contrary to courtship copulations, in sneak copulations there was no correlation between the number of sperm delivered and male size. However, once the data were standardized for sperm reserve, small males delivered a larger proportion of their available sperm during sneak copulation. The rate of sexual acts (sigmoid and thrust rate) before copulation was not correlated with the number of sperm available. After the occurrence of a copulation in both the courtship and sneak copulation groups, the sexual activity of the male decreased in proportion to the amount of sperm he previously inseminated.

Complementary right and left hemifield use for predatory and agonistic behaviour in toads

CEREBRAL lateralization, the differing specializations of the right and left sides of the brain once thought to be unique of humans, is now well known to occur in both birds and mammals. Here we report that in toads the right hemisfield of vision guides predatory tongue-striking responses towards moving prey and the left hemisfield guides agnostic tongue-striking responses towards conspecifics. This indicates, for the first time, complementary cerebral specializations for visual processing in anurans, and strongly supports the hypothesis that lateralized brain functions in birds and mammals may have arisen from a common lateralized ancestor. Complementary specializations in visual processing may have originally evolved to avoid problem of response competition during control of medial organs such as the tongue in organisms with laterally placed eyes and, in organisms with wider binocular overlap, it appears to be retained for initial detection of stimuli in the extreme lateral fields.

The genome of the platyfish, Xiphophorus maculatus , provides insights into evolutionary adaptation and several complex traits

Several attributes intuitively considered to be typical mammalian features, such as complex behavior, live birth and malignant disease such as cancer, also appeared several times independently in lower vertebrates. The genetic mechanisms underlying the evolution of these elaborate traits are poorly understood. The platyfish, X. maculatus, offers a unique model to better understand the molecular biology of such traits. We report here the sequencing of the platyfish genome. Integrating genome assembly with extensive genetic maps identified an unexpected evolutionary stability of chromosomes in fish, in contrast to in mammals. Genes associated with viviparity show signatures of positive selection, identifying new putative functional domains and rare cases of parallel evolution. We also find that genes implicated in cognition show an unexpectedly high rate of duplicate gene retention after the teleost genome duplication event, suggesting a hypothesis for the evolution of the behavioral complexity in fish, which exceeds that found in amphibians and reptiles.

Do fish count? Spontaneous discrimination of quantity in female mosquitofish

The spontaneous tendency to join the largest social group was used to investigate quantity discrimination in fish. Fish discriminated between shoals that differed by one element when the paired numbers were 1vs2, 2vs3 and 3vs4, but not when 4vs5 or larger. Using large numerosities (>4), the ability to discriminate between two numbers improved as the numerical distance between them increased and a significant discrimination was found only with ratios of 1:2 or smaller (4vs8, 8vs16 and 4vs10). Experiments to control for non-numerical variables evidenced the role played by the total area of stimuli with both large and small numerosities; the total quantity of movement of the fish within a shoal appeared also important but only when large numerosities were involved. Even though the pattern of discrimination exhibited by female mosquitofish is not fully consistent with any of the existing models of quantity representation, our results seem to suggest two distinct mechanisms in fish, one used to compare small numbers of objects and one used when larger numerosities are involved.

Lateralisation of predator avoidance responses in three species of toads

Lateralisation of responses to presentation of a simulated predator was investigated in three species of toads: two European species (the common toad, Bufo bufo, and the green toad, Bufo viridis) and one species introduced to Australia from South America, the cane toad Bufo marinus. First a simulated snake was presented moving rapidly towards the toad in the frontal field of vision and the toads escape responses, including jumps to the right and to the left, were recorded. No significant bias in left or right side jumping was apparent in this test. Next the simulated snake was presented in the left or right lateral field of vision in random order. Escape and defensive responses were elicited more strongly, in all three species, when the stimulus was on the toads left side compared to its right side. Reaction times scored in the experiments with B. marinus, alone, did not differ from left to right. There were, however, species differences in the types of escape responses with respect to the laterality: B. viridis and B. marinus showed similar patterns of more sideways jumps with left presentation and more frontal jumps with right presentation. Sideways jumps were not lateralised in B. bufo, but this species showed more frontal jumps when the presentation was on the left side. These findings suggest that the selective involvement of structures located in the right side of the brain (left monocular visual field) in emotional responses (particularly fear responses) could be a phylogenetic ancient trait.

Roots of brain specializations: preferential left-eye use during mirror-image inspection in six species of teleost fish

It has recently been reported that predator inspection is more likely to occur when a companion (i.e. the mirror image of the test animal) is visible on the left rather than on the right side of mosquitofish Gambusia holbrooki. This very unexpected outcome could be consistent with the hypothesis of a preferential use of the right eye during sustained fixation of a predator as well as of a preferential use of the left eye during fixation of conspecifics. We measured the time spent in monocular viewing during inspection of their own mirror images in females of six species of fish, belonging to different families-G. holbrooki, Xenotoca eiseni, Phoxinus phoxinus, Pterophyllum scalare, Xenopoecilus sarasinorun, and Trichogaster trichopterus. Results revealed a consistent left-eye preference during sustained fixation in all of the five species. Males of G. holbrooki, which do not normally show any social behaviour, did not exhibit any eye preferences during mirror-image inspection. We found, however, that they could be induced to manifest a left-eye preference, likewise females, if tested soon after capture, when some affiliative tendencies can be observed. These findings add to current evidence in a variety of vertebrate species for preferential involvement of structures located in the right side of the brain in response to the viewing of conspecifics.