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The Neuroscience
of
Human Relationships
Attachment and the
Developing Social Brain

Second Edition

Louis Cozolino

W. W. Norton & Company

New York • London

2
Dedication

For Susan
Thank you for allowing me to
dig deep,
fly high,
and smile wide.

3
 Contents

Cover
Title Page
Dedication
Preface to the Second Edition
Introduction: I, Me, Mine
Part I: The Emergence of Social Neuroscience: An Overview
1: The Social Brain
2: The Evolving Brain
Part II: The Social Brain Structures and Functions

3: The Developing Brain

4: The Social Brain: A Thumbnail Sketch
5: Social and Emotional Laterality
Part III: Bridging the Social Synapse
6: Experience-Dependent Plasticity: The Science of Epigenetics
7: Reflexes and Instincts: Jump-Starting Attachment
8: Addicted to Love
9: Implicit Social Memory
10: Ways of Attaching
Part IV: I See You
11: I’ve Just Seen a Face
12: Getting to Know You
13: Monkey See, Monkey Do: Imitation and Mirror Neurons
14: Resonance, Attunement, and Empathy
Part V: The Power of Relationships
15: Sociostasis: How Relationships Regulate Our Brains
16: The Impact of Early Stress
17: Interpersonal Trauma
Part VI: Disorders of the Social Brain

18: Social Phobia: When Others Trigger Fear

19: Borderline Personality Disorder: When Attachment Fails

4
 20: Psychopathy: The Antisocial Brain
21: Autism: The Asocial Brain
Part VII: Social Neural Plasticity
22: Self and Others
23: From Neurons to Narratives
24: Healing Relationships
25: From Social Brain to Group Mind
References
Acknowledgments
Credits
Index
The Norton Series on Interpersonal Neurobiology
Also Available in the Norton Series on Interpersonal Neurobiology
Copyright

5
 Preface to the Second Edition

Since the publication of the first edition, the field of social neuroscience has grown at a mind-numbing pace.
On the one hand, technical advances provide more windows into our inner neural universe. On the other,
terms like attachment, empathy, compassion, and mindfulness regularly appear in the scientific literature and
highlight the deepening appreciation for the essential interdependence of brain and mind. More and more
parents, teachers, and therapists are asking how brains develop, grow, connect, learn, and heal. The challenge
for the first edition was to seek out and discover significant and relevant research. The challenge for the
second edition was to organize an abundance of new scientific riches.
A number of interesting developments have emerged between the two editions. Our understanding of
mirror neurons and their significance to human relationships has continued to expand and deepen. As
predicted in the first edition, the insula and cingulate cortices have gained increasing focus as researchers have
turned their attention to mind-body connectivity and the importance of subjective experience. Another
important development has been the gradual shift in focus from individual brain structures to functional
neural systems—an important and necessary step forward.
Exploration of what has alternatively been called the default mode network and cortical midline structures
is providing a new window into the exploration of the self. Something that is growing increasingly apparent is
that our attention to and analysis of others seems to have appeared earlier in our evolutionary history than
self-awareness. Human self-awareness appears to be an emergent function arising from a combination of
relationships, our ability to symbolize, and the tools provided to us by culture. A great deal of neural overlap
has been discovered in brain activation when we are thinking about others and ourselves. This raises many
questions, including how we come to know others and whether the notion of an “individual self” is anything
more than an evolutionary strategy to support our interconnection.
All scientific journeys seem to lead us back to the old adage: The more we learn, the more we realize
how much there is yet to learn. Fasten your seatbelts, hold on, and enjoy the ride.

Louis Cozolino
Los Angeles, California
January 2013

6
 Introduction: I, Me, Mine

The miracle is that the universe created a part of itself to study the rest of it, and that this part, in studying
itself, finds the rest of the universe in its own inner realities.
—John Lilly

Humans exist within a paradox: We conceive of ourselves as individuals yet spend our lives embedded in
relationships that build, shape, and influence our brains. Despite our fundamental social nature, the operative
term remains I. I have relationships, I make plans with friends, I keep in touch with family. Our sense of
reality is grounded in the experience of a separate self, and it is from this perspective that Western science
explores the brain. Yet, while we are busy cherishing our individuality, our brains and minds are being
stimulated, influenced, and regulated by those around us (DeVries et al., 2003; Hofer, 1984, 1987).
Gradually, we are discovering that we are social creatures with brains and minds that are part of larger
organisms called families, communities, and cultures (Wilson, 2012). This awareness is making it increasingly
clear that to understand a person, we need to look beyond the individual.
Half a century ago, these insights led family systems theorists to shift the focus of psychotherapy from
the individual patient to the family unit. The symptoms of the “identified patient” were thereby reinterpreted
as a by-product of the family’s struggle for homeostasis. But is the family the best frame of reference from
which to understand human experience? Should we zoom even further out to tribes or cultures, or zoom back
in to an individual’s biochemistry to get the best picture?
If we use Mother Nature as a guide, we see that when she likes an idea she sticks with it by conserving
structures and strategies through increasing layers of complexity. Assuming this is true (which I do), we stand
to learn a great deal from zooming in and out, from “neurons to neighborhoods,” while resisting the urge to
become attached to any particular frame of reference. In this way, we may gain a deeper understanding of the
interwoven tapestry of the biological, psychological, and social processes that constitute human life.

Unveiling the Social Synapse

Look closely at the body and you will discover layer upon layer of highly complex, interlocking systems. As
you examine each layer, you will discover countless individual cells that differentiate and migrate to specific
locations throughout the body. These cells, in turn, grow into an infinite variety of forms, organize into
functional systems, integrate with other systems, and, ultimately, create an individual. This process we accept
easily; but what about the notion that nature used this same strategy to connect individual animals (humans)
into larger biological organisms, which we call families, tribes, and species?
Individual neurons are separated by small gaps called synapses. These synapses are not empty spaces by
any means; rather, they are inhabited by a variety of chemical substances engaging in complex interactions that
result in synaptic transmission. It is this synaptic transmission that stimulates each neuron to survive, grow, and
be sculpted by experience. In fact, the activity within synapses is at least as important as what takes place
within the neurons themselves. We know that neurons activate and influence one another through multiple
biochemical messengers. Over vast expanses of evolutionary time, synaptic transmission has grown ever more
intricate to meet the needs of an increasingly complex brain.
When it comes right down to it, doesn’t communication between people consist of the same basic
building blocks? When we smile, wave, and say hello, these behaviors are sent through the space between us.
These messages are received by our senses and converted into electrical and chemical signals within our
nervous systems. These internal signals generate chemical changes, electrical activation, and new behaviors
that, in turn, transmit messages back across the social synapse.

7
 The social synapse is the space between us—a space filled with seen and unseen messages and the
medium through which we are combined into larger organisms such as families, tribes, societies, and the
human species as a whole. Because our experience as individual selves is lived at the border of this synapse and
because so much communication occurs below conscious awareness, this linkage is mostly invisible to us.
Much of this book focuses on unveiling the social synapse and exploring some of its mechanisms. Through
this exploration we will examine how people, like neurons, excite, interconnect, and link together to create
relationships.
If you can accept the idea of a social synapse, perhaps you might consider a second theoretical leap.
Neurons have three sequential levels of information exchange that are called first, second, and third messenger
systems. They are (1) the communication across the synapse that (2) changes the internal biochemistry of the
cell, which, in turn, (3) activates mRNA (messenger ribonucleic acid, the material that translates protein into
new brain structure) and protein synthesis to change cellular structure. It is through these processes that the
brain changes in response to experience. These three levels of information exchange are also taking place
between individuals. In other words, when we interact, we are impacting each other’s internal biological state
and influencing the long-term construction of each other’s brains. This, in essence, is how love becomes flesh.

The Discovery of the Brain

Honestly, when was the last time you thought about your brain? Except for the occasional headache that feels
like it is in the brain, we don’t even remember we have brains. In essence, a well-functioning brain is invisible,
which may account for why, at this point in our history, we know more about the movement of the planets
than the workings of our brains. In fact, not too long ago, anatomists and physicians thought that the seat of
consciousness resided in the heart, with the brain serving as the body’s air conditioner, cooling the blood as it
passed through.
The brain’s deeper significance is infinitely more complex than anything scientists have ever
encountered. Studying the brain is like exploring a vast and ancient country with diverse landscapes, cultures,
and customs. Our brains defy reduction to simple cause-and-effect relationships and anatomical boundaries.
Like complex cultures, many of the interactions are subtle to the point of invisibility. To understand a culture,
you need to be immersed in it and stay alert for small clues that may carry deep significance. Even a subtle
diversion of gaze in the town square can tell the story of two people or two nations. Adding to this complexity
is the fact that each of our brains is a unique interplay of our convoluted evolutionary history and the millions
of personal experiences that shape it throughout life.
Our brains are built in the enigmatic interface between experience and genetics, where nature and
nurture become one (Crabbe & Phillips, 2003; LeDoux, 2003). At first, genes serve as a template to organize
the brain and trigger critical and sensitive periods; later, they orchestrate the ongoing transcription of
experience into genetic material. Through the biochemical alchemy of template and transcription genetics,
experience becomes flesh, attachment takes material form, and culture is passed through a group and carried
forward through time.
Like every living system—from single neurons to complex ecosystems—the brain depends on
interactions with others for survival. Each brain is dependent on the scaffolding of caretakers and loved ones
for its growth and well-being. So we begin with what we know: The brain is a social organ of adaptation built
through interactions with others. To write the story of this journey, we must begin our guidebook with the
understanding that there are no single human brains—brains only exist within networks of other brains.
The fact that the brain is such a highly specialized social organ of adaptation is both good news and
bad news. The good news is that if unexpected challenges emerge, our brains have a greater chance to adapt
and survive. When good-enough parenting combines with good-enough genetic programming, our brains are
shaped in ways that benefit us throughout life. And the bad news? We are just as capable of adapting to
unhealthy environments and pathological caretakers. The resulting adaptations may help us to survive a
traumatic childhood but impede healthy development later in life. The family is the primary environment to
which our young brains adapt, and our parents’ unconscious minds are our first reality. Because the first few
years of life are a period of exuberant brain development, early experience has a disproportionate impact on
the development of neural systems. In this way, early negative interpersonal experiences become a primary
source of the symptoms for which people seek relief in psychotherapy.

Interpersonal Neurobiology

8
Interpersonal neurobiology, along with social neuroscience (Adolphs, 2003a), affective neuroscience
(Panksepp, 1998), and sociophysiology (Gardner, 1997; Adler, 2002) are among the emerging fields of study
attempting to bridge the gap between the biological and social sciences. They all share the goal of
understanding individuals within the context of the relationships into which we are born, in which we
develop, and through which we live our lives.
Interpersonal neurobiology assumes that the brain is a social organ built via experience. Through
interdisciplinary exploration it seeks to discover the workings of experience-dependent plasticity, or the ways
in which the brain is constructed by experience. At the core of interpersonal neurobiology is a focus on the
neural systems that organize attachment, emotion, attunement, and social communication. The bidirectional
causality between neural structure and experience requires a continual shift in focus from the brain to social
behavior and back again to the brain.
The social construction of the brain and the role of attachment relationships are particularly important
in interpersonal neurobiology, as is the application of scientific data to parenting, psychotherapy, and
education. In addition to data from neuroscience and psychology, interpersonal neurobiology utilizes research
from psychoanalysis, ethology, comparative anatomy, genetics, and evolution. In examining some of the
processes that take place within the social synapse we will explore a wide range of other fields that study
narratives, storytelling, eye contact, touch, attachment patterns, and body language.
Thus far, those of us interested in interpersonal neurobiology are primarily psychotherapists and
educators attempting to utilize neuroscientific data to inform and improve our work (Cozolino, 2010; Schore,
1994; Siegel, 2012). Like curious toddlers, we are full of questions, such as

•Which neural networks compose the social brain?

•How is the brain built and rebuilt by relationships?
•How do brains regulate one another during moment-to-moment interactions?
•How do parents, therapists, and educators activate and guide neuroplastic processes?
•What are the effects of isolation, stress, and trauma on the social brain?

Caregiver nurturance sets us on a course of physical and psychological health—or, when it is lacking,
physical and mental illness. Because of the causal link between interpersonal experiences and biological
growth, we are particularly interested in the impact of these early caretaking relationships when the neural
infrastructure of the social brain is forming. We also know that the brain is capable of change at any time and
that social interactions are a primary source of brain regulation, growth, and health. Those of us who study
interpersonal neurobiology believe (and research supports) that friendships, marriage, psychotherapy—in fact,
any meaningful relationship—can reactivate neuroplastic processes and actually alter the structures and
biochemistry of the brain.
In thinking about these processes a multitude of questions arise: How does therapy work? What are
the best ways for parents to help build their baby’s brain? Why do some people seem to have no conscience
whereas others are crippled with shame and guilt? Why do some find cues to abandonment in almost every
human interaction? How does the brain stay healthy and how can we regain mental health after we fall ill?
Parents, educators, and therapists—those of us who should be most concerned with shaping minds—
have traditionally paid little attention to the brain. I have heard therapists say that psychotherapy is an art and
that the brain is irrelevant to their work. I would respond, as with any art, that a thorough knowledge of our
materials and methods can only enhance our skills and capabilities. The brain is a treasure trove of
information about where we have come from, what we are capable of, and why we act as we do. It holds many
secrets about how we can know ourselves better and improve the way we do psychotherapy, teach, and parent
our children.
As a therapist, I am especially interested in how relationships reshape the brain throughout life. Tens
of thousands of hours of interacting with clients have provided me with an intuitive sense of how and why
therapy works. I have watched as my focused attention, consistency, and caring have been taken in like water
at a desert oasis. I have experienced the gradual building of confidence and strength as my presence has been
integrated and used as a source of security, guidance, and emotional safety. I have also experienced how
working with my clients has changed me, inspired me, and helped me to grow. It is the power of being with
others that shapes our brains. Exploring how these insights apply to therapy and everyday life is one of the most
exciting aspects of the work that I do as a therapist, and it is what has inspired me to share my ideas about the

9
brain and the mind with you.

10
The Neuroscience
of
Human Relationships

Second Edition

11
 Part I
The Emergence of Social Neuroscience: An Overview

12
Chapter 1

The Social Brain

The history of the evolution of mammals is the history of the evolution of the family.
—Paul MacLean

A fundamental characteristic of Western philosophy is the conception of the thinker as alone rather than
embedded within a human community. It is a way of understanding the world that leads us to look for
answers to human problems through theories and technology rather than within lived experiences and social
interactions. Grounded in this philosophy, researchers in neurobiology and neuroscience study the brain in
scanners and on dissection tables but neglect the fact that the brain evolved to function within a matrix of
other brains.
The struggle between these paradigms is nowhere more apparent than in psychiatry, with its dual
histories in psychoanalysis and neurology. Reiss expressed this ongoing tension when he said, “Psychiatry has
been forced into the chronically uncomfortable position of straddling biomedicine and the social sciences and
seems always to hunger for relief” (Reiss et al., 1991, p. 290). Although relief is usually gained by choosing
sides between the brain and the mind, either perspective alone is inadequate.
One of the challenges of combining the social and biological sciences lies in the disparity of
perspectives and personalities between the two groups. Scientists are, admittedly, not particularly social
people, and few think of modern physicians as paragons of empathy. A tragic example of this disparity comes
from the recent history of the treatment of children in orphanages. In response to a high number of deaths,
physicians attempted to keep the children safe from infectious diseases by separating them from one another
and ordering that their handling be kept to a minimum. Yet they still died at such alarming rates that
admission forms and death certificates were signed at intake for the sake of efficiency. It was not until the
children were held, rocked, and allowed to interact with one another that their survival rate improved (Blum,
2002).
Scientists have had to expand their thinking to grasp the idea that individual neurons or single human
brains do not exist in nature. Without mutually stimulating interactions, people and neurons wither and die. In
neurons this process is called apoptosis; in humans it is called depression, grief, and suicide. From birth until
death, each of us needs others who seek us out, show interest in discovering who we are, and help us feel safe.
Thus, understanding the brain requires knowledge of the healthy, living brain embedded within a community
of other brains: Relationships are our natural habitat. Because therapists, teachers, and parents intuitively grasp
this profound reality, just as laboratory scientists often do not, we decidedly “nonscience” types who teach
preschool, do psychotherapy, or study group behavior have a great deal to offer neuroscience. We are in a
position to help research scientists know where to look as they explore how the brain grows, learns, and
thrives throughout life.
Viewing the brain as a social organ emerged in neuroscience in the 1970s. The theory that primates
possess neural networks dedicated to social cognition was initially proposed by Kling and Stecklis (1976). In
the process of observing monkey colonies in captivity, they would lesion the brains of certain monkeys and
monitor their social behavior. They found that damage to certain brain structures resulted in aberrations of
social behavior and a decline in group status. There is, however, no one module in the brain dedicated to
social behavior; rather, there are multiple sensory, motor, cognitive, and emotional processing streams that
contribute to the emergence of social intelligence (Karmiloff-Smith et al., 1995).

13
Why Relationships?
Think about meeting a man at a party. Your brain is simultaneously processing his tone of voice, direction of
gaze, body language, hand gestures, and eye movements, as well as the content of what he says. You are
having physical and emotional reactions to him based on gender, appearance, odor, and whom he reminds you
of both consciously and unconsciously. Based on these quick observations, you decide what to say, how to act,
and whether to approach him, ignore him, or move to the opposite end of the room. All of this is but a small
fraction of the information your brain and body are processing during even the most superficial interactions.
When the other is significant for us, as a source of either affection or danger, countless additional evaluative
processes become activated. Those of us who can better predict the intentions and actions of others have an
obvious advantage in terms of safety, competition, and mating. Neural networks dedicated to the evaluation of
others have a long evolutionary history.
But why do we have relationships, maternal instincts, friendships, family, and society? Why not be like
a reptile that digs a hole, lays some eggs, and moves on? The newborns of some species even have to flee from
their parents to avoid being eaten! Wouldn’t life be easier without gossip, grudges, and in-laws? Perhaps not.
Using evolution as an organizing principle, we begin with the assumption that our social brains have emerged
during natural selection because being social enhances survival.
Our best guess is that larger and more complex brains allow for a greater variety of responses in
challenging situations and across diverse environments that enhance the probability of the survival of certain
genes. Our brains allow us to fashion clothing, build climate-controlled houses, and create space stations with
artificial environments that let us expand our habitats and sources of food. So while the existence of genes and
natural selection may explain the why of relationships, we are still left with the question of how relationships
have evolved, function, and impact our lives. Many of the answers to these questions lie ahead in the frontiers
of social neuroscience.
We do know a few things. We know that the expansion of the cortex in primates corresponds with
increasingly larger social groups. There is not only safety in numbers but also the ability for task specialization
such as hunting, gathering, and caretaking. So, whereas many animals need to be born immediately prepared
to take on the challenges of survival, human infants have the luxury of years of total dependency, during which
their brains can grow, adapt, and be shaped by very specific experiences. As the size of primate groups
expanded, the grooming, grunts, and hand gestures adequate in small groups were gradually shaped into
spoken language. As social groups grew even larger, more cortical geography was needed to process
increasingly complicated social information. This coevolution of language and brain allowed for the
development of higher levels of symbolic and abstract functioning—and the emergence of culture. In other
words, relationships are a fundamental and necessary condition for the evolution of the contemporary human
brain.

Survival of the Nurtured

Our first months of life are dedicated to getting to know our mother: her smell, taste, and feel and the look of
her face. We gradually experience her ability to attune to us and soothe our distress as her presence becomes
synonymous with safety. Our mothers and fathers shape our brains from the inside out in a dance of
interacting instincts. For human babies, survival doesn’t depend on how fast they can run, whether they can
climb a tree, or if they can tell the difference between edible and poisonous mushrooms. Rather, they survive
based on the abilities of their caretakers to detect the needs and intentions of those around them. For humans, other
people are our primary environment. If we are successful in relationships, we will have food, shelter,
protection, and children of our own. We get what we need through our interdependence with others.
When I think of Darwin’s survival of the fittest, I picture bodybuilders, alpha male gorillas, or lions
stalking their ultimately doomed prey. These images have little to do with natural selection and everything to
do with a misunderstanding of Darwin’s theory. Fitness in Darwin’s terms is the ability to adapt to the
environment. As environments change, those best suited to it will survive, reproduce, and reflect the new
features of adaptability. But what does it mean to be the “fittest” in our modern society? At the beginning of
the 21st century, we are adapting to information overload, spiraling expectations, and being stuck in traffic.
The freeway is our savanna, the Internet superhighway our Galapagos. Could the fittest in our society actually
be the average citizen, going about his or her daily routine with a solid sense of self, able to successfully
navigate relationships and regulate the stress of sitting through business meetings?
In contemporary society the real challenges are multitasking, balancing the demands of work and

14
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