Part Of: Affective Neuroscience sequence
Content Summary: 1800 words, 18 min read.

Homeothermy and the Vagal Brake

Mammals saw the emergence of homeothermy (being “warm-blooded”). Homeothermy initially evolved to allow mammals to capitalize on cave ecosystems. But after the dinosaur extinction, this mammalian technology rapidly spread to other ecosystems.

When idling, the average mammal requires four to five times more fuel than an idling reptile of the same size. If reptiles represent vehicles with 1-L engines, then mammals are vehicles with 5-L engines. Reptiles move with a reliable but underpowered engine, and mammals locomote with a supercharged engine that can function for only short periods of time without refueling.

Recall the autonomic nervous system contains two systems:

1. Sympathetic nervous system (SNS, “fight or flight”): responsible for metabolic expenditure and emergent responses.
2. Parasympathetic nervous system (PNS, “rest and digest”): responsible for bodily restoration and digestive processes.

Being underpowered, the reptile can use the full horsepower of his heart indefinitely. There is a stop-go tradeoff between the the PNS and SNS, respectively. In contrast, mammals cannot use their full horsepower indefinitely, without risking cardiovascular catastrophe (i.e., chronic stress). Mammals require a third option besides stop/go. Mammals need controlled activation by default. Mammals need a vagal brake on the heart.

The Polyvagal Theory

Porges’ theory was initially inspired by the vagal paradox:

• Increased vagal tone (high PNS activity) produces bradycardia (dangerous slowing of the heart)
• Decreased vagal tone (low PNS activity) suppresses suppressing respiratory sinus arrhythmia (RSA)
• Bradycardia occurs during periods of suppressed RSA.

It seems like no matter whether vagal tone is high or low, the PNS will cause bradycardia. How can that be? Porges’ solution is the polyvagal theory: there are two branches within the vagus nerve.

• The old vagus is the body’s response to life threat: it feigns death, and produces behavioral shutdown. It is implemented in the unmyelinated section of the vagus, and controlled by dorsal motor nucleus of the vagus (DVC). The old vagus promotes bradycardia.
• The new vagus is the body’s default mode, which activates when the organism feels safe. It is implemented in the myelinated (more efficient) section of the vagus and is controlled by the nucleus ambiguus (NA). The new vagus promotes protective factor RSA.

Evolution of the New Vagus

This new vagus would nicely serve the mammalian need for a vagal brake. But is there evidence that it is mammalian?

Yes. Comparing anatomical structure across species reveals a gradual accretion of structures which participate in mobilization vs restoration.

• Jawless fish don’t have an autonomic nervous system at all; they merely possess excitatory chromaffin tissue (CHM).
• Cartilaginous fish add the ability to inhibit the heart with the dorsal vagal complex (DVC)
• Bony fish and amphibians  see the invention of the sympathetic nervous system (SNS).
• Reptiles also introduce the adrenal medulla (ADm), part of the HPA axis i.e., the stress response.
• Finally, mammals feature all of these systems, but also are unique in possessing the ventral vagal complex (VVC), including the nucleus ambiguus and its myelinated vagal fibers.

We can observe this consecutive series of innovations on the phylogenetic tree of life, to get a sense for the timetable.

The Social Engagement Network

In virtue of homeothermy, mammals need a vagal brake. The new vagus applies the brake when the organism feels safe, and removes it (mobilizes) when safety is threatened.

In virtue of breastfeeding, mammalian infants are enormously dependent on their mothers for survival. Safety became correlated with social relationships. If the mother-child bond is functioning well, the baby will feel safe & thereby use the new vagus. If the baby detects social distance (e.g., the mother is out of sight), this will trigger behavioral fight-or flight (e.g., a panicked cry).

What sort of social behaviors does the new vagus promote? Stimulating the controller of the new vagus, the nucleus ambiguus, promotes the following behaviors:

• Make eye contact
• Vocalize with inflection and rhythm.
• Display contingent facial expressions
• Modulate the middle-ear muscles to distinguish the human voice from background sounds more efficiently.

When the new vagus is deactivated, which occurs spontaneously in response to neuroception of (internal or external) danger, the following occur:

• The eyelids droop
• The voice loses inflection
• Positive facial expressions dwindle
• Awareness of the sound of the human voice becomes less acute
• Sensitivity to others’ social engagement behaviors decreases.

In our article on the Social Behavior Network, we looked at six subcortical structures that give rise to parental care aggression, and lust. This ancient network is conserved across all vertebrates. The polyvagal theory posits the existence of a Social Engagement Network, built on top of the new vagus. From the above list of symptoms, this network seems to promote three distinct functions:

1. The construction of meaningful social relationships among conspecifics, and connects the status of such relationships to one’s overall sense of safety. This is the basis of social attention and relational attachment.
2. Emotional content to be displayed on one’s face, and thereby provide a reliable signal into the limbic state of an organism. This is the basis of empathy and commitment signaling.
3. The advent of new communication systems, which typically used higher frequency bands outside the range of competing reptiles. Mammals did not possess language of course; but this system was used to find mates, to soothe, and to sound the alarm. It is the basis of prosody in the human voice.

Jacksonian Dissolution

One of the most important things a brain can track is safety: how safe is my body at the moment?  Let neuroception refer to the module that computes safety in one’s current situation. The neuroceptive module must respond to both cognitive information (e.g., nearby predator) and visceral data (e.g., fighting infection).

Neuroception explains why a baby coos at a familiar caregiver but cries at the approach of a stranger, or why a toddler enjoys a parents gentle embrace but interprets the same gesture from a stranger as an assault. 

A neuroception of safety is necessary before social engagement behaviors can occur. Neuroception thus provides a basis for Maslow’s old hierarchy of needs. As long as the organism feels safe, the new vagus (incl. the social engagement network) is active. But if the organism detects a threat (real or imagined), it transitions to the sympathetic nervous system. If that fails, and the organism faces a life threat, then it reverts to the immobilization system of the old vagus. In the below image, the mouse isn’t dead: it is subject to the old vagus reflex to freeze: losing muscle tone, reduced heart rate, and reduced pain sensitivity.

The principle of Jacksonian dissolution is the principle that new adaptations come first, older systems are deployed if they fail. On this view, the three autonomic systems form a phylogenetically ordered hierarchy of responses. It explains the phenomenology of feeling overwhelmed, of depression, and of dissociation.

On this view, many of the psychosocial ailments that plague our species can be ameliorated by interventions that target the new vagus. These include

1. The new vagus is promoted by exhalation; the SNS by inhalation. This is why yoga and meditation focus on breathing in such detail: it is a simple physiological trick to combat stress and promote calmness.
2. The new vagus communication system is thought to be the basis of music therapy. Music is designed to be in the same frequency range as the human voice (from middle C to two octaves above). We tend to find lower frequencies threatening, and higher frequencies tend to provoke anxiety.  

My Take

Porges brings a useful perspective to the table. But the scope of his research is frustratingly limited. A metaphor may motivate this complaint: the brain is a vehicle, with many interlocking subsystems contributing to overall driving performance. Porges only pays attention to the wheels (the autonomic nervous system). He is correct in saying that other major theories of cars ignore the wheels (he explicitly faults Panksepp’s Affective Neuroscience for discounting the periphery). But if Porges focuses on the wheels and Panksepp focuses on the engine, there is no one working to illustrate how these two systems interact.

Before Porges, the autonomic nervous system was described in the language of paired antagonism: the SNS turns behavior on, the PNS turns it off. Porges’ instead conceives the ANS a tiered, phylogenetically ordered response hierarchy. And this is a meaningful advance. There are three categories of tires, not two.

But Porges’ “taxonomy of tires” tries to explain too much. A host of psychiatric disorders (autism, social anxiety, post-traumatic stress disorder, borderline personality disorder, and more) are explained by anomalies in RSA (and thus, dysfunction in the social engagement system). He is probably right in linking the new vagus to this disorders. But a single system cannot explain the incredibly diverse set of symptoms represented by these disorders.

How might we explain the diversity of these phenomena? Two methods suggest themselves:

1. The syndromes share the same ANS signature, but different neural mechanisms (same tire, different engine).
2. The syndromes have subtly different expressions in ANS signature (same category of tire, different specific implementation).

Porges spends a lot of time reiterating his theory of a response hierarchy. I wish he spent more time exploring autonomic biology in more detail (the second method above). Which particular subsystems of the old vagus produce immobilization? How do they differ from those that simply regulate homeostasis? What are the different functions served by different tracts, and/or different neurotransmitter chemistries? What does the ANS interact with the immune system?

The polyvagal theory does gesture in how each autonomic system might serve as the basis for primary emotions (a unified theory of cars). These include the obvious (fear is implemented in the SNS!). But there are more interesting assertions, such as,

1. Rough-and-tumble play is a hack where the organism feels safe, but mobilizes resources for behavior (approach motivation and safety).
2. Social tranquility is a hack of the immobilization system (immobilized fear becomes immobilized love). This is a putative explanation for breastfeeding and certain sexual behaviors, and is thought to be mediated by oxytocin.
3. Social protection behaviors are thought to mobilize resources through vasopressin.

While this is a good start, a Unified Theory of Emotions must link the neural substrate of reactive anger (a whole neural network, including e.g., the medial amygdala) to the neural substrate of the mobilization system (the lateral hypothalamus). We need an account of how cars work, not just tires and engines.

Until next time.

Related Resources

• Panksepp (1998). Affective Neuroscience
• Panksepp & Biven (2012). Archaeology of Mind: Neuroevolutionary Origins of Human Emotions
• Porges (2011). The Polyvagal Theory: Neurophysiological Foundations of Emotions, Attachment, Communication, and Self-regulation