the oral apparatus of rodents

The Oral Apparatus of Rodents:Variations on the theme of a

Gnawing Machine

Robert E. Druzinsky

Dept. of Oral Biology, College of Dentistry, University of Illinois at Chicago

Mastication in Rodents

• Sciurids retain “primitive” tribosphenicmammalian pattern (Butler, 1984)

• Many rodents retain basic lateral-medial, anteriorly directed power stroke

• Propalinal chewing not primitive – has evolved many times independently

• “Bi-lateral” chewing uncommon, if it occurs at all

Frontal view of one chewing cycle in Aplodontia

“Bilateral” chewing in Cavia (guinea pig) Byrd, 1984

4 “types” of rodent masticatory muscles

• Historically, sub-orders of the Rodentia have been based on these “types” of masticatory muscles

• Do the “types” of rodent masticatory muscles represent biomechanical strategies for the production of jaw

closing forces during chewing?

Landry, 1999

Protrogomorph Sciuromorph

Hystricomorph Myomorph

Wood, 1974

The moment arm of the adductor muscles is relatively longer in sciuroidea than in the protrogomorph, Aplodontia.

Removal of the anterior masseter makes the species similar

The Rodent Masticatory Complex

• A functional complex for propalinal chewing movements?

• NO!

Rodents are all GNAWING MACHINES

What are the requirements of a gnawing machine?

To gnaw, incisors must be sharp

• How do mammals make sharp incisors?

Some primates have very little enamel on the lingual surface of the central

incisors

These teeth are tools that sharpen themselves through use –

Self-sharpening incisors

Shellis and Hiiemae, 1986

Lev Tov Chatta et al., 2010

Hogg et al., 2011

Many texts describe the incisors of rodents (and lagomorphs) as

“self-sharpening”

BUT THEY ARE NOT

• Glires actively sharpen upper and lower incisors

Rodents Gnaw

• A mechanical complex for gnawing with specializations of the

– Jaws

– Jaw joints

– Incisors

Diastema

Loss of lingual enamel

Glires

Rodentia

Lagomorpha

Continuously

erupting incisor

Synapomorphies of Glires

Specializations of the Jaws

• Large diastemata that separate the cheek teeth from the incisors

Diastema

Separation of functions of incisors and cheek teeth

Specializations of the Incisors

• Loss of lingual enamel• Ever-growing

Specializations of the Jaw Joint

• Loss of the articular eminence

Articular Eminence

Scapino, 1997

Lagomorphs have an

articular eminence but no

bony glenoid fossa

Rodents have lost

the articular

eminence

Diastema


Glires

Rodentia

Lagomorpha

Loss of second upper incisor

Loss of articular

eminence

Continuously

erupting incisor

Synapomorphies of Rodents

Ends of wear facets represent the limits of excursion of the lower incisors

Tip of the lower incisor wears the lingual dentin of the upper incisor

Tip of the upper incisor wears the lingual dentin of the lower incisor

How to measure sharpness?

1. Radius of curvature

Rodent: Paraxerus veillarius

Radius of Curvature

A-P width

𝐴 = 𝜋𝑟2

𝑟=𝐴

π

Lagomorph: Pronolagus randensis

Radius of Curvature

A-P width

𝐴 = 𝜋𝑟2

𝑟=𝐴

π

Hypothesis:

Rodents and lagomorphs should be able to sharpen the upper

incisors equally well

But

Rodents should have

sharper lower incisors

than lagomorphs

0 1 2 3 4 5 6

0.02

0.04

0.06

0.08

0.10

0.12

0.14

0.16

0.18

0.20

0.22

R

R

R

L

LL

LLL

L

L

L

LL

L

L

LL

L

R R

R

R

RR

RR

R

R

R

R R

R

R

R

Upper Incisors

Sca

led

Ra

diu

s (

r/W

)

AP Width (mm)

t=-1.89515

p=0.0666

Sca

led

Ra

diu

s (

r/W

)

AP Width (mm)

0 1 2 3 4 5 6

0.00

0.05

0.10

0.15

0.20

0.25

0.30

0.35

0.40

RRRR

LLLL L

L

LL

L

L

LL

LLL

LLL

RR R

RRR

R

R

RR RR R

R

R R

Lower Incisors

t= -2.61424p= 0.01298

How to measure sharpness?

1. Radius of curvature

2. How much tooth (dentin) is removed?

Tip

Shaft

Amount of Material Removed

Lepus (Lagomorph) 36.4%Cavia (Rodent) 60.0%

Lower Incisors of Rodents are Sharper than those of Lagomorphs

Procumbent Incisors

Mechanical properties of incisors

• Is sharpness the only thing that is important?

Similar to tungsten carbide chisels

Osborn, 1969

Linear actuator mounted in a µCT

Three “types” of incisors compared in mice

• Wild type

• Sprouty transgenic (SPRY 2+/-,4-/-)

• Amelogenin knock out transgenic (AMELX -/-)

“Sprouty tooth” – lingual enamelAmelogeninKnock-out

No enamel

Labial surfaces

“Wild type tooth” – no lingual enamel

Micro-CT AP Slices

A B C

Labial Lingual

Wild Type Sprouty AmelogeninKO

Incisors Loaded in Compression

• Approx. 4 micron voxels

• Image stacks imported into Avizo as binary files

• Incisors scanned unloaded and at 15 microns and 30 microns of compression

• Surface renderings created in Avizo comparing unloaded and 30 micron scans

Wild type incisor

Distance map

36µm

27µm

Spry incisor

Sprouty incisor

Deformation in Axial Loading

Wild Type – no lingual enamel Amelogenin KO – no enamel

0 20 40 60 80 100

100

200

300

400

500

600

700

800

Ba

se

to

Tip

Difference in Microns

0 20 40 60 80 100

100

200

300

400

500

600

700

800

Ba

se

to

Tip


Asymmetrical phenotype in some Sprouty individuals

Deformation in Axial Loading

0 20 40 60 80 100

100

200

300

400

500

600

700

800

Ba

se

to

Tip


0 20 40 60 80 100

100

200

300

400

500

600

700

800

Ba

se

to

Tip


Spry – lingual enamel Spry – no lingual enamel

Sprouty incisor

“Wild-type” incisor

Brassey et al. 2013

Figure 10.

Von Mises stress under

bending loading regime.

J. R. Soc. Interface

Loading to Catastrophic Failure

0

20

40

60

80

100

120

140

160

8196

7693

Co

mp

ress

ion

(in

mic

ron

s)

Sprouty

Normal

Incisors of Rodents are

• Sharp –

– Oral apparatus allows sharpening movements

– Tungsten-carbide chisel model

• Flexible - Mechanically tough?

– The sharp tips can be driven into an object and then they bend rather than break

Loss of the Articular Eminence

• Allows rodents to sharpen lower incisors

Extant rodents represent 2000+ variations of the basic gnawingmachine

Co-workers:Weizmann Institute of Science, Israel

• Gili Naveh• Steve Weiner• Vlad Brumfeld

Univ. of California, San Francisco• Cyril Charles (ENS de Lyon, France)• Ophir Klein

Univ. of Illinois, Chicago• Hannah Koeppl• Tom Diekwisch• Xianghong Luan• David Reed

Charles et al., 2011

Spry1 −/−;Spry2 −/− embryos do not form a glenoid fossa.

But the condyle and articular disc is essentially normal

.

Purcell, P., Jheon, A., Vivero, M. P., Rahimi, H., Joo, A., & Klein, O. D. (2012). Spry1 and spry2 are essential for development of the temporomandibular joint. Journal of Dental Research, 91(4), 387-393

Jheon et al., 2012 WIREsDevBiol Figure 2

• In a typical mammalian tooth enamel covers the surface of the crown

h

Clemente, 2010

Xradia Micro XCT-400

Klein et al., 2008

Sprouty Mice

• Enamel on the lingual surface of the incisor

Diastema


Glires

Rodentia

Lagomorpha

Loss of second incisor

Loss of articular

eminence

Continuously

erupting incisor

Specializations of the Incisors

• Loss of lingual enamel• Ever-growing

• Rodents have a single central incisor

Diastema


Glires

Rodentia

Lagomorpha

Loss of second incisor

Loss of articular

eminence

Continuously

erupting incisor