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_____________________ Dog Tails as Tell-Tales: The Evolution of Brain-Hemisphere Specialization Peter F. MacNeilageUniversity of Texas at AustinA dog earns its reputation as best friend in part because it wags its tail in joy at the sight of its owner. But as a team of Italian researchers led by the University of Bari's Angelo Quaranta reveal in a recent article in Current Biology ("Asymmetric tail-wagging responses by dogs to different emotive stimuli," 20 March 2007), the wag of a dog's tail tells a much larger story. Quaranta and colleagues, examining closely the lesser-remarked fact that dogs wag their tails not just in pleasure but also when they are uneasy with an animal they are encountering, found a dog wags its tails differently in these two types of encounters: it wags the tail more to the right while greeting its owner but more to the left when meeting an unfamiliar dominant dog. Because the brain's control of the body is crossed, a bias in one direction means more activation of the brain hemisphere on the opposite side. Thus a dog's tail reveals which half of its brain is responding. This finding ties into a fascinating line of research regarding hemispheric specialization, evolution, specialized tasks versus routine, and how much like monkeys -- or dogs -- we humans might be.A hemispheric division of laborThis study is important partly because it subjected a single population to a single experimental paradigm. This provides a more powerful demonstration than if the findings came from different paradigms applied to different subject groups; it compares apples to apples. And these tail-wagging biases fit into a general evolutionary perspective -- a sort of division of labor between right and left brain -- that involves not just mammals but also other major vertebrate groups, including fish, reptiles and birds. A bit of background will help.Left wag, right brainWith respect to the leftward wag bias, Vallortigara and Rogers, in a 2005 review in Behavioral and Brain Sciences [pdf download], summarized evidence showing that in all major vertebrate groups (fish, amphibians, reptiles, birds and mammals) the brain's right hemisphere is more responsive than is the left hemisphere to stimuli that induce negative affect, such as the sight of a predator. In addition, other studies (such as a 2004 paper by Davidson [pdf download] on well-being and affective styles) have found evidence that in humans and monkeys the right hemisphere also tends to mediate avoidance responses. And in a 2006 review of brain-imaging studies of humans, Fox and colleagues concluded that the right hemisphere hosts a specialized system "involved in reorienting attention in response to salient environmental stimuli." Right wag, left brainAs to the rightward-wag bias, Davidson, in the same study mentioned above, also found that humans and other primates have a left-hemisphere-governed "approach" counterpart to the right-hemisphere avoidance tendency. I found similar evidence myself: in chapters in Milner's Comparative Neuropsychology and a book on the evolution of hemispheric specialization to be published this month, I propose that in most vertebrates the left hemisphere takes prime responsibility for routine actions (what Vallortigara and Rogers call "considered responses") -- a role complementary, as I see it, to the right hemisphere's dominant role in responding to emergencies or threats. Evidence for this includes Andrew, Tomassi and Ford's 2000 paper demonstrating that that chickens rely more heavily on their right eyes (connected to their left hemispheres) for the routine task of picking out grains of food from their surroundings. Bianki, meanwhile, showed in 1987 that a rat will maintain or increase its routine activity patterns if you anesthetize its right hemisphere but will radically reduce normal activity if you anesthetize its left hemisphere. A consistent picture emerges: Left brain for routine, right brain for oddities and emergencies.How do other findings of hemispheric specialization relate to this left brain:right brain/routine:nonroutine parallel? Consider a perceptual split found in both human and chicken visual processing. In both species, the left brain processes detailed (local) stimuli better than the right does, while the right hemisphere specializes in overall (global) aspects of a spatial array and makes more use of geometric coordinates. Thus routine activity may be facilitated by close, detailed examination of the environment whereas emergency reactions may be facilitated by a "quick-take" that rapidly analyzes the entire stimulus field. Ties to the pastIn some species, new specializations appear to have evolved atop older ones. For example, some evidence suggests that an early right-hemisphere specialization for species recognition (a skill crucial to predator detection) may have evolved into a right-brain-dominant capacity for recognizing faces within species -- and, eventually, recognition of affective information conveyed by the face. Thus your ability to read facial expression may be derived from some evolutionary ancestor's ability to tell shark from manatee. Another example: the left hemisphere's affinity for routine action may have evolved in some species into species-wide dominance of right-handedness, which has recently been found to be common not just in people but in monkeys and apes. Finally, left-hemisphere communication specialization, present in songbirds, monkeys and humans, may have evolved out of the generalized left-hemisphere control of routine action. These deep evolutionary linkages, although still vaguely defined, stand to challenge a strongly anthropocentric intellectual climate. Until the past 20 years or so, only humans were deemed to have significant hemispheric specializations. In that view, left-hemisphere language was considered to evolve from an entirely new left-hemisphere specialization, unique to humans and early humans, underlying right-handedness for tool construction and use. Our right-hemisphere spatial specialization, meanwhile, was thought to have evolved by default after the left-hemisphere specialization. Meanwhile, little attention was paid to the right hemisphere's emotion-related specialization. Much of this anthropocentrism has its roots in Rene Descartes and Western religion. As part of his distinction between mind and brain, Descartes asserted that only humans have minds. Thus he gave us mind as a purely cognitive entity, a rational tool unsullied by affective or emotional dimension -- and unstained, as it were, by animal urges, which he assigned to the body. A consequence of these attitudes has been an emphasis in much neuroscientific research on real-time human brain function -- how the two hemispheres work now -- in purely rational operations rather than on how both sides of the brain got to where they are by evolution of integrated mind-body packages. But the work described above joins other strands from ethology in insisting on a more evolutionary model, one in which the skills and capacities we've long thought most "human" -- tool use, language and analytical thought, as well as complex affective and emotional responses -- rise from neural structures and specializations that go deep into the evolutionary past. Quaranta and colleagues, aided by the 30 dogs they studied, add to this push away from an anthropocentric focus on purely rational, real-time mental processes. In this sense, dog tail act as tell-tales: they show us which way the wind is blowing not just in the dogs' minds but in the world of cognitive neuroscience. Peter MacNeilage is a professor of psychology at the University of Texas, where he studies the evolution of complex cogntive and action systems.