Variation is the norm

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Chapter 1 endnote 28, from How Emotions are Made: The Secret Life of the Brain by Lisa Feldman Barrett.
Some context is:

What does it mean that four meta-analyses, summarizing hundreds of experiments, revealed no consistent, specific fingerprints in the autonomic nervous system for different emotions? It doesn’t mean that emotions are an illusion, or that bodily responses are random. It means that on different occasions, in different contexts, in different studies, within the same individual and across different individuals, the same emotion category involves different bodily responses. Variation, not uniformity, is the norm.

Variation is the norm in emotional experience. When a person experiences the same emotion in the same situation multiple times (such as experiencing anger when being berated by an experimenter, or when watching a film), she can vary in her physical changes depending on what action she takes. The same emotion can also vary across multiple contexts, such as being angry when berated by an experimenter, bumped in a hallway by a stranger, unfairly evaluated in a stressful interview, and while recalling a frustrating event.

The same is true in non-human animals. For example, when a rat hears a tone that, in the past, was paired with an electric shock, the rat typically freezes, its heart rate goes up, and the conductivity of its skin goes up. These changes are taken as evidence that the animal has learned fear, and mean that the rat is showing an increase in sympathetic nervous system activity combined with a decrease in parasympathetic activity. Yet when animals are restrained in position as they hear the tone (i.e., they need not freeze because their body is held still), their heart rates decrease.[1] This decrease is associated with just the opposite pattern of physiological change: an decrease in sympathetic nervous system activity combined with an increase in parasympathetic activity. Both patterns are evidence that the rat has learned that the tone predicts the shock (i.e., both are evidence of "fear learning"), but the pattern itself depends on the starting physiological state of the rat.

A human can tremble in fear, jump in fear, freeze in fear, scream in fear, gasp in fear, hide in fear, attack in fear, and even laugh in the face of fear. But this in no way implies that some central state of fear exists that is controlling all these behaviors in an attempt to protect the self from harm. When a human freezes as part of an instance of the category “fear,” this in no way implies that his brain state is identical to when he runs in fear.  In fact, there are different neural circuits for different actions, all of which are perceived as fear.[2] 

If you shock a rat and measure the action of running away ("flight"), you cannot validly use that data to understand “fear.” The neural circuitry that supports flight is a part of fear when the animal flees in the face of threat; but when an animal flees during anger, then the neural circuitry that supports flight becomes part of anger in that instance.

Notes on the Notes

  1. Iwata, Jiro, and Joseph E. LeDoux. 1988. "Dissociation of associative and nonassociative concomitants of classical fear conditioning in the freely behaving rat." Behavioral Neuroscience 102 (1): 66-76.    
  2. Gross, Cornelius T., and Newton Sabino Canteras. 2012. "The many paths to fear." Nature Reviews Neuroscience 13 (9): 651-658.