A Myelin Map of Trunk Folds in the Elephant Trigeminal Nucleus

Author:

Reveyaz Noémie1ORCID,Schneeweiß Undine1,Heise Olivia1,Gerhardt Ben1,Gui Andreea M1,Kaufmann Lena V12,Alfken Jette3,Reichmann Jakob3ORCID,Salditt Tim3ORCID,Hildebrandt Thomas4,Brecht Michael15ORCID

Affiliation:

1. Bernstein Center for Computational Neuroscience Berlin, Humboldt-Universität zu Berlin

2. Berlin School of Mind and Brain, Humboldt-Universität zu Berlin

3. Institut für Röntgenphysik, Universität Göttingen Friedrich-Hund-Platz 1

4. Leibniz Institute for Zoo and Wildlife Research

5. NeuroCure Cluster of Excellence, Humboldt-Universität zu Berlin

Abstract

Elephants have elaborate trunk skills and large, but poorly understood brains. Here we study trunk representations in elephant trigeminal nuclei, which form large protrusions on the ventral brainstem. These ventral brainstem protrusions have previously been referred to as inferior olive, but a delineation of the olivo-cerebellar tract reveals these (trigeminal) nuclei are not connected to the cerebellum via climbing fibers. In contrast, the olivo-cerebellar tract connects to a large dorsolateral nucleus with a serrated cellular architecture, the putative elephant inferior olive. Dense vascularization and intense cytochrome-oxidase reactivity distinguish several elongated trigeminal putative trunk modules, which repeat in the anterior-posterior direction. We focus on the most anterior and largest of these units, the putative nucleus principalis trunk module. Module neuron density is low and non-neural cells outnumber neurons by ∼108:1. Dendritic trees are elongated along the axis of axon bundles (myelin stripes) transversing the trunk module. Synchrotron X-ray-phase-contrast tomography suggests myelin-stripe-axons transverse the trunk module. We show a remarkable correspondence of trunk module myelin stripes and trunk folds. Myelin stripes show little relation to trigeminal neurons and stripe-axons appear to often go nowhere; we suggest that myelin stripes might serve to separate trunk-fold domains rather than to connect neurons. Myelin-stripes-to-folds mapping allowed to determine neural magnification factors, which changed from 1000:1 proximally to 5:1 in the trunk finger. Asian elephants have fewer (∼640,000) trunk-module neurons than Africans (∼740,000) and show enlarged representations of trunk parts involved in object wrapping. The elephant trigeminal trunk module is exquisitely organized into trunk-fold-related units.

Publisher

eLife Sciences Publications, Ltd

Reference48 articles.

1. Vibrissae representation in subcortical trigeminal centers of the neonatal rat;Journal of Comparative Neurology,1979

2. The inferior olive. Notes on its comparative anatomy, morphology, and cytology;Olivocerebellar projection: a review,1980

3. Barrelettes without barrels in the American water shrew;PLoS One,2013

4. A star in the brainstem reveals the first step of cortical magnification;PloS one,2011

5. Mémoire sur les espèces d’éléphants vivantes et fossiles;Mémoires de L’institut National des sciences et arts,1796

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