Birds have little blobs of tissue sticking out on either side of the spinal cord in the lumbosacral region (solid black arrow in the image above). These are the accessory lobes of Lachi, and they are made up of mechanosensory neurons and glycogen-rich glial cells (but they are not part of the glycogen body, that’s a different thing that lies elsewhere — see this post).

These accessory lobes have been known since at least 1889, when they were first described by Lachi. But the function was mysterious until recently.

Starting in the late 1990s, German anatomist and physiologist Reinhold Necker investigated the development, morphology, and function of the lumbosacral canals of birds. These are not pneumatic spaces, they’re fluid-filled tubes that arch above (dorsal to) the spinal cord in the lumbosacral regions of birds. In a sacral neural canal endocast they look like sets of ears, or perhaps caterpillar legs (below image in the above slide).

Here’s the same slide with the top image labeled, by me.

In our own bodies, the meningeal sac that surrounds the spinal cord is topologically simple, basically a single long bag like a sock with the spinal cord running through the middle. In the lumbosacral regions of birds, the meningeal sac is more like a basket in cross-section, with dorsally-arching loops — the lumbosacral canals — forming the basket handles (lower image in the above slide). Evidently cerebrospinal fluid can slosh through these meningeal loops and push on the accessory lobes of Lachi, whose mechanosensory neurons pick up the displacement. This is essentially the same system that we (and all other vertebrates) have in the semicircular canals in our inner ears, which give us our sense of equilibrium.

Evidence that the lumbosacral canals function as organs of equilibrium comes not only from anatomy but also from the behavior of experimentally-modified birds. If the lumbosacral canals are surgically severed, creating the ‘lesion’ mentioned in the above figure, the affected birds have a much harder time controlling themselves. They can do okay if they are allowed to see, as shown on the left side of the above figure, but if they are blindfolded, they don’t know how to orient themselves and flop around clumsily. Meanwhile, blindfolded birds with their lumbosacral canals intact can balance just fine.

All of this is documented in a series of papers by Necker and colleagues — particularly useful are Necker (1999, 2002, 2005, 2006) and Necker et al. (2000). Necker (2006) seems to be the summation of all of this research. It’s very well-documented, well-reasoned, compelling stuff, and it’s been in the literature for over a decade.

So why is no-one talking about this? When I discovered Necker’s work last spring, I was stunned. This is HUGE. In general, the central nervous systems of vertebrates are pretty conserved, and animals don’t just go around evolving new basic sensory systems willy-nilly. Minimally I would expect congressional hearings about this, broadcast live on C-SPAN, but ideally there would be a talk show and a movie franchise.

I was equally blown away by the fact that I’d never heard about this from inside the world of science and sci-comm. Necker’s discovery seemed to have been almost entirely overlooked in the broader comparative anatomy community. I searched for weaknesses in the evidence or reasoning, and I also searched for people debunking the idea that birds have balance organs in their butts, and in both cases I came up empty-handed (if you know of counter-evidence, please let me know!). It’s relevant to paleontology, too: because the lumbosacral canals occupy transverse recesses in the roof of the sacral neural canal, they should be discoverable in fossil taxa. I’ve never heard of them being identified in a non-avian dinosaur, but then, I’ve never heard of anyone looking. You can also see the lumbosacral canals for yourself, or at least the spaces they occupy, for about three bucks, as I will show in an upcoming post.

Incidentally, I’m pretty sure this system underlies the axiomatic ability of birds to run around with their heads cut off. I grew up on a farm and raised and slaughtered chickens, so I’ve observed this firsthand. A decapitated chicken can get up on its hind legs and run around. It won’t go very far or in a straight line, hence the jokey expression, but it can actually run on flat ground. It hadn’t occurred to me until recently how weird that is. All vertebrates have central pattern generators in their spinal cords that can produce the basic locomotor movements of the trunk and limbs, but if you decapitate most vertebrates the body will just lie there and twitch. The limbs may even make rudimentary running motions, but the decapitated body can’t stand up and successfully walk or run. Central pattern generators aren’t enough, to run you need an organ of balance. A decapitated bird can successfully stand and run around because it still has a balance organ, in its lumbosacral spinal cord.

You may recognize some of the slides that illustrate this post from the Wedel et al. (2018) slide deck on the Snowmass Haplocanthosaurus for the 1st Palaeontological Virtual Congress. Those were stolen in turn from a much longer talk I’ve given on weird nervous system anatomy in dinosaurs, which I am using piecemeal as blog fuel. Stay tuned!

So, birds have balance organs in their butts. We should be talking about this. The comment thread is open.

References

  • Lachi, P. 1889. Alcune particolarita anatomiche del rigonfiamento sacrale nel midollo degli uccelli. Lobi accessori. Att Soc Tosc Sci Nat 10:268–295.
  • Necker, R. 1999. Specializations in the lumbosacral spinal cord of birds: morphological and behavioural evidence for a sense of equilibrium. European Journal of Morphology 37:211–214.
  • Necker, R. 2002. Mechanosensitivity of spinal accessory lobe neurons in the pigeon. Neuroscience Letters 320:53–56.
  • Necker, R. 2005. The structure and development of avian lumbosacral specializations of the vertebral canal and the spinal cord with special reference to a possible function as a sense organ of equilibrium. Anatomy and Embryology 210:59–74.
  • Necker, R. 2006. Specializations in the lumbosacral vertebral canal and spinal cord of birds: evidence of a function as a sense organ which is involved in the control of walking. Journal of Comparative Physiology A, 192(5):439-448.
  • Necker, R, Janßen A, Beissenhirtz, T. 2000. Behavioral evidence of the role of lumbosacral anatomical specializations in pigeons in maintaining balance during terrestrial locomotion. Journal of Comparative Physiology A 186:409–412.
  • Wedel, M.J., Atterholt, J., Macalino, J., Nalley, T., Wisser, G., and Yasmer, J. 2018. Reconstructing an unusual specimen of Haplocanthosaurus using a blend of physical and digital techniques. Abstract book, 1st Palaeontological Virtual Congress, http://palaeovc.uv.es/, p. 158 /  PeerJ Preprints 6:e27431v1
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In short, no. I discussed this a bit in the first post of the Clash of the Dinosaurs saga, but it deserves a more thorough unpacking, so we can put this dumb idea to bed once and for all.

As Marco brought up in the comments on the previous post, glycogen bodies are probably to blame for the idea that some dinosaurs had a second brain to run their back ends. The glycogen body is broadly speaking an expansion of the spinal cord, even though it is made up of glial cells rather than neurons — simply put, help-and-support cells, not sensory, motor, or integration cells. When the spinal cord is expanded, the neural canal is expanded to accommodate it; as usual, the nervous system comes first and the skeleton forms around it. This creates a cavity in the sacrum that is detectable in fossils.

avian lumbosacral specializations - glycogen body

Giffin (1991) reviewed all of the evidence surrounding endosacral enlargements in dinosaurs (primarily sauropods and stegosaurs) and concluded that the explanation that best fit the observations was a glycogen body like that of birds. I agree 100%. The endosacral cavities of sauropods and stegosaurs (1) expand dorsally, instead of in some other direction, and (2) expand and contract over just a handful of vertebrae, instead of being more spread out. Of the many weird specializations of the spinal cord in birds, the glycogen body is the only one that produces that specific signal.

If any part of the nervous system of birds and other dinosaurs might be described as a ‘second brain’, it wouldn’t be the glycogen body, it would be the lumbosacral expansion of the spinal cord, which really is made up of neurons that help run the hindlimbs and tail (more on that in this previous post). But there’s nothing special about that, it’s present in all four-limbed vertebrates, including ourselves. Interestingly, that bulk of extra neural tissue in the sacral region of birds was referred to as a sort of ‘second brain’ by Streeter way back in 1904, in reference to the ostrich, but it’s clear that he meant that as an analogy, not that’s it’s literally a second brain.

So to sum up, a gradual expansion of the spinal cord to help run the hindlimbs and tail IS present in dinosaurs — and birds, and cows, and frogs, and us. But if that qualifies as a ‘second brain’, then we also have a ‘third brain’ farther up the spinal cord to run our forelimbs: the cervical enlargement, as shown in the above figure. These spinal expansions aren’t actual brains by any stretch and referring to them as such is confusing and counterproductive.

The sharp expansion of the neural canal over just a few vertebrae in birds does not house a ‘second brain’ or even an expansion of the neural tissue of the spinal cord. It contains the glycogen body, which is not made of neurons and has no brain-like activity. The sacral cavities of non-avian dinosaurs replicate precisely the qualities associated with the glycogen bodies of birds, and there’s no reason to expect that they contained anything else. That we don’t know yet what glycogen bodies do, even in commercially important species like chickens, may make that an unsatisfying answer, but it’s what we have for now.

The next installment will be way weirder. Stay tuned!

References

  • Giffin, E.B.,1991. Endosacral enlargements in dinosaurs. Modern Geology 16: 101-112.
  • Streeter, G.L. 1904. The structure of the spinal cord of the ostrich. American J. Anatomy 3(1): 1-27.

I planned to post this last spring but I never got around to it. I think I have a mental block about discussing the glycogen body. Partly because I’ve been burned by it before, partly because no-one knows what it does and that’s unsatsifying, partly because I didn’t want to plow through all the new literature on it (despite which, the function remains unknown).

Then I decided, screw it, I’ll let the slides speak for themselves, and the actual text of the post can just be navel-gazing and whingeing. Which you are “enjoying” right now.

So, there’s the glycogen body. It balloons out between the dorsal halves of the spinal cord, it’s made of glial cells (neuron support cells) that are packed with glycogen, and nobody knows why it’s there. On the graph of easy-to-find and frustrating-to-study it is really pushing the envelope.

Update: the role of the glycogen body in the ‘second brain’ myth is covered in the next post.

Previous entries in the “Bird neural canals are weird” series:

Here are some stubbornly-not-updated references for the images I used in the slides:

  • Huber, J.F. 1936. Nerve roots and nuclear groups in the spinal cord of the pigeon. Journal of Comparative Neurology 65(1): 43-91.
  • Streeter, G.L. 1904. The structure of the spinal cord of the ostrich. American Journal of Anatomy 3(1):1-27.
  • Watterson, R.L. 1949. Development of the glycogen body of the chick spinal cord. I. Normal morphogenesis, vasculogenesis and anatomical relationships. Journal of Morphology 85(2): 337-389.

If you followed along with the last post in this series, you now have some bird vertebrae to play with. Here are some things to do with them.

1. Learn the parts of the vertebrae, and compare them with those of other animals

Why are we so excited about bird vertebrae around here? Mostly because birds are reasonably long-necked living dinosaurs, and although their vertebrae differ from those of sauropods in relative proportions, all of the same bits are present in roughly the same places. If you know the parts of a bird vertebra and what each one does, you have a solid foundation for inferring the functions of sauropod vertebrae. Here’s a diagram I made for my SVP poster with Kent Sanders way back in 1999. I used an ostrich vertebra here but you should be able to find the same features in a cervical vertebra of just about any bird.

These are both middle cervical vertebrae in right lateral view. A middle cervical vertebra of a big ostrich will be between 3 and 4 inches long (7.5-10 cm), and one from a big brachiosaur like Giraffatitan will be about ten times longer.

I should do a whole post on neck muscles, but for now see this post and this paper.

2. Put the vertebrae in order, and rearticulate them

It is often useful to know where you are in the neck, and the only way to figure that out is to determine the serial position of the vertebrae. Here’s an articulated cervical series of a turkey in left lateral view, from Harvey et al. (1968: pl. 65):

Harvey’s “dorsal spine” is the neural spine or spinous process, and his “ventral spine” is the carotid process. The “alar process” is a sort of bridge of bone connecting the pre- and postzygapophyses; you can see a complete version in C3 in the photo below, and a partial version in C4.

Speaking of that photo, here’s my best attempt at rearticulating the vertebrae from the smoked turkey neck I showed in the previous post, with all of the vertebrae in left dorsolateral view.

These things don’t come with labels and it can take a bit of trial and error to get them all correctly in line. C2 is easy, with its odd articular surface for the atlas and narrow centrum with a ventral keel. Past that, C3 and C4 are usually pretty blocky, the mid-cervicals are long and lean, and then the posterior cervicals really bulk out. Because this neck section had been cut before I got it, some of the vertebrae look a little weird. Somehow I’m missing the front half of C6. The back half of C14 is also gone, presumably still stuck to the bird it went with, and C7 and C12 are both sectioned (this will come in handy later). I’m not 100% certain that I have C9 and C10 in the right order. One handy rule: although the length and neural spine height change in different ways along the column, the vertebrae almost always get wider monotonically from front to back.

And here’s the duck cervical series, in right lateral view. You can see that although the specific form of each vertebra is different from the equivalent vert in a turkey, the same general rules apply regarding change along the column.

Pro tip: I said above that these things don’t come with labels, but you can fix that. Once you have the vertebrae in a satisfactory order, paint a little dot of white-out or gesso on each one, and use a fine-point Sharpie or art pen to write the serial position (bone is porous and the white foundation will keep the ink from possibly making a mess). You may also want to put the vertebrae on a string or a wire to keep them in the correct order, but even so, it’s useful to have the serial position written on each vertebra in case you need to unstring them later.

3. Look at the air spaces

One nice thing about birds is that all of the species that are readily commercially available have pneumatic traces on and in their vertebrae, which are broadly comparable to the pneumatic vertebrae of sauropods.

The dorsal vertebrae of birds are even more obviously similar to those of sauropods than are the cervicals. These dorsal vertebrae of a duck (in left lateral view) show a nice variety of pneumatic features: lateral fossae on the centrum (what in sauropods used to be called “pleurocoels”), both with and without foramina, and complexes of fossae and foramina on the neural arches. Several of the vertebrae have small foramina on the centra that I assume are neurovascular. One of the challenges in working with the skeletal material of small birds is that it becomes very difficult to distinguish small pneumatic foramina and spaces from vascular traces. Although these duck vertebrae have small foramina inside some of the lateral fossae, the centra are mostly filled with trabecular, marrow-filled bone. In this, they are pretty similar to the dorsal vertebrae of Haplocanthosaurus, which have fossae on the neural arches and the upper parts of the centra, but for which the ventral half of each centrum is a brick of non-pneumatic bone. For more on distinguishing pneumatic and vascular traces in vertebrae, see O’Connor (2006) and Wedel (2007).

This turkey cervical, in left posterolateral view, shows some pneumatic features to nice advantage. The lateral pneumatic foramina in bird cervicals are often tucked up inside the cervical rib loops where they can be hard to see and even harder to photograph, but this one is out in the open. Also, the cervicals of this particular turkey have a lot of foramina inside the neural canal. In life these foramina are associated with the supramedullary diverticula, a set of air-filled tubes that occupy part of the neural canal in many birds — see Atterholt and Wedel (2018) for more on this unusual anatomical system. The development of foramina inside the neural canal seems to be pretty variable among individuals. In ostriches I’ve seen individuals in which almost every cervical has foramina inside the canal, and many others with no foramina. For turkeys it’s even more lopsided in my experience; this is the first turkey in which I’ve found really clear pneumatic foramina inside the neural canals. This illustrates one of the most important aspects of pneumaticity: pneumatic foramina and cavities in bones show that air-filled diverticula were present, but the absence of those holes and spaces does not mean that diverticula were absent. Mike and I coined the term “cryptic diverticula” for those that leave no diagnostic traces on the skeleton — for more on that, see the discussion section in Wedel and Taylor (2013b).

Finally, it’s worth taking a look at the air spaces inside the vertebrae. Here’s a view into C12 of the turkey cervical series shown above. The saw cut that sectioned this neck happened to go through the front end of this vertebra, and with a little clean-up the honeycomb of internal spaces is beautifully displayed. If you are working with an intact vertebra, the easiest way to see this for yourself is to get some sandpaper and sand off the front end of the vertebra. It only takes a few minutes and you’ll be less likely to damage the vertebrae or your fingers than if you cut the vertebra with a saw. Similar complexes of small pneumatic cavities are present in the vertebrae of some derived diplodocoids, like Barosaurus (see the lateral view in the middle of this figure), and in most titanosauriforms (for example).

I have one more thing for you to look for in your bird vertebrae, and that will be the subject of the next installment in this series. Stay tuned!

References

When I started working on sauropods, I thought their vertebrae were cool but they were loaded with weird structures that I didn’t understand. Then I dissected my first ostrich neck and suddenly everything made sense: this was a muscle attachment, that was a pneumatic feature, this other thing was a ligament scar. Everyone who is interested enough to read this blog should give themselves the same “Aha!” moment. You don’t even have to eat the birds yourselves, lots of people don’t like bird necks and will give them away if you ask.

If you get a whole bird, the neck is usually included with the giblets. Around Thanksgiving and Christmas you can often find bundles of spare turkey necks at your grocer or butcher.

This spring I picked up some smoked turkey necks at the grocery store. I wanted to make turkey stew and I figured I might as well get some toys in the bargain. Here are some neck segments in the crock pot.

And here they are after a few hours of cooking. Time to separate the meat from the bones. That neck segment in the middle of the above photo is a pretty good match for the ostrich neck cross-section in this post.

Here are parts of three vertebrae with the long, multi-segment muscles removed, but with the shorter single-segment muscles still connecting them. Anterior is to the right; that’s a cervical ribs sticking out at the lower right “corner”.

Here’s a single intact cervical in left lateral view with most of the meat off, but ready for a long simmer to loosen the remaining crud. This is roughly the same orientation as the lateral view of Mike’s famous turkey cervical.

Meat goes back in the pot.

Bones go on to the next stage: simmering. One of the nice things about the stepwise process of cleaning bones is that you can stop at any point, put the bones in the freezer, and come back days or months later. This bowl of bones went into the freezer in exactly the state you see here, and I didn’t pull them out and finish cleaning them until last week.

If you have a pot-sized strainer, it makes things easier, especially for rinsing. These aren’t turkey vertebrae, these are the verts from my Thanksgiving ducks. But the principle and the process are the same.

After simmering for an hour or two, it’s time to pick off the loosened muscles, ligaments, cartilage, and so on. Here are two similar turkey cervicals after simmering, in dorsal view with anterior to the right. The one on the left has not been cleaned and has all kinds of crud stuck to it, including a big chunk of intervertebral ligament sticking out between the rami of the postzygapophyses. The one on the right has been through a first-pass cleaning.

What tools should you use? Whatever you have to hand. I like old toothbrushes for scrubbing off little bits of muscle and tendon, toothpicks for shoving spinal cord bits through the neural canal and for picking bits of meat out of hard-to-reach places, and the Mark 1 thumbnail for planing off articular cartilage, as shown here with the back end of a duck cervical.

Here’s the outcome of a cleaning session: on the left, the bowl I used for cleaning the vertebrae. In the top middle, the pile of gloop I pulled off. And on the right, a bowl of cleaned turkey and duck vertebrae, ready for degreasing.

Here are the vertebrae of a couple of ducks after soaking overnight in 3% hydrogen peroxide, the ordinary stuff you get at the drugstore or dollar store.

Here’s another bowl with turkey vertebrae. They were all at the bottom of the bowl when I went to bed, floating when I got up the next morning. This is pretty common with lightweight pneumatic vertebrae: the oxygen bubbling out of the hydrogen peroxide has gotten trapped in the internal air spaces and made the vertebrae buoyant.

After a night in the hydrogen peroxide, it’s time to rinse and dry the vertebrae. I put this mixed lot of turkey and duck verts on a plate with a paper towel and left them out on the kitchen counter. In the summertime, when it’s hot and dry, I might put them outside for a bit and they’d be dry in a couple of hours. Indoors in the winter it can take a couple of days for the vertebrae to get completely dry.

Here’s the same batch of vertebrae a couple of days later, clean and dry and ready for whatever comes next.

Which bird should you use? Bigger birds have vertebrae that are easier to clean, harder to damage, and more fun to look at, but use whatever you can get your hands on. This photo shows the axis, a middle cervical, and a posterior cervical from the turkey (top) and duck (bottom). Note that the duck was so young that the cervical ribs hadn’t fused and they fell off during the cleaning process.

If you’ve been following along, you have some nice clean bird vertebrae to play with. So what now — what should you do with them? That will the subject of an upcoming post. Stay tuned!

Turkeys lie

December 18, 2018

We all know what turkeys look like, right?

Turns out that two thirds of that bird is a lie. Here’s a diagram produced for hunters on which part of the turkey to shoot. (It’s all over the Internet, and I can’t trace the original source, but I got it from here):

Bascially, if you fire an arrow at a visible turkey, there’s a 2/3 chance that it’ll pass straight through feathers and completely miss the actual bird.

Now, then: what do we think a theropod looked like in life? Probably not much like what skeleton reconstructions show as the flesh envlope, as for example in Scott Hartman’s Guanlong:

Instead, it might have looked like this:

(Note: this is not in any way a criticism of Scott’s fine work, which is a scientific restoration of the soft tissue, and does not address integument at all.)

And now that pterosaurs have feathers, too(*), we have to assume that they, too, probably had body outlines bearing little resemblance to the flesh-on-bone shapes we’ve been used to seeing.

 


(*) As Matt pointed out: “I can’t be bothered to write “integumentary structures” when I mean “feathers”. I realize they may be independently derived, but eyes evolved independently like 40 times and we don’t refer to the other 39 instances as “photoreceptive structures”.” (He actually wrote “I can’t be arsed”, but I changed it to “bothered” to make him appear more professional.)

 

What it says on the tin. This is a specimen from the UCMP comparative collection.

I was just going to post this photo with zero commentary, but I can’t help myself. Note that on the two vertebrae in the middle, the crista transverso-obliqua (what in non-avian dinos would be the spinopostzygapophyseal lamina or SPOL) rises higher than either the neural spine apex or the epipophyses. That’s crazy. And it demonstrates something we also see in sauropods, which is that laminae are not merely the plates of bone left behind after pneumatization has scooped all of the unnecessary material out of a normal vertebra–sometimes they are additive structures, too.

If all of that sounded like gibberish, I can sympathize. I spent my first few months as a sauropodologist just learning the lingo (another thing I should blog about sometimes). Here’s a labeled version:

As long as I’m yapping, note the light shining through the honeycombed internal structure of these highly pneumatic vertebrae. For more on the ridiculous pneumaticity of pelican bones, see this post and this one. For more on the homology of bird and sauropod vertebrae, see Wedel and Sanders (2002), and for more on laminae as additive versus reductive structures, see the discussion on pages 210-212 of Wedel (2007).

References