Fear of Predators Suppresses Neurogenesis in the Brains of Wild Songbirds

Abstract

Fear of predation can lead to behavioral changes indicative of an enduring memory of fear, as acknowledged by both ecologists and biomedical scientists studying post-traumatic stress disorder (PTSD). Enduring memories are often linked to suppressed neurogenesis in laboratory rodents as a potential mechanism to prevent the replacement of existing memories. We used predator vocalizations to assess the enduring effects of fear on neurogenesis in a wild songbird, black-capped chickadees (Poecile atricapillus), quantifying cell proliferation (PCNA immunoreactivity), and immature neurons (doublecortin immunoreactivity) in both sexes. Seven days after predator cue exposure, we found suppression of hippocampal cell proliferation in males, with no effect in females, and suppression of immature neurons in the avian amygdala (medial ventral arcopallium) in both sexes. Our results are consistent with the hypothesis that animals retained an enduring memory of fear, with potential sex differences in the behavioral and ecological consequences of these enduring neuronal changes. Finding effects indicative of an enduring memory of fear in wild caught animals supports the notion that there may be evolutionarily adaptive value to retaining an enduring, PTSD-like memory.

Fig. 1

(A) Photomicrograph of a Nissl stained coronal section of chickadee telencephalon. Boxes depict locations where images were taken for DCX quantification within each brain region measured (L: lateral, M: medial, V: ventral). (B) Higher magnification photomicrograph of DCX immunoreactivity in the AMV.

Fig. 2

(A) Photomicrograph of a Nissl stained coronal section of chickadee telencephalon. Boxes depict locations where images were taken for PCNA quantification. (B) Higher magnification photomicrograph of PCNA immunoreactivity taken in the Hp.

Fig. 3

Cell proliferation: The effects of predator induced fear on the PCNA + cell density in the (A) hippocampus (Hp), (B) medial ventral arcopallium (AMV), and (C) the caudolateral nidopallium (NCL). Bars indicate means ± standard error, filled circles indicate individual data. Example photomicrographs of PCNA immunoreactivity in the Hp of a (D) non-predator female, (E) predator female, (F) non-predator male, and (G) predator male.

Fig. 4

Immature neurons: The effects of predator-induced fear on the percent cover of DCX + cells in the (A) hippocampus (Hp), (B) medial ventral arcopallium (AMV), and (C) the caudolateral nidopallium (NCL). Bars indicate means ± standard error, filled circles indicate individual data. Example photomicrographs of DCX immunoreactivity in the AMV of a (D) non-predator female, (E) predator female, (F) non-predator male, and (G) predator male.