Comparative histological study of reinforced area of saccular membrane in mammal

Igarashi, M.

English

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Research Report 
COMPARATIVE HISTOLOGICAL STUDY OF THE REINFORCED 
AREA OF THE SACCULAR MEMBRANE IN MAMMALS" 
Makoto lgarashi 
With the technical assistance of 
Samuel M. Lansdon, Glenda J . Sessions, and Constance N . Coulter 
Bureau of Medicine and Surgery 
Subtask 1 Report No. 101 
Project MR005.13-6001 
NASA Order No. R-93 
Approved by - Released by 
Captain Ashton Graybiel, MC USN Captain H. C. Hunley, MC USN 
Director of Research Commanding Officer 
14 October 1964 
"This research was conducted under the sponsorship of the Office of Life Science 
Programs, National Aeronautics and Space Administration. 
U. S. NAVAL SCHOOL OF AVIATION MEDICINE 
U. S. NAVAL AVIATION MEDICAL CENTEB 
PENSACOLA, FLORIDA 
SUMMARY PAGE 
THE PROBLEM 
The reinforced area of the saccular membrane i s  probably a structure protecting 
the macular end organ. An attempt has been made to investigate and compare this 
structure microscopically in 65 mammalian inner ears, including those of man. 
FINDINGS 
A definite reinforced area of the saccular membrane existed in al l  of the human 
ears examined. I t s  existence was also demonstrated in a l l  of the squirrel monkey ears 
studied; however, some of these showed narrow or questionable formations. The ears 
of al I the four-legged mammals investigated, on the other hand, showed no reinforced 
area except those of the flying squirrel. It i s  possible that, as a stimulus receptor, the 
function of the saccule in primates differs from that of the saccule in lower mammals. 
ACKNOWLEDGMENT 
Grateful appreciation i s  expressed to Captain Ashton Graybiel , MC, USN , 
for his warm support. 
.. 
I I  
. 
* 
INTRODUCTION 
The reinforced structure at the anterior part of the saccular membrane was f i r s t  
described by Perlman in 1940 (4), and he termed it a "differentiated reenforced area 
of the saccular wal I .I' Because of the presence of t h i s  area in man and i t s  absence in 
the lower mammalian forms he examined, Perlman suggested that the saccule i n  man 
may have a function different from that in lower mammalian forms. In other words, the 
experimental findings in  these lower forms of an acoustic function for the saccule in- 
dicated to him that these findings might not hold for man or the monkey Macacus rhesus. 
Also, Perlman stated i t  w u l d  be more reasonable to expect that "this differentiated 
area of saccular wall in man has a functional significance and that i t does not represent 
merely a support for a few extremely small blood vessels." These anatomical findings 
were later conf irmed by Bast and Anson (1). 
-
The present study i s  an extension of those previous ones but differs in that it i s  
concerned primarily with a lower primate. Because the squirrel monkey i s  used exten- 
sively in the study of vestibular function, a comparative histological investigation was 
performed using mainly the Saimiri sciureus, a species of South American monkeys 
which i s  a definitely l o w e r x n t h e a c a c u s  rhesus, an Old World monkey. -
MATERIAL AND METHODS 
A total of 65 temporal bones were examined. These consisted of 36 squirrel monkey 
ears, 10 human ones, 7 ears from cats, 4 from guinea pigs and from rats, and two ears 
from dogs and from flying squirrels. 
Al l  temporal bones were fixed (most of the animals were intravitally perfused), 
decalcified, neutralized, dehydrated, embedded in celloidin, and serially sectioned 
in horizontal plane at 20 microns. One of each ten sections was stained in hematoxylin- 
eosin or hematoxyl in-phloxine and investigated microscopical I y . 
RESULTS AND DISCUSSION 
As can be seen from Table I, which summarizes the findings, al l  10 human ears 
showed an evident reinforced area at the anterior one third of the saccular membrane. 
This reinforcement was  an extension of the connective tissue between two epithelial 
cell layers from the anterior margin of the saccular membrane (Figures 1,2). Small 
blood vessels were sometimes observed in this area, especially in young and in fetal 
inner ears. 
This reinforced area i s  quite probably a protective structure. It may be protecting 
the saccular end organ from excessive or intensive perilymphatic displacement, especially 
from the anterior edge of the footplate. More extensive displacement of the footplate i s  
suspected at that point from the anatomical features of the annural ligament and stapedial 
tendon. When rupture of the saccular membrane, either pre or p o s t  mortem, i s  observed 
in  human temporal bones, it i s  not in the reinforced area (Figure 3). 
1 
Table I 
Incidence with which a Reinforced Area of the Saccular Membrane 
Was Found in 65 Mammalian Ears 
~ ~~ ~~ 
Reinforced Area 
Number Short, Narrow, 
Anima I of Ears Evident or Thin Quest ionabl e Negative 
Human 10 10 0 0 0 
Squirrel monkey 36 13 19 4 0 
Cat 7 0 0 0 7 
Dog 2 0 0 0 2 
Guinea pig 4 0 0 0 4 
Rat 4 0 0 0 4 
Flying squirrel 2 2 0 0 0 
Microphotographs representative of the findings in the squirrel monkey ears (Table 
I) are seen in Figures 4-8. An additional observation in a rhesus monkey ear (not part 
of the present study) confirmed Perlman's finding (4) of a well-defined area in this 
particular species. A questionable reinforcement of the saccular membrane in the 
squirrel monkey which was found in 4 of the 36 ears examined may be due to an Infra- 
order difference in the animal kingdom. 
South American monkeys, such as the Saimiri sciureus, belong to the lnfraorder 
Platyrrhini and are distinguishable by the lateral opening of their nostrils. Old World 
monkeys, such as Macacus rhesus, apes, and men, belong to the definitely higher Infra- 
order Catarrhini w - n a  opening dow ward. The biological classification of 
experimental animals, especially in functiona researches, should be submitted for more 
careful consideration. 
2 
. 
The ears of the two-legged mammals investigated, which have unstable head 
positioning against the gravitoinertial forces, as a rule contained the reinforced area. 
Of the ears from four-legged animals that were examined, only those of the flying 
squirrel showed a reinforced area (Figure 9). It i s  interesting to recognize that this 
animal makes very sudden stop and start movements, both horizontally and vertically, 
as well as a gliding movement. The negative reinforcement of the saccular membrane 
in cat ears (Figure 10A,B) i s  typical of that seen in  the other four-legged animals. 
After Perlman's suggestion (4) of an acoustic function for the saccule in lower 
animals, McCabe and Lawrence (3) found saccular lesions along with cochlear lesions 
in guinea pig ears after extensive acoustic stimulation. The noise levels used were 
150 db and 136 db above 0.0002 dyne/cm2 level, for twenty minutes, and the saccular 
or otolithic membrane lesions were observed in 23 out of 26 animals. In each case the 
other vestibular labyrinth remained intact. 
locus minosus. Also, the degree of the saccular damage was parallel to the cochlear 
damage. 
The saccule seemed definitely the vestibular 
A cat that had been exposed to exceptionally severe and repeated head blows was 
reported by Schuknecht and Davidson (8) to have had saccular collapse. The remain- 
ing nine cats studied, but not exposed to the same head blows, showed no vestibular 
end organ damage at al I. 
No saccular lesion was observed in three human cases of stimulation deafness 
reported by Igarashi,Schu knecht,and Myers (2). Two of the individuals had histories 
of exposure for Ion periods of time to extremely high intensity noise (well over 120 db 
re 0.0002 dyne/cm ), such as that caused by riveting machines in small compartments 
and boilers of ships. The other person had a history of severe head trauma from falling 
down a fl ight of stairs. The severity of the stimulation might differ between humans 
and experimental animals, but the difference among the different species cannot be 
neglected since, in man, cochleo-saccular degeneration has been observed after inner 
ear infection , in congenital malformation, and presbyacousis (6,7). 
9 
3 
. 
REFERENCES 
1. Bast, T. H., and Anson, 8. J., The Temporal Bone and the Ear. Springfield, 1 1 1 . :  - ---- 
Charles C Thomas, 1949. 
2. lgarashi, M., Schuknecht, H. F., and Myers, E. N., Cochlear pathology in 
humans with stimulation deafness. J .  Laryng., - 78:115-123, 1964. 
3. McCabe, B. F ., and Lawrence, M., The effects of intense sound on the non-auditory 
labyrinth. - Acta otolaryng., Stockh., - 49:147-157, 1958. 
4. Perlman, H. B., The saccule. Observations on a differentiated reenforced area of 
the saccular wal I in man. Arch. Otolaryng . , - 32678-691, 1940. -
5. Romer, A .  S., The - Vertebrate Body. Philadelphia: W. B. Saunders Co., 1949. 
6. Schuknecht, H. F., Benitez, J., Beekhuis, J., Igarashi, M., Singleton, G., and 
Ruedi, L., The pathology of sudden deafness. Laryngoscope, - 72:1142-1157, 
1962. 
7. Schuknecht, H. F., Igarashi, M., and Gacek, R. R., Cochleo-saccular 
degeneration. Submitted for publication to - Acta otolaryng ., Stockholm. 
8. Schuknecht, H . F., and Davison, R. C., Deafness and vertigo from head injury. 
Arch. Otolaryng . 63513-528, 1956. - - 
4 
. 
Figure 1 
Showing the reinforced a rea  at  the anterior part  of the saccular 
membrane. Human adul t .  AI  I black arrows, appearing in this 
f igure and subsequent microphotographs, indicate the posterior 
end  of the reinforced a r e a .  70 x 
5 
Figure 2 
Showing rather thin re inforced areas  from another  human a d u l t  e a r .  
70 x 
6 
P 
,Af' 
' 
Figure 3 
Demonstrating the rupture of saccular membrane which usually occurs 
at the posterior part (broad white arrow). Human adult. The ruptur- 
ing edge usually curls up. 70 x 
7 
Figure 4 
Showing a relatively thick reinforced area in a squirrel monkey. 
Otolithic membrane preservation i s  good in this case. 80 x 
8 
Figure 5 
Showing a fairly thick, but narrow reinforced area in another 
squ irre I rnon key. 130 x 
9 
Figure 6 
Shows a wide, but thin, reinforced area in a squirrel monkey. 
Normal saccular macula and otolithic membrane. 80 x 
10 
Figure 7 
Another thin reinforced a r e a  in a squirrel monkey. Normal saccular 
macula and  otolithic membrane. Note the  saccular  nerve goes through 
the bony lamina rather anteriorly to the saccular  macula,  and turns 
posteriorly. 80 x 
F: Footplate of t he  stapes 
1 1  
Figure 8 
Very narrow and questionable reinforcement of the saccular membrane 
in a squirrel monkey. Saccular end organ i s  normal. 
V: Utriculo-endolymphatic valve (or fold) 
80 x 
12 
Figure 8 
Demonstrating the reinforced area in a flying squirrel. The saccular 
mccula is severely damaged from post-mortem degeneration and 
otolith membrane is  dislocated. 70 x 
F: Concave footplate of the stapes 
0: Otolithic membrane 
I 
13 
Figure 10 A 
Figure 10 
Figure 10B 
A and B: Negative reinforcement of the saccular membrane in a cat. 
Normal saccular end organ. 1OA - 80 x 
Fig. 10 B is a high power view of Fig. 10 A. 150 x 
14 


Comparative histological study of the reinforced area of the saccular membrane in mammals

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