Brain imaging reveals neuronal circuitry underlying the crow's perception of human faces

Abstract

Crows pay close attention to people and can remember specific faces for several years after a single encounter. In mammals, including humans, faces are evaluated by an integrated neural system involving the sensory cortex, limbic system, and striatum. Here we test the hypothesis that birds use a similar system by providing an imaging analysis of an awake, wild animal's brain as it performs an adaptive, complex cognitive task. We show that in vivo imaging of crow brain activity during exposure to familiar human faces previously associated with either capture (threatening) or caretaking (caring) activated several brain regions that allow birds to discriminate, associate, and remember visual stimuli, including the rostral hyperpallium, nidopallium, mesopallium, and lateral striatum. Perception of threatening faces activated circuitry including amygdalar, thalamic, and brainstem regions, known in humans and other vertebrates to be related to emotion, motivation, and conditioned fear learning. In contrast, perception of caring faces activated motivation and striatal regions. In our experiments and in nature, when perceiving a threatening face, crows froze and fixed their gaze (decreased blink rate), which was associated with activation of brain regions known in birds to regulate perception, attention, fear, and escape behavior. These findings indicate that, similar to humans, crows use sophisticated visual sensory systems to recognize faces and modulate behavioral responses by integrating visual information with expectation and emotion. Our approach has wide applicability and potential to improve our understanding of the neural basis for animal behavior.

Fig. 1.

Experimental protocol. Different rubber masks, molded from actual people, were used to create threatening and caring faces that single crows responded to during stimulation. During i.p. injection and induction, crow’s faces were covered to prevent them from glimpsing humans.

Fig. 2.

Exemplar of FDG uptake by a crow. (Upper) In this nonquantitative depiction, the FDG-PET brain image has been contrast-enhanced to highlight the fact that the visual network is activated during stimulation following the injection of FDG. (Lower) A similar regional distribution of tracer was not observed in the crow brain that was under anesthesia during the uptake period.

Fig. 3.

Differences in brain activation patterns of crows shown familiar human faces vs. no human face. (A) The activation pattern of crows viewing a familiar face (either threatening or caring; n = 9) compared with a group shown an empty room (n = 3) indicated as voxel-wise subtractions converted to group-wise z-scores that have been superimposed onto the MRI template for better anatomical localization. Coronal slices (from anterior to posterior; coordinates refer to Japanese jungle crow atlas; ref. 31) illustrate peak activations (voxels with Z > 1.64 are colored; those with Z > 3.8 are considered significant with associated structures as indicated). (B) Individual values for normalized (global) uptake in each structure that met the threshold for statistical significance on z-score voxel-wise mapping. Horizontal lines indicate group mean. Z values indicated are from peaks in voxel-wise mapping, and P values were derived from one-tailed t tests of volumes of interest (VOIs) centered on peak activation coordinates. Activated structures: N/M: nidopallium/mesopallium, 12.2% increased, Z = 4.25, P = 0.0000142; LSt: lateral striatum, 8.1% increased, Z = 3.99, P = 0.000044; H: hyperpallium, 11.6% increased, Z = 3.80, P = 0.000091.

Fig. 4.

Brain activation patterns from crows shown human faces that have previously threatened or cared for them. (A) As in Fig. 3, voxel-wise subtractions converted to z-score maps are superimposed to a structural MRI template of the crow brain for better anatomical localization. (Top) The activation pattern of crows viewing a threatening face (n = 5) compared with a group shown an empty room (n = 3). (Middle) The activation pattern of crows shown a caring face (n = 4) compared with the empty room group. (Bottom) Voxel-wise direct comparison of the group shown a threatening face with those shown the caring face (the areas activated by threatening and not caring faces are indicated). Coronal slices (from anterior to posterior; coordinates refer to Japanese jungle crow atlas; ref. 31) illustrate peak activations in one or more group subtractions (voxels with Z > 1.64 are colored; those with Z > 3.8 are considered significant with associated structures as indicated). (B–D) Individual values for normalized (global) uptake in each structure that met the threshold for statistical significance on z-score voxel-wise mapping. Horizontal lines indicate group mean. Z values indicated are from peaks in voxel-wise mapping, and P values were derived from one-tailed t test of VOIs centered on peak activation coordinates. (B) Activated structures for threatening face vs. empty room. A/TnA: arcopallium/nucleus taeniae of the amygdala, 11% increased, Z = 4.42, P = 0.00000425; BS: brainstem nuclei surrounding tractus occipitomesencephalicus including nucleus isthmo-opticus, locus coeruleus, and substantia grisea centralis, 5.9% increased, Z = 4.26, P = 0.0000084; N/M: nidopallium/mesopallium, 12.9% increased, Z = 4.14, P = 0.000020; N: nidopallium, 10.6% increased, Z = 3.93, P = 0.000052. (C) Activated structures for caring face vs. empty room. POA: preoptic area, 7.6% increased, Z = 3.99, P = 0.000011; MSt: medial striatum, 5.9% increased Z = 3.94, P = 0.000052; M: mesopallium, 5.9% increased, Z = 3.87, P = 0.000091; H: hyperpallium, 8.3% increased, Z = 3.81, P = 0.000055. (D) Activated structures for threatening face vs. caring face. THL: dorsal thalamus including dorsolateralis posterior thalami, 11.6% increased, Z = 4.18, P = 0.000019; TnA: nucleus taeniae of the amygdala, 6.5% increased, Z = 4.02, P = 0.000033; Cb: cerebellum, 12.9% increased, Z = 3.99, P = 0.000043.

Fig. 5.

Brain activation patterns associated with individual blinking behavior. (A) Voxel-wise linear regression with blink rates in crows shown a familiar face (threatening + neutral; n = 9; recorded during experiments) where the derived correlation coefficients were converted to z-score maps and superimposed to a structural MRI template of the crow brain for better anatomical localization. (Upper) Regions that were correlated positively with blink rates. (Lower) Regions where increased activation was associated with decreased blinking. Coronal slices (from anterior to posterior; coordinates refer to Japanese jungle crow atlas; ref. 31) illustrate peak activation in linear regression (voxels with Z > 1.64 are colored; those with Z > 3.8 are considered significant with associated structures as indicated). (B) Reduced blinking in nature by crows viewing threatening people (social, 19 crows averaged 29 blinks per min, SE = 2.0, while foraging with conspecifics; scold, 11 others averaged 16 blinks per min, SE = 1.1, as they scolded a threatening person; caught, 11 crows averaged 19 blinks per min, SE = 3.6, as we held them during capture; Kruskal–Wallis H₍₂₎ = 17.2, P < 0.001). (C) Positive relationships between significant peak activation and blinking. Blinking rates were greatest for birds viewing the caring face (circles). All r > 0.93, P < 0.0001). (D) Negative relationship between significant peak activation and blinking. Blinking rates were least among crows viewing the threatening face (squares ). All r = −0.96, P < 0.00001. H, hyperpallium; LSt, lateral striatum; BS, brainstem nuclei surrounding tractus occipitomesencephalicus, including locus coeruleus.