New paper: Atterholt et al. (2024) on neural canal ridges in dinosaurs

New paper out, er, yesterday:

Atterholt, J., Wedel, M.J., Tykoski, R., Fiorillo, A.R., Holwerda, F., Nalley, T.K., Lepore, T., and Yasmer, J. 2024. Neural canal ridges: a novel osteological correlate of postcranial neuroanatomy in dinosaurs. The Anatomical Record, 1-20. https://doi.org/10.1002/ar.25558

This one started a bit over 10 years ago, on April 9, 2014. That morning I was at the off-site storage facility of the Perot Museum in Dallas, looking at juvenile Alamosaurus material from Big Bend National Park. I found this cute little unfused caudal neural arch, BIBE 45885:

As you can see from my notes, I clocked the little ridges on the inside of the neural canal, but I didn’t know what to make of them. (BTW I’ve used this little feller in a bunch of talks and in my MTE paper last summer with Jessie — see Wedel & Atterholt 2023 and this post.)

That afternoon I was at SMU’s Shuler Museum of Paleontology looking at the holotype of Astrophocaudia, SMU 61732, which was then a new genus, having only been named the year before by Mike D’Emic (2013). And what should I see in this nice caudal:

Now I am not always the fastest on the uptake, but if you smack me in the face twice I start paying attention. Surely it was not a coincidence that the caudal vertebrae of these two not-super-closely-related sauropods had little ridges inside their neural canals. The problem was, I had no idea what they were. For a brief period I got excited by the possibility that they might be some epiphenomenon of big spinal veins, like those of crocs, or big paramedullary diverticula, like those of birds, but they didn’t look quite right for either of those applications (more on this in a future post, maybe, and in the discussion section of the new paper, definitely). I was just flat stumped.

Fast forward to the summer of 2018, by which time I was working with Jessie Atterholt on paramedullary diverticula — laying the groundwork for what would become Atterholt & Wedel (2022) — and generally getting interested in all things neural canal related, including the weird expanded neural canals in the Snowmass Haplocanthosaurus (see Wedel et al. 2021). I wrote to David and Marvalee Wake at Berkeley, both of whom had served on my dissertation committee, and who between them knew more about vertebrate morphology than anyone else I knew, to ask of they’d ever seen similar expansions of the neural canal. To my delight, David wrote right back, “This is a mystery to me. In salamanders there are little strut-like processes from the inside of the neural canal extending inward to support the cord. These are at least partly bony.” That didn’t help with Haplocanthosaurus — at that time still the newer mystery — but it did seem to solve my then 4-year-old quest to figure out what was going on in the Alamosaurus and Astrophocaudia caudals.

We’ll come back to sauropods, I promise. But first we gotta talk about meninges for a bit.

What’s the mater?

One of the bedrock bits of the chordate body plan is a connective tissue notochord running down the body axis, with a big nerve cord sitting on top and a big artery hanging just below. In vertebrates the notochord is mostly replaced by the vertebral column, and we refer to the big nerve cord as the spinal cord and to the big artery as the aorta. The vertebral column doesn’t just give the body stiffness and flexibility and something to hang muscles on, it also has a dorsal bony loop to protect the spinal cord, which we call the neural arch, and in the tail a ventral bony loop to protect the aorta, which we call the hemal arch (the V-shaped hemal arch bones are more commonly referred to as ‘chevrons’). The spinal cord runs through the neural arches of successive vertebrae, which collectively form a protective tube: the neural canal.

(NB: in human anatomy we tend to call the hole for the spinal cord in any one vertebra the ‘vertebral foramen’, and the canal formed by the stacked vertebral foramina the ‘spinal canal’, but in comparative anatomy we tend to use ‘neural canal’ for both the neural arch passage in a single vertebra and the tube formed by all the neural arches.)

The spinal cord isn’t just flopping around in the neural canal willy-nilly. Like the brain, the spinal cord is jacketed in a series of protective membranes collectively called the meninges (singular: meninx). Mammals and most (all?) other tetrapods have three meninges:

• outermost is the dura mater, or “tough mother” (same root as ‘durable’)
• just inside the dura is the continuous layer of the arachnoid mater, or “spider(web) mother”
• below the continuous layer of the arachnoid is the subarachnoid space, where cerebrospinal fluid (CSF) circulates; this space is crossed by numerous strands of arachnoid that reach down to the pia, and which look like spiderwebs in dissection, hence the name ‘arachnoid’ (thin blue radiating lines in the diagram above)
• innermost, sitting intimately on top of the spinal cord and spinal nerve roots, is the pia mater, or “tender mother”

In mammals the space between the dura mater and the bony walls of the neural arch is filled with epidural fat. This isn’t unhealthy fat, this is fat used as packing peanuts — the lightest, cheapest thing the body can build.

(We’re a fat-0bsessed culture so it may sound weird to hear fat described as ‘light’ and ‘cheap’, but in fact it is. The metabolic demand of keeping fat cells alive is negligible,* and every other tissue or fluid is heavier and more expensive to maintain. The yellow marrow in the shafts of your long bones is made of fat, and your body will not use that fat for energy even if you are starving to death, because it would just have to be replaced with something heavier and more costly.

*Negligible, but not zero, and the work required to push blood through the extra miles of arteries that serve the fat deposits in obese people can put a lot of extra strain on the heart.)

Last but not least there are denticulate ligaments, little sideways extensions of the pia mater that anchor the spinal cord to the inside of the dura mater. I drew them in pink in the diagram, but in dissection they are shiny white or silver; ‘denticulate’ means ‘little tooth’.

Some of these terms have entered the popular lexicon from medicine, particularly ‘meningitis’ and ‘epidural’. Meningitis is an inflammation of the meninges around the brain and spinal cord, which is exactly as horrible and life-threatening as it sounds. An epidural injection is used to deposit anesthetic medication into the epidural fat, where it can soak down through the meninges and bathe the dorsal half of the spinal cord, where the sensory pathways (including pain) are located. In a lumbar puncture, a needle is driven through the dura and the continuous layer of the arachnoid into the subarachnoid space, usually to draw CSF for diagnostic purposes.

Here’s an important fact I didn’t know in 2014, having been educated most deeply on humans: many non-mammals don’t have epidural fat. Instead, the dura mater can be in contact with or even fused with the periosteum lining the inside of the neural arch, and the denticulate ligaments don’t just go to the dura, they go through it, to contact bone. And any time there’s connective tissue anchoring to bone, there’s a possibility that it will leave an attachment scar.

How do we know this? Salamanders, baby! Bony spinal cord supports were first identified in the northern two-lined salamander, Eurycea bislineata, by Wake and Lawson (1973) — Wake here meaning David Wake, who 41 years later would give me the clue I needed to interpret what I was seeing in sauropod caudal vertebrae. The trail went cold for a while after the 70s, but Skutschas (2009) and Skutschas & Baleeva (2012) found bony spinal supports — a.k.a. neural canal ridges — in a host of salamanders and fish.

The Floodgates Open

Standing on shoulders of Wake & Lawson and Skutschas & Baleeva, Jessie and I started finding neural canal ridges in all kinds of critters. We visited the herpetology collections at the LACM to verify that we could find them in salamanders, and documented them for the first time in the giant salamanders Andrias japonicus and Andrias davidianus. Skutschas & Baleeva (2012: fig. 5) had figured NCRs in a salmon (Salmo); on a visit to the OMNH I found them in a tuna (Thunnus). Jessie and I visited Dinosaur Journey in Fruita, Colorado, and found examples in Camarasaurus, Diplodocus, and more Apatosaurus vertebrae than you can shake a stick at (as always, many thanks to the MWC Director of Paleontology Julia McHugh for being an awesome host!).

Then other people started finding them. Jessie gave a talk on NCRs at SVPCA in 2019, the lovely meeting on the Isle of Wight, and Femke Holwerda said she’d seen them in a cetiosaur. At the same meeting Mick Green showed us rebbachisaruid material he’d collected from the Isle of Wight, and we found them in a rebbachisaur caudal. Jessie and I went to look for NCRs in the Raymond Alf Museum right here in Claremont, California, and Tara Lepore, who was helping us that day, found them in a hadrosaur caudal.

We even started finding them in previously published papers. Here’s a caudal vertebra of a juvenile Rapetosaurus from Curry-Rogers (2009: fig. 27):

This was a watershed moment — it meant that we could potentially expand our search for NCRs using the published literature. Later Jessie visited the Field Museum and was able to confirm the presence of NCRs in all the real (not cast or reconstructed) vertebrae of the mounted Rapetosaurus.

It gets better! Back in 2009 some goober named Wedel had been an author on the paper describing Brontomerus, and whadda we have here in Figure 6 of that paper?

Truly, we notice what we are primed to notice, and sometimes not a heck of a lot more. In my defense, since getting my antennae out for NCRs I have had my hopes raised and then dashed many times by slightly offset cracks that just happen to run through the midpoint of the neural arch (it makes sense, the bone is thinnest there and most likely to crack), which is presumably what I inferred back when. For a better look at the NCRs in Brontomerus, see Figure 6 in the new paper.

In 2020, Alexander Averianov and Alexey Lopatin described neural canal ridges in the holotype of the Mongolian sauropod Abdarainurus, and they identified them as bony spinal cord supports of the kind described by Skutschas & Baleeva (2012) — correctly, in our view. They’d been unaware of our work, which is not surprising since we’d only presented it in 2019 at SVPCA, and we’d been unaware of theirs. I was, in truth, a little chagrined to have dawdled long enough to be beaten into print (he writes, four and half years later!), but I sent Alexander a congratulatory note and he sent a very gracious response. Anyway, Jessie and I were happy to have more examples, and happy that Averianov & Lopatin’s interpretation of the NCRs agreed with ours.

And yes, Colin Boisvert, your groady perverted waaaay-too-abundant Allosaurus gets a look in. I hope you’re happy. Traitor.

What now? A short NYABPQ

(Not Yet Asked But Plausible Questions)

How do we know these things in sauropods and other dinos are ossified spinal cord supports and not some other wacky thing? I’d like to write a whole post on this, but in the meantime check out section 4.1 “Alternative hypotheses” on pages 14-16 of the new paper.

But what does it all mean? Section 4.2, “Functional implications”, has some half-baked ideas, but in truth we don’t know yet! We’re hoping someone else will figure that out.

What’s your favorite table in any paper ever? What an oddly specific and specifically flattering question, fictional interlocutor! The answer is Table 3 on page 17 of the new paper, in which we categorize the zoo of neural canal weirdness that we knew of when the paper went to press.

Wait — “that we knew of when the paper went to press”? What the heck does that obvious hedge mean? It means this rabbit hole goes all the way down, and we haven’t yet hit terminal velocity.

You’re kind of a weird dork, huh? Accurate!

I found NCRs in some critter in which they haven’t been documented yet — what should I do? Publish — publish! Jessie and I just spent six years getting this damned thing done and out, and we still have a shedload of weird neural canal stuff we haven’t even touched yet. We are the opposite of territorial, we’d strongly prefer for everyone and their dog to come play in our sandbox (not really ours but you know what I mean) and find lots of cool things and publish a million awesome papers and make neural canals the next hot thing. See Section 4.3, “Directions for future work”.

I haven’t found NCRs but I’d like to — what should I do? Go look in a bunch of neural canals. Seriously. That’s the gig. You might find some in the literature, but I wouldn’t count on a lot. You know who figures dinosaur caudals (1) in AP view (2) with the neural canals fully prepped (3) at sufficient detail to spot NCRs? Very few folks. At a reviewer’s request I spent some time plowing through a bunch of dino literature, and out of all the papers I checked, Susie Maidment’s stegosaur was the only new hit (Maidment et al. 2015, and kudos to Susie for the comprehensive illustrations). But someone who had access to a collection to ‘crawl’, logging all the NCRs, could do bang-up business. I know because that’s what Jessie and I did at Dinosaur Journey in 2018 and 2022, which is why there are so many MWC specimens in the new paper. Outside of Sauropoda we’ve found NCRs in Allosaurus, Ceratosaurus, Stegosaurus, and an indeterminate hadrosaur, and I don’t need to tell you that that is hardly a comprehensive survey of Dinosauria. We didn’t do more because we’re mortal and we wanted to get our sauropod paper out before it metastasized further, not because we were done, or even started, really. So if you want to discover new anatomy in dinosaurs, here’s a path with a very high likelihood of success.

What are you going to do next? The Greater Atterholt-Wedel Neural Canal Exploration Project (GAWNCEP) is still rolling, mostly under Jessie’s direction at the moment. As promised above, more weirdness is coming, watch this space. And when I’m not GAWNCEPtualizing, I, ahem, owe some folks some work on some projects. Just a few!

Special Thanks

Because you’re not supposed to thank your own coauthors in the acknowledgements: many thanks to Ron Tykoski and Tony Fiorillo for never giving up during the entire decade that it took to get from our first coauthored conference presentation to our first coauthored paper. Thanks to Femke and Tara for finding more NCRs and joining us on the paper, to John Yasmer for CT wizardry, and to Thierra Nalley for 3D recon wizardry and for being our resident non-sauropod vertebra expert. Y’all are great folks and it’s a pleasure to share the byline with you.

At a crucial point in this project I needed a translation of Dingler (1965), which is was only available in German. I hired my son, London Wedel, then a high school senior taking German 4, to translate it. That translation will go up on the Polyglot Paleontologist at some point, but in the meantime you can get it here (Dingler 1965 bird spinal cord paper (translation)) and at the hyperlink in the references below. London just started classes at European University Viadrina Frankfurt (Oder), pursuing his long-held dream of attending university in Germany, and I couldn’t be prouder.

David Wake was the lecturer for the evolution course in my first semester at Berkeley. I invited him to serve on my qualifying exam committee because I knew he would terrify me into working my butt off — not, I must clarify, because he was a terrifying person, but because the depth and breadth of his erudition intimidated the crap out of me. I invited him to serve on my dissertation committee for the same reason. He always pushed me to think more broadly — in time, space, development, function, phylogeny, and evolution. Those seeds didn’t all germinate right away, but I can see that a lot of my intellectual range now is a result of his example and his prodding back then. I never had the opportunity to collaborate with David directly, but I get immense satisfaction from the fact that this entire project was born out of a suggestion of his. My coauthors Jessie Atterholt and Tara Lepore are also proud Berkeley grads, and we’re all happy to dedicate the new paper to the memory of David Wake.

References

• Atterholt, J., & Wedel, M. J. (2022). A computed tomography-based survey of paramedullary diverticula in extant Aves. The Anatomical Record, 306(1), 29–50. https://doi.org/10.1002/ar.24923
• Atterholt, J., Wedel, M.J., Tykoski, R., Fiorillo, A.R., Holwerda, F., Nalley, T.K., Lepore, T., and Yasmer, J. 2024. Neural canal ridges: a novel osteological correlate of postcranial neuroanatomy in dinosaurs. The Anatomical Record, 1-20. https://doi.org/10.1002/ar.25558
• Averianov, A. O., & Lopatin, A. V. (2020). An unusual new sauropod dinosaur from the Late Cretaceous of Mongolia. Journal of Systematic Palaeontology, 18(12), 1009–1032.
• Ceylan, D., Tatarlı, N., Abdullaev, T., Şeker, A., Yıldız, S. D., Kele¸s, E., Konya, D., Bayri, Y., Kılıç, T., & Çavdar, S. (2012). The denticulate ligament: Anatomical properties, functional and clinical significance. Acta Neurochirurgica, 154, 1229–1234.
• Curry Rogers, K. (2009). The postcranial osteology of Rapetosaurus krausei (Sauropoda: Titanosauria) from the Late Cretaceous of Madagascar. Journal of Vertebrate Paleontology, 29, 1046–1086.
• D’Emic, M. D. (2013). Revision of the sauropod dinosaurs of the Lower Cretaceous Trinity Group, southern USA, with
  the description of a new genus. Journal of Systematic Palaeontology, 11(6), 707–726.
• Dingler, E. C. (1965). Einbau des Rückenmarks im Wirbelkanal bei Vögeln [Positioning of the spinal cord in the vertebral canal in birds; in German]. Verhandlungen der Anatomischen Gesellschaft, 115, 71–84. (Dingler 1965 bird spinal cord paper (translation))
• Maidment, S. C. R., Brassey, C., & Barrett, P. M. (2015). The postcranial skeleton of an exceptionally complete individual of the plated dinosaur Stegosaurus (Dinosauria: Thyreophora) from the Upper Jurassic Morrison Formation of Wyoming, USA. PLoS One, 10(10), e0138352.
• Skutschas, P. P. (2009). Re-evaluation of Mynbulakia Nesov, 1981 (Lissamphibia: Caudata) and description of a new salamander genus from the Late Cretaceous of Uzbekistan. Journal of Vertebrate Paleontology, 29(3), 659–664.
• Skutschas, P. P., & Baleeva, N. V. (2012). The spinal cord supports of vertebrae in the crown-group salamanders (Caudata, Urodela). Journal of Morphology, 273(9), 1031–1041.
• Taylor, M. P., Wedel, M. J., & Cifelli, R. L. (2011). A new sauropod dinosaur from the Lower Cretaceous Cedar Mountain Formation, Utah, USA. Acta Palaeontologica Polonica, 56(1), 75–98. https://doi.org/10.4202/app.2010.0073
• Wake, D. B., & Lawson, R. (1973). Developmental and adult morphology of the vertebral column in the plethodontid salamander Eurycea bislineata, with comments on vertebral evolution in the Amphibia. Journal of Morphology, 139(3), 251–299.
• Wedel, M. J., & Atterholt, J. (2023). Expanded neurocentral joints in the vertebrae of sauropod dinosaurs. In R. K. Hunt-Foster, J. I. Kirkland, & M. A. Loewen (Eds.), 14th Symposium on Mesozoic Terrestrial Ecosystems and Biota. The Anatomical Record, 306(S1), 256–257.
• Wedel, M. J., Atterholt, J., Dooley, A. C., Jr., Farooq, S., Macalino, J., Nalley, T. K., Wisser, G., & Yasmer, J. (2021). Expanded neural canals in the caudal vertebrae of a specimen of Haplocanthosaurus. Academia Letters, 911. https://doi.org/10.20935/AL911

Source: https://svpow.com/2024/08/29/new-paper-atterholt-et-al-2024-on-neural-canal-ridges-in-dinosaurs/