Hoisted from a recent email thread with the estimable Jim Davies:
“You wrote to me once that the brain has two fear channels, cognitive and reactive. Do you have a citation I can look at for an introduction to that idea?”
So I didn’t have a citation off the top of my head, though I do now - LeDoux’s 1998 book The Emotional Brain - but I did remember what I told Jim: that we have two fear channels, one fast, one slow. The fast one is primarily sensory, reactive, and can learn bad associations which are difficult to unlearn, as in PTSD (post-traumatic stress disorder); the slow one is more cognitive, deliberative, and has intellectual fear responses.
It turns out that it ain’t that simple, but I was almost right. Spoiling the lead a bit, there are two conditioned fear channels, the fast “low road” and slow “high road” and they do function more or less as I described: the low road has quick reactions to stimuli, a direct hotline from sensory processing in your thalamus to the amygdala which is a clearinghouse for emotional information; the high road involves the sensory cortex and confirms the quick reaction of the low road. The low road’s implicated in PTSD, though PTSD seems to involve broader areas of brain damage brought on by traumatic events.
Where that needs tweaking is that there’s also a third fear channel, the instructed or cognitive fear channel. This allows us to become scared if we’re told that there’s a tiger behind a door, even if we haven’t seen the fearsome beast. This one relies on an interaction between the hippocampus and the amygdala; if your hippocampus is damaged, you will likely not remember what you’re told, whereas if your amygdala is damaged, you may react appropriately to instruction, but you might not feel the appropriate emotional response to your situation (which could lead you to make poor choices).
So, anyway, that’s the gist. But, in the spirit of Check Your Work, let me show my work from my conversation with Jim.
Ok, I have an answer for you (description based on [Gazzaniga et al 2002], though I found similar information in [Lewis et al 2010]).
There are two fear channels: one involving fast sensory processing and one involving slower perceptual information. Based on the work of LeDoux [1996] these are sometimes called the "low road" (quick and dirty connection of the thalamus to the amygdala, a crude signal that a stimulus resembles a conditioned stimulus) and the "high road" (thalamus to sensory cortex to amygdala, a more refined signal which is more reliable); both of these channels help humans learn implicit conditioned fear responses to stimuli.
This "low road" and "high road" concept was what my understanding of PTSD is based on, that individuals acquire a fast low-road response to stimuli that they cannot readily suppress; I don't have a reference for you, but I've heard it many times (and it's memorably portrayed in Born on the Fourth of July when veterans in a parade react to firecrackers with flinches, and later the protagonist after his experience has the same reaction). A little research seems to indicate that PTSD may actually involve events traumatic enough to damage the amygdala or hippocampus or both, but likely involving other brain areas as well ([Bremner 2006], [Chen et al 2012]).
There's a couple more wrinkles. Even patients with amygdala damage have unconditioned fear responses; conditioned responses seem to involve the amygdala [Phelps et al 1998]. Instructed fear (warning a subject about a loud noise that will follow a flashing light, for example) seems to involve the hippocampus as well, though patients with amygdala damage don't show fear responses even though they may behave appropriately when instructed (e.g., not showing a galvanic skin response even though they flinch [Phelps et al 2001]). This amygdala response can influence storage of emotional memories [Ferry et al 2000]. Furthermore, there's evidence the amygdala is even involved in perceptual processing of emotional expression [Dolan and Morris 2000].
So to sum, the primary reference that I was talking about was the "low road" (fast connection from thalamus to amygdala, implicated in fast conditioned fear responses and PTSD, though PTSD may involve trauma-induced damage to more brain areas) and "high road" (slow reliable connection from thalamus to sensory cortex to amygdala, implicated in conditioned fear responses), but there's also a "sensory" path (conditioned fear response via the thalamus to the amygdala, with or without the sensory cortex involvement) vs "cognitive" path (instructed fear response via the hippocampus, which functions but shows reduced emotional impact in case of amygdala damage).Hope this helps!
Bremner, J. D. (2006). Traumatic stress: effects on the brain. Dialogues in clinical neuroscience, 8(4), 445.
LeDoux, J. (1998). The emotional brain: The mysterious underpinnings of emotional life. Simon and Schuster.
Chen, Y., Fu, K., Feng, C., Tang, L., Zhang, J., Huan, Y., ... & Ma, C. (2012). Different regional gray matter loss in recent onset PTSD and non PTSD after a single prolonged trauma exposure. PLoS One, 7(11), e48298.
Dolan, R. J., & Morris, J. S. (2000). The functional anatomy of innate and acquired fear: Perspectives from neuroimaging. Cognitive neuroscience of emotion, 225-241.
Ferry, B., Roozendaal, B., & McGaugh, J. L. (1999). Basolateral amygdala noradrenergic influences on memory storage are mediated by an interaction between β-and α1-adrenoceptors. The Journal of Neuroscience, 19(12), 5119-5123.
Gazzaniga, M.S., Ivry, R.B., & Mangun, G.R. (2002) Cognitive Neuroscience - The Biology of the Mind (2e) W. W. Norton & Company.
Lewis, M., Haviland-Jones, J. M., & Barrett, L. F. (Eds.). (2010). Handbook of emotions. Guilford Press.-the Centaur
Phelps, E. A., LaBar, K. S., Anderson, A. K., O'connor, K. J., Fulbright, R. K., & Spencer, D. D. (1998). Specifying the contributions of the human amygdala to emotional memory: A case study. Neurocase, 4(6), 527-540.
Phelps, E. A., O'Connor, K. J., Gatenby, J. C., Gore, J. C., Grillon, C., & Davis, M. (2001). Activation of the left amygdala to a cognitive representation of fear. Nature neuroscience, 4(4), 437-441.
Pictured: a few of the books I looked at to answer Jim’s question.