Progress 06/16/11 to 12/31/12
Outputs
OUTPUTS: We completed a strong pilot study of crow brain imaging. We completed two basic studies: 1. The first study contrasted the neural response of crows as they recalled pleasant and fearful memories. My previous research found that 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. But the neural basis for how a crow (or for that matter any bird or wild animal) recognized people had not been done. Our approach was to provide the first imaging analysis of an awake, wild animal's brain as it performed an adaptive, complex cognitive task. 2. Our second study expanded these findings to two other situations: the observation of a never before seen person as that person held a dead crow, and the observation of a robotic predator (a taxidermy mounted red-tailed hawk). Here we probed the neurobiology frontier by imaging the whole brains of wild animals to reveal the neural circuits activated by a variety of dangers. While crows scold and mob natural dangers, including predators, dead conspecifics, and threatening people, the brain regions commanding these behaviors are unknown. We again used positron emission tomography to identify differential use of forebrain regions including the amygdala, hippocampus, and the ventrolateral portion of the caudal nidopallium as crows viewed each of these dangerous stimuli. Our findings produced the image of the day for MSNBC and Science Now (http://news.sciencemag.org/sciencenow/2012/09/bird-brains-show-their -fear-of-f.html), were featured on the BBC special "Super Smart Animals," and will be featured in Science in the next few months (writer just left and is working on special article on the new advances in bird cognition). PARTICIPANTS: John Marzluff, Professor, University of Washington School of Environmental and Forest Sciences. Managed the project, co-designed the research, performed the research, analyzed the data, and co-wrote the PNAS article. Donna Cross, Research Assistant Professor, University of Washington School of Medicine, Department of Radiology. Co-designed the research, performed the research, analyzed the data, and co-wrote the PNAS article. Robert Miyaoka, Research Associate Professor, University of Washington School of Medicine, Department of Radiology, performed the research, analyzed the data, and co-wrote the PNAS article. Satoshi Minoshima, Professor and Vice Chair for Research, University of Washington School of Medicine, Department of Radiology, co-designed the research and co-wrote the PNAS article. Jack Delap, graduate student, University of Washington School of Environmental and Forest Sciences. Ila Palmquist, University of Washington undergraduate student, completed her capstone thesis within our project. TARGET AUDIENCES: Target audiences include neuroscientists, wildlife scientists, behavioral scientists, educators, students, and the general public. PROJECT MODIFICATIONS: Not relevant to this project.
Impacts
The outcomes of our two studies: 1. We showed 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 hyper-, nido-, and 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. 2. Our analysis suggests that mobbing behavior is guided by unique neural circuits that are responsive to differences in the mental processes -- learning, memory retrieval, and decision making -- required to appropriately nuance a risky behavior to the variety of natural stimuli evoking it. Importantly we show that the same behavior of a crow may conceal many minds -- those that are fearful, making decisions, and storing memories. Our work has had impact. We supported an undergraduate student (Ila Palmquist) as she completed her capstone thesis within our project. Graduate student Jack Delap was also partially supported by our award. By pioneering a new approach to understanding animal cognition we are opening doors for other researchers. Already a team from Knox College has come to UW to apply our approach to their research and two other groups are planning on the same.
Publications
- Marzluff, J. M., Miyaoka, R., Minoshima, S., and Cross, D. J. 2012. Brain imaging reveals neuronal circuitry underlying the crow's perception of human faces. PNAS 2012 109 (39) 15912-15917; published ahead of print September 10, 2012, doi:10.1073/pnas.1206109109.
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