Abstract
Fear is defined as a fundamental emotion promptly arising in the context of threat and when danger is perceived. Fear can be innate or learned. Examples of innate fear include fears that are triggered by predators, pain, heights, rapidly approaching objects, and ancestral threats such as snakes and spiders. Animals and humans detect and respond more rapidly to threatening stimuli than to nonthreatening stimuli in the natural world. The threatening stimuli for most animals are predators, and most predators are themselves prey to other animals. Predatory avoidance is of crucial importance for survival of animals. Although humans are rarely affected by predators, we are constantly challenged by social threats such as a fearful or angry facial expression. This chapter will summarize the current knowledge on brain circuits processing innate fear responses to visual stimuli derived from studies conducted in mice and humans.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Abbas SY, Hamade KC, Yang EJ, Nawy S, Smith RG, Pettit DL (2013) Directional summation in non-direction selective retinal ganglion cells. PLoS Comput Biol 9:e1002969
Ball W, Tronick E (1971) Infant responses to impending collision: optical and real. Science 171:818–820
Barrett LF, Bar M (2009) See it with feeling: affective predictions during object perception. Philos Trans R Soc Lond Ser B Biol Sci 364:1325–1334
Caterina B, Mattia P, Davide B, Elisabetta L (2018) Pulvinar lesions disrupt fear-related implicit visual processing in Hemianopic patients. Front Psychol 9:2329
Dean P, Mitchell IJ, Redgrave P (1988) Responses resembling defensive behaviour produced by microinjection of glutamate into superior colliculus of rats. Neuroscience 24:501–510
Dean P, Redgrave P, Westby GW (1989) Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 12:137–147
Evans DA, Stempel AV, Vale R, Ruehle S, Lefler Y, Branco T (2018) A synaptic threshold mechanism for computing escape decisions. Nature 558:590–594
Garvert MM, Friston KJ, Dolan RJ, Garrido MI (2014) Subcortical amygdala pathways enable rapid face processing. NeuroImage 102(Pt 2):309–316
Hartline HK (1938) The response of single optic nerve fibers of the vertebrate eye to illumination of the retina. Am J Phys 121:400–415
Huang L, Yuan T, Tan M, Xi Y, Hu Y, Tao Q et al (2017) A retinoraphe projection regulates serotonergic activity and looming-evoked defensive behaviour. Nat Commun 8:14908
Keay KA, Redgrave P, Dean P (1988) Cardiovascular and respiratory changes elicited by stimulation of rat superior colliculus. Brain Res Bull 20:13–26
King SM, Dykeman C, Redgrave P, Dean P (1992) Use of a distracting task to obtain defensive head movements to looming visual stimuli by human adults in a laboratory setting. Perception 21:245–259
Koller K, Rafal RD, Platt A, Mitchell ND (2018) Orienting toward threat: contributions of a subcortical pathway transmitting retinal afferents to the amygdala via the superior colliculus and pulvinar. Neuropsychologia 128:78–86
Kveraga K, Boshyan J, Bar M (2007) Magnocellular projections as the trigger of top-down facilitation in recognition. J Neurosci 27:13232
Li L, Feng X, Zhou Z, Zhang H, Shi Q, Lei Z et al (2018) Stress accelerates defensive responses to looming in mice and involves a locus coeruleus-superior colliculus projection. Curr Biol 28:859–871
LoBue V, DeLoache JS (2010) Superior detection of threat-relevant stimuli in infancy. Dev Sci 13:221–228
McFadyen J, Mermillod M, Mattingley JB, Halász V, Garrido MI (2017) A rapid subcortical amygdala route for faces irrespective of spatial frequency and emotion. J Neurosci 37:3864–3874
McFadyen J, Mattingley JB, Garrido MI (2019) An afferent white matter pathway from the pulvinar to the amygdala facilitates fear recognition. elife 8:e40766
Mendez-Bertolo C, Moratti S, Toledano R, Lopez-Sosa F, Martinez-Alvarez R, Mah YH et al (2016) A fast pathway for fear in human amygdala. Nat Neurosci 19:1041–1049
Mogg K, Bradley B (2010) Orienting of attention to threatening facial expressions presented under conditions of restricted awareness. Cognit Emot 13:713–740
Morris J, Dolan R (2001) The amygdala and unconscious fear processing. In: De Gelder B, de Haan E, Heywood CA (eds) Out of mind: varieties of unconscious processes. Oxford Univ. Press, New York, pp 186–204
Morris JS, O¨ hman A, Dolan RJ (1999) A subcortical pathway to the right amygdala mediating bunseenQ fear. Proc Natl Acad Sci U S A 96:1680–1685
Münch TA, da Silveira RA, Siegert S, Viney TJ, Awatramani GB, Roska B (2009) Approach sensitivity in the retina processed by a multifunctional neural circuit. Nat Neurosci 12(10):1308–1316
Pegna AJ, Khateb A, Lazeyras F, Seghier ML (2005) Discriminating emotional faces without primary visual cortices involves the right amygdala. Nat Neurosci 8:24–25
Rafal RD, Koller K, Bultitude JH, Mullins P, Ward R, Mitchell AS et al (2015) Connectivity between the superior colliculus and the amygdala in humans and macaque monkeys: virtual dissection with probabilistic DTI tractography. J Neurophysiol 114:1947–1962
Rakison DH, Derringer J (2008) Do infants possess an evolved spider-detection mechanism? Cognition 107:381–393
Rudrauf D, David O, Lachaux JP, Kovach CK, Martinerie J, Renault B et al (2008) Rapid interactions between the ventral visual stream and emotion-related structures rely on a two-pathway architecture. J Neurosci 28:2793–2803
Sahibzada N, Dean P, Redgrave P (1986) Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats. J Neurosci 6:723–733
Salay LD, Ishiko N, Huberman AD (2018) A midline thalamic circuit determines reactions to visual threat. Nature 557(7704):183–189
Schenberg LC, Costa MB, Borges PC, Castro MF (1990) Logistic analysis of the defense reaction induced by electrical stimulation of the rat mesencephalic tectum. Neurosci Biobehav Rev 14:473–479
Shang C, Liu Z, Chen Z, Shi Y, Wang Q, Liu S et al (2015) BRAIN CIRCUITS. A parvalbumin-positive excitatory visual pathway to trigger fear responses in mice. Science 348(6242):1472–1477
Shang C, Chen Z, Liu A, Li Y, Zhang J, Qu B et al (2018) Divergent midbrain circuits orchestrate escape and freezing responses to looming stimuli in mice. Nat Commun 9:1232
Tamietto M, Castelli L, Vighetti S, Perozzo P, Geminiani G, Weiskrantz L et al (2009) Unseen facial and bodily expressions trigger fast emotional reactions. Proc Natl Acad Sci USA 106:17661–17666
Tamietto M, Pullens P, de Gelder B, Weiskrantz L, Goebel R (2012) Subcortical connections to human amygdala and changes following destruction of the visual cortex. Curr Biol 22:1449–1455
Vuilleumier P, Pourtois G (2007) Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 45:174–194
Vuilleumier P, Armony JL, Driver J, Dolan RJ (2003) Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat Neurosci 6:624–631
Ward R, Calder AJ, Parker M, Arend I (2007) Emotion recognition following human pulvinar damage. Neuropsychologia 45:1973–1978
Wei P, Liu N, Zhang Z, Liu X, Tang Y, He X et al (2015) Processing of visually evoked innate fear by a non-canonical thalamic pathway. Nat Commun 6:6756
Whalen PJ, Rauch SL, Etcoff NL, McInerney SC, Lee MB, Jenike MA (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 18:411–418
Yilmaz M, Meister M (2013) Rapid innate defensive responses of mice to looming visual stimuli. Curr Biol 23:2011–2015
Zhou Z, Liu X, Chen S, Zhang Z, Liu Y, Montardy Q et al (2019) A VTA GABAergic neural circuit mediates visually evoked innate defensive responses. Neuron 103:473–488.e6
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Ren, C., Tao, Q. (2020). Neural Circuits Underlying Innate Fear. In: Wang, H. (eds) Neural Circuits of Innate Behaviors. Advances in Experimental Medicine and Biology, vol 1284. Springer, Singapore. https://doi.org/10.1007/978-981-15-7086-5_1
Download citation
DOI: https://doi.org/10.1007/978-981-15-7086-5_1
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-15-7085-8
Online ISBN: 978-981-15-7086-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)