Cerebrum Spring 2020

S P R I N G 2 0 2 0


The Mind of a

and Bond with Humans DOG

A Renaissance in Canine Cognitive Science Sheds Light on How They See the World


Gregory Berns, M.D., Ph.D. Decoding the Canine Mind Page 10

Gregory Berns, M.D., Ph.D., is the Distinguished Professor of Neuroeconomics at Emory University, where he directs the Center for Neuropolicy and Facility for Education & Research in Neuroscience. He is also a professor in the psychology department and a founding member of the Society for Neuroeconomics. His has penned two books about canine cognition, What It’s Like to Be a Dog (Basic Books, 2017), and How Dogs Love Us (New Harvest, 2013), a New York Times bestseller. Berns specializes in the use of brain imaging technologies to understand human and canine motivation and decision-making. He is the co-founder of Dog Star Technologies, a company using neuroscience to enhance the dog-human partnership. Lee Alan Dugatkin, Ph.D., is a professor of biology and a College of Arts & Sciences Distinguished Scholar at the University of Louisville. He has studied the evolution of cooperation, the evolution of aggression, the interaction between genetic and cultural evolution, the evolution of antibiotic resistance, the evolution of senescence, and the evolution of risk-taking. He has been a contributing author to Slate Magazine , Scientific American , and The New Scientist , and author of The Altruism Equation (Princeton University Press, 2006), Mr. Jefferson and the Giant Moose (The University of Chicago Press, 2009) and co-author, with Lyudmila Trut, of How to Tame a Fox and Build a Dog (The University of Chicago Press, 2017). Carl Sherman has written about neuroscience for the Dana Foundation for ten years. His articles on science, medicine, health, and mental health have appeared in national magazines including Psychology Today , Self , Playboy , and Us . He has been a columnist for GQ and Clinical Psychiatry News , and is the author of four books. He holds a doctorate in English literature and has taught at various universities. When not writing about the mind, the brain, and the interesting things people do with them, he enjoys travel, listening to music, looking at art, and copyediting. He lives and works in New York City. Brenda Patoine is a freelance science writer, reporter, and blogger who has been covering neuroscience research for more than 30 years. Her specialty is translating complex scientific findings into writings for the general public that address the question of “what does this mean to me?” She has interviewed hundreds of leading neuroscientists over three decades, including six Nobel Laureates. She founded ScienceWRITE Medical Communications in 1989 and holds a degree in journalism from St. Michael’s College. Other areas of interest are holistic wellness, science and spirituality, and bhakti yoga. Brenda lives in Burlington, V.T., with her cat Shakti.

Lee Alan Dugatkin, Ph.D. Jump-Starting Evolution Page 16

Carl Sherman Neurosteroids: A Major Step Forward Page 22

Brenda Patoine Tracking the Neural Footprints of Consciousness Page 26




FEATURES 10 Decoding the Canine Mind

POINTS OF INTEREST NOTABLE FACTS IN THIS ISSUE 4 Serotonin and norepinephrine reuptake inhibitors, like fluoxetine (Prozac), are some of the most commonly prescribed drugs in veterinary behavioral medicine. Decoding the Canine Mind , Page 10 4 2020 marks the start of the seventh decade of this experiment, making it one of the longest, continually running, controlled experiments ever undertaken. Jump-Starting Evolution , Page 16 4 Researchers are considering therapeutic possibilities of neurosteroids for disorders ranging from schizophrenia and post-traumatic stress disorder to autism and Alzheimer’s disease. Neurosteroids: A Major Step Forward , Page 22 4 The two models are in stark contrast to one another: their definitions of consciousness differ, their assumptions about what constitutes consciousness differ, and their whole approach to the subject is fundamentally different. Consciousness: A New Search for Answers , Page 26 4 The case has raised a fierce debate in scientific journals over the ethics of conducting the trial and reporting the results through the media rather than a peer- reviewed scientific paper. Troubling Regulatory Standards , Page 8

Curious about a dog’s perception of the world and how a pooch’s brain works? Gregory S. Berns is using brain scanning and other strategies to find answers. By Gregory Berns, M.D., Ph.D. 16 Jump-Starting Evolution Three years after a best-selling book, a co-author explains how the silver fox- domestication experiment continues to help us better understand genetics and evolution. By Lee Alan Dugatkin, Ph.D. 22 Neurosteroids: A Major Step Forward Research that began three-quarters of a century ago has led to one of the first new drugs to treat depression in 60 years—and the potential to treat much more. By Carl Sherman 26 Consciousness: A New Search for Answers Two leading theories that are diametrically opposed are part of a new $20 million international research program to explore how consciousness arises and correlates in the brain. By Brenda Patoine

SECTIONS 5 Advances Notable brain science findings 6 Briefly Noted Worry and Stress; Recommended Brain Science & Health Articles; Music and Preterm Babies; By the Numbers 7 Bookshelf A few brain science books that have recently caught our eye 8 Neuroethics: Troubling Regulatory Standards By Philip M. Boffey

2 Contributors | 4 From the Editor | 30 Advisory Board | 32 Editorial Staff




It’s a Doggy Dog World

BY BILL GLOVIN Executive Editor, Dana Foundation W hen we began putting together this issue, no one had ever heard the term “coronavirus.” But now, with physical distancing, businesses closed, and humans going stir-crazy in the house, dogs may be one of the pandemic’s main beneficiaries, as they are being showered with ample amounts of attention. What better way to get a change of scenery and some exercise than leashing up your pooch for a long walk? In fact, a study by the Human Animal Bond Research Institute and Mars Petcare in 2019 revealed that 80 percent of people reported that pets reduced their loneliness, and 75 percent agreed that pets reduced feeling of social isolation. This second issue comes to you as we explore new ways to reimagine and deliver content. We divide our feature well in half: two long-form articles on brain research by neuroscientists and two on brain research or policy issues by science journalists. My ten-person advisory board suggests both topics and specific neuroscientist authors to address those topics, and reviews submitted articles for scientific accuracy. I’ve found that the board can be a tough nut to crack when it comes to article suggestions. All accomplished neuroscientists (see Page 30), they take into consideration recent advances, scientific merit, replication, and the potential of the research to change lives. So, to my great surprise—at the end of a conference call last fall—I told them I had been pitched the idea for an article about a fox domestication experiment. One of my longtime advisers, Bruce McEwen, was the first to chime in: “I’ve read about this project and it was an absolutely fascinating book,” he told the group. Seconds later, another adviser suggested that we spotlight a neuroscientist who uses fMRI to gain insights into canine cognition. “Why don’t we publish companion pieces?” another suggested. Soon, there was unanimous agreement that half our feature well should focus on canine cognition and behavior. My own research has since found at least 25 research centers throughout the world where canine cognition and behavior are studied—many of them forming in the last five years or so. In the U.S. alone, there are research centers at Duke, Yale, Arizona State, Barnard, and the University of Kentucky—just to name a few. The more we know about dogs, the more we help people—from service dogs for the disabled, to puppy training to make pet owners lives easier, to satisfying our curiosity about the behavior and intelligence of different breeds. Bruce, who so enthusiastically endorsed the idea to focus on dogs, will never get to read our two articles. After a brief illness, he passed away early this year at the age of 81. Bruce touched so many lives in his legendary career, and clearly had a soft spot in his heart for man’s (and woman’s) best friend. He wouldn’t be surprised to hear that dogs are helping their owners through this terrible pandemic. l


Bill Glovin Executive Editor

Seimi Rurup Assitant Editor


Brandon Barrera Editorial Assistant

Carl Sherman Copy Editor

Carolyn Asbury, Ph.D. Scientific Consultant

Bruce Hanson Art Director

Cerebrum is published by the Charles A. Dana Foundation, Incorporated. DANA is a federally registered trademark owned by the Foundation. © 2020 by The Charles A. Dana Founda- tion, Incorporated. All rights reserved. No part of this publication may be repro- duced, stored in a retrieval system, or transmitted in any form by any means, electronic, mechanical, photocopying, recording, or otherwise, without the prior written permission of the publish- er, except in the case of brief quotations embodied in articles. Letters to the Editor Cerebrum magazine 505 Fifth Avenue, 6th Floor New York, NY 10017 or cerebrum@dana.org Letters may be edited for length and clarity. We regret that we cannot answer each one.


ADVANCES Notable brain science findings

More news that plenty of SLEEP is important for health: A recent Penn State cohort study (which follows people over a long stretch of time) suggests that middle-aged adults who have high blood pressure or type 2 diabetes were at


A 2019 Boston University study published in the Annals of Neurology found that for every 5.3 years tackle football players played the game, they doubled their risk of developing the worst forms of CTE (chronic traumatic encephalopathy), a degenerative brain

greater risk of earlier death if they slept less than six hours a night. Other studies suggest sleep is when the body cleanses and restores itself; the brain washes away dead cells and toxins as well as consolidating the days’ memories. The Penn State researchers, writing in the Journal of the American Heart Association , suggest that people with diabetes or blood- pressure issues make sure they get help to get enough sleep as part of their treatment for those issues. l Book snobs might not have cause to be so quick to discount AUDIOBOOK lovers as “nonreaders” or something other, researchers at University of California say. In a study published in the Journal of the brain are stimulated whether we hear words or read them on a page, educators and others might consider offering audio as an alternative for some kids. l Studies have shown a small but significant relationship between noticeable HEARING LOSS and dementia. Now, a study published late last year in the journal J AMA Otolaryngology—Head and Neck Surgery suggests that even small losses of hearing can translate to reduced scores on cognitive tests. Researchers examined data on hearing and cognitive performance from more than 6,400 people 50 and older and found those whose hearing was not as good as before but had not yet gone past the range of “normal hearing” had proportionally lower cognitive scores. While it’s not yet known what could be causing this—increased cognitive load on circuits? changes in brain structure over the years?—some Neuroscience , they report that functional brain imaging of people who spent hours reading or listening to narrative stories showed the same patterns in the areas used for forming semantic meaning. If the finding holds that the same cognitive and emotional areas of

disease linked to repeated head hits. Some NFL players have cited CTE in their decision to retire early, most recently Luke Kuechy, 28. The linebacker for the Carolina Panthers was one of only four defensive players who made all-pro NFL at least five times in the 2010s. l

A growing number of studies suggest that the gut MICROBIOME—all the genetic material in the many types of single- celled organisms that live in your digestive system—may offer a rich target for treating mental health troubles. In one recent

study in the Journal of Affective Disorders , researchers took repeated readings of the microbiomes of 111 people shortly after they were admitted into inpatient treatment for psychiatric disorders until they were released, and found a series of measurable differences. The more severe a person’s depression or anxiety was, the less variety of bacteria researchers found in their microbiome. Next question to answer: Does psychiatric illness lead to changes in gut health, or vice versa? l ORGANOIDS—3-D clusters of cultured brain cells once optimistically called “mini-brains” or “brains in a dish”—might not be as directly or speedily helpful as once hoped. The cells appear to start developing similarly to normal brain cells, but the way they are grown in a culture dish itself puts them under

unusual metabolic stress. This alters how the cells transport proteins, break down sugars, and differentiate into mature cell types, according to a new study in Nature . Comparing the cells in organoids with cells collected from embryonic tissue, the researchers found some parts matched,

researchers suggest that people who notice they’re starting to have problems might do better by getting hearing aids earlier, and not waiting for the loss to pass the currently accepted measure of at least 25 decibels. l

including glia and some types of neurons, but not in the same proportions, and they could not match up some of the organoid cells with any type of naturally occurring cell. The researchers suggest finding new ways to grow these micro- tissues. l



Worry, Stress, and Anxiety “WORRY HAPPENS in your mind, stress happens in your body, and anxiety happens in your mind and your body. In small doses, they can be positive forces. But research shows that most of us are too worried, too stressed, and too anxious. The good news, according to Luana Marques, an associate professor of psychiatry at Harvard Medical School and president of the Anxiety and Depression Association of

MUSIC composed for preterm babies has been shown to strengthen the development of neural networks and may help counteract the neurodevelopment delays experienced by many who are born prematurely, according to an imaging study published in the Proceedings of the National Academy of Sciences . Composer Andreas Vollenweider tested many instruments and found infants most responsive to punji (a flute), harp, and bells. Researchers at the University Hospitals of Geneva then played the music he composed for some premature infants in their care and not for others nor for a control group of full-term infants. The brains of the babies who listened to the music showed patterns of connection that looked more like the full-term babies than the non-music preemies. These children are now six, and are undergoing cognitive and socio-emotional tests to see if this change has translated into reduced developmental delay. l

America, is that there are ways to regulate your symptoms: Get enough sleep; eat regular, nutritious meals, and move your body.” — Smarter Living, from the New York TImes l

BY THE NUMBERS $1.5 billion was raised in 2019 to find new drugs by artificial intelligence drug startups. 2 months is the time it took for multiple sclerosis patients to benefit from intermittent fasting. Popular regimens range from ingesting few, if any, calories all day every other day or several times a week to fasting 16 hours or more every other day.

60 is the number of chemical compounds (known as cannabinoids) found in a cannabis plant. 2,474 was the number of languages used to study cross-cultural emotional expression. 60,000 people in the U.S. suffer from frontotemporal degeneration, the most common form of dementia for those under the age of 60.

6 months of an aerobic training program helps improve brain glucose metabolism and executive function and has shown to help people with a genetic predisposition to Alzheimer’s disease. 300 Alzheimer’s drug trials have failed so far, including two recent trials for solanezumab (from Eli Lilly) and gantenerumab (from Roche).


BOOKSHELF A few brain science books that have recently caught our eye

Sex in the Brain: How Seizures, Strokes, Dementia, Tumors, and Trauma Can Change Your Sex Life by Amee Baird Although a rare phenomenon, it’s possible for sex to blow your mind. And that’s not speaking metaphorically. According to clinical neuropsychologist Amee Baird, Ph.D., the quality, location, and climactic


The Angel and the Assassin: The Tiny Brain Cell That Changed the Course of Medicine by Donna Jackson Nakazawa As recently as 2012, the medical world stood at the threshold of a new frontier. Microglia— tiny, non-neural cells oft-described as housekeepers of the brain—were revealed to be much, much more. In a series of

(or anti-climactic) qualities of sex can trigger severe brain conditions: strokes, burst aneurysms, and even transient global amnesia (temporary memory loss). In Sex in the Brain (Columbia University Press), Baird explores the titillating subject without stepping into the salacious. Instead, she presents the personal accounts of patients (and their partners) who found themselves coping with radical changes in sexual behavior—sometimes humorous, at other times startling— and the knowledge gleaned from these fascinating case studies. The book is careful in explaining the science behind changes in sexual behavior and effective in diffusing the stigmas often associated with sexuality. (This is especially true of neurological changes affecting sexual behavior following neurosurgery, traumatic brain injuries, or brain disorders and their treatments.) l

groundbreaking discoveries, microglial cells graduated from humble removers of dead neurons and cells to the horticulturist of the brain, pruning its neuronal circuitry during development and, if triggered, ravaging the neural landscape into dysfunction. In The Angel and the Assassin (Random House/Ballantine) science journalist Donna Jackson Nakazawa, herself previously immobilized by a rare autoimmune disease, chronicles the breakthroughs, inviting readers into top research labs throughout the U.S. to speak with the neurobiologists furthering this knowledge and to hear directly from patients with autoimmune diseases who stand to benefit. Her work reveals that harnessing these tiny cells could help “those suffering with depression, anxiety, obsession, distraction, or forgetting … finally escape the thieves that can rob them of whole lifetimes.” l

Concentration: Staying Focused in Times of Distraction by Stefan Van der Stigchel; Translated by Danny Guinan A fierce and relentless contest rages—the participants are legion, the ploys endless, and the prize dear to each of us: our attention. Social media, mobile devices, and advertisers all vie for our engagement. For Stefan Van

Conscience: The Origins of Moral Intuition by Patricia S. Churchland, Evolutionary changes in the brain’s circuitry across millennia have made it likely that mothers will care for their vulnerable offspring. This bond—between mother and child—should be viewed as the platform for social and moral behavior, according to

der Stigchel, Ph.D., attention expert and Professor of Cognitive Psychology at Utrecht University, the “attention crisis” is a conflict that’s ours to win—we only have to make the right choices. Concentration: Staying Focused in Times of Distraction (MIT Press) is Van der Stigchel’s treatise on resisting distraction and reclaiming your ability to focus. In it, Van der Stigchel describes the intricacies of concentration, the precarious balancing act of multitasking (it’s not always a bad thing), and how to tame attention: your own and others’. If concentration is a muscle (and Van der Stigchel likens it so), then reading Concentration: Staying Focused in Times of Distraction will provide for you a fitness regimen to keep the skill deployment ready—no easy task in these content-saturated times. l

neurophilosophy pioneer and Dana Alliance member Patricia S. Churchland, Ph.D. In essence, the bond is a progression of self- care extending to include my children , expanding to include my clan , and so on. This crude reconstruction of Churchland’s argument is only a pale imitation of the ideas found in Conscience (W. W. Norton), a work rife with the research and neuroscience of conscience. Besides the mother-child bond, she cites fascinating studies on psychopaths, sharing the knowledge gleaned from studying brains with “atypical wiring” and reveals the data from studies with twins, suggesting that political attitudes may well be hereditable traits. For Churchland, who argues that morality transcends “pure reason,” neurobiology is a promising path to ethical discovery. l




BOOKSHELF A few brain science books that have recently caught our eye

Troubling Regulatory Standards BY PHILIP M. BOFFEY O rdinarily, I would not base a column about a new stem cell treatment on a single dramatic case, or even a dozen cases, of clinical improvement. But an announcement by scientists at a Japanese medical school claimed such miraculous results in largely curing one man of spinal cord paralysis, and restoring some functioning to others, that it begs for close analysis. In 2015, a 47-year-old teacher who was high diving at a local pool hit his head on the bottom and damaged his spinal cord, leaving him mostly paralyzed. He was enrolled in a clinical trial of Stemirac, a new stem cell treatment for spinal cord injuries, at Sapporo Medical University. He showed immediate improvement the next day and seven months later left the hospital under his own power. Although he remains clumsy, he can cook, drive, and teach math online. The stem cells used, known as mesenchymal stem cells, were isolated from his bone marrow, multiplied in the laboratory, and injected back into the bloodstream intravenously. The case has raised a fierce debate in scientific journals over the ethics of conducting the trial and reporting the results through the media, rather than a peer-reviewed scientific paper. There is no question that the procedure was legal under Japan’s relatively lenient approach to drug and therapy approvals. The process—and the questions it raises—is ably described in a comprehensive overview by Amos

The Deep History of Ourselves: The Four-Billion-Year Story of How We Got Conscious Brains by Joseph LeDoux Behavioral scientists often compare the neurobiology of different animal groups (think rodents and flies, for example), searching for similarities and differences to further our understanding of human behavior. Certain ‘survival actions’—activities such as fluid balancing,

reproduction, eating, drinking—are so universal, says neuroscientist and Dana Alliance member Joseph LeDoux, Ph.D., that they are exhibited by organisms predating nervous systems altogether, revealing just how early these behaviors manifested. Ambitious in scope, The Deep History of Ourselves (Penguin Random House) stretches back to protocells and the earliest microbial life, tracing behavior’s lineage from the simplest of origins in bacteria and protozoa. The content is grouped by theme, allowing readers direct access to the subject matter of their preference: survival and behavior, the dawn of complex organisms, vertebrates, neurons, cognition, consciousness, and emotion, just to name a few. An expansive work, The Deep History of Ourselves is a retrospective and welcoming journey for all seeking a better grasp on human behavior and self-awareness. l

Brain on the Web A few brain-related articles we recommend:

> OCD and anxiety disorder treatment can be complicated by coronavirus fears

> COVID-19: dealing with social distancing > A psychologist’s science-based tips for emotional resilience during the coronavirus crisis > From a doctor, a reminder to keep pushing on > Five years after a nasty crash, a symbolic layup for Josh Speidel


In a worst-case scenario, if nations keep lowering the bars for approval, one expert warns that we could go back to the days when most medical products didn’t work and we didn’t know it.

with Stemirac did only as well as patients enrolled in the untreated control groups in previous trials testing other potential treatments for spinal cord injuries. Some experts believe the small trial should have been double-blinded, with neither the doctors nor patients knowing who had received the stem cells and who got a placebo. That would have been easy to do. The stem cells were injected, and a placebo could have been injected, too; but the researchers did not do that since Japan’s regulations didn’t require it. Critics also object that none of the data has been published, apparently because the Japanese Health Ministry believes such publications would amount to “promotional materials.” The university was allowed to promise great results from its therapy in an advertisement without any data, but it was forbidden to publish its data in a journal for experts to evaluate, a twisted logic which Nature’s article called “Kafkaesque.” A final caveat: All of the work has been conducted by researchers at a single institution—Sapporo Medical University, on Japan’s northernmost island, Hokkaido—limiting the ability of other experts to detect and correct possible biases or errors. The Sapporo researchers and their

Zeeberg, a freelance journalist based in Phnom Penh, Cambodia, in Undark , a highly respected digital journalism site that examines issues raised by the sciences, and in a news report by David Cyranoski in Nature , based on interviews with ten independent experts. Japan, which hopes to become a global leader in regenerative medicine, has set up a system to fast-track therapies based on hints of efficacy so long as researchers collect follow- up data to justify final approval. Last December, the Japanese health ministry gave conditional approval of Stemirac, which allows the inventors to market and sell the drug for the next seven years, as long as they collect data from the participants to show that it works. Most of the participants’ $140,000 cost will be paid by Japan’s National Health Insurance. The short-term clinical trials that claimed to show efficacy were based on only 13 participants, including the injured diver, and lacked a control group. Critics of the fast-track approval cite a host of objections. Most important, the lack of a control group makes it impossible to be sure the therapy had any efficacy at all. It is possible the participants would have improved naturally, even without the stem cell treatment. Indeed, patients injected

backers retort that the results achieved were “unprecedented” and amply justify making the product available on a conditional basis while further studies are conducted to support a full approval. They also note that other advanced countries, including the United States, have taken steps to speed drugs to patients suffering from devastating diseases based on preliminary evidence that the drugs appear safe and effective. There is a trend toward giving individuals a greater role in deciding what risks to take to improve their own health. My own feeling is that if I were paralyzed by a spinal cord injury, I would take substantial risks to improve my motor function. True, there could be unexpected side effects in the future that the fast-track process failed to detect, but it is hard to believe those would be worse than near total paralysis. The chief danger is to the regulatory system itself, which could be eroded to the point where no one really knows if a therapy is safe or effective, leaving patients prey to peddlers of dubious nostrums while wasting money that could be spent more productively. In an apocalyptic worst-case scenario, if nations keep lowering the bars for approval, one expert warns that we could go back to the days when most medical products didn’t work and we didn’t know it. l Phil Boffey is former deputy editor of the New York Time s Editorial Board and editorial page writer, primarily focusing on the impacts of science and health on society. He was also editor of Science Times and a member of two teams that won Pulitzer Prizes. The views and opinions expressed are those of the author and do not imply endorsement by the Dana Foundation.

The university was allowed to promise great results from its therapy in an advertisement without any data but it was forbidden to publish its data in a journal for experts to evaluate, a twisted logic which Nature’s article called “Kafkaesque.”



ecoding the



ur author, the Distinguished Professor of Neuroeconomics at Emory University and co-founder of Dog Star Technologies—a company using neuroscience to enhance the dog-human partnership—has put more than 100 dogs through a brain scanner. His article addresses a dog’s perception of the world, social cognition findings, canine mental health, and more.


Instead of treating the dogs as research subjects, we treated them as voluntary participants, meaning they were afforded the same basic rights as human volunteers.

T here is no official census for dogs and cats, but in 2016, the American Veterinary Medical Association estimated that 59 percent of households in the United States had a pet. Although the numbers of dogs and cats remains debatable, dogs continue to gain in popularity with 38 percent of households having at least one. Families with children are even more likely to have a dog (55 percent). With all due respect to cats, dogs have insinuated themselves into human society, forming deep emotional bonds with us and compelling us to feed and shelter them. Worldwide, the dog population is approaching one billion, the majority free-ranging. Even though many people are convinced they know what their dog is thinking, little is actually known about what is going on in dogs’ heads. This may be surprising because the field of experimental psychology had its birth with Pavlov and his salivating dogs. But as dogs gained traction as household pets, in many cases achieving the status of family members, their use as research subjects fell out of favor. In large part, this was a result of the Animal Welfare Act of 1966, which set standards for the treatment of animals in research and put an end to the practice of stealing pets for experimentation. How strange it is then that these creatures, whose nearest relatives are wolves, live with us and even share our beds, yet we know almost nothing about what they’re thinking. In the last decade or so, however, the situation has begun to change, and we are in the midst of a renaissance of canine cognitive science. Research labs have sprung up around the world, and dogs participate not as involuntary subjects, but as partners in scientific discovery. This new research is beginning to shed light on what it’s like to be a dog and the nature of the dog-human bond.

leave some food on the perimeter. And a friendship is born. Eventually wolf- dogs, even if they didn’t hunt, could act as sentries, alerting humans to intruders. The evolution of cooperation is what allowed humans to dominate the planet, and at the dawn of civilization, we extended our ability to cooperate with each other to another species: dogs. Although there is no fossil record of behavior, there is increasing genetic evidence for this sort of co-evolution. In 2017, a team of researchers found a correlation between sociality in dogs with variants of several genes that had previously been identified in Williams- Beuren syndrome (WBS), a rare genetic disorder in humans. A core feature of WBS is hyper-sociality. When the team evaluated dogs and wolves on tasks that measured sociality, they found two canine genes in the WBS locus that are associated with this hyper-sociality in humans. These results suggest that the key evolutionary event that turned wolves into dogs was an amplification of genes related to sociality. If that is true, dogs may hold the key to helping humans achieve what can often be a struggle: to be more social, more generous, more loving, more forgiving. What It’s Like to Be a Dog So what is going on in a dog’s head? The traditional approach, pioneered by Pavlov, is to measure a dog’s behavior under different circumstances and try to infer why they do what they do. But consider a common example: teaching a dog to fetch. Some dogs, like retrievers, may do this instinctively, but others do not. Is this because the non-performers don’t understand what is being asked of them? Or is it that they understand but would rather do something else? It is all too tempting to project a human explanation onto the

Dogs are Special When scientists use animals in research, they often turn to species that are closely related to humans. “Close” is relative, as even chimpanzees and bonobos diverged from hominids at least 5 million years ago. Monkeys diverged about 25 million years ago, and to find a common ancestor with the dog—indeed with any carnivore—you have to go back 97 million years. But this summary overlooks the very thing that makes dogs special: their evolution has been altered to make them more socially compatible with us than any other animal. They were, in fact, the first animal to have been domesticated. The million- dollar questions are when and where this happened. We know that dogs existed at the time of the first human settlements in the eastern Mediterranean. In the area known as the Fertile Crescent, their remains have been found buried alongside humans, and these have been dated to 11,000 years ago. Cats, for comparison, did not appear until 8,000 years ago and probably didn’t change into their modern form until 4,000 years later. It is fair to say that only dogs were present at the dawn of human civilization. The world these early dogs and humans inhabited looked quite different from ours. Even though the last ice age was ending, the climate was still colder than now. This probably brought wolves (an ancestor of the dog) into more frequent contact with humans as the ice sheets retreated. One theory is that wolves and humans helped each other hunt. It seems increasingly likely, though, that the more social wolves began hanging around human settlements to scavenge for leftovers. It is not hard to imagine a curious wolf, probably a juvenile, approaching the edge of a tribe. A human, maybe a child who wouldn’t know any better, might


dog, to anthropomorphize. The fetch example also highlights an important point: dogs, like people, are individuals. We must be careful in generalizing about dog findings, as there is no such thing as a generic dog. Just like there isn’t a generic human. Because of the limits of interpreting behavior, my colleagues and I turned to the use of brain imaging to figure out what dogs are really thinking. When we began ten years ago, our approach was different from most animal research. Instead of treating the dogs as research subjects, we treated them as if they were voluntary participants, affording them the same basic rights as human volunteers. We did not use sedation or restraints. Instead, we developed a training program that taught the dogs to walk into a functional magnetic resonance imaging (fMRI) scanner, place their heads in custom-designed chin rests, and lie comfortably while scanning their brains (music video). Since then, we have trained over 100 dogs for fMRI. Many of them have been participating for their entire lives and have become so used to the scanner that it is hard to get them to leave! Before getting into how a dog’s brain works, it should be understood, if obvious, that dogs do not have the same amount of neural infrastructure that humans do. As a rule, larger animals have larger brains. The encephalization quotient (EQ) accounts for the relationship between brain and body size, such that an EQ=1 means an animal has an average brain size for its body weight. Humans have an exceptionally large EQ of about seven, while dogs are a bit better than your average mammal, with an EQ of 1.2. However, we can see from an MRI of a dog brain that even though it is smaller than a human brain, all of the same basic structures are present. This is

Dog brain (left) and human brain (right). Images are not to scale as the dog brain is approximately one-tenth the weight of the human brain. (Dog brain image courtesy of Thomas Fletcher, University of Minnesota.)

true for large regions like the cerebral cortex and the cerebellum, as well as for smaller, subcortical structures like the brainstem, hippocampus, amygdala, and basal ganglia, which have important roles in movement, memory, and emotion. Dogs also have large olfactory systems, comprising about two percent of the total brain weight (compared to 0.03 percent in humans). Where dogs fall short is in the cortex. Apart from being smaller, there are fewer folds, which means less surface area and fewer neurons. The frontal lobe, which in humans occupies the front third of the brain, is relegated to a paltry ten percent in dogs. The commonality of brain structures is true across all mammals. While there may be differences at a microscopic level, we all carry around the same basic hardware. Scientists and philosophers continue to debate whether a dog’s experience is the same as a human’s, but the commonality of brain structure suggests a certain commonality in function as well. Dogs have a hippocampus because they have to remember things, too. They have an

amygdala because they get aroused and excited and scared, just like we do. They may even suffer similar mental problems (more on that later). We have discovered many things about dogs’ perceptual experience of the world, but the ones that are most interesting are in the domain of social cognition. The first question many people ask is, “Does my dog love me?” Without getting into the nuances of love, the question gets to the heart of the dog-human relationship, namely, what are a dog’s motives? Is it all about food, or can dogs experience positive emotions for purely social reasons? To answer the question, we used fMRI to measure activity in a structure at the heart of the brain’s reward system: the caudate nucleus. Before scanning, we trained the dogs on a simple association between toys and rewards (video). Each toy was held in front of the dog for ten seconds and then followed by either a treat or by their owner popping into view and praising them with, “Good dog!” The toy set up a state of expectation, which we could measure in the caudate. We found that 13 of 15 dogs had equal or greater activation for praise than for


Dogs may hold the key to helping humans achieve what can often be a struggle: to be more social, more generous, more loving, more forgiving.

food. Is that love? We don’t know, but it does show that most dogs have brain systems highly tuned to social rewards, and some even respond more to their owner’s praise than food itself. How does this social bond form? Humans, like most primates, are born ready to bond with their parents and other members of their social group. Faces carry a wealth of social information and, in the 1990s, neuroscientists discovered that primates have an area of their visual systems dedicated to processing faces, called the fusiform face area. To see if dogs have equivalent areas, we showed pictures and videos to dogs while they were in the MRI scanner. We showed faces (dog and human), objects, scenes, and scrambled images. And just as in humans, we found an area of the dog visual system that is strongly and specifically activated by faces. We called it the “dog face area.” Like the praise experiment, this demonstrates that dogs have more in common with us than we realized, and that they have the basic tools to process human faces. While we humans identify people by their appearance, dogs may rely on their sense of smell. In an early fMRI study, we presented dogs in the scanner with five scents: their owner, an unfamiliar person, another dog in the house, an unfamiliar dog, and their own scent. Human scents were obtained from underarm wipings and dog scents from the area that dogs like to smell—their butts. Although we expected to find the strongest response to the smell of other dogs, in fact we found that the scent of the owner elicited the greatest activation in the reward system of the dog’s brain. This means that dogs cannot only identify us by smell, they seem to like the smell of their human best (to the extent that reward system activation means they like something.)

Auditory Processing What about dogs’ ability to

real words activate language areas more than fake words, presumably because humans immediately recognize gibberish and stop trying to extract meaning from it. But in the dogs, we found the opposite. The gibberish words caused more activation in auditory areas than the real words. These areas extended beyond what is considered primary auditory cortex, and so we think they represent rudimentary language processing areas. This tells us two important things. First, dogs can discriminate between words they have heard before and those they haven’t. Second, their reaction to novel words is different from humans’. Instead of immediately recognizing that they have no meaning, dogs pay close attention to novel words, perhaps to figure out what their human is trying to communicate. This response may derive from their hyper-sociality and desire to please. (However, you can be sure that a dog will learn to ignore you if you constantly speak gibberish). What about complex emotions, like guilt? Although many people believe their dog knows when they have done something wrong, researchers continue to debate whether dogs have the capacity to experience emotions like shame or guilt. Unfortunately, we can’t use fMRI to look for a neural signature of guilt in a dog, in large part, because we haven’t found one in humans. (This may seem surprising, but it has been devilishly hard to find reliable neural markers of human emotional states in general.) However, we have found evidence for something like envy in the dog’s brain. In this experiment, the dog had to watch their owner feed a realistic statue of a dog. As a control condition, the owner placed food in a bucket. We found evidence for amygdala activation, which is a neural marker for arousal, when the fake dog was fed. Although not quite the same as envy, arousal

understand human speech? Here, we have to be careful in what we mean by “understand.” Dogs seem to understand basic commands like “sit” and, to varying degrees, “come,” but that does not mean that they understand words the way humans do. We use words as symbolic placeholders. We are also very noun-centric. There are roughly ten times as many nouns as verbs, in part, because we label everything. A dog, however, may find actions more salient than names. Humans know that the word “ball” represents a whole class of objects, and its precise meaning derives from how it is used in a sentence. When a dog hears the word “ball,” do they conjure up an image in their mind’s eye like a human would? Maybe “ball” to a dog means the act of retrieving something, or maybe dogs pick up salient information by the tone of our voices when we say the word. As a first step toward answering these questions, we taught some of the MRI dogs the names of two new toys. To do this, the owner would point to a stuffed animal and say its name, for example, “monkey.” When the dog moved toward it, they would get a treat. Gradually, we removed the pointing. When the dog learned the name of one toy, we then introduced a second. After they learned that, they had to make the correct choice by name when both were present. Before they were deemed ready to scan, a dog had to demonstrate their knowledge by being 80 percent accurate in picking the correct toy on command, much like the famous dog, Chaser, who was reported to know the names of 1,000 toys. With the dog in the scanner, the owners spoke the names of the toys. As a control condition, they also spoke gibberish words that the dogs hadn’t heard before. When this type of experiment is done in humans,


Research labs have sprung up around the world, and dogs participate not as involuntary subjects, but as partners in scientific discovery.

Dogs and Mental Health If dogs have evolved to be man’s best friend, is it possible that they also suffer from some of the same mental disorders as people do? Growing evidence suggests the answer is yes, and this is all the more reason to take a closer look at what is going on in dogs’ heads. Human mental illness is diagnosed largely by symptoms. According to the American Psychiatric Association’s Diagnostic and Statistical Manual of Mental Disorders (DSM-5), depression is characterized by depressed mood, diminished pleasure, slowed thinking, fatigue, feelings of worthlessness or guilt, and thoughts of death. The only objectively measurable symptom is weight change. Similarly, generalized anxiety disorder is associated with excessive anxiety and worry, restlessness, fatigue, decreased concentration, irritability, muscle aches, and sleep problems. Dogs, of course, cannot speak, so they can’t report whether they’re feeling sad or anxious. Although neuroimaging may soon change things, we currently have to rely on dogs’ behavior to infer what they are feeling. For example, when dogs are scared, they behave in characteristic ways, which include trembling, hiding in closets or under furniture, chewing or scratching doors to escape, pacing, barking, whining, and defecating or urinating in the house. When these occur in the context of being left alone, they are often labeled “separation anxiety.” Aggression is another frequently misunderstood manifestation of emotional states in dogs. What humans label as aggression may be a normal part of a dog’s behavioral repertoire, which includes barking, growling, and biting. Any dog can bite, and most will do so if provoked sufficiently. However, when

for each subject. This would seem impossible for a dog, but with each visit to the scanner, we have found that the MRI dogs get more and more comfortable with the environment. We have several dogs who are content to lie there, watching whatever content we create for them. Preliminary results suggest that it is possible to decode brain states in some dogs. In the language study, for example, we were able to decode which word was spoken from about half of the dogs’ brains. As we extend this approach to more complex stimuli, we may soon be able to decode emotional states and learn what makes them so hyper-social and lovable.

might be a response to envy. This wasn’t universal, though. Only the dogs who displayed aggressive traits toward other dogs had this amygdala response. Again, this highlights the individuality of dogs. A complementary approach toward decoding emotional states uses machine learning to mine brain data obtained while a person (or dog) watches videos with different types of emotional content. Building on early results of decoding content of visual images from the brain, this new approach suggests a map of emotions in the human visual system, including states like anxiety, awe, fear, disgust, joy, and adoration. Machine learning techniques require a lot more data than conventional fMRI experiments provide—typically hours in the scanner

Callie in the MRI scanner while watching pictures of faces.


they bite, dogs can cause serious injury, especially to children. Interestingly, dogs with behavioral problems often improve when they are treated with human medications for depression and anxiety. Serotonin and norepinephrine reuptake inhibitors, like fluoxetine (Prozac), are some of the most commonly prescribed drugs in veterinary behavioral medicine. Others include benzodiazepines, tricyclic antidepressants, beta- blockers, and even lithium. Indeed, the psychopharmacopeia for dogs is nearly the same as for humans. The fact that these medications work in dogs speaks to common biological mechanisms of mood regulation. And unlike humans, dogs are not susceptible to placebo effects (although their owners might be, by expecting improved behavior.) Notwithstanding their emotional quirks, dogs are used in a variety of capacities to help people with disabilities. Service dogs are trained for specific tasks that a person cannot do by themselves, which might include picking up items, opening doors, and alerting to sounds. A psychiatric service dog might be trained to detect the onset of psychiatric episodes, or to turn on lights for someone with post-traumatic stress disorder. In contrast, emotional support dogs are not trained for specific tasks, but used for companionship, to alleviate loneliness, and to aid in the treatment of depression and anxiety. While service dogs are afforded certain protections under the Americans with Disabilities Act, emotional support animals are not (although they may be covered by other laws, like the Fair Housing Act and Air Carrier Access Act.) Because service dogs often require extensive training, the cost may be prohibitive for many people, up to $50,000. Most dogs are not cut out for

this kind of work, so there is a need to identify those that are and not waste resources training those who will not be good service dogs. Brain imaging may play a role here. In a study of 50 dogs- in-training, we were able to predict with 91 percent accuracy whether a dog would or would not graduate service dog training. In particular, we found that amygdala activation was negatively correlated with success, suggesting that dogs that are prone to arousal—either because they are anxious or simply want to play—are not good candidates for service dogs. It is worth keeping in mind, however, that dogs are not simply treatments to be prescribed for various conditions. Like people, dogs have a wide variety of skills and personalities. And while there are some differences between breeds in any particular personality trait, there seems to be as much variability within a breed. The key to a strong dog- human bond is in the match between dog and human, but this may be as hard to predict as the match between two people. Future research, both with brain imaging and other physiological measures, may soon shed light on the canine side of the equation. l

All good dogs? Yes, but which ones have what it takes to be a service dog?

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