Sunday, December 13, 2009

Spindle Neurons in Elephants and Dolphins: Convergent Evolution in Large-Brained Mammals?


Fig. 1 (Hakeem et al., 2009). Photomicrographs of VENs in the brain of the African elephant. A: VENs in frontoinsular cortex (area FI). Scale = 25 μm.

Spindle neurons, or Von Economo neurons (VENs), are a unique type of large, bipolar neuron found in layers III and V in the anterior cingulate cortex and the frontoinsular cortex of humans. In 1999, Nimchinsky and colleagues discovered that among the 28 nonhuman primate species they examined, only great apes had VENs (see Spindle Neurons: The Next New Thing?). Primate cerebral cortex (generally) consists of six layers, and the VENs and other large pyramidal cells in layer V are projection neurons. VENs are also seen in humpback, fin, sperm, and killer whales (Hof & Van der Gucht, 2007).

More recently, spindle neurons have been found in elephants (Hakeem et al., 2009) and cetaceans such as the bottlenose dolphin, Risso’s dolphin, and the beluga whale (Butti et al., 2009).



Fig. 3 (Hakeem et al., 2009). VEN-containing regions of the elephant brain indicated on coronal section outlines. The locations of the sections are indicated by the vertical lines on the inset tracing of the medial aspect of the brain. The left hemisphere is on the left side of the figure. A: VENs in a dorsolateral [DL] frontal cortical area. B: VENs were present in subgenual [SG] anterior cingulate cortex (ACC)... C: Area FI [frontoinsular], in which VENs were abundantly present. Scale = 1 cm. DM = dorsomedial.

In elephants, VENs are located not only in ACC and FI, but also in dorsolateral frontal cortex. In cetaceans they can also be found in frontopolar cortex, as in humpback whales (Hof & Van der Gucht, 2007). According to Hakeem and colleagues:
The VEN morphology appears to have arisen independently in hominids, cetaceans, and elephants. The VEN specialization may parallel the emergence of very large brain size in these mammals. The evolution of large brain size may place a special premium on overcoming geometric constraints to maintain rapid transmission of crucial information, and this need may explain the independent emergence of the VENs in these species. There are a few mammals apart from hominids, cetaceans, and elephants that have brains somewhat larger than the apes. It would be interesting to determine whether or not these mammals, such as the giraffes and hippopotamuses, have VENs in parts of the brain corresponding to FI and ACC. If they are present, it would suggest that the VEN morphology may be primarily related to absolute brain size. If not, it would suggest that the VENs may be related to behavioral specializations common to hominids, whales, and elephants.
That's the more measured interpretation, because the abstract says:
The VEN morphology appears to have arisen independently in hominids, cetaceans, and elephants, and may reflect a specialization for the rapid transmission of crucial social information in very large brains.
As of now, the projection targets of the layer V spindle neurons are unknown, but are speculated to include (Butti et al., 2009):
...projections to subcortical regions, such as the amygdala, hypothalamus, and periaqueductal gray, to which the ACC and FI/AI are known to project in primates. Altogether, VENs may be involved in the integration of emotions, vocalization control, facial expression, or social conduct as well as regulation of autonomic visceral, olfactory, and gustatory functions.
Interestingly, another recent paper looked at convergent patterns of adaptive evolution in elephant and human ancestries (Goodman et al., 2009) -- see The Convergent Brains of Humans and Elephants.

References

ResearchBlogging.org

Butti, C., Sherwood, C., Hakeem, A., Allman, J., & Hof, P. (2009). Total number and volume of Von Economo neurons in the cerebral cortex of cetaceans The Journal of Comparative Neurology, 515 (2), 243-259 DOI: 10.1002/cne.22055


Goodman, M., Sterner, K., Islam, M., Uddin, M., Sherwood, C., Hof, P., Hou, Z., Lipovich, L., Jia, H., Grossman, L., & Wildman, D. (2009). Phylogenomic analyses reveal convergent patterns of adaptive evolution in elephant and human ancestries. Proceedings of the National Academy of Sciences 106:20824-20829.

Hakeem, A., Sherwood, C., Bonar, C., Butti, C., Hof, P., & Allman, J. (2009). Von Economo Neurons in the Elephant Brain The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, 292 (2), 242-248 DOI: 10.1002/ar.20829

Hof PR, Van Der Gucht E. (2007). Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anatom Rec Part A, 290:1-31.

Nimchinsky EA, Gilissen E, Allman JM, Perl DP, Erwin JM, Hof PR. (1999). A neuronal morphologic type unique to humans and great apes. Proc Natl Acad Sci 96:5268-73.


Fig. 5 (Hakeem et al., 2009). The phylogenetic distribution of the VENs. Species in which VENs have been observed are indicated by underlines; species which have been examined and found to possess no VENs are indicated by italics. Note that while the African and Indian elephants have VENs, they share this trait only with other large-brained groups (the cetaceans and humans/great apes) and not with their nearest relatives, the rock hyrax, manatee, giant elephant shrew, and tenrecs.

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4 Comments:

At December 14, 2009 10:13 AM, Blogger Tantalus Prime said...

How coincidental... One of the qualifying exam questions I was given this summer was on the link between Von Economo neurons and social behavior. Whoever wrote the question must have had Hakeem et al in mind.

Not the question I chose to answer, but perhaps the one I should have gone with.

 
At December 19, 2009 3:08 AM, Blogger Neuroskeptic said...

Fascinating stuff!

 
At December 21, 2009 12:05 AM, Anonymous P. Jennings said...

This is sort of old, took me a while to go find it.

Behavior like that which is described in the article (brief excerpt below, full text at URL) seems to me to validate the idea of spindle neurons and their functions.

In brief - humpback whale was trapped and effectively tied up tight by crab traps, etc. Humans come to the rescue --

"Moskito and three other divers spent about an hour cutting the ropes with a special curved knife.

"The whale floated passively in the water the whole time, he said, giving off a strange kind of vibration. 'When I was cutting the line going through the mouth, its eye was there winking at me, watching me,' Moskito said. 'It was an epic moment of my life.'

"When the whale realized it was free, it began swimming around in circles, according to the rescuers.

"Moskito said it swam to each diver, nuzzled him and then swam to the next one. 'It seemed kind of affectionate, like a dog that's happy to see you,' Moskito said. 'I never felt threatened. It was an amazing, unbelievable experience.'"

Article at:
http://www.sfgate.com/cgi-bin/article.cgi?f=/c/a/2005/12/14/MNGNKG7Q0V1.DTL

 
At December 21, 2009 10:40 PM, Blogger The Neurocritic said...

Thanks for the link, P. Jennings. That does sound like an awesome experience for the divers.

 

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