RAPID COMMUNICATION
ZIPGRAM
DIRECT EFFERENT AND AFFERENT CONNECTIONS OF THE HIPPOCAMPUS WITH THE NEOCORTEX I N THE MARMOSET MONKEY WALTER K. SCHWERDTFEGER Max P1 anck- I n s ti t u t f u r H i rnforschung , Deutschordenstr. 46 , D-6000 Frankfurt/M. 71 ABSTRACT Ante ograde and r e t r o g r a d e t r a n s p o r t was s t u d i e d f o l l o w i n g i n j e c t i o n s o f H-pro1 i n e and/or horseradish peroxidase i n t o hippocampal and n e o c o r t i c a l areas o f t h e common marmoset monkey. Reciprocal connections between t h e f r o n t a l and temporal neocortex and t h e subiculum are prominent; sparse connections e x i s t a l s o w i t h f i e l d s CA7 and CA2/3 o f Ammon's horn. E n t o r h i n a l c o r t e x , parasubiculum and presubiculum are r e c i p r o c a l l y connected w i t h f r o n t a l and temporal neocortex.
5
Recently, g r e a t i n t e r e s t has been focused on t h e f i b e r connections o f t h e hippocampus formation, since, f o r example, Leichnetz and Astruc ( ' 7 5 ,
'76)
and Rosene and Van Hoesen ( ' 7 7 ) described hippocampal e f f e r e n t s and a f f e r e n t s reaching t h e f r o n t a l neocortex i n t h e rhesus monkey and t h e s q u i r r e l monkey. I n s t e a d o f Ammon's horn, t h e subiculum has been suggested t o be t h e main nodal p o i n t o f f i b e r connections o f t h e hippocampus (Rosene and Van Hoesen, '77; Meibach and Siege1 , '77).
The present communication deals w i t h p r o j e c t i o n s
o f t h e hippocampus o f t h e common marmoset monkey, C a l l i t h r i x jacchus, t o d i f f e r e n t n e o c o r t i c a l areas, as w e l l as afferent i n p u t s from these regions. MATERIALS AND METHODS
Under deep Nembutal anesthesia , e i g h t a d u l t
marmosets received pressure i n j e c t i o n s (0.4-0.8
111) o f 50% horseradish
peroxidase (HRP; Serva) and/or 3H - p r o l i n e (Amersham-Buchler; 200 V C i ) s t e r e o t a x i c head-holder.
, using
a
I n j e c t i o n s were given i n t o t h e hippocampus , and,
t o check t h e v a l i d i t y o f t h e r e s u l t s , i n t o t h e f r o n t a l , t h e temporal , and t h e p a r i e t a l neocortex.
A f t e r s u r v i v a l times o f two o r t h r e e days, t h e b r a i n s 77
were fixed by perfusion i n t o t h e heart.
Frozen sections (40
pm)
were cut.
One s e r i e s of sections was reacted with diaminobenzidine (Graham and Karnovsky, '66) t o study retrograde intra-axonal t r a n s p o r t .
Anterograde t r a n s p o r t of
t r i t i a t e d proline was demonstrated by autoradiography:
Sections were coated
with I l f o r d L4 emulsion, and t h e autoradiographs developed a f t e r exposure times of 4 t o 8 weeks, cover-slipped unstained o r counterstained with Cresylechtviolett (Serva) . RESULTS After i n j e c t i o n of HRP i n t o t h e caudal part of f i e l d CA1 of the hippocampus, proper, and t h e adjacent subiculum ( f i g . l c ) , many labelled c e l l s were found i n diencephalic and telencephalic nuclei i n a l a t e r paper.
, which will be described
S t r i k i n g l y , there were a l s o labelled c e l l s in layers I11
and, mainly, V and VI o f area 7 of the p a r i e t a l cortex ( f i g . 2 ) , and i n layer Vof temporal area 22 ( t h e c l a s s i f i c a t i o n of Brodmann ( ' 0 9 ) i s used f o r t h e neocortical a r e a s ) , both areas 2.5 t o 3 mm r o s t r a 1 t o t h e i n j e c t i o n s i t e . Other labelled c e l l s were detected i n layers V and VI ( f i g . 3) of temporal area 20, from 2 mm posterior t o 2 mm a n t e r i o r t o the i n j e c t i o n s i t e ; i n the posterior cingulate cortex (layers I11 , V); and in entorhinal and perirhinal cortex ( f i g . 3) i n layers 111, V , and VI. When t h e i n j e c t i o n s i t e involved middle parts of CA1 and CA2/3 ( f i g . a few HRP-marked c e l l s were located in t h e a n t e r i o r area 6 ( l a y e r V ) and i p s i l a t e r a l and c o n t r a l a t e r a l p a r t s of area 7 ( l a y e r s V , VI).
Some c e l l s
were found in the caudal temporal areas including 21 ( l a y e r s 111, VI), an i n layers I11 and VI of t h e p o s t e r i o r cingulate cortex.
In t h i s case, e f f e r e n t s
t o f r o n t a l areas 10/11 (layers I , I I ) , area 4 of the precentral cortex (layers I , I1 , VI , a l s o c o n t r a l a t e r a l l y ) , and areas 20-22 were revealed by autoradiography
. Proline i n j e c t i o n s i n t o caudal CA2/3 and subiculum gave s i m i l a r r e s u l t s 78
t o those seen with HRP.
After i n j e c t i o n of proline and HRP i n t o t h e dorsal
caudal CA1 ( f i g . I d ) , a few c e l l s were labelled by the HRP reaction product in layers V and VI of t h e midtemporal and caudal areas 7 , 20, and 21, and many c e l l s i n t h e subiculum.
From t h i s experiment, e f f e r e n t s could be traced t o
layer IV of areas 20-22 and t o t h e subiculum.
When t h e i n j e c t i o n s i t e included only t h e fimbria and a small p a r t of t h e adjacent CA2/3 ( f i g . l b ) , autoradiographic l a b e l l i n g could be detected in caudal area 7 ( l a y e r 11). T h e control experiments performed yielded t h e following r e s u l t s : 1.
Injection i n t o t h e p a r i e t a l cortex overlying t h e caudal hippocampus:
Many labelled c e l l s were found i n layer I11 o f areas 6 , 7 , 21, and 22.
Few
labelled c e l l s were seen i n layers 111, V , VI of area 20, and, by autoradiographic l a b e l l i n g , i n layers IV and VI of area 20. 2.
Injection i n t o the grey matter of f r o n t a l areas 9/10:
T h i s resulted
Few c e l l s were found a t t h e
i n heavy HRP-labelling a l l over t h e subiculum.
rostra1 beginning o f the hippocampus proper, and very few c e l l s in m ddl e p a r t s of CA1 and CA2/3 and in dorsal caudal CA1. 3.
Injection i n t o the grey matter of temporal areas 20/21:
numerous labelled subicular c e l l s .
Th s yielded
Again, very few marked c e l l s could be
detected i n middle levels of CA2/3 and i n dorsal caudal CA1.
Efferents traced
by autoradiography spread t o t h e subiculum ( f i g . 4 ) , CA1 and adjacent CA2/3. These i n j e c t i o n s i n t o t h e f r o n t a l and temporal c o r t i c e s a l s o revealed reciprocal connections with t h e entorhinal cortex, presubiculum and parasubiculum. DISCUSSION
From these r e s u l t s , t h e following conclusions can be drawn:
The subiculum and, l e s s prominently, a l s o CA1 and CA2/3, have reciprocal connections w i t h the f r o n t a l and temporal neocortex. t h e white matter, perforant path, and alveus.
79
These f i b e r s pass through
T h i s i s suggested because
injections involving fimbria o r dorsal CA1, only, reveal a f f e r e n t s from the cingulate cortex and f a i n t connections w i t h the parietal cortex.
The l a t t e r
possibly o r i g i n a t e i n the cortex overlying the hippocampus. The findings presented f i t well with the investigations of Leichnetz and Astruc ( '75, '76) and Rosene and Van Hoesen ( '77) mentioned above. Subicular connections with the temporal neocortex i n the rhesus monkey were described i n a recent paper of Van Hoesen and Rosene ( '78). Our r e s u l t s (1) support the opinion t h a t the subiculum i s t h e main nodal point f o r e x t r i n s i c hippocampal connections, ( 2 ) confirm the existence of a hippocampal output t h a t does not pass through the fimbria, and ( 3 ) suggest an increased significance o f the primate hippocampus influencing association and memory cortex, not only involving other p a r t s of the limbic system i n d i r e c t l y , b u t also by monosynaptic connections.
In t h i s respect, i t i s o f great i n t e r e s t t h a t neuroanatomical evidence gained by a1 1ometri cal comparisons shows t h a t i n primates the hi ppocampal FIGURE LEGENDS 1 Diagrams of cross-sections a t middle ( a , b) and caudal ( c , d ) l e v e l s of the hippocampus, showing d i f f e r e n t i n j e c t i o n sites (black d o t s ) . d dentate gyrus, l g l a t e r a l geniculate body, p presubiculum, r red nucleus, rt r e t i c u l a r thalamic nucleus, s subiculum, s c superior c o l l i c l e , 1 CA1, 3 CA2/3, VIII vestibulocochlear nerve. 2 HRP-labelled c e l l s (arrowheads) i n layers 111 and VI of p a r i e t a l cortex (HRP-injection i n t o CA1 and subiculum). Borders o f layers I-VI and white matter (wm) a r e marked a t the r i g h t . Bar = 100 pm. 3 HRP-labelled c e l l s in layers 111, V , VI o f the perirhinal cortex (above the border marked by arrows), some also i n t h e adjacent area 20 (below arrows). HRP-injection i n t o CA1 and subiculum. Photograph Borders o f layers I-VI and white matter (wm) a r e turned by 90'. marked on t h e top. Bar = 100 vm. 4 Dense autoradiographic l a b e l l i n g over t h e subiculum. Injection o f HRP+proline i n t o grey matter of areas 20/21. Photograph turned by sh sulcus hippocampi. Bar = 100 pm. 90°. Figures 2-4 a r e s l i g h t l y retouched t o remove d i r t and excessive background 1abel 1 i ng .
80
formation i s a progressive s t r u c t u r e from t h e aspect of phylogeny and reaches i t s r e l a t i v e l y l a r g e s t s i z e i n man (Stephan and Andy, '70).
I t i s suggested
t h a t t h e r e has been a progressive neocorticalisation o f hippocampal connections during the phylogenic evolution o f primates, a s no d i r e c t hippocampo-neocortical connections a r e known from other animals. The systematic position of C a l l i t h r i x i s t h a t of a lower simian primate
w i t h a r e l a t i v e l y unspecialized brain.
Further comparative s t u d i e s a r e intended
which may help t o e l u c i d a t e t h e question a t which phylogenic level t h e formation of monosynaptic hippocampo-neocortical connections was established. ACKNOWLEDGMENTS The author thanks Prof. Dr. Rolf Hassler f o r h i s i n t e r e s t and discussion, Barbara Hechler f o r technical assistance,and Dr. John Sarvey f o r reading t h e English manuscript.
LITERATURE CITED Brodmann, K. 1909 Vergleichende Lokalisationslehre der Groghirnrinde. Johann Ambrosius Barth, Leipzig. Graham, R . C . , M . J . Karnovsky 1966 The e a r l y stages of absorption o f injected horseradish peroxidase i n t h e proximal tubules of mouse kidney: u l t r a s t r u c t u r a l cytochemistry by a new technique. J . Histochem. Cytochem., 14: 291-302. Le chnetz, G . R . , J . Astruc 1975 Preliminary evidence f o r a d i r e c t projection of t h e prefrontal cortex t o the hippocampus i n t h e s q u i r r e l monkey. Brain Behav. Evol . , 11: 355-364. Le chnetz, G. R., J . Astruc 1976 The e f f e r e n t projections of the medial prefrontal cortex i n t h e s q u i r r e l monkey (Saimiri sciureus). Brain Res., 109: 455-472. Meibach, R . C . , A. Siege1 1977 Subicular projections t o t h e posterior cingulate cortex in r a t s . Exp. Neurol., 57: 264-274. Rosene, D. L., G. W. Van Hoesen 1977 Hippocampal e f f e r e n t s reach widespread areas o f cerebral cortex and amygdala i n the rhesus monkey. Science, 198: 315-317. Stephan, H., O.J. Andy 1970 The allocortex in primates. In: The Primate Brain. Advances i n Primatology Volume 1. C . R. Noback and W . Montagna, eds.,Appleton-Century-Crofts, New York, pp. 109-135. Van Hoesen, G. W . , D. L. Rosene 1978 Non-entorhinal projections t o t h e subiculum from temporal neocortex i n t h e rhesus monkey. Anat. Rec., 190: 570.
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82
ZIPGRAM
DIRECT EFFERENT AND AFFERENT CONNECTIONS OF THE HIPPOCAMPUS WITH THE NEOCORTEX I N THE MARMOSET MONKEY WALTER K. SCHWERDTFEGER Max P1 anck- I n s ti t u t f u r H i rnforschung , Deutschordenstr. 46 , D-6000 Frankfurt/M. 71 ABSTRACT Ante ograde and r e t r o g r a d e t r a n s p o r t was s t u d i e d f o l l o w i n g i n j e c t i o n s o f H-pro1 i n e and/or horseradish peroxidase i n t o hippocampal and n e o c o r t i c a l areas o f t h e common marmoset monkey. Reciprocal connections between t h e f r o n t a l and temporal neocortex and t h e subiculum are prominent; sparse connections e x i s t a l s o w i t h f i e l d s CA7 and CA2/3 o f Ammon's horn. E n t o r h i n a l c o r t e x , parasubiculum and presubiculum are r e c i p r o c a l l y connected w i t h f r o n t a l and temporal neocortex.
5
Recently, g r e a t i n t e r e s t has been focused on t h e f i b e r connections o f t h e hippocampus formation, since, f o r example, Leichnetz and Astruc ( ' 7 5 ,
'76)
and Rosene and Van Hoesen ( ' 7 7 ) described hippocampal e f f e r e n t s and a f f e r e n t s reaching t h e f r o n t a l neocortex i n t h e rhesus monkey and t h e s q u i r r e l monkey. I n s t e a d o f Ammon's horn, t h e subiculum has been suggested t o be t h e main nodal p o i n t o f f i b e r connections o f t h e hippocampus (Rosene and Van Hoesen, '77; Meibach and Siege1 , '77).
The present communication deals w i t h p r o j e c t i o n s
o f t h e hippocampus o f t h e common marmoset monkey, C a l l i t h r i x jacchus, t o d i f f e r e n t n e o c o r t i c a l areas, as w e l l as afferent i n p u t s from these regions. MATERIALS AND METHODS
Under deep Nembutal anesthesia , e i g h t a d u l t
marmosets received pressure i n j e c t i o n s (0.4-0.8
111) o f 50% horseradish
peroxidase (HRP; Serva) and/or 3H - p r o l i n e (Amersham-Buchler; 200 V C i ) s t e r e o t a x i c head-holder.
, using
a
I n j e c t i o n s were given i n t o t h e hippocampus , and,
t o check t h e v a l i d i t y o f t h e r e s u l t s , i n t o t h e f r o n t a l , t h e temporal , and t h e p a r i e t a l neocortex.
A f t e r s u r v i v a l times o f two o r t h r e e days, t h e b r a i n s 77
were fixed by perfusion i n t o t h e heart.
Frozen sections (40
pm)
were cut.
One s e r i e s of sections was reacted with diaminobenzidine (Graham and Karnovsky, '66) t o study retrograde intra-axonal t r a n s p o r t .
Anterograde t r a n s p o r t of
t r i t i a t e d proline was demonstrated by autoradiography:
Sections were coated
with I l f o r d L4 emulsion, and t h e autoradiographs developed a f t e r exposure times of 4 t o 8 weeks, cover-slipped unstained o r counterstained with Cresylechtviolett (Serva) . RESULTS After i n j e c t i o n of HRP i n t o t h e caudal part of f i e l d CA1 of the hippocampus, proper, and t h e adjacent subiculum ( f i g . l c ) , many labelled c e l l s were found i n diencephalic and telencephalic nuclei i n a l a t e r paper.
, which will be described
S t r i k i n g l y , there were a l s o labelled c e l l s in layers I11
and, mainly, V and VI o f area 7 of the p a r i e t a l cortex ( f i g . 2 ) , and i n layer Vof temporal area 22 ( t h e c l a s s i f i c a t i o n of Brodmann ( ' 0 9 ) i s used f o r t h e neocortical a r e a s ) , both areas 2.5 t o 3 mm r o s t r a 1 t o t h e i n j e c t i o n s i t e . Other labelled c e l l s were detected i n layers V and VI ( f i g . 3) of temporal area 20, from 2 mm posterior t o 2 mm a n t e r i o r t o the i n j e c t i o n s i t e ; i n the posterior cingulate cortex (layers I11 , V); and in entorhinal and perirhinal cortex ( f i g . 3) i n layers 111, V , and VI. When t h e i n j e c t i o n s i t e involved middle parts of CA1 and CA2/3 ( f i g . a few HRP-marked c e l l s were located in t h e a n t e r i o r area 6 ( l a y e r V ) and i p s i l a t e r a l and c o n t r a l a t e r a l p a r t s of area 7 ( l a y e r s V , VI).
Some c e l l s
were found in the caudal temporal areas including 21 ( l a y e r s 111, VI), an i n layers I11 and VI of t h e p o s t e r i o r cingulate cortex.
In t h i s case, e f f e r e n t s
t o f r o n t a l areas 10/11 (layers I , I I ) , area 4 of the precentral cortex (layers I , I1 , VI , a l s o c o n t r a l a t e r a l l y ) , and areas 20-22 were revealed by autoradiography
. Proline i n j e c t i o n s i n t o caudal CA2/3 and subiculum gave s i m i l a r r e s u l t s 78
t o those seen with HRP.
After i n j e c t i o n of proline and HRP i n t o t h e dorsal
caudal CA1 ( f i g . I d ) , a few c e l l s were labelled by the HRP reaction product in layers V and VI of t h e midtemporal and caudal areas 7 , 20, and 21, and many c e l l s i n t h e subiculum.
From t h i s experiment, e f f e r e n t s could be traced t o
layer IV of areas 20-22 and t o t h e subiculum.
When t h e i n j e c t i o n s i t e included only t h e fimbria and a small p a r t of t h e adjacent CA2/3 ( f i g . l b ) , autoradiographic l a b e l l i n g could be detected in caudal area 7 ( l a y e r 11). T h e control experiments performed yielded t h e following r e s u l t s : 1.
Injection i n t o t h e p a r i e t a l cortex overlying t h e caudal hippocampus:
Many labelled c e l l s were found i n layer I11 o f areas 6 , 7 , 21, and 22.
Few
labelled c e l l s were seen i n layers 111, V , VI of area 20, and, by autoradiographic l a b e l l i n g , i n layers IV and VI of area 20. 2.
Injection i n t o the grey matter of f r o n t a l areas 9/10:
T h i s resulted
Few c e l l s were found a t t h e
i n heavy HRP-labelling a l l over t h e subiculum.
rostra1 beginning o f the hippocampus proper, and very few c e l l s in m ddl e p a r t s of CA1 and CA2/3 and in dorsal caudal CA1. 3.
Injection i n t o the grey matter of temporal areas 20/21:
numerous labelled subicular c e l l s .
Th s yielded
Again, very few marked c e l l s could be
detected i n middle levels of CA2/3 and i n dorsal caudal CA1.
Efferents traced
by autoradiography spread t o t h e subiculum ( f i g . 4 ) , CA1 and adjacent CA2/3. These i n j e c t i o n s i n t o t h e f r o n t a l and temporal c o r t i c e s a l s o revealed reciprocal connections with t h e entorhinal cortex, presubiculum and parasubiculum. DISCUSSION
From these r e s u l t s , t h e following conclusions can be drawn:
The subiculum and, l e s s prominently, a l s o CA1 and CA2/3, have reciprocal connections w i t h the f r o n t a l and temporal neocortex. t h e white matter, perforant path, and alveus.
79
These f i b e r s pass through
T h i s i s suggested because
injections involving fimbria o r dorsal CA1, only, reveal a f f e r e n t s from the cingulate cortex and f a i n t connections w i t h the parietal cortex.
The l a t t e r
possibly o r i g i n a t e i n the cortex overlying the hippocampus. The findings presented f i t well with the investigations of Leichnetz and Astruc ( '75, '76) and Rosene and Van Hoesen ( '77) mentioned above. Subicular connections with the temporal neocortex i n the rhesus monkey were described i n a recent paper of Van Hoesen and Rosene ( '78). Our r e s u l t s (1) support the opinion t h a t the subiculum i s t h e main nodal point f o r e x t r i n s i c hippocampal connections, ( 2 ) confirm the existence of a hippocampal output t h a t does not pass through the fimbria, and ( 3 ) suggest an increased significance o f the primate hippocampus influencing association and memory cortex, not only involving other p a r t s of the limbic system i n d i r e c t l y , b u t also by monosynaptic connections.
In t h i s respect, i t i s o f great i n t e r e s t t h a t neuroanatomical evidence gained by a1 1ometri cal comparisons shows t h a t i n primates the hi ppocampal FIGURE LEGENDS 1 Diagrams of cross-sections a t middle ( a , b) and caudal ( c , d ) l e v e l s of the hippocampus, showing d i f f e r e n t i n j e c t i o n sites (black d o t s ) . d dentate gyrus, l g l a t e r a l geniculate body, p presubiculum, r red nucleus, rt r e t i c u l a r thalamic nucleus, s subiculum, s c superior c o l l i c l e , 1 CA1, 3 CA2/3, VIII vestibulocochlear nerve. 2 HRP-labelled c e l l s (arrowheads) i n layers 111 and VI of p a r i e t a l cortex (HRP-injection i n t o CA1 and subiculum). Borders o f layers I-VI and white matter (wm) a r e marked a t the r i g h t . Bar = 100 pm. 3 HRP-labelled c e l l s in layers 111, V , VI o f the perirhinal cortex (above the border marked by arrows), some also i n t h e adjacent area 20 (below arrows). HRP-injection i n t o CA1 and subiculum. Photograph Borders o f layers I-VI and white matter (wm) a r e turned by 90'. marked on t h e top. Bar = 100 vm. 4 Dense autoradiographic l a b e l l i n g over t h e subiculum. Injection o f HRP+proline i n t o grey matter of areas 20/21. Photograph turned by sh sulcus hippocampi. Bar = 100 pm. 90°. Figures 2-4 a r e s l i g h t l y retouched t o remove d i r t and excessive background 1abel 1 i ng .
80
formation i s a progressive s t r u c t u r e from t h e aspect of phylogeny and reaches i t s r e l a t i v e l y l a r g e s t s i z e i n man (Stephan and Andy, '70).
I t i s suggested
t h a t t h e r e has been a progressive neocorticalisation o f hippocampal connections during the phylogenic evolution o f primates, a s no d i r e c t hippocampo-neocortical connections a r e known from other animals. The systematic position of C a l l i t h r i x i s t h a t of a lower simian primate
w i t h a r e l a t i v e l y unspecialized brain.
Further comparative s t u d i e s a r e intended
which may help t o e l u c i d a t e t h e question a t which phylogenic level t h e formation of monosynaptic hippocampo-neocortical connections was established. ACKNOWLEDGMENTS The author thanks Prof. Dr. Rolf Hassler f o r h i s i n t e r e s t and discussion, Barbara Hechler f o r technical assistance,and Dr. John Sarvey f o r reading t h e English manuscript.
LITERATURE CITED Brodmann, K. 1909 Vergleichende Lokalisationslehre der Groghirnrinde. Johann Ambrosius Barth, Leipzig. Graham, R . C . , M . J . Karnovsky 1966 The e a r l y stages of absorption o f injected horseradish peroxidase i n t h e proximal tubules of mouse kidney: u l t r a s t r u c t u r a l cytochemistry by a new technique. J . Histochem. Cytochem., 14: 291-302. Le chnetz, G . R . , J . Astruc 1975 Preliminary evidence f o r a d i r e c t projection of t h e prefrontal cortex t o the hippocampus i n t h e s q u i r r e l monkey. Brain Behav. Evol . , 11: 355-364. Le chnetz, G. R., J . Astruc 1976 The e f f e r e n t projections of the medial prefrontal cortex i n t h e s q u i r r e l monkey (Saimiri sciureus). Brain Res., 109: 455-472. Meibach, R . C . , A. Siege1 1977 Subicular projections t o t h e posterior cingulate cortex in r a t s . Exp. Neurol., 57: 264-274. Rosene, D. L., G. W. Van Hoesen 1977 Hippocampal e f f e r e n t s reach widespread areas o f cerebral cortex and amygdala i n the rhesus monkey. Science, 198: 315-317. Stephan, H., O.J. Andy 1970 The allocortex in primates. In: The Primate Brain. Advances i n Primatology Volume 1. C . R. Noback and W . Montagna, eds.,Appleton-Century-Crofts, New York, pp. 109-135. Van Hoesen, G. W . , D. L. Rosene 1978 Non-entorhinal projections t o t h e subiculum from temporal neocortex i n t h e rhesus monkey. Anat. Rec., 190: 570.
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82
