Close to my apartment in the outskirts of Basel, green fields and some small woods lie basically in front of my house door. This is also where some flocks of crows gather around, partly searching the fields for food, partly watching out in the topmost trees. Meeting them once every day, I started wondering whether these animals would qualify for being an animal model for neuroscience and especially neurophysiology.

Nowadays, mainstream neuroscience focuses on mice; next, on drosophila, zebrafish, C. elegans, some monkeys and the rat. Everything else (frog, honey bee, lizard, ferret …) is considered rather exotic – although there are millions of animal species on our planet, each of them with a different brain organization. Of course it does make sense to focus on a common species (that is ideally genetically tractable) as a community,  in order to profit from synergies. But at the same time this narrows the mind. In my opinion, it is useful to have some researchers (although not the majority of them) work on exotic animal models – on those animals that stand out by a striking organization, by the simplicity of their brain, or by behaviors reminding of human behavior.

There is a long tradition, going back to John J. Audubon (*1785), Johann F. Naumann (*1780) and beyond of trying to embrace the world of birds by patient observation and detailed description. Until now, there is a large community of ‘birders’ who often content themselves with observing birds and the behaviors and features that help to identify a bird species. At some point – quite late, and probably later than for other animal species -, cognitive neuroscience questions that were targeted at birds came up: how intelligent are birds? do birds recognize themselves in mirrors? can birds count? what kind of language do they use? do birds form human-like families?

But is there any neurophysiological research on crows? What behaviors do they exhibit? Do they have brain structures homologues to the human brain? And, to start with, what are crows anyway, viewed in the context of the tree of life?

How are crows related to other species?

To visualize the phylogenetic tree of corvids in the context of other birds and standard neuroscience animal models, I used some information provided by the Tree Of Life project and put it together in a small drawing.

From this, it is clear that, for example, the ancestors of zebrafish branch very early from the human ancestors (430 ma, million years ago). Then reptiles including birds (312 ma), whereas mice are much closer to primates (90 ma). Drosophila and C. elegans (both almost 800 ma) are very far from all the vertebrates. In the bird family chicken and pigeons are very far from the songbirds, and given this broader context, corvids and other songbirds like zebra finches are phylogenetically close (44 ma, compared to ca. 82 million years between crows and falcons/pigeons/owls/parrots or 98 million years between crows and chicken). I looked up the times using www.timetree.org.

Of course this summary alone does not allow to perfectly choose an animal model. But it gives a first idea about the relationships. And I admit that I found it very instructive to make this drawing.

What kind of behaviors do crows show?

Crows do talk to each other using calls, by which they not only articulate their inner status, but also communicate information about the environment to others, e.g. about predators. A large variety of raven calls have been documented by Bernd Heinrich, Thomas Bugnyar and others (see e.g. [1]). However, calls are often locally or individually different, which makes the collection of a complete repertoire of calls impossible or at least meaningless.

Ravens are able to understand the capabilities and limitations of others, e.g. competitors [2]. To have an internal conception of the knowledge of specific others is an ability that might be related to the concept of empathy and therefore be an interesting field of study.

The smallest unit of corvid social life is the mating partnership, and crows usually choose their partner for a lifetime, but they also participate in larger social assemblies, e.g. for sharing information, sleeping and for hunting.

Similar to humans, and different from mice, crows rely mostly on visual and acoustic stimuli, rather than olfactory ones.

Crows are usually rather shy, but curious at the same time. The shyness is, of course, a problem for researchers wanting to work with crows. Especially wild crows are very difficult to tame, and it requires a lot of continuous work and personal care to raise a crow or a raven.
Bernd Heinrich tells about his rearing raven nestlings. He observes that curiosity and exploratory fearlessness dominates in the first months, after which shyness towards humans and a general extremely neophobic behavior dominates [3].

Unlike most other birds, crows are able to count [4]. For more context on the representations of numbers in crows, as compared to in primates, see [5].

At SfN 2016, I talked to some crow researchers (mainly working on memory tasks), and I was told that crows can often learn the same tasks as monkeys can, like a delayed choice task, on a very similar learning time scale.

Crows are well-known for their creativity (e.g. dropping walnuts on streets, where they are cracked by vehicles running over) and famous for using tools, especially the New Caledonian crow. Personally, I got the impression that crows plan ahead in time much more than any other birds – maybe this is also related to them being so shy.

Are there homologies between crow brains and human brains?

In a popular view held since the early 20th century, most of the avian telencephalon was seen as homologous to the striatum, which does not seem to play the central role for mammalian cognition. Around 2000, his theory was reversed by evidence from anatomy and genetic markers [6], now converging to the theory that a large fraction of the avian brain is actually of pallial and not striatal origin. The nuclei of which the avian telencephalon consists are supposed to be somewhat similar in connectivity to the layers of cortex.

The drawing below (modified from [7]) is a coronal section through the brain of a jungle crow, with the cutting position indicated on the left side (at least that’s my guess).

In an anatomical study done in chicken [8], local interlaminar recurrent circuits comparable to the laminar organization of mammalian cortex were found between the enteropallium (E in the schematic above, yellow) and the mesopallial ventro-lateral region (MVL, green), provided with input from thalamic structures (around ‘TFM’). This similarity to mammalian cortex organization is suggested to be due to convergent evolution, but not necessarily an organizational principle of a common ancestor. A short and readable, but very informative review of theories about homologies between bird and mammalian brains and convergent evolution has been put together by Onur Güntürkün [9], in whose lab also a first functional characterization of the – possibly associational – target areas of the enteropallium (NFL, MVL, TPO and NIL) is given by checking the expression of the immediate early gene ZENK [10].

What physiological methods are established for use with crows?

Not in crows, but in zebra finch, calcium imaging and optogenetic experiments [11] have been performed. The crow brain, however, is ca. 2 cm in size and therefore too big for invasive methods based on scattering light. I would guess that calcium imaging with virally expressed or synthetic calcium dyes would still be feasible on the brain surface. However, the avian brain probably does not expose its interesting ‘cortical’ structures at the outer surface, as do mammalian brains. Plus, an interesting brain structure, the nidopallium caudolaterale (NCL, [12]), which is supposed to work on similar tasks as the mammalian prefrontal cortex, is nicely accessible in pigeons, but located at the difficult-to-access lateral side of the brain in crows. Probably ultrasound-based methods that have been developed for rats [13] for coarse level activity imaging would be a good compromise, although they do not go down to cellular resolution.

Despite the challenges, the NCL is one of the corvid brain regions that has been recorded from [12], with 8 chronically implanted microelectrodes recording simultaneously in a delayed response behavioral task (similar to the classic experiments developed for prefrontal cortex in monkeys), where neurons firing in the waiting period of the behavioral task seem to encode an abstract rule that is lateron used for decision.

Other neurophysiological methods applied to crows include functional imaging using fMRI and the previously mentioned study using expression levels of the immediate early gene ZENK in order to find out tuning to motion or color [10], but all of this is clearly at very early and exploratory stages.

Further reading about crows and videos about crows.

• This is an excellent basic FAQ on daily life interactions with crows, written by an academic researcher.
  .
• A well-written book by raven behavior researcher Bernd Heinrich: Mind of the Raven, basically consisting of a large and sometimes a bit lengthy set of anecdotal stories. He writes among others about the struggles of raising raven nestlings and about the difficulties of mating them.
  .
• A video documentary on crow intelligence (video 52:01 min – good as a starter, The Incredible Intelligence of Crows).
  .
• An amateur crow researcher describing his crows and their typical behavior (video 18:15 min, german).
  .

Conclusion.

In my eyes, the corvid family is a very interesting animal model, since corvids show complex behavior like planning, creativity, tool-use and the ability to fly. On the other hand, they are more difficult to keep and raise than mice (which can simply be ordered for a couple of bucks). Their shyness is also a problem – try to approach a crow in the field, and you will know that it is not easy (although there are some exceptional, more curious crow individuals).

Realistically, I do not expect crows to become one of the major animal models – technique-wise, the field is simply too much behind the mouse- or monkey-field. But crow research might offer an important differing view on the brain. Probably some, even higher-order computations in crows and primates are very similar, and it would be interesting to see whether their implementations on a neuronal level are also similar and have developed in a convergent manner.

———————-

1. Bugnyar, Thomas, Maartje Kijne, and Kurt Kotrschal. “Food calling in ravens: are yells referential signals?” Animal Behaviour 61.5 (2001): 949-958. (link)
2. Bugnyar, Thomas, and Bernd Heinrich. “Ravens, Corvus corax, differentiate between knowledgeable and ignorant competitors.” Proceedings of the Royal Society of London B: Biological Sciences 272.1573 (2005): 1641-1646. (link)
3. Heinrich, Bernd, and Hainer Kober. Mind of the raven: investigations and adventures with wolf-birds. New York: Cliff Street Books, 1999. (link)
4. Ditz, Helen M., and Andreas Nieder. “Numerosity representations in crows obey the Weber–Fechner law.” Proc. R. Soc. B. Vol. 283. No. 1827. The Royal Society, 2016. (link)
5. Nieder, Andreas. “The neuronal code for number.” Nature Reviews Neuroscience (2016). (link)
6. Jarvis, Erich D., et al. “Avian brains and a new understanding of vertebrate brain evolution.” Nature Reviews Neuroscience 6.2 (2005): 151-159. (link with paywall)
7. Izawa, Ei-Ichi, and Shigeru Watanabe. “A stereotaxic atlas of the brain of the jungle crow (Corvus macrorhynchos).” Integration of comparative neuroanatomy and cognition (2007): 215-273. (link)
8. Ahumada‐Galleguillos, Patricio, et al. “Anatomical organization of the visual dorsal ventricular ridge in the chick (Gallus gallus): layers and columns in the avian pallium.” Journal of Comparative Neurology 523.17 (2015): 2618-2636. (link)
9. Güntürkün, Onur, and Thomas Bugnyar. “Cognition without cortex.” Trends in cognitive sciences 20.4 (2016): 291-303. (link)
10. Stacho, Martin, et al. “Functional organization of telencephalic visual association fields in pigeons.” Behavioural brain research 303 (2016): 93-102. (link)
11. Roberts, Todd F., et al. “Motor circuits are required to encode a sensory model for imitative learning.” Nature neuroscience 15.10 (2012): 1454-1459. (link with paywall)
12. Veit, Lena, and Andreas Nieder. “Abstract rule neurons in the endbrain support intelligent behaviour in corvid songbirds.” Nature communications 4 (2013). (link)
13. Macé, Emilie, et al. “Functional ultrasound imaging of the brain.” Nature methods 8.8 (2011): 662-664. (link)

Photos/Pictures/Videos:
Alpine cough (Alpendohle) on Mt. Pilatus/Switzerland, Summer 2016.
Raven soaring on Hawk Hill next to San Francisco, Fall 2016.