Spotlight on Research: On the Neurobiological Basis of Affiliation

Two things caused a group of psychologists and neuro-scientists to come together recently at Georgetown University in Washington, DC: neurobiology and affiliation. Convened for a New York Academy of Sciences conference, titled The Integrative Neurobiology of Affiliation, the group sought to examine the anatomy and physiology of the complex social interaction called affiliation.

The conference was supported in part by the National Institute of Mental Health, and the proceedings are scheduled to be published by the Academy in December of this year.

Focusing on only a sampling of the 29 total invited presentations, we highlight here the research of two of the five APS member presenters: Stephen W. Porges (University of Maryland-College Park) and David Crews (University of Texas-Austin). The other APS members included on the program of distinguished speakers were: Steven E. Brauth (Univ. of Maryland-College Park), Mary Carlson (Harvard Medical School), and William S. Hall (Univ. of Maryland-College Park).

Evolution‘s Quirky Logical Legacy

Both Porges and Crews study the evolution of the parts of the nervous system, and how those evolving parts function within the context of social behavior. To some degree, mammalian neural structures and functions can be traced to their ancient reptilian origins, and the ancient functional origins of modem behaviors and brain structures can elucidate the rather quirky logic that evolution bestows on neural systems underlying current-day mammalian social behavior.

Crucial to this evolutionary process is “exaptation,” the process whereby an old structure is recruited to perform a new function. To put it another way, an old part of the nervous system is coopted for use in a new function, and the modern structure and function bear the stamp of both the logic of the ancient function it evolved from and the logic of the new function it now performs. While some aspects of the old function may be present, it is far from obvious in advance what part will be conserved and what aspect will be changed. Lest you think that behavior linked to the basic biological functions must remain boringly affixed to the system it first evolved to serve, here are two tales of exaptation.

Emotions and the Vagal Nerve Theory

Psychological study of the emotions can be a puzzling business. It often seems that all emotions are characterized as activations of the sympathetic nervous system, and the specific emotions are differentiated from each other on the basis of their cognitive components.

Stephen Porges has developed the “polyvagal theory of the emotions,” a new way of looking at our feelings. Porges’s theory, elaborately detailed in the April 30 issue of the New York Times, resurrects the role of the parasympathetic nervous system and analyzes its multiple functions in light of evolutionary changes. His contribution to the symposium, “Emotion: An Evolutionary By-Product of the Neural Regulation of the Autonomic Nervous System” could provide a way to put more “guts” into emotion research. Rather than concentrating on the sympathetic nervous system, which releases adrenaline in response to stress and activates the “fight-or-flight” response, Porges emphasizes the other half of the autonomic nervous system- the parasympathetic system-which basically mediates immobilization, and the conservation of metabolic energy.

Scared to Death

The single most important nerve in this system is the vagus nerve, or tenth cranial nerve. When strongly activated, the vagus nerve slows heart rate, slows or stops respiration (depending on species), and causes the digestive tract to empty. These are the hallmarks of complete terror, which essentially causes homeostatic systems to shut down. If severe enough, this response causes one to literally die of fright.

How can this make evolutionary sense? This extreme response is, for humans and for all warm-blooded animals, a vestigial remnant of an ancient response that serves the cold-blooded vertebrates quite well: When all else fails, a reptile can “play dead” for a few minutes, during which time the danger just might go away. However, once mammals became warm-blooded, they lost the ability to survive oxygen deprivation for more than a few seconds.

So what happened to the vagal system for shutting down homeostatic systems to facilitate “playing dead”? Part of it survives as this vestigial system that has the power to cause death from fright, but the rest of it became modified into our complex system of control over our organs of emotional expression- the facial muscles and the larynx, for example-and into a finely adjustable ”brake” that allows us to rapidly adjust our metabolic output, for example to rapidly switch from speaking to listening. without involving the sympathetic nervous system at all. In short, an old system for regulating one of the most basic needs (i.e., oxygen intake) has been exapted to enable us to get what we need from other individuals (e.g., by smiling, frowning, talking), and in the process has created a whole new universe of physiological responses. The graded interplay of the ancient vagal “play dead” response, the sympathetic “fight or flight” activation pathway, and the newest vagal modulatory pathways, plus the visceral afferents by which we sense our bodies’ responses, combine to create the emotional component of our experience.

Neurogenic Evidence

A crucial piece of physical evidence Porges advances to support this interpretation is that the muscles and nerves involved in the expression of complex emotions (i.e., the facial and laryngeal muscles and the nerves that control them) all develop from the branchial arches of the embryo. These are the structures that become gills in fish, the structures originally dedicated to the regulation of oxygen supply. Known as the “vagabond” of the cranial nerves because of its wide, wandering path of innervation throughout the body, the vagal nerve appears to suffer from an ever-wandering function, as well!

On Pseudo-Sex, Lizards, and Evolution

The evolution of behavior must usually be inferred, rather than observed, because ancestral species are usually extinct, but David Crews finds among whiptail lizards a unique opportunity for the study of the evolution of sexual behavior; an ancestor and a descendant species live side by side, and can be directly compared. In this case, the descendants are parthenogenic (i.e., all the individuals are females), and they reproduce without sperm.

The loss of sexual reproduction in these animals must be relatively recent, because the immediate ancestor species (confirmed by genetic analysis) has both males and females and reproduces in the usual way. Although the parthenogenic lizards can reproduce without any sexual behavior if housed in isolation, they nortnally “go through the motions,” alternating between male-like bebavior (mounting) and female-like behavior (being mounted). In the bisexual species, male sexual behavior is stimulated by testosterone, acting on the anterior hypothalamus-preoptic area (AHPOA), and the AHPOA is larger in males than in females.

One might expect that this same brain nucleus, which is involved in the pseudo-male behavior of the parthenogenic lizards, would be enlarged since the pseudo-copulatory behaviors very closely resemble male behavior in the bisexual species. But it is not, and the sexual behaviors are not stimulated by androgen. Instead, progesterone has been coopted to playa role in initiation of male-like behaviors, and the AHPOA remains small and inactive, regardless of which pseudo-sexual phase the individual is going through. What’s more, the typically “female” part of the hypothalamus, the ventromedial hypothalamus, is as well-developed in these animals as it is in the females of the ancestral species.

How did this behavior and its hormonal trigger evolve? Individual males of the ancestral bisexual species vary in their response to progesterone; some show typical courtship behavior in response to progesterone just as they do to testosterone. This preexisting variation in hormone response was therefore probably present in the individuals that gave rise to the new species and was incorporated as an essential part of its behavioral repertoire.

It may seem unexceptional to say, as did many participants at this conference, that behavior can be at the leading edge of evolutionary change. Perhaps what is most surprising is to uncover the ways in which complex behaviors have been cobbled together form bits and pieces of the most basic biology. To order the full proceedings of the conference, contact the New York Academy of Sciences toll-free (800-843-6927 ext. 341).

Observer Vol.9, No.5 September, 1996

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