studies on the functions and fiber connections of the amygdaloid nuclei and periamygdaloid cortex....

Folia Psychiatrica et Neurologica Japonica Vol. 6, NO. 2, 1952.

STUDIES ON THE FUNCTIONS AND FIBER

AND BERIAMYGDALOID CORTEX. EXPERIMENTS ON GASTROINTESTINAL MOTILITY AND

BODY TEMPERATURE IN CAT

CONNECTIONS OF THE AMYGDALOID NUCIAEI

% Haruyoshi Koikegami, Hiroshi Kushiro

and Atsushi Kimoto

(Department of Anatomy, Ni iga la University School of Medicine)

Experiments on the miygdaloid complex of the cnt and rabbit in our laboratory have shown that the main amyydaloid nuclei and surrounding cortex are associated with the respiratory movements (29 . Further observation made i t possible to say that certain nuclear group of the amygdaloid complex is really referred to the vegetative function in several respect. The present article is devoted to an anslysis of experiments concerning body temperature and gastrointestinal motility in cat.

I. Results on body temperature

A s to the reguhtory centre of the body temperature a number o f researches have been presented ever since the famous experiment o f ilYo)Jsot2 and Snrizs I 18851 who recognized elevation of the tempzriture of the animal body produced by puncturing the anterior part of the c:iudate nucleus. Experimental results reported by O t t (1884 89 . Ricliet i18851. Wlii ie i1890), Brunin)i i1929) a. 0. a reno t inconip.itible with the result of Aroiisohn and Snclzs, while some aiithors. nsmely Christinrii ~1885)~ Riclzei \ 18851, Bnculo (1890), i lzscmint 119Wi, Sirecrnth (19101 a. 0. indicated the thalamus opticus ;IS another effective area and other authors as Eztlekiburg rind Lniidois f 1876 I , W h i t e (1891 I a. o recognized hyperthermia in case of 1w:ilized cortical lesion. Attentims were, however, concen- trated recently upon the hy-aothalmius by niriny authors, for example f sciischiizicl ind S c l z t ~ i ~ z l c r I 19141, Rn)iso)z et 31. I 1935-431, h'nrplzts and Krc id l (1909 11 I , h-uroiszc et al. i 1938 401, Bnzei t , A l p e r s and E r b (19331, Frnzier , A l p e r s and Leicig 119361 etc.

We recognized alteration of the body temperature through electrical or chemical stimulation of a limited part of amygddla in the

~~~ ~ ~ ~ ~~ ~

heceived for publication, June 30, 1952.

Amygdaloid Nuclei and Periamygdaloid Cortex 77

I No. 5 38.2 36.0 36.6 NO. 6 38.1 37.0 37.5 No. 7 38.0 37.0 37.7 No. 20 38.5 38.2 33.3 NO. 29 38.0 36.7 -

cat. The grade of temperature change is almost the same as in the stimulation cases of hypothalamus.

Before operation rectal temperature has been taken 2 or 3 times daily for several days to determine the standard temperature. To avoide effect of operative procedure, the skull in the lower part of the temporal bone war opened preliminarily in extension of about 1.5 to 2cm. to be ready for insertion of electrode. Two or three days later, namely, after recovery of the animal to ordinary condition, the amygdaloid region was electrically or chemically stimulated as described in the previous papers (29, 55). We used simply Porter's inductorium of 2 or 4 volts power, at a coil distance of 7 to 10 cm mostly. The electrode used was an ordinary bipolar form completely insulated except for the tips or a bipolar silver electrode in form of injection needle. Duration of stimulation ranged from 20 to 6J seconds, with frequencies of 80 to 100 per second. The wound has been kept strictly antiseptic. Neither meningitis nor cerebral abscess has occurred in any of the experiments. The stimulated portion was investigated histologically by frontally cut celloidin series stained by Nissl's method. The normal temperature of cat shall be according to Shirai and Ando (1932) 37.6" to 39"5C, according to Matsuda (1949) as 38.5"C and according to Hasamsl (1929) commonly 37.4" to 38.3"C, ranging up to 38.9" and downward to36.5cC. Changesin temperature caused by the preliminary operation are recorded in Table I. Body temperature tends to fall by body fixation and during

No. 30 1 58.0

Table 1.

;7.7 37.71

operation, to regain rapidly normal height after operation and to rise then beyond the normal level. Alteration in temperature after this preliminary operation is less than 1°C. Influence of the second operation is meagre, as the reopening of the wound and removal of the celluloid plate overlapping the wound are quite easy. The insertion of the electrode is also ineffective. Through electric dis-

78 H. Koikegaini, H. Kushiro, and A. Kimoto:

No. 4 38.4 - 39.7 - 1 39.8 LO.?

so. ;- L 38.0, - 29.1

charge temperature gets lowered suddenly, to rise then hypernormsl gr*idually. In order to produce these changes stimulat'on of amyg- dd:i in one side was sufficient. Date of No. 4 13360 g , 5 ) , stimulated 3 times, each in 10 seconds duration with 30 seconds interval, 8cm coil distance and 2 volts power under 19" to 21'C room temperature, and that of Na. 5 1 %450g, 2 I , stimulated twice, each in 10 second3 duratim, 7.5cm coil distance and 2 volts power under 17°C rooni temperdture. are shown in Table 2 icf. also Fig. 1). The data of another examples are more or less akin to the above cases.

40.4 -

Fig. 1. Change in body temperature due to the preliminary operation and stimulation of amygdala in the cat, No. 5 (body weight 2450g. P ). Ahsciss. : number of days, ordinate: temperature ("C). Preliminary operation in the fourth day indicated with arrows A and B. Hourly temperature scala (1 6) following operation. The second operation in t h e seventh day performed a t C. Amygdala stimulated a t D. Hourly temperature scala (1-11 ) following stimulation.

The stimuldted nuclei and the d,imaged cortioal portion through electrode insertion in the amygdaldid region are shown in Tables 3, 4 and 5.


Case number

No. 4

5 11

12 14

17

18

19

22 29

33 34

40

*43 44

Degree of Amygdala Periamygdaloid Periamygda- rise of proper nuclei loid cortex Hippo- tempera- campus ture W ) M j TI 1 T I S , D i i + T p & j P a m : i P a m j I

- - I - - + + ) - 1 - - - - 1 - - 1 + I + I - - -

2.7 + + ft H I 1 ! - - * I + -

- +

2.4 - 1.6 + tt tt + ] * I - l - ~ - - ti+ tt +

- 1 + ; - , 1.8 + + - - - - - 2.6 + - - 1 - 1 - 1 2.0 + tt + - 1 . 6 , + + + I - ! - - - 1 + I + I - +

~~~

Degree of Amygdala

l tu re ni 1 T' 1 T Case rise of proper number tempera-

~~

Per:amygdaloid Periamygda- nuclei loid cortex Hippo-

B 1 D ~ E I K ,ParnllPam,:Pam:i I i campus

All in all, effect of the stimulation of the amygdaloid nuclei is expressed in rise in body temperature. I t reaches the maximum at 6 to 8 hours usually to become almost normal at 24 houxs. Accor- ding to its degree, alteration can be divided into three groups roughly :

1) Cases with tempzrature rise above 1.6'C are regarded as distinctly effective. Histologically, the lateral amygdaloid nucleus

No. 10 1.2 + ' + 1 - 1 - - - 20 1.0 * i - i - ~ - - 1 -

23 1 . 3 + + + * + - - 1 + 24 1.1 * - 1 - 1 - - I - 38 1.4 - - I + l + , - ' -

33 I.? + I + - - 1 - -

- - + - + I - - - + I + - 1 - - - * + - I -

80 H. Koikegami, H. Kushiro. and A. Kimoto:

Fig. 2. No. 34, A-issl-stain. .'11. XI: lateral nucleus. Pam, & Pam:: periamygdaloid cortex, Pu: putamen, S : stimulated portion. Tr. op: Tractus opticus. T': intermediate nucleus. T : medial nucleus of amygdala proper.

of amygdala proper (nucleus M of Volsclt) was found more or less affected through all examples. (See Table 3, and Figs. 2, 3 and 4) .

2, Cases with temperature rise from 1.0" to 1.5"C are regarded as slightly effective. In these cases the nucleus M was not stimulated so widely or not a t all. (Table 4 and Fig. 5 ) .

3) Cases with temperature rise below 0.9'C (Fig. 6) are summarized in Table 5. In No. 28, 36 and 42. the amygdaloid nuclei are damaged on one side through diathermy cauterization or mechanical lesion extensively (%Fig. 71. In one case [No. 26, not indicated in the ,table!, in which area entorhinalis intermedia of Rose was


Fig. 3. No. 29, Nissl-stain. x17. A small stirnulat-d lesion (S) in the lateral nucleus (M).

Fig. 4. No. 5, Nissl-stain. x10. A small hemorrhage in the veitro- medial part of the lateral nucleus (M). The intermediate nucleus (TI) partially affected. D : nucleus D of Volsch. Another abbreviations same as in Fig. 2.

82 H. Koikegami, H. Kushiro? and A. Kimoto:

Fig. 5. No. 35, Nissl-stain. i 8.5 The periampgdaloid cortex damaged by stimulation. The medial n x l e u s of amygdala proper (TI involved partially. E : cintral nu:leus. K : intercalated small-celled nucieus, Another abbreviations same as in Fig. 2.

Fig. 6. No. 7, Nissl-stain. .;7.5.

stimulated, tempiraturz rise stood a t 0.9‘C. Damage in the hippocsmpsl region took place in a few exception.

The periamygdaloid ares did not participate in temperature change.

2. Result on gastrointestinal motility

Concerning the effects on the gastrointestinal motility through stimulation of telencephwlon many researches were made since Bo- c h c f o n f n i n e (‘18761, but those induced through stimulation of amygdaloid nuclei have not yet been reported actually. We were able to


produce considerable effects especially on the gastric motility in the cat through electrical or chemical stimulation of the said nuclei on one side. By this experiment antisepsis was not perfect, because the animals were killed soon after the experiments. The final depth of electrode penetration was marked by means o€ a small electrolytic lesion. To the purpose of recording gastrointestinal motility a small rubber ball connected to a Nelaton’s catheter No. 5 was inserted into the cat’s stomach resp. small intestine. The inner pressure of this ball was made mesurable by manometer. When i t stands in adequate level, for example, in cases of stomach in 1) to 18cm H.0, i t is

Fig. 7. No. 28. Nissl-stain. x8.5. Hip: hippxampus.

Fig. 8 a. No. 49, right side. Nissl-stain. x17.5. S: lesion.

8.1 H. Koikegarni, H. Kushiro, and A. Kimoto:

Fig. 8 b. No. 49. ?dotion of stomach. Time signal in 6 seconds interval.

Fig. 9 a. NQ. 40. left side. Nissl-stain. 17. T h e stimulated par t marked with a large h morrhage.

Fig. 9 b. Time signal in G seconds interval.

No. 40. Inhibitory effect upon the motion of stomach.

Amygdaloid Nuclei and Periamygdaloid Cortex

Fig. 10a. No. 17. right side. Nissl-stain. x12.

Fig. 10 b. No. 17. The upper curve: the motion of stomach, Inhibitory effect. the lower: the motion of small intestine.

Time signal in I second interval.

induced to Marey’s tambour and further to the kymograph. Insertion of the rubber ball into the stomach takes place by way of esophagus, but in the case of small intestine opening of the abdomen comes needed. This makes naturally the interpretation of results in the latter case somewhat complicated.

As to the normal motion of the cat’s stomach, Ogaia (1952) discriminated two types, namely, a large and a small one, as are also observable here. The wave of the small motion is about 5 to 6 frequencies per minute and that of the large motion about 6 to 7

Tab

le

6.

I A

noth

er r

egiu

ns o

f s t

i mul

n ti

on

Sti

mul

ated

are

a

-- No.

N

o.

i N

o.

7

No

37

No

37

No.

.<

)

No.

40

No.

40

No.

45

No.

48

No.

48

No.

49

No.

51

No.

53

No.

54

I

left

le

ft

righ

t le

ft

(pos

teri

or p

art)

ri

ght

left

(a

n te

rior

par

t)

righ

t (a

nter

ior

par

t)

left

le

ft

left

(m

edia

l pa

rt)

rig

ht

righ

t le

ft

left

I

righ

t ~

(cm

. I

4 8

4 8

or

4 8

,

~-

I-

~

a~m

vg

dal

a Per

iam

ygda

- P

eria

myg

d.

1

prop

er

loid

nu

cle~

co

rtex

H

ippo

- P

uta

"

RI

T

'r' ~

15

+'+

* -

I -I+

+

-

*+

+-

8

or

5

n

8, 6

, or

4

8o

r

G

8, 6

. or

4

7, 4,

or 2

7 8 7

* + f

1 cam

pus1

m

en

I) R

Pam

l Pa

m:

Pam

. I

+

-

-1

-

-t

t-

-

++

- -

*

+-

- -

- - +

- - -

tt

-

- - +

-I

-

-

- +-

I-

- -

tt

-

f

+ +

-,

-

+ i

t+

--

tt

++

--

-

+~

*

+ - -

HI

+

-

Am ygdaloid Nuclei and Periamygdaloid Cortex 87

frequencies per 10 minutes. The respiratory effects can be seen as very small vibrations accompanying both types, and effects from the abdominal aorta were unrecognizable.

Our experiments on 40 cats reveal that impulse setting off from a limited part of amygdala inhibited or stopped completely the motion of stomach in some cases. The effect falls most evident in those cases summarized ;n Table 7. In these experiments we stimulated arnygdala twice or thrice on one side, when the first stimulation responded not so evidently. Details of each experiment ‘are entrusted to the tables appended. By examination of appropriate’sections in all these cases the medial nucleus of amygdala proper (T of Viilsch) was found affected. Stimulation of the lateral nucleus (M of Volsch) or of the intermediate nucleus (l” of V6lsch) of amygdala proper looks to remain ineffective (s. Table 8)- Experiments by the chemical substance are also the same (s. Table 9 and Fig. 11 a and bj. The

Fig. 11a. No. 30, right side. N i s s f stain. ~17 .5 . B : cortical nucleus ( B of Volsch). S: lesion

Fig. 11 b. No. 30. Inhibitory effect upon the motion of stomach (injection of sodium glutaminate into the amygdala). Time signal in 6 seconds interval.

88 H. Koikegami, H. Kushiro, and A. Kimoto:

Table

~ - 1 - Stimulus Case coil I Am ygdala number side (' part ' voltage distance ,J'ope'- ~

I -

(cm.) 1 hl T , T' ~~

K@. 5 right 4 8 t t + t t No. 38 - 8 o r 4 tt f + 7

right KO. "0 1 (anter isr par t ) I 2 8 t t f +

$ o r 2 - + f , (medial par t ) ~

xo. "9

Table

Stimulus Stimulated ~- -

Case coil A-mygdala PGiamXda-

(cm.) hl T T' E I D B 1 number side (& p a r t ) ' I voltage distance properp loid I

I

~- -

lef t

left No. ;7 (anterior par t ) 1 2 No. j8 right (antero-

lateral par t ) No. ;8 right ( a n t e r e

medial par t ) left

No. j0 (posterior part)l 2 1

left No. 4s (lateral par t ) 2

lef t No. 49 (lateral part)

I 8

1 8 * f + - I - , -

8

No 50 right No 53 right No. 52

No. 55 right 7 No. 55 left

stimulation of the periamygdaloid cortex exerts no inhibitory effect upon the mation of stomach is. Table 10). I n few cases, hippocampus and capsula externa were partially involved in stimulation, but never so profoundly.


7.

Stimulated area Another regions of stimulation - - ~ - Periamygda-i Periamygd. loid nuclei 1 cortex

E 1 D I B Pam1 1 Pam:!

8.

area ~ Another regions of stimulation

Periamygd. cortex

Pam:; Pam1 Pam?

tt

tt

+ -

+ * tt +

i f t I + 1 -

+ - -

+ + -

+ tt tt + + + -

Claust- r um

G!obus pallidus

Hippo- campus

To elucidate the neuronal connection with regard to this pheno- menon, we made several experiments of amygdala stimulation following its isolation from another regions. For instance, connection between the amygdala on one side and trigonum olfactorium, external

90 H. Koikegami, H Kushiro, and A. Kimoto:

Table

I 1 1 mol Stimulated amygdaloid

I na te (c. c.) I j h ! T T ’ l E ~ D B I

Case sodium number ~ side glutami- lelfect - ~

~~ ~ -- -~ - -- - ,

~ - - - ~ - ~ _ _ _ _ N3. 33 right 0.05 H i + * * - + - NJ. 45 right 0.1 No. 46 left No. 47 right No. 47 left

Table 10.

Another ragions

- 1- Capsula Hippo-

Id Stimulus ’ Stimulated area of I-- $ side

8 $ 5 (& part) voi- o c , (cm.) o,

coil distance Paml P z m ~ Pam; les te rna campus

No. 36 lef t (anterior Lart) 2 8 o r 5 *

No. 36 right 2 8 - # - - + + 8, 6, or 4 - t t f

N3. 51 right 2 7,4,or 2 - - + - - - No. 63 left 2 - i + + - - - -

capsule, hippocampus or area 13 of the orbital surface of the frontal lobe on the other side the inhibitory response to the gastric motility remained still recognizable upon stimulation of the amygdaloid region. After cutting the fornix or stria terminalis through the parietal region, stimulus upon the amygdaloid nucleus showed just the same. But, following destruction of the hypothalamus on one side, stimulation on the amygdala on the same side called no jnhibition forth.

From these expcriments it should readily be maintained that the neurons of the effective amygdaloid nuclius seem to give off their axons immediately t3 the center of the hypDthalamus of the same side.

For motility of the small intatine the same region of the amygdala stands seemingly also responsible, but the details will be preferably to dealt with in another paper with certain adjacent evidences drawn from subsequent expcrirnents.


9.

Tractus optic u s

~

- - - - +

Summary

Through electrical or chemical stimulation of a limited part of the amygdaloid complex unilaterally, elevation of temperature of the animal body and inhibition of the gastrointestinal motility can be recognized. By histological investigation of experlmented cases it was revealed that to the former effect the lateral amygdaloid nucleus of amygdala proper (M of Viilsch) and to the latteI the medial amygdaloid nucleus (T of ViiCsch) were precisely responsible. The periamygdaloid cortex stands definitely unparticipsted in these pheno- menon. Further it was conczivable that the impulse from the amygdala reaches to the visceroeffective center of the hypothalamus apparently without interruption of its neuronal connection to work inhibitory upon the gastrointestinal mDtility. These results certainly speak for our assumption that the amygdaloid complex comprises a link of the autonomic representation for regulation of visceral functions.

3)

4)

5)

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Amygdaloid Nuclei and Periarnygdaloid Cortex 93

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* Written in Japanese.

studies on the functions and fiber connections of the amygdaloid nuclei and periamygdaloid cortex....

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