Abstract

Different types of predator odors engage elements of the hypothalamic predator-responsive circuit, which has been largely investigated in studies using cat odor exposure. Studies using cat odor have led to detailed mapping of the neural sites involved in innate and contextual fear responses. Here, we reviewed three lines of work examining the dynamics of the neural systems that organize innate and learned fear responses to cat odor. In the first section, we explored the neural systems involved in innate fear responses and in the acquisition and expression of fear conditioning to cat odor, with a particular emphasis on the role of the dorsal premammillary nucleus (PMd) and the dorsolateral periaqueductal gray (PAGdl), which are key sites that influence innate fear and contextual conditioning. In the second section, we reviewed how chemical stimulation of the PMd and PAGdl may serve as a useful unconditioned stimulus in an olfactory fear conditioning paradigm; these experiments provide an interesting perspective for the understanding of learned fear to predator odor. Finally, in the third section, we explored the fact that neutral odors that acquire an aversive valence in a shock-paired conditioning paradigm may mimic predator odor and mobilize elements of the hypothalamic predator-responsive circuit.

Highlights

  • Specialty section: This article was submitted to Systems Biology, a section of the journal Frontiers in Neuroscience

  • We reviewed how chemical stimulation of the PMd and PAGdl may serve as a useful unconditioned stimulus in an olfactory fear conditioning paradigm; these experiments provide an interesting perspective for the understanding of learned fear to predator odor

  • Primal responses to predator odors involve a neural system formed by the medial amygdalar nucleus, the medial hypothalamic predator-responsive circuit and the dorsal PAG, and elements of this neural system seem to be critical in supplying instructive signals to corticohippocampal-amygdalar circuits related to fear conditioning to promote fear learning

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Summary

Neural Mediation of Innate Fear Responses to Predator Odor

Predator odors are thought to work as kairomones, which are semiochemicals that are released by one species and have a favorable adaptive effect on a different “receiving” species but no favorable effect on the transmitting species (Dicke and Grostal, 2001; Wyatt, 2014). Locus coeruleus lesions decrease both unconditioned and conditioned fear responses (Neophytou et al, 2001) In line with this view, systemic administration of propranolol (a centrally acting beta-blocker) reduced unconditioned defensive behaviors and PMd Fos expression in response to cat odor (Do Monte et al, 2008). This effect of noradrenergic transmission on fear responses should be, at least in part, mediated by noradrenergic projections from the locus coeruleus to the PMd (Sobrinho and Canteras, 2011; Figure 1), where beta-adrenoceptor blockade before cat odor exposure has been shown to reduce defensive responses to cat odor (Do Monte et al, 2008). The predator-responsive circuit is further modulated by significant noradrenergic input from the locus coeruleus (which likely plays a critical role in the response to predator odors) and projects to the dorsal PAG, which is involved in the expression of innate defensive responses

Neural Mediation of Learned Fear Responses to Predator Odor
Stimulation of the PMd and Dorsal PAG Supports Fear Learning
Concluding Remarks
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