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An eminent fear researcher argues for an about-face in how we conceive of emotions

The Deep History of Ourselves: The Four-Billion-Year Story of How We Got Conscious Brains

Joseph LeDoux
Viking
2019
432 pp.
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Evolution, behavior, brains, consciousness, and emotions are topics of enduring fascination. In The Deep History of Ourselves, Joseph LeDoux embraces all five in earnest. His ambitious endeavor to cover them in an integrated fashion is successful in many respects, but controversial in others.

LeDoux is a renowned neuroscientist and a pioneer in studying fear conditioning and other aspects of what has traditionally been considered emotion-related behavior in rodents. His primary motivation in writing the current book is to articulate and defend a major recent shift—indeed, an about-face—in how he conceives of and uses the term “emotion.”

LeDoux now equates emotions with feelings and stipulates that feelings only exist in creatures having conscious self-awareness (autonoesis). He concludes that although other species might have emotions, we currently can only be sure that they occur in humans. Before delving into this, the other sections of the book warrant discussion.

The book’s first half is devoted to evolutionary “deep history.” It begins with theories on the origin of cellular life (though short shrift is given to the possible role of viruses). A major theme is that “behavior”—defined broadly as interaction with one’s environment—emerged early in evolution.

Single-celled organisms show approach and avoidance behaviors to environmental cues, notes LeDoux, and some unicellular eukaryotes show evidence of learning and memory. More complex behaviors emerged with the appearance of nervous systems.

LeDoux focuses on the emergence of intercellular communication via neuronal action potentials and chemical synaptic transmission. Puzzlingly, he fails to mention that many non-neural epithelial cells have action potentials and are electrically coupled to one another, which may have set the stage for neural signaling.

The second half of the book begins with a discussion of brains, behavior, emotion, and cognition in the broad context of vertebrate evolution. It progresses to considering the anatomical and functional specializations of the human brain. LeDoux is enamored of the idea that the frontal pole is a uniquely specialized region of human cerebral cortex, but his theory is speculative and left this neuroanatomist unconvinced.

LeDoux mentions many published theories of consciousness fleetingly but fairly, then focuses on his favorite: a variant of the “higher-order theory” (HOT) advanced by Hakwan Lau and David Rosenthal that involves both unconscious and conscious representations in working memory interacting with lower-level sensory representations. Here, LeDoux proposes that human consciousness is intimately linked to the aforementioned frontal pole. The hypothesis is intriguing but, again, highly speculative and not well framed in relation to recent human neuroimaging studies.

The book’s final sections return to LeDoux’s controversial theory of emotion. What is an emotion, he asks, and who (or what) has them? Can a dog be thirsty, have a sense of fear, or experience pleasure and, if so, are these properly considered emotions? What about a rat, a frog, or a fly?

Much of the debate surrounding this issue is fundamentally semantic, depending critically on how one defines “emotion.” By equating emotions with feelings that can only be experienced by creatures having autonoetic consciousness, LeDoux positions himself at one extreme of a broad spectrum.

A narrow definition like his comes at a price. LeDoux advocates major terminological shifts, such as using “defensive survival” instead of “fear” when referring to nonhumans. Time will tell whether this gains traction but there are grounds for skepticism.

Strong counterarguments to LeDoux’s perspective have been lucidly articulated by Ralph Adolphs and David Anderson in The Neuroscience of Emotion. In their view, emotions represent fundamentally distinct internal states. The neural circuits that mediate a given emotion vary greatly across species, they argue, but many emotion-related behaviors share core commonalities.

The cognitive correlates of emotional states differ dramatically and include conscious perception in only some species. However, the same can also be said for many other biological processes, including, for example, vision. Yet it is not controversial to assert that countless vertebrate and invertebrate species have a visual system irrespective of the richness of their perceptual capabilities. Why not the same for emotional systems?

Though at times speculative, LeDoux ultimately succeeds in putting behavior, brains, consciousness, and emotions into a broad evolutionary context. One does not need to agree with all of his arguments to appreciate his lucid and engaging synthesis.

About the author

The reviewer is at the Department of Neuroscience, Washington University School of Medicine, St. Louis, MO 63110.