The cingulate bridge between allocortex isocortex and thalamus.

The Cingulate Bridge between Allocortex, lsocortex
and Thalamus
ERVIN W. POWELL
Department ofAnatomy, College of Medicine, University ofArkansas for Medical
Sciences, Little Rock, Arkansas 72201
ABSTRACT
The Fink-Heimer silver impregnation and the autoradiographic
methods were used to study the fiber projections of the cingulate cortex in the
squirrel monkey. I t was found t h a t this cortex provides inputs to the striatum,
thalamus and several areas of isocortex. Evidence was found for a number of fiber
projections (1) Fibers from the anterior limbic area were traced to the central
part of the head of the caudate nucleus, putamen, septum, dorsomedial nucleus of
the thalamus, anterior hypothalamus and lateral basal nucleus of the amygdala.
(2) Projections from the cingulate area were traced to the lateral part of the head
of the caudate nucleus, putamen, and to t h e centromedian, anterior, lateral dorsal, and lateral ventral thalamic nuclei and to medial nuclei of the base of the
pons. (3) There were projections from t h e retrosplenial area of the anterior, latera l dorsal, dorsomedial, and posterior thalamic nuclei and lateral nuclei of the
pons. These results indicate t h a t most of the cingulate gyrus is a n intermediate
structure between the thalamus and overlying cortex. The anterior limbic area
forms a bridge between the thalamus and other areas of the cingulate gyrus and
the frontal cortex. (4) The retrosplenial area and the posterior part of the cingulate area bridge the adjacent visual sensory association cortex and pelvic areas of
the sensory motor cortex, respectively. These areas of the cingulate gyrus project
directly to the striatum as well as to the thalamus, structurally providing limbic
system input to subcortical motor structures.
The cingulate gyrus has been considered a n
important cortical component of the limbic
system since Papez ('37) proposed a n anatomical system of emotion. Although projections of
the cingulate gyrus have been studied in the
rat and cat, knowledge of the role and connections of the cingulate gyrus as applicable to
primates is not yet adequate (Adey and Meyer,
'52; Showers, '59; Kreig, '63; Siegel et al., '73).
The anterior thalamic nuclei have been described as receiving most of the topographi c a l p r o j e c t i o n s of t h e c i n g u l a t e g y r u s
(Gerebtschoff and Wauters, '41-'43; Kreig,
'63; Siegel et al., '73; Powell et al., '74). On
t h e other hand, some studies have suggested
the absence of cingulothalamic projections
(Cragg and Hamlyn, '59; Powell and Cowan,
'64). Other workers have reported a large
number of connections from the cingulate
gyrus to extracingulate cortical gyri in the cat
(Airapetyants and Sotnichenko, '67; Powell et
al., '74). The purpose of this study is to investiANAT. REC. (1978) 190: 783-794.
gate the projections from the cingulate gyrus
and to discern what are the major nuclei of
termination of those projections in a primate,
the squirrel monkey. If, as implied above,
cingulothalamic projections are sparse, and
cingulocortical projections are more numerous than subcortical ones, then the cingulate
gyrus may be a n important limbic system link
between the thalamus and isocortex.
MATERIALS AND METHODS
Adult squirrel monkeys of both sexes weighing a t least 500 g were used in these studies.
Anesthesia was induced by ketamine hydrochloride, 25 mg/kg intramuscularly, supplemented as needed. Prior to stereotaxic surgery, analgesia of the scalp was produced locally with 2%Xylocaine containing epinephrine.
Electrolytic lesions were produced in 22 aniReceived July 25, '77. Accepted Oct. 31, '77
783
784
ERVIN W. POWELL
mals, unilaterally, in one of three loci (fig. 1):
(a1 anterior limbic region Brodmann's areas
24, 25, 32 (A 15-23, L 0.25, H 10.0); (b) cingulate region Brodmann's area 23 (A 6-12, L
0.25, H 10.5); and (c) retrosplenial region
Brodmann's areas 29, 30 (P 1-A 2, L 0.25, H 810) according to Emmers and Akert ('63). The
lesions were produced by 2 ma of current acting for 15 seconds, using a 0.3-mm calibre electrode as the anodal pole.
After allowing six days for the development
of maximal argyrophilia of degenerating axons, preterminals and terminals (Powell and
Schnurr, '721, the animals were perfused with
10% formalin in 0.9% saline while deeply
anesthetized; and the brains were treated subsequently essentially as described by these
authors. The brains were immersed in 30% sucrose solution for three days prior to cutting
frozen coronal sections. Selected sections were
impregnated with silver a s described by Fink
and Heimer ('67) and modified by Powell and
Brown ('75). Additional sections were counterstained with cresyl violet to localize the lesion
and the nuclei of the brain stem.
Tritiated leucine was used in eight other
monkeys to label the fast protein anterograde
component in loci corresponding to those in
which lesions had been placed. The same procedures were followed except a 26-gauge needle (attached to a 10-pl Hamilton syringe),
instead of an electrode, was placed stereotaxically using the same coordinates (fig. 1).
Aliquots (0.2 pl) of L-(4,5-3H-)leucine in normal saline were injected a t 1-minuteintervals
until five injections had been made (1 p l
total). The needle was left in place another
five minutes to minimize reflux and dispersion of the solution. The labeled leucine (New
England Nuclear) had a specific activity of 5
Ci/mmole and was concentrated to 10 Ci/pl.
The animals were allowed a period of 24 to
26 hours for translocation of the labeled fast
protein component (Lasek, '701, and then were
sacrificed and prepared as described above.
Rather than frozen sections, however, 8-pm
paraffin sections were cut and every twentieth section from genu to splenium of the carpus callosum was selected. The sections were
mounted on slides, processed for autoradiographic study, and counter-stained with
cresyl violet according to the procedure described by Cowan e t al. ('72). Silver grains
were resolved satisfactorily at a magnification of 1,000 x microscopically, and counts
per 1,000 pm2 were made with the aid of
a square grid ocular reticule. Background
counts were obtained from blank slides similarly processed, and from contralateral neutral areas of sections such as isocortex, pons,
and ventral lateral nucleus of the hypothalamus.
RESULTS
Both methods produced evidence of projections to cingulate cortex and to isocortical
areas overlying the cingulate gyrus. Other
cortical areas receiving projections were the
superior frontal gyrus, the parietal operculum
and the hippocampal gyrus (figs. 2-41. All of
the described projections were observed to be
most abundant on the side of the lesion or
injection site and therefore the ipsilateral projections only were studied in detail.
Differences in the topography of projection
appear in the results between the two methods
used and may be explained on several different bases:
1. The silver method as opposed to the autoradiographic method, destroys overlying cortical and fiber projections in addition to those of
the cingulate gyrus and cingulum due to penetration of the electrode. This destruction results in argyrophilia which could account for
projections seen using the silver method and
which were not seen using autoradiographic
methods.
2. Some topographic differences could be
attributed to slight differences of size and
location of foci since none could be expected to
be exactly identical from one brain to the
next, e.g., anterior nuclei (SM-70) vs. those for
(SM-85).
3. The different staining chemistry of the
two methods could account for some seeming
indiscrepancies, i.e., the chemistry of silver
impregnation of a degenerating axon is different than that of incorporating radioactive
amino acids into neuronal protein constituents. In the case of the latter, possibly, only
the larger functional ones are successfully labeled. In the case of using silver impregnation
methods, possibly certain terminals are less
tenaciously impregnated. This is most often
attributed to their small size rather than to
their metabolic state. The negative data of
either method used in this study is not helpful.
My opinion after using both is that the silver
impregnation methods usually reveal degeneration that is not clearly relevant to the anatomical system being studied and the autoradiographic method is reluctant to label all of
785
CINGULATE PROJECTIONS
A bbreuiations
Ac, Anterior commissure
Ag, Silver impregnation method
Ah, Anterior hypothalamus
Al, Anterior limbic area
Am, Anteromedial nucleus of thalamus
Av, Anteroventral nucleus of thalamus
B, Background grain count11.000 pm*
Cb, Cerebellum
Cc, Corpus callosum
Cd, Caudate
Cg, Cingulate gyrus
Cm, Centromedian nucleus of thalamus
Cn, Cingulate area
Cp, Cerebral peduncle
Cr, Corona radiata
Dm, Dorsomedial nucleus of thalamus
Ec, External capsule
Fb, Fornixbody
Fc, Fornix column
Gp, Globus pallidus
3H, Autoradiographic method
Hg, Hippocampus gyrus
Hp, Hippocampus
Ic, Internal capsule
In, Insular cortex
Ip, Interpeduncular nucleus
Lb, Basal lateral nucleus of amygdala
Ld, Lateral dorsal nucleus of thalamus
Lg, Lateral geniculate body
Lp, Lateral posterior nucleus of thalamus
Mb, Mammillary body
Oc, Optic chiasma
Ot, Optic tract
Pg, Periaqueductal gray
Pn, Pons
Ps, Presubiculum
Pt, Pretectum
Pu, Putamen
Pv, Pulvinar
Re, Retrospinal area
Sb, Subiculum
Sc, Superior colliculus
Se, Septum
Sf, Superior frontal gyrus
Sm, Squirrel monkey (case number follows)
Sn, Substantia nigra
So, Supraoptic nucleus
Sp, Superior cerebellar peduncle
Su, Subthalamus
Th, Thalamus
V, Ventricle
Va, Ventral anterior nucleus of thalamus
V1, Ventral lateral nucleus of thalamus
Vp, Ventral posterior nucleus of thalamus
Cb
Fig. 1 Foci for three representative pairs of cases. Three cases illustrate t h e results obtained using the silver impregnation method in this study (SM-71,SM-60 and SM-70). and three were selected to illustrate the results obtained using the
autoradiographic method (SM-84, SM-80 and SM-85). The cytoarchitectural areas of the medial hemisphere are indicated
by Brodmann’s numbers. The cytoarchitecture of the cingulate gyrus for lesions anterior to SM-60 and SM-80 was agranular cortex typical of the anterior limbic area, while for SM-60and SM-80 and lesions posterior to them it was granular cortex, found in cingulate and retrosplenial areas.
SM-84
'H
SM-71
Ag
Fig. 2 Degeneration (SM-71) and grain (SM-84) patterns observed as projecting from the anterior limbic area. Grain
counts for the most dense 1,000/*m' are shown for the main structures. B = 6 indicates the background level. The count for
the cingulate gyrus was taken 3 mm posterior to the injection focus. The A-P stereotaxic coordinates for diagrams from left
to right are: A,51(note lesion and injection foci), A,,, A,,,, and A,,, respectively (Emmers and Akert, '63).
CINGULATE PROJECTIONS
TABLE 1
Grain counts obtainedl1,OOO pn'
Structure
SM-84
cg
Sh
Pu
Cd
Lh
12
7
so
133
92
v1
Av
Am
Ld
Dm
LP
Cm
Pv
Ah
Pt
Pn
Background
23
21
20
8
s7
6
8
7
38
8
6
6
'
SM-80
SM-85
138
12
43
86
cil
75
14
43
91
19
20
17
25
73
18
20
12
17
8
12
159
133
-
155
158
Is2
8
71
16
53
e
43
10
8
' Only the counts underlined are considered t o represent targets
above background counts.
the reported known anatomy of the system
being studied.
Anterior limbic area
Degenerated fibers of passage, as impregnated by t h e Fink-Heimer I method, were consistently traced across the cingulum and corona radiata into the internal capsule (fig. 2:
SM-71). Collateral branches were traced to
t h e central part of t h e head of the caudate nucleus and putamen where argyrophilia representative of preterminals and terminals was
observed. Most of the axons traced through
t h e internal capsule coursed to the thalamus
via the dorsal thalamic peduncle (fig. 2).
Argyrophilia, which included terminal and
preterminal degeneration, was observed in
lateral thalamic nuclei, dorsomedial nucleus,
subthalamus, and dorsal hypothalamus (figs.
2, 5).
A number of fibers were traced posteriorly
in the medial part of the cerebral peduncle to
degeneration in the ipsilateral medial nuclei
of t h e basis pontis. Some fine argyrophilia was
seen in t h e dorsal periaqueductal gray. No
axons or terminals were impregnated in t h e
anteroventral and anteromedial nuclei of the
thalamus from this area of the cingulate
gyrus. I t would be i n t e r e s t i n g t o know
whether or not t h e density in the number of
argyrophilic deposits representing axonal de-
787
generation in a target nucleus is indicative of
the number of preterminal and terminal fibers
in t h a t structure.
Results using the autoradiographic method
also revealed t h e central part of the caudate
and putamen to be targets of projections from
this area of t h e cingulate gyrus (fig. 2: SM-84;
table 1). There was some spread of leucine to
cells in t h e ventromedial part of the superior
frontal gyrus in this case. Dark grains, representing transported 3H-leucine,were observed
in the septum, lateral part of the dorsomedial
nucleus of t h e thalamus, anterior hypothalamus (level not shown), and in the basal lateral
amygdaloid nucleus. No grains above background levels were observed in other amygdaloid, thalamic, or hypothalamic nuclei,
subthalamus, base of pons, or periaqueductal
gray.
Cingulate area
Degenerated axons impregnated by use of
t h e Fink-Heimer method were traced laterally
across the cingulum to the corona radiata and
internal capsule (fig. 3: SM-60). Degeneration
in target nuclei, including associated terminals and preterminals hereafter referred to as
terminal degeneration, was observed in the
dorsolateral head of the caudate nucleus and
dorsolateral part of t h e putamen (fig. 3 , 5 ) . Degenerating fibers of passage were traced from
the internal capsule into the dorsal thalamic
peduncle to terminal degeneration in the
anteroventral nucleus of the thalamus. Terminal degeneration was also seen in the lateral part of t h e centromedian and lateral thalamic nuclei. Other fibers were traced from
t h e internal capsule into the subthalamus,
dorsal hypothalamus and substantia nigra via
the lenticular and thalamic fascicles. Degenerating terminals were observed in t h e ipsilatera1 medial nuclei of the base of the pons. A
few fibers in the external capsule were continuous with coarse terminals in the hippocampal gyrus.
Silver grains developed using autoradiography were obvious in the dorsal lateral part of
t h e head of t h e caudate nucleus, in the dorsal
lateral part of the putamen, and in the centromedian nucleus of the thalamus (figs. 3,
5:SM-80). Silver grains indicating target nuclei were observed over the ventral lateral,
medial part of the ventral posterior, and
anteroventral, thalamic nuclei, and the medial nuclei of t h e base of the pons (fig. 3; table
1).No grain counts above background levels
788
ERVIN W. POWELL
789
CINGULATE PROJECTIONS
TABLE 2
Comparison of results obtained usingsilver and autoradiographic methods
Limbic
Cingulate
Retrosplenial
Structure
cg
Sb
Pu
Cd
Lb
v1
Av
Am
Ld
Dm
LP
Cm
Pv
Ah
Pt
pg
Pn
Ag
3n
Ag
3n
Ag
w
+
0
+
+
+
+
+
0
0
0
+
+
+
+
0
+
+
+
0
+
0
0
0
0
(0
+)
0
(0
+)
(0
0
0
0
0
+
+
0
(0
+
+
+
+
+
+
+ )'
0
0
0
0
+
0
0
+)
+
0
0
0
+
+
+
+
+
0
+
+
+
+
0
0
+
+
0
0
0
0
+
0
0
0
0
+
+
+
+
+
0
(0
0
(0
+
+
0
+
+
+
+
0
+)
0
+)
0
+
' Data in parentheses represent areas positive for grain counts but negative in similar silver-impregnated cases. These differences appear to be due to the differences between the two techniques (fibers of passage and cell soma) and to the larger area of
the injection site, especially for the retrosplenial area.
were observed in the hippocampus, lateral
part of the ventral posterior nuclei of the thalamus, subthalamus, hypothalamus, substantia nigra or interpeduncular nucleus.
Retrosplenial area
Degenerated fibers of passage were traced
from the lesion through the corona radiata to
the white matter of the hippocampal gyrus
and subiculum and anteriorly in the cingulum
to more rostra1 areas of isocortex (fig. 4: SM70). Some coarse degeneration was followed
through the subiculum to the lacunar layer of
the hippocampus. The main bundle of degenerated fibers, however, was traced anteriorly
through the corona radiata to the dorsal thalamic peduncle where they entered the thalamus. Degenerated terminals were seen in the
lateral posterior, lateral dorsal and dorsomedial nuclei. A few were observed in the ventral part of the anteromedial nucleus, medial
part of the head of the caudate nucleus, periaqueductal gray, and lateral nuclei of the base
of the pons. None were found in the putamen.
Silver grains developed using autoradiography were seen in the medial part of the head of
the caudate nucleus, the anteroventral, anteromedial, lateral dorsal, dorsomedial, lateral posterior and pulvinar thalamic nuclei as
well as in the pretectum and lateral nuclei of
the base of the pons (figs. 4, 5; table 1:SM-85).
Grain counts slightly above background were
observed in the presubiculum (table 1) and
prestriatal cortex. No grains were seen in the
hippocampus or periaqueductal gray in contrast to the degenerated fibers seen using the
Fink-Heimer method (table 2).
DISCUSSION
The results support previous studies in the
abundance and in the specificities of projections found (Adey and Meyer, '52; Airapetyants and Sotnichenko, '67; Powell et al., '74).
The cingulate gyrus has been suggested as
forming a link between allocortex and
isocortex (Sanides, '70;Chronister and White,
'75). The proposal by Papez ('37) and the data
from retrograde studies of thalamic nuclei
show that the cingulate gyrus receives many
connections from anterior thalamic nuclei.
The anterior thalamic nuclei are structures
where there is convergence of anatomical projections from the hippocampus, septum, mammillary body, and parts of the cingulate gyrus
(Powell, '73; Powell e t al., '74; this study).
Data from this anterograde study (cingulothalamic projections) and data from retrograde (thalamocingulate projections) studies
of others (Cowan and Powell, '54; Yakovlev e t
al., '60; Powell and Cowan, '64) imply that
there are more thalamocingulate projections
than there are cingulothalamic ones. Our observations also indicated that anterior parts
of the cingulate gyrus have many connections
790
ERVIN W. POWELL
CINGULATE PROJE CTIONS
791
Fig. 5 Top half, comparison of silver-impregnated sections (Ag) and grain PH)densities using autoradiographic methods in the anteroventral nucleus (Av) none from the anterior limbic area (SM-71and SM-841, the cingulate area (SM-60 and
SM-80) and the retrosplenial area (SM-70 and SM-85). Bottom half, comparison of silver-impregnated sections (Ag) from
SM-60 with the grain density, using autoradiographic methods, from SM-80 in caudate (Cd),putamen (Pu),and centromedian (Cm) from the cingulate area. The possible reasons for differences in amounts of projection shown by the two methods
are stated on page 784. These photographs represent the quantitative comparisons made on the basis of counts given in
table 1 and the impressions gained from a continuous study of the silver impregnated material. The calibration mark applies for all photographs in each row.
792
ERVIN W. POWELL
ISOCORTEX
Frontal Cortex
tl'
ALLOCORTEX
CINGULATE
BRIDGE
Fig. 6 Diagram of cingulate bridge between allocortex, isocortex and thalamus as proposed in this paper.
posteriorly while posterior areas of the cingulate gyrus have many projections anteriorly
via the cingulum. Therefore, the cingulate
gyrus provides an anatomical bridge between
the thalamus and isocortex as well as between
the allocortex and proisocortex and isocortex
as suggested by Chronister and White ('75).
This structural bridge for the anterior limbic
area would be primarily from the anterior nuclei to the frontal lobes. These connections
might account for the short latency responses
recorded by Desiraju ('76) in the frontal cortex following stimulation of the anterior limbic area.
This study shows cingulate connections to
the centromedian nucleus of the thalamus.
Functional and anatomical relations between
the centromedian nucleus and the striatum
have been reported (Powell and Cowan, '56;
Krauthamer and Bagshaw, '63; Bowsher, '66).
Projections from frontal and cingulate cortex
to the centromedian nucleus provide a structural basis for interal activation (selective?)
a t the revel of the caudate nucleus. Bowsher
('66) found that stimulation of the centromedian nucleus inhibited unit firing in the caudate nucleus in the monkey. Talairach et al.
('73) reported that stimulation of the anterior
limbic area produced patterns of sucking,
palpation, or nibbling accompanied by EEG
rhythms of 3-8 c/sec. Such effects on motor activity would be in addition to primary motor
regulation from the cerebellum through ventrolateral and centromedian nuclei.
This study supports claims (Adey and
Meyer, '62; Raisman et al., '65; Airapetyants
and Sotnichenko, '67; Pandya et al., '73) that
fibers of the retrosplenial area of the cingulate gyrus terminate in the hippocampal
gyrus and presubiculum but do not terminate
in Ammon's horn. Argyrophilia seen in layers
of Ammon's horn was probably due to damage
of fibers other than cingulofugal ones contained in the angular bundle, since no terminals were found nearer to the hippocampus
than the presubiculum in any of the sections
studied using the autoradiographic method.
Connections of the cingulate gyrus to cortical association areas, i.e., limbic area to frontal cortex, cingulate area to somatosensory
cortex, and retrosplenial area to visual association cortex, as well as those to sensory association nuclei of the thalamus (Locke and Kerr,
'73; Granier e t al., '70; Yakovlev and Locke,
'611, form pathways which could provide sensory information to limbic structures of the
temporal lobe and insula. This further supports the idea of the cingulate gyrus as a
structural bridge of proisocortex between
allocortex on one hand and isocortex on the
other (fig. 6).
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