Angelo Quaranta

Asymmetric tail-wagging responses by dogs to different emotive stimuli.

We thank the Waltham Foundation for a grant to G.V. and A.Q., Elisabetta Versace for help with data analyses, and Lesley J. Rogers and Zsofia Viranyi for commenting on the manuscript. Financial support provided by the following institutions to G.V. is also gratefully acknowledged: MIPAF “Ben-o-lat” via Dip. Sci. Zootecniche, Univ. di Sassari, and Project EDCBNL (Evolution and Development of Cognitive, Behavioural and Neural Lateralization - 2006/2009), supported by the Commission of the European Communities (Programme “Integrating and strengthening the European Research Area” Initiative “What it means to be human”).

Hemispheric specialization in dogs for processing different acoustic stimuli

Considerable experimental evidence shows that functional cerebral asymmetries are widespread in animals. Activity of the right cerebral hemisphere has been associated with responses to novel stimuli and the expression of intense emotions, such as aggression, escape behaviour and fear. The left hemisphere uses learned patterns and responds to familiar stimuli. Although such lateralization has been studied mainly for visual responses, there is evidence in primates that auditory perception is lateralized and that vocal communication depends on differential processing by the hemispheres. The aim of the present work was to investigate whether dogs use different hemispheres to process different acoustic stimuli by presenting them with playbacks of a thunderstorm and their species-typical vocalizations. The results revealed that dogs usually process their species-typical vocalizations using the left hemisphere and the thunderstorm sounds using the right hemisphere. Nevertheless, conspecific vocalizations are not always processed by the left hemisphere, since the right hemisphere is used for processing vocalizations when they elicit intense emotion, including fear. These findings suggest that the specialisation of the left hemisphere for intraspecific communication is more ancient that previously thought, and so is specialisation of the right hemisphere for intense emotions.

Paw preference in dogs: relations between lateralised behaviour and immunity

Paw use in a task consisting of the removal of a piece of adhesive paper from the snout was investigated in 80 mongrel and pure-bred domestic dogs (Canis familiaris). Population lateralisation was observed, but in opposite directions in the two sexes (animals were not desexed): males preferentially used their left paw, females their right paw. The relationship between immune function and paw preference was then investigated. Some immune parameters (total number of white blood cells including lymphocytes, granulocytes and monocytes; leukocyte formula; total proteins; gamma-globulins) were investigated in a sample of left-pawed (n = 6), right-pawed (n = 6) and ambidextrous (n = 6) dogs. The results showed that the percentage of lymphocytes was higher in left-pawed than in right-pawed and ambidextrous dogs, whereas granulocytes percentage was lower in left-pawed than in right-pawed and ambidextrous dogs. Moreover, total number of lymphocytes cells was higher in left-pawed than in right-pawed and ambidextrous dogs, whereas the number of gamma-globulins was lower in left-pawed than in right-pawed and ambidextrous dogs. These findings represent the first evidence that brain asymmetry modulates immune responses in dogs.

Dogs turn left to emotional stimuli.

During feeding behaviour, dogs were suddenly presented with 2D stimuli depicting the silhouette of a dog, a cat or a snake simultaneously into the left and right visual hemifields. A bias to turn the head towards the left rather than the right side was observed with the cat and snake stimulus but not with the dog stimulus. Latencies to react following stimulus presentation were lower for left than for right head turning, whereas times needed to resume feeding behaviour were higher after left rather than after right head turning. When stimuli were presented only to the left or right visual hemifields, dogs proved to be more responsive to left side presentation, irrespective of the type of stimulus. However, cat and snake stimuli produced shorter latencies to react and longer times to resume feeding following left rather than right monocular visual hemifield presentation. Results demonstrate striking lateralization in dogs, with the right side of the brain more responsive to threatening and alarming stimuli. Possible implications for animal welfare are discussed.

Why Amphibians Are More Sensitive than Mammals to Xenobiotics

Dramatic declines in amphibian populations have been described all over the world since the 1980s. The evidence that the sensitivity to environmental threats is greater in amphibians than in mammals has been generally linked to the observation that amphibians are characterized by a rather permeable skin. Nevertheless, a numerical comparison of data of percutaneous (through the skin) passage between amphibians and mammals is lacking. Therefore, in this investigation we have measured the percutaneous passage of two test molecules (mannitol and antipyrine) and three heavily used herbicides (atrazine, paraquat and glyphosate) in the skin of the frog Rana esculenta (amphibians) and of the pig ear (mammals), by using the same experimental protocol and a simple apparatus which minimizes the edge effect, occurring when the tissue is clamped in the usually used experimental device. The percutaneous passage (P) of each substance is much greater in frog than in pig. LogP is linearly related to logKow (logarithm of the octanol-water partition coefficient). The measured P value of atrazine was about 134 times larger than that of glyphosate in frog skin, but only 12 times in pig ear skin. The FoD value (Pfrog/Ppig) was 302 for atrazine, 120 for antipyrine, 66 for mannitol, 29 for paraquat, and 26 for glyphosate. The differences in structure and composition of the skin between amphibians and mammals are discussed.

Sniffing with the right nostril: Lateralization of response to odour stimuli by dogs

Lateralization in dogs, Canis familiaris, has been reported for paw usage and response to visual and acoustic stimuli. Surprisingly, however, no investigation of possible lateralization for the most relevant sensory domain of dogs, namely olfaction, has been carried out. Here we investigated left and right nostril use in dogs freely sniffing different emotive stimuli in unrestrained conditions. When sniffing novel nonaversive stimuli (food, lemon, vaginal secretion and cotton swab odours), dogs showed initial preferential use of the right nostril and then a shift towards use of the left nostril with repeated stimulus presentation. When sniffing arousal stimuli such as adrenaline and veterinary sweat odorants, dogs showed a consistent right nostril bias all over the series of stimulus presentations. Results suggest initial involvement of the right hemisphere in processing of novel stimuli followed by the left hemisphere taking charge of control of routine behaviour. Sustained right nostril response to arousal stimuli appears to be consistent with the idea that the sympathetic hypothalamic–pituitary–adrenal axis is mainly under the control of the right hemisphere. The implications of these findings for animal welfare are discussed.

Lateralised behaviour and immune response in dogs : Relations between paw preference and interferon-γ, interleukin-10 and IgG antibodies production

The production of specific antibodies (IgG), interleukin-10 (IL-10) and interferon-gamma (IFN-gamma) was evaluated in dogs in relation to behavioural lateralisation as assessed by paw preference. Left-handed, right-handed and ambidextrous dogs of mixed breed were selected on the basis of their performance in a task consisting of the removal of a piece of adhesive paper from the snout. All dogs were immunised with rabies vaccine. IgG anti-rabies antibody response was evaluated by indirect immunofluorescence (IIF) test. Serum IFN-gamma and IL-10 levels were measured by ELISA in animals showing significant individual left-, right- or no-paw preferences in the behavioural test. The results showed that the direction of behavioural lateralisation influenced the immune response in dogs. The titers of anti-rabies antibodies were lower in left-pawed dogs than in right-pawed and ambidextrous dogs. Similarly, the IFN-gamma serum levels were lower in left-pawed dogs than in right-pawed and ambidextrous dogs. IL-10, on the contrary, seemed to be an immune parameter, which was not affected by lateralisation. These findings suggest that immunomodulation can be correlated with brain laterality in canine species by the regulation of the production of antibodies and some cytokines like IFN-gamma, which are molecules involved in the immune-neurohumoral crosstalk.

Expression Patterns of Two Serine Protease HtrA1 Forms in Human Placentas Complicated by Preeclampsia with and without Intrauterine Growth Restriction

Preeclampsia (PE) and intrauterine growth restriction (IUGR) are pregnancy-specific disorders that have in common abnormal placental implantation, a marked proliferation of villous cytotrophoblastic cells and focal necrosis of the syncytiotrophoblast. Several studies show an ischemic placenta with a high-resistance vasculature, which cannot deliver an adequate blood supply to the feto-placental unit. The cause of PE is a matter of debate, but recently studies in mice suggest that the primary feto-placental lesions are sufficient to initiate the disease. HtrA1, a member of the family of HtrA proteins, is a secreted multidomain protein with serine protease activity. It is expressed in first and third trimester of gestation. In specimens from the first trimester of gestation, immunostaining for HtrA1 is generally found in both layers of villous trophoblast, syncytiotrophoblast and cytotrophoblast. Cytoplasm of extravillous trophoblast and extracellular matrix of cell islands and cell columns are labeled for HtrA1. Specimens from third trimester of gestation show a more intense positivity for HtrA1 in the syncytiotrophoblast than in cytotrophoblast. The extravillous trophoblast and the decidual cells, is positive for HtrA1. The purpose of this study is to investigate the expression pattern of HtrA1 in placentas from PE without IUGR (maternal PE) and with IUGR (fetal PE) by quantitative western blotting and immunohistochemistry. By quantitative western blotting analysis we observed a significant upregulation of approximately 30 kDa HtrA1 form in PE. Differently, we detected a significant total HtrA1 down-regulation in PE-IUGR. Moreover, immunostaining for HtrA1 was positive in the villous trophoblast, in the syncytial knots and irregularly in the fetal vessel walls in PE placentas while immunostaining for HtrA1was present particularly in the syncytial knots in PE-IUGR placentas. In conclusion, we suggest that the approximately 30 kDa HtrA1 form can be correlated to maternal PE while that the significant down-regulation of total HtrA1 can be correlated to placental PE. These HtrA1 alterations could be considered as possible markers to discriminate placental PE from maternal PE.

Influence of behavioural lateralization on interleukin-2 and interleukin-6 gene expression in dogs before and after immunization with rabies vaccine

Evidence in several species, including dogs, has been collected demonstrating that the brain hemispheres modulate the immune system in an asymmetrical way. To study the interactions between immune response and lateralization, three groups of mixed breed dogs were selected on the basis of their performance in a paw preference test involving removal of a piece of sticky tape from the snout. The expression of interleukin-2 (IL-2) and interleukin-6 (IL-6) genes was measured in left-pawed, right-pawed and ambidextrous dogs before and after immunization treatment with a rabies vaccine. The results revealed a relationship between the mRNA expression of IL-2 and IL-6 genes and the direction of behavioural lateralization. Under basal conditions, IL-2 and IL-6 gene expression was higher in left-pawed dogs than in right-pawed and ambidextrous dogs. After the vaccine administration, decreasing levels of IL-2 and IL-6 gene expression were observed in left-pawed and right-pawed dogs, but not in ambidextrous dogs. These findings represent the first evidence that brain lateralization may influence the immune system in dogs by the modulation of mRNA gene expression of cytokines such as IL-2 and IL-6, which have been recognized as key immune-regulatory proteins.

Visual Lateralization in Wild Striped Dolphins (Stenella coeruleoalba) in Response to Stimuli with Different Degrees of Familiarity

Background Apart from findings on both functional and motor asymmetries in captive aquatic mammals, only few studies have focused on lateralized behaviour of these species in the wild. Methodology/Principal Findings In this study we focused on lateralized visual behaviour by presenting wild striped dolphins with objects of different degrees of familiarity (fish, ball, toy). Surveys were conducted in the Gulf of Taranto, the northern Ionian Sea portion delimited by the Italian regions of Calabria, Basilicata and Apulia. After sighting striped dolphins from a research vessel, different stimuli were presented in a random order by a telescopic bar connected to the prow of the boat. The preferential use of the right/left monocular viewing during inspection of the stimuli was analysed. Conclusion Results clearly showed a monocular viewing preference with respect to the type of the stimulus employed. Due to the complete decussation of the optical nerves in dolphin brain our results reflected a different specialization of brain hemispheres for visual scanning processes confirming that in this species different stimuli evoked different patterns of eye use. A preferential use of the right eye (left hemisphere) during visual inspection of unfamiliar targets was observed supporting the hypothesis that, in dolphins, the organization of the functional neural structures which reflected cerebral asymmetries for visual object recognition could have been subjected to a deviation from the evolutionary line of most terrestrial vertebrates.