Bird Brains? Transitive inference Episodic memory Object constancy (follow disappeared object) Tool manufacture Social learning Theory of mind (Nihei and Higuchi 2001)

Courtesy of Alex Weir, Oxford

How in the World do They do it?? Brain power Sociality Longevity

How in the World do They do it?? Brain power Sociality Longevity New Caledonia Crow

The Cost of Brainpower

Complex Tool Use (Nihei and Higuchi 2001)

Insight

Play

Delinquency?

Warfare?

Compassion?

Sometimes the body is surrounded by sticks (courtesy of Jeff Stephenson, Denver Museum of Nature and Science)

Threatening Face Amygdala Hippocampus New Face Holding Dead Crow

What About Gifting? Gary Clark, 2006, Marysville, WA

Hypotheses: 1.Crows understand the spoken and written word 2.Someone pulled Gary’s chain 3.Gary pulled my chain 4.The crow was trained / imprinted 5.Gifting is a mistake 6.Gifting is adaptive

Is Gifting Adaptive? Gifting would be an effective strategy for a noisy, brash, and often reviled pest of a bird to charm its way into our society. And this unique charm lures people to enjoy and be part of their natural world. Alternatively it may be a form of social bonding or courtship

A New View of The Bird Brain

Many Functions

Hippocampus Amygdala Different architecture in Pallium (Jarvis et al. 2005)

Mouse Bird 6 horizontally aligned cell and fiber layers, millions of vertically organized, functional columns of cells and synaptic connections Uncertain homology with neocortex but synaptically complex pathways connect muscles (Butler and Cotterill 2006)

Hippocampus In birds and mammals most medial part of pallium Spatial memory (caches, location of danger) Changes in size with seasonal needs

Amygdala Compares neural expectation with actual sensory input (does answer match question) Important in processing wide range of emotionally relevant information—facial expression (Olsson and Phelps 2007, Adolphs 2008) Plays role in acquisition, storage, and expression of conditioned fear (Olsson et al. 2007)

All Bird Brains are Not Equal (Emery and Clayton 2004)

Mechanics of Learning Probe environment with muscle (question) Detect and experience sensory feedback (answer) –“Exploration-information” not “stimulus-response” –Working memory (perceptual consciousness) enables pairing of question with answer and therefore learning If mammals are conscious, and we can tell what motor-neural pathways enable it, then we can compare such pathways between mammals and birds, and finally infer ability of birds to be conscious (Butler and Cotterill 2006)

Our Brains Share Basic Design Features Inherited From a Common Ancestor

A Diversity of Sensory Inputs

Complex Associations

Brain Chemicals Motivate and Reward

Learning, Reconsidering, and Dreaming

Mammal (L) and Bird (R) Brain Connections and Circuit Loops likely involved in Consciousness (Butler and Cotterill 2006) Gray = neocortex, Blue = thalamic nuclei, Yellow = basal ganglia and cerbellum, Orange = brainstem motor relays, Magenta = sensory receptors

Lateralization and Brain Complexity Complex neural connections and lateralization –Left hemisphere for complex integration and learning New Caledonian Crows are mostly right-billed (tilting to use right eye), using left hemisphere to guide tool making and use Song learning is also controlled from left hemisphere (Cnotka et al. 2008)

Neural Circuits: Listening

Neural Circuits: Thinking Before Speaking

A Grand Repertoire Mates Dueting Mrs. Hurlbutt’s Raven Talking Female Knocking Young Birds Trilling Hungry Birds Yelling Territorial Defense Courtship Knocking Photo by Greg Zimmerman

Language?

Sleep Experiencing a vivid dream proves we form mental images of events, play them back, and experience them—it is a glimse at our “mind” My dogs dream Birds dream (birds have all phases of sleep documented in mammals) –And they can do it with one eye shut! Zebra Finches rehearse learned songs in sleep (Dave and Margoliash 2000) –Neurons firing during singing also fire in sleeping bird

Unique Sleep and Brain Complexity High-amplitude slow-waves during sleep (Rattenbord et al. 2009) –Slow wave sleep (deep sleep) may be a necessity of a complex brain with many interconnections enabling complex cognition. –Learning during the day is encoded as memories by strengthening and increasing the number of synapses between neurons Cannot continue or further plasticity of brain (ability to form new synapses and therefore memories) is reduced and energy demands spiral out of control SWS may function to reduce absolute strength of connections and prune rarely used connections thus resetting the brain for new learning For more on how synapses work and brain plasticity, see m m For basics on neurobiology of learning seehttp:// 19.html

Learning about friends and foes is necessary in a dangerous, changing environment pace of change may favor individual and social learning May be Important for Corvids and other birds that live close to people

We captured a small number of crows at each site and later score their responses to us in the site as we walk a set route either wearing the mask we used during trapping (“dangerous mask”), or another mask (“neutral mask”). We count the number of birds that scold us (see video clip here for a demonstration of scolding the dangerous mask), identify them if banded, determine if a mob (more than 1 crow scolding) forms, and record calls on a tape recorder.

And, They Don’t Seem to Forget Capture Feb. 6, 2006 Most Recent Test February 19, 2014

What About Ordinary Faces? LindaVivianMichelle HirooJoeScott

The Dangerous Face is Always Recognized, and Especially Likely to Attract a Mob But not Perfectly Figure 1-4. Scolding and formation of mobs (mean + 1 SEM) by American Crows to six masks at four study sites as recorded by 10 observers at each site that were blind to the experimental design. The dangerous mask was scolded (A) and mobbed (B) most at each site (black bars), and significantly more than some neutral masks at each site (open bars below lower 95% confidence interval of mean response to dangerous mask; horizontal line).

Who is Scolding?

Learning in the Mob

Social Learning We put a radio tag on this crow (without ourselves wearing a mask) and he scolded us in the mask that his parents viewed as dangerous. Here he is independent of parental care and scolds the mask, something he has learned from observing his parents scold this mask.

Spread in the Geographical Extent of Scolding the Extraordinary Face over 2.8 Years Figure 2-4. Spatial increase in intensity and extent of scolding at the UW site. Locations of consistent (crosshatched circles) and inconsistent (filled circles) scolding to the dangerous mask from (A) 2 weeks, (B) 1.25 years and (C) 2.8 years post-trapping. Circle diameter is proportional to the number of scolding crows: smallest circles represent single crows; largest represent groups of ?? crows. Map D depicts scolding (filled circles) and neutral (open circles) responses during the expanded search done 2.8 years after trapping.

A Variety of Neurobiology Studies Identify Specialized Areas in Mammal Brains for Face Recognition Humans Monkeys Sheep (Broad et al. 2000, European J. Neurosci; Pinsk et al PNAS; Haxby et al Trends in Cognitive Science)

And Modulation of Recognition by Others Areas Tuned to Meaning of Face (Haxby et al Trends in Cognitive Science) Activation of amygdala by fearful face

Into the Lab, and then the Brain Robert Miyaoka, Greg Garwin, Heather Cornell, Donna Cross

Virtual Sections and Statistics Lateral View Cross Sectional Views

A7.0 NEW FACE A19.4-A17.4 EE N S Emotional Response to Dangerous Person

A7.0 NEW FACE A19.4-A17.4 N S Expectation of Care From a Known Person

A7.0 NEW FACE A19.4-A17.4 N S Less Consideration, but No Fear of A New Person Crows seem to give new people the benefit of the doubt!

Scary Scenes

But Their MINDS Are DISTINCTIVELY VARIED Spatial Memory May Underlie “Funerals” Learning about A Dangerous Place

“Slicing” from Front to Back MRI of Crow Brain

Consciousness? Consciousness is a biological phenomenon that results from specific neural activity Primary or Perceptual consciousness –Mental image of the present –Widely known from vertebrates Higher level consciousness –Self awareness Reflective consciousness –Theory of mind, deception How to study –Experiments –Brain waves –Brain architecture

(Butler and Cotterill 2006)

(Emery and Clayton 2004)

Does Brain Size Matter? Big brains increase ability to behaviorally respond to changing environmental conditions This is a likely explanation for fact that brainy birds survive at higher rates than less brainy birds (Sol et al. 2007)

Big, Complex Brains May Have Aided Crossing the K-T Boundary Telencephalic expansion present in two marine birds of Lower Eocene (end of Mesozoic –Brains similar to modern seabirds Further evolution of increased telencephaic volume throughout Cenozoic by expansion of eminetia sagittalis –Poorly developed eminetia sagittalis (wulst area) in fossil bird brain casts (40-55 mya) –Absent from Archeopteryx (147mya) –Part of hyperpallium which is involved infeatures such as visual integration, learning and cognition (Reiner et al., 2005). –Big brains may have enabled them to avoid KT extinction (10my earlier). Likely present before these specimens, maybe within Cretaceous (Milner and Walsh 2009)

Brain Areas in Pigeon eminentia sagittalis (Reiner et al. 2005)

Changes in Relative Size of Complex Brain Relative brain size in modern birds showing enlargement of eminentia sagittalis (es) and expansion of telencephalon (t). A/B: Rock Pigeon; C/D: Woodcock: E/F: Tawny Owl; G/H: Macaw; I/J: Common Raven (Milner and Walsh 2009)

Sometimes People Get Too Much Nature Cultural Carrying Capacities Can Be Exceeded People respond with a host of cultural shifts That our actions reside in each others’ memories provides a mechanism for cultural coevolution That crows think about our actions demand that we also think carefully before we react (often with lethal control) to their success

Our Actions are Reflected in the Behavior and Diversity of Crows and Ravens

Literature Butler, A. B. and R. M. J. Cotterill Mammalian and avian neuroanatomy and the question of consciousness in birds. Biological Bulletin 211: Cnotka, J., Gunturkun, O., Rehkamper, G., Gray, R. D. and G. R. Hunt Extraordinary large brains in tool-using New Caledonian crows (Corvus moneduloides). Neuroscience Letters 433: Dave, M. S. and D. Margoliash Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290: Emery, N. J Cognitive ornithology: the evolution of avian intelligence. Phil. Trans. R. Soc. B 361: Emery, N. J. and N. S. Clayton The mentality of crows: convergent evolution of intelligence in corvids and apes. Science 306: Milner, A. C. and S. A. Walsh Avian brain evolution: new data from Palaeogene birds (Lower Eocene) from England. Zool. Journal of the Linnean Soc. 155: Rattenborg, N. C., Martinez-Gonzalez, D., and J. A. Lesku Avian sleep homeostasis: convergent evolution of complex brains, cognition and sleep functions in mammals and birds. Neuroscience and Biobehavioral Reviews 33: Reiner, A Avian evolution: from Darwin’s finches to a new way of thinking about avian forebrain organization and behavioural capabilities. Biology Letters 5: Reiner, A., Yamamoto, K, and H. J. Karten Organization and evolution of the avian forebrain. The Anatomical Record Part A 287A: Sol, D., Szekely, T., Liker, and L. Lefebvre Big-brained birds survive better in nature. Proc. Roy. Soc. London B 274: Marzluff, J. M. and T. Angell In the Company of Crows and Ravens. Yale U. Press. Marzluff, J. M. and T. Angell The Gifts of the Crow. Free Press.