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A retino-pulvinar projection in the macaque monkey as visualized by the use of anterograde transport of horseradish peroxidase
A IIET'L.~IO.-PLrJLV]IN_ARPRO~ECTION IN THE ~ACA, QUE .~.ONKEY AS V ~ . , I k ~ Z E D IIY THE USE OF ANTEIIO(;I~ADIE TRANSPOFGI" OF ~.~Dl$~ ~XiDASE
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freezing m~crotome. For the t',_istc,chemicai demonstration of the enzyme all sections containing tke pulvinar ,nuclei were treated with 'etramethylbenzidine (TMB'~ [8~, or with benz~dme dihydr~ochluride through a proce]ure modified from that descr-bed by de Olm,os and Heicner [4]. l'he sections treated with TMB were coL,,.,ersta;ned with I% neutral red. In ~II monkeys, ~:iusters of HRP-positive fine granules, suggesting anterogradelylabeled optic fiber terminals, were seen bilateratly, with a contralateral predominance, in the suprachiasmatic nucleus, pregeniculate nucleus, lateral geniculate nucleus, dorsal and lateral nuclei of the accessory optic tract, terminal nucleus of the cptic tract and olivary nucleus of the l:,retectum, and superficial layer of the supei ior coll!culus. A few small clusters of HRP-positive fine granules were found in restricted regions o1 the inferior 13ulvinar nucleus (i-Pul) (Fig. 1). They were distributed along the medial border of the i-Ful bilaterally, with a contralateral predominance. They appeared to be dcriv,:d from collaterals of the optic fibers passing over the medial genifutate nucleus on their way to the superior colliculus (Figs. lb and 3b). These clust~:rs of la~,e[ed optic fiber terminai'~ were se':n in 20-26 consecutive frontal or horizomal sections through the middle portions of the i-Pul (Figs. 2-4). Since ne labeled neuronal soma were found ia the lateral geniculate nucleus and ,,uperior c:Jlli,.'ultls, and since nu labeh:d ax,Jn terminal,, v~erc found in the parabJg~:minal n,,cleus and vi,,ual corlical areas, possibilities o! transneuronul transport ol HRP ,: ~ukl be excluued in the present study.
I Ig. 1. I)ark-t tel~ p h o t o m i f r o g r a p i l s of l~ollta[ sfL:ttons ~+hrough the m l f r i o : pul' inar, sho~ mg clu,,t el • t~f ItRP-pos~tive t'il~e granule,; (arro~,,s). I exel,, a and b corr¢.,pon~ to th,~e in F i g 2a and b r~,'Sl"~',:ti~,'ely. Op. opt,¢ fiber,. × 6,s+
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Fig. 2. P h o t o m c m g r a p h s of frontal sectiens, indicating the distribution zones (arrows) of rel!nopulvinar fiber ~: .minals. The level of a is 8"-0 ~m distant roslrally from that of b. H, habcnula; MG, medial geniculaF, nucleus; Pi, inferior pulvin~.r nucleus; PI, lateral p u l v i e a : nticleus; Pro, mcdiat puivinar nucleus; Pt, pr,")ectum, x 6.
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fig. 3. Pholorai~rogrl phs of horieontal .,eclmn~. il)(licatln-, th- di,,)ribtmcm zone', (qraigh! a r , , ) , . ~ < , ) o l retino-pulvin;ir lib~ r t,:rniinaN. The [ewc', oi t~ i> 42o ,.m dr, at,) :r'.-.,)~l, I~,,:,~ ~l,a~ ~t !~ ( u,.(.'cl arr(.v,,. point to l a b d i n g of rc)ino-collicular fiber terminaN. CP ~.':rcbral pcduncl,-, ON, o c u ' o m o t o r u,.'rvc; R, red nucleus; .~:,(:, ,>u))e.;c,!: coIlicu[u',; 5,N, ,:ub;).an,,ia r.tgrz',. I-or o,)l-~er abbr :va),ia~e,. ~,cc l.ie. 2. ," 6.
Fig. 4. Pholomicrographs of a horizontal rc'ction throu~.h the inferior puivinaz Clusters of HRP-labeted possible terminals of optic fibers in the region pointed to with a straight arrow in a are shown at a higher magnification in b (arrows). A curved arrow in a points to labeling of retino.pre~ectai fiber terminals. The level of this figur,: is 6~)/~m distant cranially from that of Fig. 3a. LG. late-al geniculate nucleus, For othel abbrevalions, ;~¢eFigs. Z and 3. a, x 9; b, × 160.
Hassler and Wagner reported two cases of human cong:nital anophthalmia, which were associated with a complete aplasia of the lateral g~l~iculate nucleus and a considerable ,'¢ductio:~ in s!zc of the intergeniculate nucleus ~f the pulvinar (cited from ref. 9). These findi.zgs suggested the existence of cirect retino-pulvinar connections in primates. In the baboon and the rhesus monkey, Campo~-Ortcipt et ai. [31 described termination of optic fibers in d-,e 'latcro-ventrai' margin of the i-Pul. In the present study, however, optic fiber terminals in :he i-Ful were found mainly in the 'medial' margin adjv,~r;t to the medial $eniculaXe nucleus. According to an el~'trophysiological study in the rhesus monkey [Ill, the i-Pul neurons are visually responsive, and the contralateral visual IR'mifie|d is rein'cscnted in the i-Pul. The retino-recipient i-Pul regions adjacent to the medial I~nk,'ulat¢ mucieus appear to lie in the area where the peripheral visual riced (around 50 o) i,~ represented. The photographic help of Mr. Akira Uesugi and the support of the Ni',va Medical Research Fop.nda~ion are gralefully acknowledgo.-d, I I~,~]¢r, D,B., Retino;.opi¢ or~mization of macaque pul~,inar, J. H(u~ophysiol., 46 (Iq)gl) 6/2-693. 2 Bcrman, N. a~ld Jones. F.G,, A retino-pulvmar projection in the cat. Brain Rcs., 134 (1977) 237-248. 3 Campos-Ort~a, J.A., Hay]'ow. W,R. and ClOver. P.F. de V., A note on the problem of retinal project.ons to the pulvinar ~ ucleus of primates. Brain R~., 22 (1970) 126-130.
203 4 de Otmos, J S. and Heimer, L., Mapping of collateral projection with the lff~P method, Neurosci. Lett,, 6 (1~77) 107-114. 5 Itoh, K., Mzuno, N., Sugin'oto, T., Nomura, S., Nakamura, Y. anc K~.mshi, A., A cerebellopulvino-coff. :A and a retino pulvino-cortical pathways in the cat as revealed by the use of the anterograde ann :,~;.rograde transport of horseradish peroxidase, J. comic. Neurol.. 187 (1979) 349--358. 6 Kawamura, S., Fukushima, N. and Hattori, S., Topographical origin a,~d ganglion cell type of the retino-pulvinar projection in the cat, Brain Res., 173 (1979) 419-429. 7 Leventhal, A.G., Keens, J. and TOrk, I., The afferent ganglion ceils and cortica! projections o,~ the retinal recipien¢ zone (RRZ) of the cat's "pulvinar complex', 3. comp Neurol., 194 (1980) 535-4554. 8 Mesulam, M.-M., Tetramethyl bcnzidine for horseradish peroxidase neurohistochemistry: a noncarcinogenic blue reaction-product with superior sensitivity for visuaizing neural afferents and efferents, J. Histochem. Cytoch~m., 26 (1978) 106-117, 9 Somogyi, G., Hajdu, F., Hastier, R. and Wagner, A., An experimental elcctrorl microscopical s~udy of a direct retinopulvinar pathway in the tree shrew, Exp. Brain Res., 43 (1981) 447--450. 10 Trojanowski, J.Q. and Jacobson, S., Peroxidase labeled subcortical afferents to puivinar in rhesus monkey, Brain Res., 9? (1975) 144-150.
, ~ O t t D I l U ..Mt~L~t,iO, K . 4 Z 1 . D l ' i ' O H . K U N ! i ( O
~!~i,
UCHtDA,
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U[Mt.'~-t-'~.t~Ml,
and
tem o f ~.>rll A.,~r~tolt~. " t,),~ Division). _~'hc,o# ::f De,tistO. Hir~ih;m¢ Uni~'~si~y, L,ro.~":i.'~n:
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T h e i"~i~).~ln,~ o f r¢lino-~)P,'~n~
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freezing m~crotome. For the t',_istc,chemicai demonstration of the enzyme all sections containing tke pulvinar ,nuclei were treated with 'etramethylbenzidine (TMB'~ [8~, or with benz~dme dihydr~ochluride through a proce]ure modified from that descr-bed by de Olm,os and Heicner [4]. l'he sections treated with TMB were coL,,.,ersta;ned with I% neutral red. In ~II monkeys, ~:iusters of HRP-positive fine granules, suggesting anterogradelylabeled optic fiber terminals, were seen bilateratly, with a contralateral predominance, in the suprachiasmatic nucleus, pregeniculate nucleus, lateral geniculate nucleus, dorsal and lateral nuclei of the accessory optic tract, terminal nucleus of the cptic tract and olivary nucleus of the l:,retectum, and superficial layer of the supei ior coll!culus. A few small clusters of HRP-positive fine granules were found in restricted regions o1 the inferior 13ulvinar nucleus (i-Pul) (Fig. 1). They were distributed along the medial border of the i-Ful bilaterally, with a contralateral predominance. They appeared to be dcriv,:d from collaterals of the optic fibers passing over the medial genifutate nucleus on their way to the superior colliculus (Figs. lb and 3b). These clust~:rs of la~,e[ed optic fiber terminai'~ were se':n in 20-26 consecutive frontal or horizomal sections through the middle portions of the i-Pul (Figs. 2-4). Since ne labeled neuronal soma were found ia the lateral geniculate nucleus and ,,uperior c:Jlli,.'ultls, and since nu labeh:d ax,Jn terminal,, v~erc found in the parabJg~:minal n,,cleus and vi,,ual corlical areas, possibilities o! transneuronul transport ol HRP ,: ~ukl be excluued in the present study.
I Ig. 1. I)ark-t tel~ p h o t o m i f r o g r a p i l s of l~ollta[ sfL:ttons ~+hrough the m l f r i o : pul' inar, sho~ mg clu,,t el • t~f ItRP-pos~tive t'il~e granule,; (arro~,,s). I exel,, a and b corr¢.,pon~ to th,~e in F i g 2a and b r~,'Sl"~',:ti~,'ely. Op. opt,¢ fiber,. × 6,s+
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Fig. 2. P h o t o m c m g r a p h s of frontal sectiens, indicating the distribution zones (arrows) of rel!nopulvinar fiber ~: .minals. The level of a is 8"-0 ~m distant roslrally from that of b. H, habcnula; MG, medial geniculaF, nucleus; Pi, inferior pulvin~.r nucleus; PI, lateral p u l v i e a : nticleus; Pro, mcdiat puivinar nucleus; Pt, pr,")ectum, x 6.
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fig. 3. Pholorai~rogrl phs of horieontal .,eclmn~. il)(licatln-, th- di,,)ribtmcm zone', (qraigh! a r , , ) , . ~ < , ) o l retino-pulvin;ir lib~ r t,:rniinaN. The [ewc', oi t~ i> 42o ,.m dr, at,) :r'.-.,)~l, I~,,:,~ ~l,a~ ~t !~ ( u,.(.'cl arr(.v,,. point to l a b d i n g of rc)ino-collicular fiber terminaN. CP ~.':rcbral pcduncl,-, ON, o c u ' o m o t o r u,.'rvc; R, red nucleus; .~:,(:, ,>u))e.;c,!: coIlicu[u',; 5,N, ,:ub;).an,,ia r.tgrz',. I-or o,)l-~er abbr :va),ia~e,. ~,cc l.ie. 2. ," 6.
Fig. 4. Pholomicrographs of a horizontal rc'ction throu~.h the inferior puivinaz Clusters of HRP-labeted possible terminals of optic fibers in the region pointed to with a straight arrow in a are shown at a higher magnification in b (arrows). A curved arrow in a points to labeling of retino.pre~ectai fiber terminals. The level of this figur,: is 6~)/~m distant cranially from that of Fig. 3a. LG. late-al geniculate nucleus, For othel abbrevalions, ;~¢eFigs. Z and 3. a, x 9; b, × 160.
Hassler and Wagner reported two cases of human cong:nital anophthalmia, which were associated with a complete aplasia of the lateral g~l~iculate nucleus and a considerable ,'¢ductio:~ in s!zc of the intergeniculate nucleus ~f the pulvinar (cited from ref. 9). These findi.zgs suggested the existence of cirect retino-pulvinar connections in primates. In the baboon and the rhesus monkey, Campo~-Ortcipt et ai. [31 described termination of optic fibers in d-,e 'latcro-ventrai' margin of the i-Pul. In the present study, however, optic fiber terminals in :he i-Ful were found mainly in the 'medial' margin adjv,~r;t to the medial $eniculaXe nucleus. According to an el~'trophysiological study in the rhesus monkey [Ill, the i-Pul neurons are visually responsive, and the contralateral visual IR'mifie|d is rein'cscnted in the i-Pul. The retino-recipient i-Pul regions adjacent to the medial I~nk,'ulat¢ mucieus appear to lie in the area where the peripheral visual riced (around 50 o) i,~ represented. The photographic help of Mr. Akira Uesugi and the support of the Ni',va Medical Research Fop.nda~ion are gralefully acknowledgo.-d, I I~,~]¢r, D,B., Retino;.opi¢ or~mization of macaque pul~,inar, J. H(u~ophysiol., 46 (Iq)gl) 6/2-693. 2 Bcrman, N. a~ld Jones. F.G,, A retino-pulvmar projection in the cat. Brain Rcs., 134 (1977) 237-248. 3 Campos-Ort~a, J.A., Hay]'ow. W,R. and ClOver. P.F. de V., A note on the problem of retinal project.ons to the pulvinar ~ ucleus of primates. Brain R~., 22 (1970) 126-130.
203 4 de Otmos, J S. and Heimer, L., Mapping of collateral projection with the lff~P method, Neurosci. Lett,, 6 (1~77) 107-114. 5 Itoh, K., Mzuno, N., Sugin'oto, T., Nomura, S., Nakamura, Y. anc K~.mshi, A., A cerebellopulvino-coff. :A and a retino pulvino-cortical pathways in the cat as revealed by the use of the anterograde ann :,~;.rograde transport of horseradish peroxidase, J. comic. Neurol.. 187 (1979) 349--358. 6 Kawamura, S., Fukushima, N. and Hattori, S., Topographical origin a,~d ganglion cell type of the retino-pulvinar projection in the cat, Brain Res., 173 (1979) 419-429. 7 Leventhal, A.G., Keens, J. and TOrk, I., The afferent ganglion ceils and cortica! projections o,~ the retinal recipien¢ zone (RRZ) of the cat's "pulvinar complex', 3. comp Neurol., 194 (1980) 535-4554. 8 Mesulam, M.-M., Tetramethyl bcnzidine for horseradish peroxidase neurohistochemistry: a noncarcinogenic blue reaction-product with superior sensitivity for visuaizing neural afferents and efferents, J. Histochem. Cytoch~m., 26 (1978) 106-117, 9 Somogyi, G., Hajdu, F., Hastier, R. and Wagner, A., An experimental elcctrorl microscopical s~udy of a direct retinopulvinar pathway in the tree shrew, Exp. Brain Res., 43 (1981) 447--450. 10 Trojanowski, J.Q. and Jacobson, S., Peroxidase labeled subcortical afferents to puivinar in rhesus monkey, Brain Res., 9? (1975) 144-150.