Brain activity underlying American crow processing of encounters with dead conspecifics

Abstract

Animals utilize a variety of auditory and visual cues to navigate the landscape of fear. For some species, including corvids, dead conspecifics appear to act as one such visual cue of danger, and prompt alarm calling by attending conspecifics. Which brain regions mediate responses to dead conspecifics, and how this compares to other threats, has so far only been speculative. Using 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) we contrast the metabolic response to visual and auditory cues associated with a dead conspecific among five a priori selected regions in the American crow (Corvus brachyrhynchos) brain: the hippocampus, nidopallium caudolaterale, striatum, amygdala, and the septum. Using a repeated-measures, fully balanced approach, we exposed crows to four stimuli: a dead conspecific, a dead song sparrow (Melospiza melodia), conspecific alarm calls given in response to a dead crow, and conspecific food begging calls. We find that in response to observations of a dead crow, crows show significant activity in areas associated with higher-order decision-making (NCL), but not in areas associated with social behaviors or fear learning. We do not find strong differences in activation between hearing alarm calls and food begging calls; both activate the NCL. Lastly, repeated exposures to negative stimuli had a marginal effect on later increasing the subjects' brain activity in response to control stimuli, suggesting that crows might quickly learn from negative experiences.

Keywords: American crow; Comparative thanatology; Dead conspecific; Functional neuroimaging; [F-18]fluorodeoxyglucose–PET imaging.

Figure 1.

Regions of interest. Left image is a structural Magnetic Resonance Image (MRI) of the crow brain. Center and right images are co-registered Positron Emission Tomography (PET) images from two subjects in the current study. Red circles indicate a priori regions of interest: Hp=Hippocampus, NCL= Nidopallium caudolaterale, St=Striatum, TnA=Nucleus taeniae of amygdala, S=Septum.

Figure 2.

Experimental stimuli. All subjects were exposed to four stimuli: A) an unfamiliar dead crow, B) an unfamiliar dead song sparrow, and C) a speaker playing one of two conspecific vocalizations including alarm calls given in response to a dead crow and food begging calls. The spectrograph shows differences in call structure between alarm calls (top) and food begging calls (bottom).

Figure 3.

Effect of number of previous exposures to dangerous stimuli (either dead crow, alarm calls, or both) on brain activity (FDG uptake) in the left amygdala during experiences with visual stimuli.

Figure 4.

Effect of number of previous exposures to dangerous stimuli (either dead crow, alarm calls, or both) on regional brain activity (FDG uptake) in the left amygdala during experiences with auditory stimuli.

Figure 5.

Individual values for FDG uptake normalized to global values in each structure and corresponding hemisphere where activation in response to the stimulus (i.e., dead crow in the case of dead crow vs. dead sparrow or dead sparrow in the case of dead sparrow vs. empty room) met the threshold for statistical significance (P<0.05). Horizontal lines indicate group mean. Individual data points represent uptake values for each subject (N=7 Dead crow, N=7 Dead sparrow, and N=3 Empty Room subjects). In all cases, Dead Crow was significantly higher than the control stimuli shown (Dead Sparrow and/or Empty Room). In one case (right NCL) Dead Sparrow was not significantly different from Empty Room subjects.

Figure 6.

Individual values for FDG uptake normalized to global values in the right NCL where activation in response to the stimulus met the threshold for statistical significance (P<0.05). Horizontal lines indicate group mean. Individual data points represent uptake values for each subject (N=7 Begging, N=7 Alarm calling, and N=3 Empty room subjects). Begging and Alarm calling showed higher activation relative to the empty room, but not each other.