Download PROJECTIONS OF THE AMYGDALOID BODY TO THE INSULAR

ACTA NEUROBIOL. EXP. 1984, 44: 151-158
PROJECTIONS OF THE AMYGDALOID BODY TO THE INSULAR
CORTEX IN THE CAT
Jwwz MORYS, Dawel SEONIEWSKI and Olgielenrd NARKIEWICZ
Jhparhmel~ztof Anatomy, Ilnstitut~eof M e d i d Biolsgy, Schotod of Meidicine
Dcbimki 1, 80-2Il1 Gd~alisk,PolLaaud
Key words: cortex, insid, ~llmygd~aloid
body, brain ~mcotICM1,cat
Abstract. Experiments were performed on brains of 15 cats with the
use of horseradish peroxidase (HRP) retrograde transport method. After
injections of HRP to the insular cortex, relatively great numbers of labeled neurons were found in all main nuclei of the amygdaloid body.
After injections to the anterior part of the granular insular cortex numerous labeled neurons were located in the lateral, central lateral, basal
dorsal and basal ventral nucleus of the amygdaloid body. Injections to the
agranular insular cortex labeled neurons in the lateral, basal dorsal and
basal ventral nucleus and in the claustrum prepiriforme. These results
indicate the presence of large projections from vast areas of the amygdaloid body to the agranular insular cortex and the anterior part of the
granular insular cortex.
The insular cortex is an area situated on the border between paleocortex and neocortex. In the cat the insular cortex is localized on the
surface of the anterior sylvian gyrus and below it in the rhinal sulcus
(Fig. 1). It is usually divided into agranular insular cortex, localized
around the rhinal sulcus and granular insular cortex lying mainly on
the surface of the anterior sylvian gyrus. There are two parts of the
insular granular cortex: anterior and posterior; that partition. seems to
have mainly topographical significance. In spite of some experiments
performed on the insular cortex, its role has not yet been strictly defined. The connections of the insular cortex are also relatively little
known. The existence of connections between the insular cortex and
amygdaloid body was proved in the post decade. They were investigated
in the rat (5, 7, 12, 16), cat (5, 7, 14), dog (4), rhesus monkey (1, 9, 15)
Fig. 1. Localization of the h l d a r ooa-tex
ion
the surface of the eat's brain.
and golden hamster (13). Most of the studies were concerned with
the descending, insulo-amygdaloid connections. Kosmal (4) investigated
the ascending, amygdalo-insular connections in the dog using the Nauta
degeneration method, Krettek and Price (5) in the rat and cat, with the
anterograde transport method. Mufson et al. (9) described both the
insulo-amygdaloid and amygdalo-insular connections in the rhesus monkey, Reep and Winans (13) - in the golden hamster. In studies on
amygdalo-insular connections in the cat the retrograde axoml transport
has not been used as yet, although this method enables a precise localization of neurons sending axons from the amygdaloid body to various
areas of the cortex.
METHODS
In 15 mature cats (2000-3500 g) surgery was performed under general anesthesia with Nembutal injected intraperitoneally in the dose of
30 mglkg body weight. Craniectomy was performed and the dura mater
cut over the appropriate area of the cerebral cortex. A glass micropipette was introduced stereotactically to the cortex and 30°/o solution of
horseradish peroxidase I(HRP; Sigma VI) was given in the amount of
0.20-0.50 pl. HRP was applied to the agranular insular cortex (4 animals),
the posterior part of the granular insular cortex (3 animals), the anterior
part of the granular insular cortex (4 animals) and to adjoining cortical
areas (4 animals). 24-48 h after surgery the animals were reanesthetized
and perfused according to Mesulam and Rosen method (8). Brains removed from the skull were cut coronally. Every third section was incubated
in a solution of 3,3'-diaminobenzidine (DAB). The next inlcubation was in
DAB solution with the addition of H,O,. The distribution of labeled
cells was examined using dark field illumination and plotted on tracings
of adjacent Cresyl' Violet stained sections.
The terminology used for the arnygdaloid body nuclei is based on
the s t u d e s by Nitecka (10, 11) and Krettek and Price (7). The nomenr
clature of the insular cortex is derived mainly from the work of Krettek
and Price (5), although in our opinion the posterior part of the insular
granular cortex is situated mo;e caudally.
After injectio:ls of HRP to various parts of the insular cortex, labeled neuroas appeared in all nuclei of the amygdaloid body. According
to the site of injection of the enzyme, a different localization of labeled
neurons was observed.
1. Injections into the agranular insular cortex (anterior part Fig. 2) usually &d not enlcroach upon other structures. Only the under-
Fig. 2. Cat-26. Iinjectiom of HRP into the agnmular inus~uliar o o h x . Upper row:
boalizatim of the injecZIi~mploltilmd om the s~wfaoeof the hain m d om the frontal
sectim through the injection ailte. Lower row: dfistniburhian of HRP LbeJeld meurms;
fsontai sections thro~ughthe d d d l e part 06 the aimygidaboid body in rostmca~dal
ondes.
lying extreme capsule contained some reaction products. Sometimes the
injection site included a limited portion of the claustrum. Apart from
these differences, in all animals a great number of labeled neurons were
localized in the lateral, basal dorsal (Fig. 3A) and basal ventral nucleus
dorsal nualeus im the cat C-26, B, fnoim the lateral nucleus of the almygdaloid
body im oat C-29.
fig. 4,. Cat-28. Iajeoticm of HRP into the amteriolr part of the @muliar insular
codex. Upper row: bcalizahiom of injection platteld m the slurface of the b a i n
amd on the froah1 seddiom ;through bhe rlnjecti~omsite. Lower row: distrib~utiarnof
HRP labeleld neurons; f ~ o n t a ltsledioms through the rni1dd1.e!part of the amygdaloid
bo~dyh mostro~cautdlalorder.
of the amygdaloid body. Some labeled cells were found also in the
claustrum prepiriforme -- (endopiriform nucleus) - laterally from the
ventral part of the lateral amygdaloid nucleus. Labeled neurons were
observed in the central lateral and central medial nucleus. In the majority of the above-mentioned nuclei labeled neurons were localized
mainly in their ventral portions. That was especially distinct in the
lateral and basal nuclei.
2. Injections of HRP into the anterior part of the granular insular
cortex - Fig. 4. In some cases the injection site included fibers situated
directly under the grey matter. However, never encroached upon the
claustrum. A great number of labeled neurons were observed in the
lateral (Fig. 3B), basal ventral and basal dorsal nucleus. Contrary to
the previous group of experimental animals, labeled cells were mainly
localized more dorsally, especially in the basal nuclei. A few labeled cells
were situated in the central medial, medial and cortical nuclei.
3. After injections into the posterior part of the granular insular
cortex (Fig. 5) distinct labeling of the amygdaloid body neurons has
not been found in any animal.
Fig. 5. Cat-33. Locali~ation of the injection in the posterior part of the granular
h u l a r cortex.
4. The injection to the adjoining areas (somatosensory cortex SII,
auditory cortex AII) produced no labeling in the amygdaloid body nuclei.
DISCUSSION
Although the retrograde axonal transport method does not allow to
draw strict quantitative conclusions, our experiments prove that projections from the amygdaloid body nuclei to the insular cortex are numerous. The great number of labeled neurons following injections of HRP
into the insular cortex allows us to assume that it might be a subcortical
projection of the second size (after the projection from the posterior part
of the thalamus) which terminates in the insular cortex. It reaches, according to our results, both the agranular insular cortex and the anterior
part of the granular insular cortex. According to Krettek and Price (5),
this projection terminates in the posterior part of the granular insular
cortex too. The above discrepancies might be caused by the use of
different methods, they might also be related to differences in the delineation of the insular cortex.
The greatest number of labeled neurons were found in the lateral
nucleus of the amygdala. Its ventral part projects mainly to the agranular insular cortex, whereas the dorsal part - to the anterior part of the
granular insular cortex. Numerous amygdalo-insular connections arising
from the lateral nucleus were also found in the dog by K o m a l (4).
According to Krettek and Price (5), the lateral nucleus in the cat
projects only to the posterior part of the agranular insular cortex, these
connections arising only in the ventral part of the lateral nucleus.
Mufson et al. (9) obsewed in Macacca the labeling of lateral nucleus
neurons after the administration of HRP to both the anterior and posterior part of the insular cortex.
Basal dorsal nucleus projects to the agranular insular cortex and
to the granular insular cortex. This is in accordance with Kasmal (4)
who noted that in the dog there is a large insulopetal projection from
the basal dorsal nucleus. Krettek and Price (5) found in the cat connections which originate in the anterior part of the basal dorsal nucleus
and r e x h the agranular and granular insular cortex. In our results
neurons projecting to the granular insular cortex are situated more
dorsally than those which have connections with the agranular insular
cortex. Contrary to the above data obtained in lower mammals, Mufson
et al. (9) observed a relatively small number of amygdalo-insular connections emerging from the basal lateral nucleus (equivalent to the
basal dorsal nucleus in the cat) of the Macncca monkey.
According to most data, the remaining nuclei of the amygdaloid
body do not have connections with the i n ~ u l a r cortex, or give only
small projections a s e.g., cortical or anterior nucleus (5). Our results
seem to prove that all main nuclei of the amygdaloid body are coninected with the insular cortex. Massive projections originate from the
basal ventral nucleus which projects mainly to the anterior part of the
agranular insular cortex and from the central lateral nucleus which
is connected with the agranular insular cortex. Moreover, after injections to the anterior part of the granular insular cortex we observed
some labeled neurons in the medial and cortical nuclei. This suggests
the existence of some insulopetsl projections emerging from those
nuclei.
The claustrum prepiriforme -- endopiriform nucleus - is basically
not a part of the amygddoid body. Its connectioizs with the insular
cortex are mentioned here only owing to close topo;graphical relations
with nuclei of the amygdala. Connections of the clanstrum prepiriforme
in the cat were described by Krettek and Price (6), who found that
it projects to the ventral subicul~un.According to our observations, it
has also a projection which ends in the agranular insular cortex.
Our results, as well as other studies (9, 14), suggest closc reciprocal
functional connections between amygdala and insular cortex. Although
the role of the insular cortex is relatively little known, it is, like tile
amygdaloid body, involved in functions of the autonomic system, in
regulation of blood pressure and cardiac action (2). Moreover, in both
structures, the insular cortex and amygdaloid body, there are neurons
which respond to electrical stimulation of the taste receptors and fibers
conducting taste information (3). All these functions are probably integrated t h r o u ~ hreciprocal connections of nuclei of the amygdala with
the insular cortex.
The lateral nucleus, basal nuclei and central lateral nucleus of the
amygdaloid body possess numerous connections with the insular cortex.
These nuclei constitute one of the main inputs from the limbic system
to structures lying on the border of paleo- and neocortex. They may influence various behavioral patterns associated with emotions and provide a major pathway by which gustatory information can reach the
insular cortex from the nucleus of the solitary tract and from parabrachial nucleus passing through the central amygdaloid nuclei. That
input, together with other viscerosensory projections, seems to be significant for the integration of visceral functions in the cerebral cortex.
LIST OF ABBREVIATIONS
- amlanulax nosular uorrltex
- basta1 domlail mwcleu~s
- basal ventnail nucleus
- claustnum
- cent,r~dlateral nuucleus
- central rneid~lalnucleus
- corrrticd nucleus
- clawstrum prepiirifoame (emdop~rifomnucleus)
- gra~nularinsular cortex
- granular jinsular oortex, anterior part
- granular ihsullas aortcxt, poistemios gm~%
- htenal nucleu~s
- medial nucleus
REFERENCES
1. AGGLETON, J. P., BURTON, M. J. and PASSINGHAM, R. E. $980. C d i o a l
and suboolrtiwl affereinik tro the aunygidda of the rhes~mmopkey (Macacca
mulatta). main Rs. 1190: 347-368.
2. ANAND, B. K. m d DUA, S. 1956. Cimcdatory m d w ~ k a h a r yahaavges inducad
by aledrioal s t i m d & m iod Ymbic sylslk~m(visceral hain). J. Ne~urqphysiol.
19: 393-400.
3. HOFFMAN, B. L. and U S M U S S E N , T. 1953. Stirnulahian s h d i e s of imuba~
oomtex of Macacca mulatta. J. Newolpihyisiol. 16: 343-351.
4. KOSMAL, A. 1976. Efferent connections of basolateral amygdaloid part of the
mcM? paileo-, and uzelolao~rtexin t k dag. A d a Newnabid. Exp. 36: 319-333.
5. KRETTEEC, J. E. and PRICE, J. L. 1977. ~Rioj~ichaus
from lthe mygd&Ld
aamrplex r
h the cembead co~rtexfaold thktdamws i n %heir;& anud at..
J. C-.
NeuroJ. 172 : 687-722.
6. KRETTEK, J. E. and PRICE, J. L. 1977. P~riojeidioas %noun the arnyadahid
complex and edjlaceuut ~~Wa~atiory
strrucftwe~s t o hhe anthomind mntex apld
to the w u b i d u m in t h e TI$ and loah. J. Clamp. Neiwd. 172: 723-752.
7. KRETTEK, J. E. aed PRICE, J. L. 1978. A ~ d a s o n ~ o09n the a u n y g d a i d
m r ~ p l e xh tlhe xmt and loat with o b s m v ~ t i mio(n ,hhraiamygld&~iid axoaatl
~ m e l o t i m s .J. Camp. Ne1m1. 178: 255-280.
8. MESULAM, M. M. and ROSEN, D. 1979. Semisriibivity in hmena~dishpemoxjdlase
muu-ocheimistry: A immipwtive and qu;yn,.bjlbaitiive shudy of mine methe&.
J. Hiish(~ehm.Cytioiahem. 27: 763-773.
9. MUFSON, E. J., MESULAM, M. M. m d PANDYIL, D. N. 198111. b u l a r interaommdbms with the amyg;daLa in the rhwns m w k e y . N a w o s c k m e 6:
1231-1248.
10. NITECKA, L. 1975. Comparative anatomic aspects of localization of acetyloc h o L k t a w l e a&viky h the amygidla~loidbody. Flolia M m p h d . 34: 167-185.
11. NITEICKA, L. 19811. The ewbcrosti~wad laffermtis of the aimyigd,afhid bojdy an~d
specifiaity of Ik nulaleh Ainp. Amid. Med. G~edianz.11: 57-77.
12. OTTERSEN, 0. P. 1982. Comol~ctiomof the mnygidlala iof tthe r a t IV: C o r t b mygdraloid and inhraamyigld!aLoird comecltiouus als sbuid~ieid udith a x i o d
trm;lpiort d obm~sanadiis~h
perloxidiaise. J. Clamp. Neunorl. 205: 3 0 4 .
13. REEIP, R. L. and WINAIWS, S. S. 1982. Afferent c~oinne~cki~ool
of domd and
v m t r ~ d agnaauhr iim~wlm-m r k x in tthe jhamister Mesocricetus aratus.
Nemascieace 7: 1265-1288.
14. RUSSCHEN, F. T. 1982. Amygdalopetal projections in the cat. I. Cortical
afferent cmmecti~om. A study with net~ogira~dem ~ dmterogmde tracing
techniques. J. Comp. Neurol. 206: 158-179.
15. TURNER, B. H., MISHKIN, M. am~d KNAPiP, M. 1980. Orglan~aiticvn of the
ernsngld1alope6alpaojel&ws f m ~ mmodlality+peclid~ic c & b d assio~dathm areas
h the momkey. J. Counrp. Nem-01. 191: 515-543.
16. VEENING, J. G. 1978. Cortical affe~emtsof the lamygdaloid >aomplex in the
m a t : am HRP stiu~dy.Neunoisid. Lett. 8: 191+1!95.
Accepted 8 March 1984