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J Neurosurg 90:720–733, 1999

Topographic anatomy of the insular region

UĞUR TÜRE, M.D., DIANNE C. H. YAŞARGIL, R.N., OSSAMA AL-MEFTY, M.D.,


AND M. GAZI YAŞARGIL, M.D.

Department of Neurosurgery, University of Arkansas for Medical Sciences, Little Rock, Arkansas

Object. The insula is one of the paralimbic structures and constitutes the invaginated portion of the cerebral cortex,
forming the base of the sylvian fissure. The authors provide a detailed anatomical study of the insular region to assist
in the process of conceptualizing a reliable surgical approach to allow for a successful course of surgery.
Methods. The topographic anatomy of the insular region was studied in 25 formalin-fixed brain specimens (50 hemi-
spheres). The periinsular sulci (anterior, superior, and inferior) define the limits of the frontoorbital, frontoparietal, and
temporal opercula, respectively. The opercula cover and enclose the insula. The limen insula is located in the depths of
the sylvian fissure and constitutes the anterobasal portion of the insula. A central insular sulcus divides the insula into
two portions, the anterior insula (larger) and the posterior insula (smaller). The anterior insula is composed of three prin-
cipal short insular gyri (anterior, middle, and posterior) as well as the accessory and transverse insular gyri. All five gyri
converge at the insular apex, which represents the most superficial aspect of the insula. The posterior insula is com-
posed of the anterior and posterior long insular gyri and the postcentral insular sulcus, which separates them. The ante-
rior insula was found to be connected exclusively to the frontal lobe, whereas the posterior insula was connected to both
the parietal and temporal lobes. Opercular gyri and sulci were observed to interdigitate within the opercula and to inter-
digitate the gyri and sulci of the insula. Using the fiber dissection technique, various unique anatomical features and
relationships of the insula were determined.
Conclusions. The topographic anatomy of the insular region is described in this article, and a practical terminology
for gyral and sulcal patterns of surgical significance is presented. This study clarifies and supplements the information
presently available to help develop a more coherent surgical concept.

KEY WORDS • insula • limbic system • anatomical study • operculum •


paralimbic system • sylvian fissure

N humans, the insula (island of Reil) is a highly devel- the putamen, the anterior and posterior limbs of the inter-

I oped structure, totally encased within the brain. Be-


cause of its location at the base of the sylvian fissure
and the covering provided by the frontoorbital, frontopari-
nal capsule, the amygdala, the hippocampus, and various
portions of the lateral ventricle necessitate opening the
sylvian fissure along its entire length, which exposes the
etal, and temporal opercula, it only becomes visible when entire insula and ensures adequate access to these areas.
the sylvian fissure is widely opened. The insula is one of Compared with the numerous published investigations
the paralimbic structures known as the mesocortex, which relating to the functional anatomy of the insula,1–3,9,13,15,
is anatomically and functionally interposed between the 19,20,25,26,33–35
there are few studies in which the topographic
allocortex and the neocortex.19 In many clinical and exper- anatomy of the insular region is described and most of
imental studies, a variety of functions have been attributed these were conducted by early anatomists.7,8,12,14,16,29,30,40,42 A
to the insula, such as memory, drive, affect, higher auto- detailed and discerning account of the topographic anato-
nomic control, gustation, and olfaction; however, the full my of the insula and its relationships with overlying oper-
and comprehensive role that it plays continues to remain cula and adjacent structures will be beneficial, offering
obscure.1,5,6,9,13,14,19,20,23,25,27,33–36,41 sound basic knowledge that will contribute to preoperative
Opening the sylvian fissure provides a “gateway” into planning and to subsequent successful realization of sur-
various regions of the brain. The circle of Willis, the sel- gical strategy. The purpose of this study is to describe the
lar and parasellar areas, and the mediobasal temporal re- anatomy of this region concisely, to present detailed
gion can be accessed after opening the sylvian fissure, anatomical relationships of the insula and opercula to
which reveals the anterobasal portion of the insula. When neighboring structures, and to supplement this informa-
epileptic foci, tumors, or vascular lesions involve the insu- tion with a sequence of composite determinants that will
la and its opercula, more extensive exploration of the syl- aid in the definitive identification of various landmarks
vian fissure is necessary. Access to deep lesions located in of insula structures intraoperatively. Implementing surgi-

720 J. Neurosurg. / Volume 90 / April, 1999


Topography of the insula

TABLE 1 opercularis. The posterior ramus separates the frontal and


Measurements of the sylvian fissure and the insula parietal lobes from the temporal lobe and forms the syl-
vian line, which in our specimens averaged 75 mm (range
Measurements (mm) 59–86 mm) in length. The posterior ramus is composed of
Structures* Average Range the diagonal sulcus, the anterior and posterior subcentral
sulci, and the terminal ascending and descending limbs, as
sylvian stem (A–B) 39 30–56 well as the side branch of the transverse temporal sulcus.
posterior ramus (A–C) 75 59–86 The horseshoe-shaped supramarginal gyrus drapes over
preinsular sulcus (sylvian vallecula) (D–E) 32 27–35
postinsular sulcus (F–C) 38 35–42 the superior boundary of the posterior ramus.
limen insula–insular apex (E–A) 14.8 12–17 The floor of the sylvian stem constitutes the preinsular
insular apex–superior insular sulcus (A–G) 19.1 17–23 sulcus (sylvian vallecula), which corresponds to the ante-
* Letter coding applies to length of structure or distances between struc- rior perforated substance. The average length of the prein-
tures, as seen in Fig. 4. sular sulcus was 32 mm (range 27–35 mm) in the brain
specimens. The sylvian stem has adapted to the contours
of the posterior border of the lesser wing of the sphenoid
cal tactics derived from this knowledge of anatomy en- bone.24,32,37,42 The floor of the posterior ramus of the syl-
sures the recognition of relevant anatomical landmarks vian fissure is composed of the insula and postinsular sul-
that guide surgical approach and enhance exploration of cus. The average length of the postinsular sulcus measured
the insula and the surrounding region. 38 mm (range 35–42 mm, Table 1 and Figs. 1–4).

Adult Insula
Materials and Methods
The human adult insula is completely enclosed and con-
The topographic anatomy of the insular region was studied in 25 cealed within the sylvian fissure; it only becomes visible
formalin-fixed adult human brain specimens (50 hemispheres). The following divarication of the fissure. Removal of the fron-
specimens were obtained after routine autopsy procedures had been
performed and were preserved in 10% formaldehyde solution for a toorbital, frontoparietal, and temporal opercula reveals the
minimum of 2 months. To maintain the true anatomical contours of entire insula in the shape of a pyramid. The anterior, supe-
the specimens, each was suspended in the solution from the basilar rior, and inferior periinsular sulci clearly demarcate the
artery. Special emphasis was placed on the following: examining insula and distinguish it from surrounding cortical areas,
the anatomical variations of the sulci and gyri of the insula and their except in the region of the limen insula. The anterior peri-
relationships to the opercula; defining the relationships between the insular sulcus separates the anterior surface of the insu-
insula and the lateral ventricle and neighboring structures; and
examining the location of the insula corresponding to surgically rel- la from the frontoorbital operculum. The length of this
evant landmarks on the brain surface, in particular the sylvian fis- sulcus averaged 28.4 mm (range 23–34 mm) in our
sure. Ten of our specimens were studied under the operating mi- specimens. The superior periinsular sulcus separates the
croscope with the aid of the fiber-dissection technique.17,18,38 This superior surface of the insula from the frontoparietal op-
ensured a comprehensive analysis of the deep structures of the brain erculum and averaged 57.6 mm (range 51–68 mm) in
as well as of the cerebral fiber system adjacent to the insula. Taking length. The inferior periinsular sulcus separates the inferi-
into account the evaluations of previous studies, we suggest an
expanded nomenclature for the various regions of the insula and or surface of the insula from the temporal operculum. The
opercula. length of this sulcus averaged 49.2 mm (range 42–61
mm). The summit of the pyramid-shaped insula is termed
the “insular apex;” its most superficial point averaged 12.6
Results mm (range 9–16 mm) from the lateral cerebral sur-
Sylvian Fissure
face. On the same plane as the insular apex, the temporal
operculum covers the inferior portion of the insula for an
The sylvian fissure is the deep and prominent cerebral average distance of 14.8 mm (range 12–17 mm). The fron-
fissure traversing the inferior and lateral surfaces of the toparietal operculum covers the superior surface of the
brain and extending from the anterior perforated sub- insula for an average distance of 19.1 mm (range 17–23
stance to the supramarginal gyrus. It separates the frontal mm, Tables 1–3 and Figs. 1–8).
and parietal lobes from the temporal lobe, and the insula The insular stem is located in the depths of the sylvian
forms its floor. The sylvian fissure is divided into anterior fissure and constitutes the anterobasal portion of the insu-
(stem) and posterior (insuloopercular) compartments. The la. The limen insula is located in the insular stem and con-
stem originates inferiorly at the anterior perforated sub- sists of a narrow strip of olfactory cortex. This structure is
stance located at the level of the ambient gyrus of the located at the narrow cleft between the insula and lateral
uncus and extends laterally between the orbital gyri and limit of the sylvian vallecula and extends along the lateral
the temporal pole. The average length of the sylvian stem aspect of the lateral olfactory stria, which conjoins the
measured 39 mm (range 30–56 mm) in the specimens insular cortex and the anterior perforated substance.31 The
studied. The temporal incisura and the frontoorbital limb average width of the sylvian vallecula measured 3.9 mm
are two side branches of the sylvian stem. As the stem (range 3–6 mm).
reaches the lateral surface of the brain, it divides into the The central insular sulcus, the main and deepest sulcus
horizontal, ascending, and posterior rami; we have named of the insula, courses obliquely across the insula, pursuing
the confluence of these three rami the “sylvian point.” The a similar direction to the central sulcus of Rolando. It
horizontal and ascending rami divide the inferior frontal divides the insula into two zones that are unequal in size:
gyrus (F3) into the pars orbitalis, pars triangularis, and pars the anterior insula (larger) and posterior insula (smaller).

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U. Türe, et al.

FIG. 1. Photographs of brain specimens. Upper: The sylvian fissure is located in the lateral aspect of the left cere-
bral hemisphere. The frontoorbital, frontoparietal, and temporal opercula cover the insula. Lower: The insula is ex-
posed, following excision of the opercula, to the level of the periinsular sulci. Abbreviations with white letters denote
sulci and fissures. alg = anterior long insular gyrus; aps = anterior periinsular sulcus; ar = ascending ramus of sylvian fis-
sure; ascs = anterior subcentral sulcus; asg = anterior short insular gyrus; cis = central insular sulcus; cs = central sulcus
of Rolando; F2 = middle frontal gyrus; f2 = inferior frontal sulcus; hr = horizontal ramus of sylvian fissure; ia = insular
apex; ips = inferior periinsular sulcus; li = limen insula; log = lateral orbital gyrus; mog = medial orbital gyrus; msg =
middle short insular gyrus; op = pars opercularis of F3; or = pars orbitalis of F3; pcg = precentral gyrus; pcis = precentral
insular sulcus; pcs = precentral sulcus; pg = postcentral gyrus; pis = postcentral insular sulcus; plg = posterior long insu-
lar gyrus; pog = posterior orbital gyrus; ps = postcentral sulcus; pscs = posterior subcentral sulcus; psg = posterior short
insular gyrus; sis = short insular sulcus; smg = supramarginal gyrus; sps = superior periinsular sulcus; tg = transverse
insular gyrus; tr = pars triangularis of F3; T1 = superior temporal gyrus; T2 = middle temporal gyrus; T3 = inferior tempo-
ral gyrus; t1 = superior temporal sulcus.

In 90% of the hemispheres under investigation the central extension was interrupted at intervals, separating the sul-
insular sulcus was well defined, extending from the supe- cus into various parts.
rior periinsular sulcus to the limen insula in an uninter- The anterior insula, the larger of the two zones, exhibits
rupted line. At its deepest point, it measured an average more gyri than the posterior insula. The anterior insula is
of 5.1 mm (range 4–6 mm). In the remaining 10% of the composed of the transverse and accessory insular gyri and
hemispheres, the sulcus was not well defined. Its line of three principal short insular gyri (anterior, middle, and

722 J. Neurosurg. / Volume 90 / April, 1999


Topography of the insula

FIG. 2. Artistic rendering of the left insular region (artificial retraction of opercula) with detailed nomenclature.
Abbreviations with white letters denote sulci and fissures. ag = accessory insular gyrus; ahg = anterior Heschl’s gyrus;
aip = anterior insular point; alg = anterior long insular gyrus; aog = anterior orbital gyrus; aps = anterior periinsular sul-
cus; ar = ascending ramus of sylvian fissure; as = acoustic sulcus; ascs = anterior subcentral sulcus; asg = anterior short
insular gyrus; atpg = anterior transverse parietal gyrus; atps = anterior transverse parietal sulcus; cis = central insular sul-
cus; cs = central sulcus of Rolando; ds = diagonal sulcus; fol = frontoorbital limb; fos = frontoorbital sulcus; gr = gyrus
rectus; gs = gyri of Schwalbe; hr = horizontal ramus of sylvian fissure; ia = insular apex; ips = inferior periinsular sul-
cus; li = limen insula; log = lateral orbital gyrus; los = lateral orbital sulcus; mog = medial orbital gyrus; mos = medial
orbital sulcus; msg = middle short insular gyrus; mtpg = middle transverse parietal gyrus; op = pars opercularis of F3;
or = pars orbitalis of F3; os = olfactory sulcus; pcg = precentral gyrus; pcis = precentral insular sulcus; pcs = precentral
sulcus; pg = postcentral gyrus; phg = posterior Heschl’s gyrus; pip = posterior insular point; pis = postcentral insular sul-
cus; plg = posterior long insular gyrus; plol = posterolateral orbital lobule; pmol = posteromedial orbital lobule; pog =
posterior orbital gyrus; pos = postinsular sulcus; ps = postcentral sulcus; pscs = posterior subcentral sulcus; psg = poste-
rior short insular gyrus; ptpg = posterior transverse parietal gyrus; ptps = posterior transverse parietal sulcus; scg = sub-
central gyrus; sis = short insular sulcus; smg = supramarginal gyrus; sopg = subopercular gyrus; sorg = suborbital gyrus;
spcg = subprecentral gyrus; sps = superior periinsular sulcus; ss = sulci of Schwalbe in polar planum; stg = subtriangu-
lar gyrus; tal = terminal ascending limb of sylvian fissure; tdl = terminal descending limb of sylvian fissure; tg = trans-
verse insular gyrus; ti = temporal incisura; tos = transverse orbital sulcus; tp = temporal pole; tpl = temporal planum;
tr = pars triangularis of F3; tts = transverse temporal sulcus; T1 = superior temporal gyrus; T2 = middle temporal gyrus;
t1 = superior temporal sulcus.

posterior). The transverse and accessory insular gyri form gyrus frequently extends completely across the anterior
the insular pole, which is located at the most anteroinferi- periinsular sulcus and becomes continuous with the corre-
or aspect of the insula. The posterior portion of the medi- sponding gyrus on the inner surface of the frontoorbital
al orbital gyrus and the medial portion of the posterior operculum as one of the suborbital gyri. In 48% of the
orbital gyrus form the posteromedial orbital lobule that hemispheres, the accessory insular gyrus was well devel-
becomes continuous with the transverse insular gyrus, oped and in 34% it was underdeveloped. In the remaining
extending to the insular apex (Figs. 1–3). The transverse 18% of the hemispheres, this gyrus was absent.
insular gyrus acts as a junction between the inferior por- The anterior and posterior short insular gyri are well
tion of the anterior insula and the posterior frontoorbital structured and convex, whereas the middle short insular
region. The transverse insular gyrus was well defined in gyrus is generally underdeveloped and only slightly con-
86% of the hemispheres; however, in the remaining 14% vex. The anterosuperior border of the anterior short insu-
it was underdeveloped. The accessory insular gyrus ex- lar gyrus, at its junction with the anterior and superior
tends from the anterior portion of the anterior short gyrus periinsular sulci, is termed the “anterior insular point.” In
and is located beneath the frontoorbital operculum, on the 8% of the hemispheres, a small depression was observed
superior aspect of the transverse insular gyrus. This small at the anterior insular point and, in 28% of the hemi-

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FIG. 3. Photographs of brain specimens. Upper: Inferolateral view of the left cerebral hemisphere following removal of the temporal
operculum through the inferior periinsular sulcus. The insula and its relationships to the frontoorbital and frontoparietal opercula are shown.
Lower: Superolateral view of the left cerebral hemisphere following removal of the frontoorbital and frontoparietal operculum through the
anterior and superior periinsular sulci, respectively. The insula and its relationship to the temporal operculum are shown. Abbreviations with
white letters denote sulci and fissures. a = amygdala; ag = accessory insular gyrus; ahg = anterior Heschl’s gyrus; aip = anterior insular point;
alg = anterior long insular gyrus; aog = anterior orbital gyrus; ar = ascending ramus of sylvian fissure; as = acoustic sulcus; ascs = anterior
subcentral sulcus; asg = anterior short insular gyrus; atpg = anterior transverse parietal gyrus; cis = central insular sulcus; cs = central sulcus
of Rolando; F2 = middle frontal gyrus; gr = gyrus rectus; h = hippocampus; hr = horizontal ramus of sylvian fissure; ia = insular apex; li =
limen insula; log = lateral orbital gyrus; los = lateral orbital sulcus; mog = medial orbital gyrus; mos = medial orbital sulcus; msg = middle
short insular gyrus; mtpg = middle transverse parietal gyrus; op = pars opercularis of F3; or = pars orbitalis of F3; os = olfactory sulcus;
pcg = precentral gyrus; pcs = precentral sulcus; pg = postcentral gyrus; phg = posterior Heschl’s gyrus; pip = posterior insular point; pis =
postcentral insular sulcus; plg = posterior long insular gyrus; plol = posterolateral orbital lobule; pmol = posteromedial orbital lobule; pog =
posterior orbital gyrus; pos = postinsular sulcus; ps = postcentral sulcus; pscs = posterior subcentral sulcus; psg = posterior short insular gyrus;
ptpg = posterior transverse parietal gyrus; scg = subcentral gyrus; sis = short insular sulcus; smg = supramarginal gyrus; spcg = subprecen-
tral gyrus; tg = transverse insular gyrus; tos = transverse orbital sulcus; tp = temporal pole; tpl = temporal planum; tr = pars triangularis of
F3; ts = temporal stem; tts = transverse temporal sulcus; T1 = superior temporal gyrus; T2 = middle temporal gyrus; t1 = superior temporal
sulcus.

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Topography of the insula

TABLE 3
Measurements from the insula to the cerebral surface
Measurements (mm)

Structures* Average Range

anterior insular point–lat cerebral surface (A–B) 24.4 23–27


posterior insular point–lat cerebral surface (C–D) 33.4 29–36
limen insula–temporal pole (E–F) 23.5 19–30
anterior insular point–frontal pole (A–G) 44.7 38–51
posterior insular point–occipital pole (C–H) 75.1 70–81
midsuperior periinsular sulcus–sagittal sinus (I–J) 47.2 40–52
FIG. 4. Schematic drawing showing the distances that were
midinferior periinsular sulcus–middle fossa (K–L) 27.1 23–31
measured relating to the sylvian fissure and the insula. Letter cod- insular apex–lat cerebral surface 12.6 9–16
ing is defined in Table 1.
* Letter coding applies to distances between structures, as seen in Fig. 8
lower.

spheres, a small sulcus had developed, forming a longitu-


dinal division in the superior portion of the anterior short
insular gyrus. In 74% of the hemispheres the area com- vian fissure as a common stem that we have named the
mon to all gyri of the anterior insula and the point from “postinsular sulcus.” The anterior and posterior long insu-
which they all appeared to originate is termed the “insula lar gyri are separated by the postcentral insular sulcus,
apex,” which is the portion nearest to the brain surface. In which was not well defined in 56% of hemispheres, its
the remaining 26% of the hemispheres, the short insular line of extension being interrupted at frequent intervals. In
sulcus, which separates the anterior and middle short insu- an additional 18% of the hemispheres, we observed only a
lar gyri, traverses the insular apex and continues as far as small depression in the posterosuperior portion of the
the limen insula. The precentral insular sulcus, which in- insula, which represented the postcentral insular sulcus. In
terposes the superior portions of the middle and posterior this latter instance, the two long gyri of the posterior insu-
short insular gyri, was merely a shallow depression in la were observed to unite at a site inferior to the postcen-
52% of the hemispheres; it was in these hemispheres that tral insular sulcus and to continue as a common stem as far
the middle short insular gyrus was found to be underde- as the limen insula. In the remaining 26% of the hemi-
veloped and only slightly convex. spheres, the postcentral insular sulcus appeared only as a
The posterior insula is separated from the anterior insu- very shallow indentation, and the posterior long gyrus was
la by the central insular sulcus and is composed of the found to be extremely underdeveloped.
anterior and posterior long gyri. The anterior long insular Measurements pertinent to the insula and related land-
gyrus is the larger and more developed. It was present marks are summarized in Tables 2 and 3.
in all hemispheres that we studied. The “posterior insular
point” is the term used to describe the confluence of the
superior and inferior periinsular sulci, which continue
along the deep portion of the posterior ramus of the syl-

TABLE 2
Measurements of the insula related to the sulci and the
lateral ventricle
Measurements (mm)

Structures* Average Range

anterior periinsular sulcus (A–B) 28.4 23–34


superior periinsular sulcus (A–C) 57.6 51–68
anterior portion (A–D) (37.8) (32–45)
posterior portion (D–C) (19.8) (13–23)
inferior periinsular sulcus (C–E) 49.2 42–61
anterior insular point–frontal horn of lat 11.5 9–15 FIG. 5. Photograph showing a sagittal section of the left cerebral
ventricle (A–F) hemisphere through the insula. Abbreviations with white letters
anterior insular point–floor of frontal horn of 11.3 10–13 denote sulci and fissures. ahg = anterior Heschl’s gyrus; alg = ante-
lat ventricle (A–G) rior long insular gyrus; aps = anterior periinsular sulcus; asg = ante-
posterior insular point–atrial portion of lat 10.9 8–13 rior short insular gyrus; atpg = anterior transverse parietal gyrus;
ventricle (C–H) cis = central insular sulcus; cs = central sulcus of Rolando; F2 =
central insular sulcus–body of lat ventricle (D–I) 20.2 16–23 middle frontal gyrus; f2 = inferior frontal sulcus; ips = inferior peri-
temporal stem (E–J) 10.8 9–14 insular sulcus; li = limen insula; msg = middle short insular gyrus;
periinsular sulcus–temporal horn (J–K) 9.2 7–11 pcg = precentral gyrus; pcs = precentral sulcus; pg = postcentral
* Letter coding applies to length of structure or distances between struc- gyrus; ps = postcentral sulcus; psg = posterior short insular gyrus;
tures, as seen in Fig. 8 upper. sps = superior periinsular sulcus; tg = transverse insular gyrus.

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U. Türe, et al.

The three opercula that cover the insula are separated by


the horizontal and posterior rami of the sylvian fis- sure.
The horizontal ramus interposes the frontoorbital and
frontoparietal opercula, and the posterior ramus interpos-
es the frontoparietal and temporal opercula.
Frontoorbital Operculum. The posterior orbital gyrus,
the posterior portion of the lateral orbital gyrus, and the
pars orbitalis of the inferior frontal gyrus (F3) constitute
the frontoorbital operculum that covers the anterior sur-
face of the insula. The anterior periinsular sulcus defines
the boundary between the frontoorbital operculum and the
insula. The posteromedial orbital lobule is located at the
medial extremity of the transverse orbital sulcus and is
composed of the posterior portion of the medial orbital
gyrus and the medial portion of the posterior orbital gyrus.
It becomes continuous with the transverse short insular
gyrus. The posterolateral orbital lobule is located at the
lateral extremity of the transverse orbital sulcus and is
composed of the lateral portion of the posterior orbital
gyrus and the posterior portion of the lateral orbital gyrus.
No clear margin between the lateral orbital gyrus and the
pars orbitalis of F3 was observed. Two suborbital gyri (su-
perior and inferior), located at the medial aspect of the
frontoorbital operculum, cover the anterior surface of
the insula. They are continuous with the accessory insular
gyrus and the anterior surface of the anterior short gyrus
(Figs. 1–8).
Frontoparietal Operculum. The pars triangularis and
pars opercularis of F3, the inferior portions of the precen-
tral and postcentral gyri, and the superior portion of the
supramarginal gyrus constitute the frontoparietal opercu-
lum, which covers the superior surface of the insula. The
posterior portion of this operculum also covers the tempo-
ral operculum, and the two opercula are separated by the
“postinsular sulcus,” which is located in the deep portion
FIG. 6. Photograph showing an axial section of the right cerebral of the posterior ramus of the sylvian fissure.
hemisphere through the insula, superior view. Abbreviations with
white letters denote sulci and fissures. ahg = anterior Heschl’s The superior periinsular sulcus defines the boundary
gyrus; alg = anterior long insular gyrus; aps = anterior periinsular between the frontoparietal operculum and the insula. The
sulcus; asg = anterior short insular gyrus; atpg = anterior transverse pars triangularis constitutes the area between the horizon-
parietal gyrus; bf = body of fornix; c = claustrum; cg = cingulate tal and ascending rami of the sylvian fissure. The hori-
gyrus; cis = central insular sulcus; cn = caudate nucleus; crf = crus zontal ramus of the sylvian fissure is an extension of the
of fornix; ec = external capsule; exc = extreme capsule; gcc = genu superior periinsular sulcus, and the ascending ramus is an
of corpus callosum; gp = globus pallidus; ic = internal capsule; extension of the anterior periinsular sulcus. The conflu-
ips = inferior periinsular sulcus; msg = middle short insular gyrus; ence of these sulci is identified as the “anterior insular
p = putamen; pcis = precentral insular sulcus; pis = postcentral point.” The medial aspect of the pars triangularis is termed
insular sulcus; plg = posterior long insular gyrus; psg = posterior the “subtriangular gyrus,” which covers and becomes con-
short insular gyrus; scc = splenium of corpus callosum; sf = sylvian
fissure; sis = short insular sulcus; t = thalamus. tinuous with the anterior short insular gyrus. The subor-
bital gyri and the subopercular gyrus cover the anterior
short insular gyrus anteriorly and posteriorly, respectively.
The pars opercularis of F3 constitutes the area between
Insula Related to the Opercula the ascending ramus of the sylvian fissure and the inferior
A layer of insular cortex lines the periinsular sulci and precentral sulcus and is known as Broca’s area (Area 44).
extends to interface each individual operculum. We cannot The diagonal sulcus traversed Broca’s area in 68% of the
confirm that the gyri and sulci of the insula are directly hemispheres. The medial aspect of the pars opercularis is
continuous with the corresponding gyri and sulci of the termed the “subopercular gyrus,” which covers the short
opercula but, in many specimens, a configuration ap- insular sulcus, the middle short insular gyrus, and the pos-
proaching continuity was observed. The anterior insula terior part of the anterior short insular gyrus. The subpre-
was observed to connect with the frontal lobe and the pos- central gyrus is located on the medial aspect of the pars
terior insula was seen to connect with both the parietal and opercularis and on the inferior precentral gyrus. It covers
temporal lobes. Gyri and sulci of the opercula were ob- the middle short insular gyrus and the precentral insular
served to interdigitate and to interdigitate the gyri and sul- sulcus.
ci of the insula. In 82% of the hemispheres the inferior extremity of the

726 J. Neurosurg. / Volume 90 / April, 1999


Topography of the insula

FIG. 7. Photograph showing a coronal section of the brain through the foramen of Monro and the amygdala, anterior
view. a = amygdala; ac = anterior commissure; ahg = anterior Heschl’s gyrus; alg = anterior long insular gyrus; bcc =
body of corpus callosum; bf = body of fornix; c = claustrum; cg = cingulate gyrus; cis = central insular sulcus; cn = cau-
date nucleus; cs = central sulcus of Rolando; ec = external capsule; exc = extreme capsule; fg = fusiform gyrus; gp =
globus pallidus; ic = internal capsule; ot = optic tract; p = putamen; ph = pes hippocampi; phg = posterior Heschl’s gyrus;
phig = parahippocampal gyrus; psg = posterior short insular gyrus; scg = subcentral gyrus; T1 = superior temporal gyrus;

central sulcus of Rolando did not extend as far as the syl- lum that covers the inferior surface of the insula and the
vian fissure. The subcentral gyrus is located at the medial anterior perforated substance. The polar planum, the ante-
aspect of both the inferior precentral and postcentral gyri rior and posterior Heschl’s gyri, and the temporal planum
and is demarcated either by the anterior or by the posteri- constitute the medial aspect of the temporal operculum
or subcentral sulcus. The subcentral gyrus covers the cen- (Figs. 2 and 3 lower). The lateral olfactory stria passes in-
tral insular sulcus. to the sylvian vallecula laterally and, at the limen insula,
The inferior postcentral gyrus and the superior portion angles medially, as far as the surface of the uncus, to be-
of the supramarginal gyrus comprise the remainder of the come, medially, the semilunar gyrus and, laterally, the
frontoparietal operculum. The anterior, middle, and poste- ambient gyrus, which are separated by the semiannular
rior transverse parietal gyri are located on the medial as- sulcus.31 The entorhinal sulcus separates the uncus and
pect of the frontoparietal operculum. The anterior trans- temporal operculum from the anterior perforated sub-
verse parietal gyrus covers the postcentral insular sulcus stance.11
and the superior portion of the anterior and posterior long The first side branch of the sylvian stem is termed the
insular gyri, which are adjacent to the anterior Heschl’s “temporal incisura,” which separates the piriform cortex
gyrus of the temporal operculum. The junction of the ante- from the temporal pole. The polar planum covers the li-
rior transverse parietal gyrus with the anterior Heschl’s men insula and the inferior surface of the insula and is
gyrus is identified as the “posterior insular point.” The adjacent to the inferior periinsular sulcus along two thirds
middle transverse parietal gyrus covers the transverse tem- of its length. Convolutions of the polar planum are termed
poral sulcus of the temporal operculum. The posterior the “sulci and gyri of Schwalbe.”13 The anterior Heschl’s
transverse parietal gyrus of the frontoparietal operculum gyrus is adjacent to the remaining third (the posterior
and the temporal planum overlap and form the medial portion) of the inferior periinsular sulcus. The trans-
aspect of the supramarginal gyrus (Figs. 1–8). verse temporal sulcus separates the anterior and posterior
Temporal Operculum. The superior temporal gyrus, to- Heschl’s gyri. The temporal planum constitutes the poste-
gether with the temporal pole and the inferior portion of rior portion of the inner surface of the temporal operculum
the supramarginal gyrus, constitute the temporal opercu- (Figs. 1–8).

J. Neurosurg. / Volume 90 / April, 1999 727


U. Türe, et al.

commissure, a portion of the occipitofrontal fasciculus,


and the inferior thalamic peduncle comprise the temporal
stem, which in our specimens measured an average of
10.8 mm in length (range 9–14 mm).
The putamen is located medial to the external capsule,
adjacent to the central portion of the insula. The average
length of the putamen was 44 mm (range 41–47 mm) and
the average height was 41 mm (range 38–44 mm). Dis-
section directed medially, in the region of the periinsular
sulci, leads directly to the internal capsule, whereas dis-
section through the central portion of the insula leads to
the putamen (Table 4 and Figs. 6, 7, 9–11).
Insula Related to the Lateral Ventricle
The insula is located adjacent to the lateral ventricle
and, with the exception of its anterobasal portion (insular
FIG. 8. Schematic drawings. Upper: Distances measured re- stem), is situated in the C-shaped curve of the ventricle.
lating to the insula and the lateral ventricle. Letter coding is defined The internal capsule separates the periinsular sulci from
in Table 2. Lower: Distances measured relating to the insula and the lateral ventricle. The superior periinsular sulcus fol-
various landmarks on the cerebral surface. Letter coding is defined lows a course adjacent to the frontal horn, body, and atri-
in Table 3. al portions of the lateral ventricle. Approximately four
fifths of the posterior portion of the inferior periinsular
sulcus follows a course adjacent to the temporal horn and
Insula Related to the Cerebral Fiber System and Basal atrial portions of the lateral ventricle. An average of 10.8
Ganglia mm (range 9–14 mm) of the anterior portion of the inferi-
or periinsular sulcus is formed by the temporal stem.
The extreme capsule, consisting of the subcortical white Approximately two thirds of the inferior portion of the
matter of the insula, unites with the white matter of the anterior periinsular sulcus is surrounded by the anterior
opercula (Figs. 6, 7, 9, and 10). Insular cortex and the limb of the internal capsule. An average of 11.3 mm
extreme capsule cover the claustrum, external capsule, (range 10–13 mm) of the superior portion of the anterior
putamen, and globus pallidus. The insula is surrounded by periinsular sulcus is located adjacent to the frontal horn.
the superior longitudinal (arcuate) fasciculus, a C-shaped In our specimens, the following measurements were
association fiber system of the brain connecting the tem- made and averages calculated: from the anterior insular
poral region to the parietal and frontal regions. The un- point to the frontal horn of the lateral ventricle, 11.5 mm
cinate fasciculus supplies the major source of inter- (range 9–15 mm); from the upper end of the central insu-
connection between limbic and paralimbic structures. For lar sulcus to the body of the lateral ventricle, 20.2 mm
instance, it links the insula to other paralimbic structures (range 16–23 mm); from the posterior insular point to the
(temporal pole and caudal portion of the orbital gyri) and atrial portion of the lateral ventricle, 10.9 mm (range 8–13
interconnects the limbic structures (the amygdala and mm); and from the midinferior periinsular sulcus to the
uncus to the subcallosal area and gyrus rectus) as the temporal horn, 9.2 mm (7–11 mm). The tip of the tempo-
fibers pass through the region of the limen insula. The ral horn was located an average of 10.8 mm (range 9–14
uncinate fasciculus can be compared with a series of mm) posterior to the limen insula, which constitutes the
leaves, placed one over the other, that are separated by temporal stem (Table 2 and Figs. 3 and 8 upper).
claustrum. The outer leaf forms part of the extreme cap-
sule, whereas the inner leaf contributes to the external cap-
sule.31 The claustrum is gray matter located between the Discussion
fibers that form the extreme and external capsules. The
occipitofrontal fasciculus passes beneath the inferior por- According to the literature, in 1786 Vicq d’Azyr39 was
tion of the insular cortex, within the extreme and external the first to declare an interest in the insula, which he
capsules, to connect the frontal, insular, temporal, and referred to as “the convolutions situated between the syl-
occipital regions. The close anatomical interrelationship vian fissure and the corpus striatum.” Monro21 published
between the occipitofrontal fasciculus and the uncinate an illustration showing three gyri of the human insula,
fasciculus prevents complete and precise dissection in this visualized after removing the ventral portion of the cere-
area (Fig. 9). brum, but he neither named nor described them. In 1809
The anterior commissure connects the homologous ol- Reil28 was the first to describe the insula, which he named
factory cortices, middle temporal gyri, and inferior tem- “die Insel,” and since that time the “insula” or “island of
poral gyri.32 The temporal stem refers to the portion of Reil” has been the accepted nomenclature for this area.
white matter that enters the temporal lobe between the During the succeeding 50 years, the insula attracted little
anterior limit of the insula and the temporal horn of the lat- attention. In approximately 1860, as a result of studies
eral ventricle. The inferior periinsular sulcus is not well designed to define anatomically the various regions of the
defined in the region of the limen insula. The long insular brain and to determine their function, renewed interest and
gyri extend to the gyri of Schwalbe in the polar planum importance was directed toward the study of the insula. It
and to the amygdala. The uncinate fasciculus, the anterior was supposed that the insula governed, at least in part, the

728 J. Neurosurg. / Volume 90 / April, 1999


Topography of the insula

FIG. 9. Photographs of brain specimens. Upper Left: Lateral surface of the left cerebral hemisphere. Following appli-
cation of the fiber dissection technique, the superior longitudinal fasciculus (slf) is revealed and the frontoorbital, fron-
toparietal, and temporal opercula, which cover the insula, are preserved. Upper Right: The sylvian fissure has been
opened completely and retraction of the opercula demonstrates the insula. Center Left: Removal of the opercula demon-
strates the relationship between the insula and the slf. Center Right: Removal of the insular cortex demonstrates the ex-
treme capsule (exc), which is connected to the white matter of the opercula (arrows). Lower: Demonstration of the un-
cinate fasciculus (uf), occipitofrontal fasciculus (of), external capsule (ec), putamen (p), and slf. ahg = anterior Heschl’s
gyrus; aip = anterior insular point; alg = anterior long insular gyrus; aps = anterior periinsular sulcus; ar = ascending
ramus of sylvian fissure; as = acoustic sulcus; ascs = anterior subcentral sulcus; asg = anterior short insular gyrus;
atpg = anterior transverse parietal gyrus; c = claustrum; cis = central insular sulcus; cs = central sulcus of Rolando; F1 =
superior frontal gyrus; f1 = superior frontal sulcus; hr = horizontal ramus of sylvian fissure; ia = insular apex; ic = inter-
nal capsule; ips = inferior periinsular sulcus; li = limen insula; log = lateral orbital gyrus; mog = medial orbital gyrus;
msg = middle short insular gyrus; mtpg = middle transverse parietal gyrus; op = pars opercularis of F3; or = pars orbital-
is of F3; p = putamen; pcg = precentral gyrus; pcis = precentral insular sulcus; pcs = precentral sulcus; pg = postcentral
gyrus; phg = posterior Heschl’s gyrus; pip = posterior insular point; pis = postcentral insular sulcus; plg = posterior long
insular gyrus; plol = posterolateral orbital lobule; pog = posterior orbital gyrus; FIG. 9 (continued)➝

J. Neurosurg. / Volume 90 / April, 1999 729


U. Türe, et al.

FIG. 10. Photograph showing the medial surface of the left hemisphere after midsagittal section. Following partial
removal of the thalamus, hypothalamus, internal capsule, globus pallidus, putamen, external capsule, claustrum, and
extreme capsule, the medial surface of the insular cortex is demonstrated. The central insular sulcus (cis) appears to be a
gyrus and the anterior long insular gyrus (alg) appears to be a sulcus. ac = anterior commissure; acs = anterior calcarine
sulcus; apes = anterior perforated substance; bcc = body of corpus callosum; bf = body of fornix; cf = column of fornix;
cg = cingulate gyrus; cis = central insular sulcus; crf = crus of fornix; cs = callosal sulcus; fi = fimbria; gcc = genu of cor-
pus callosum; istc = isthmus cinguli; oln = olfactory nerve; phig = parahippocampal gyrus; psg = posterior short insular
gyrus; rcc = rostrum of corpus callosum; scc = splenium of corpus callosum; sic = sublentiform portion of internal cap-
sule; u = uncus; us = uncal sulcus.

power of articulate speech. In 1861 Broca3 reported that, known source of reference. In the intervening decades, lit-
in patients with aphasia, there was almost always a lesion tle has transpired to expand our knowledge surrounding
located in the caudal region of the inferior frontal gyrus. the gross anatomical features of the insular region or to
This region was later named Broca’s area. In one of his illuminate the intricacies of its function.
aphasic patients, however, this area was intact, and a The hidden cortex known as the insula has long been a
lesion was discovered in the insula and in adjacent gyri
that are continuous with the inferior frontal gyrus. At the
end of the 19th century, several landmark articles were TABLE 4
published in which the anatomy of the insula and sur- Measurements relating to the insula and the putamen
rounding region were described in detail.6–8,12,14,29,30 In these
studies the authors proposed varying nomenclature to de- Measurements (mm)
fine the regions of the insula. Von Economo40 published a Structures* Average Range
book in 1929, in which appear concise detailed descrip-
tions of the brain including the insula. Unfortunately, this insular apex–putamen 14.5 14–15
publication, with comprehensive presentations illustrating posterior short insular gyrus–putamen (A–B) 11.5 11–12
the intricate gyral and sulcal patterns, is a relatively un- central sulcus–putamen (C–B) 5.5 5–6
width of putamen (B–D) 10.5 10–11
height of putamen (E–F) 41.0 38–44
pscs = posterior subcentral sulcus; psg = posterior short insular length of putamen (G–H) 44.0 41–47
gyrus; ptpg = posterior transverse parietal gyrus; scg = subcentral midanterior periinsular sulcus–putamen (I–G) 6.0 5–7
gyrus; sis = short insular sulcus; sog = suborbital gyrus; sopg = anterior insular point–putamen (J–K) 11.7 10–13
subopercular gyrus; spcg = subprecentral gyrus; sps = superior midsuperior periinsular sulcus–putamen (L–E) 5.7 5–6
periinsular sulcus; tal = terminal ascending limb of sylvian fis- posterior insular point–putamen (M–H) 9.7 8–12
sure; tdl = terminal descending limb of sylvian fissure; tg = trans- midinferior periinsular sulcus–putamen (N–O) 5.3 5–6
verse insular gyrus; tr = pars triangularis of F3; tts = transverse limen insula–putamen (P–F) 5.7 5–6
temporal sulcus; T1 = superior temporal gyrus; T3 = inferior tem- * Letter coding applies to dimension of structure or distances between
poral gyrus. structures, as seen in Fig. 11.

730 J. Neurosurg. / Volume 90 / April, 1999


Topography of the insula

subject of speculation. Proposals and theories regarding


its functional role are based on experimental animal stud-
ies, on intraoperative observations following stimulation
of the insular cortex in humans, and on clinical experience
involving patients with insular lesions.1,19,20,26,27,41 In hu-
mans, lesions involving paralimbic structures often result
in damage to adjacent limbic structures; therefore, the
degree of effect a paralimbic lesion will exert on neuro-
logical findings is difficult to analyze and determine.19,20
Applying various methods, investigators have demonstrat-
ed that the insula connects with portions of the frontal,
parietal, and temporal lobes and with the cingulate gyrus.
These investigators have also shown that the basal nuclei
(in particular, the tail of the caudate nucleus, the putamen,
and the claustrum), the amygdaloid body and other limbic
structures, and the dorsal thalamus also connect with the
insula.1,34 The results of these studies suggest that the in-
sula may function as a visceral sensory, visceral motor,
supplementary motor, and vestibular organ and may also
be related to certain aspects of speech and/or language. FIG. 11. Upper: Drawing of the coronal section through the
Penfield and Faulk,25 however, reported finding no neuro- third ventricle and insula showing the relationships between the
logical deficits related to these functions in their patients insula and the putamen. Lower: Drawing of the lateral view of
with lesions of the insula. They identified no somatic sen- the insula showing the relationship between the insula and the
sory, motor, or visceral sensory effects following removal putamen (dark area). Letter coding is defined in Table 4.
of the lesions, regardless of whether the insula was only
partially or completely excised. These observations were
confirmed by the senior author (M.G.Y.) following his (Areas 41 and 42), as well as for secondary somatic sen-
experiences involving radical surgical excision of tumors sory function and motor function (Areas 40, 43, and 44).4
both in and adjacent to this area.44,45 In the 3rd month of fetal life, a slight triangular depres-
Recent studies by Mesulam and colleagues19,20 that sion, anterosuperior to the temporal pole, becomes evident
focus on the cerebral cortex have yielded a new perspec- on the lateral surface of the cerebral hemisphere. This area
tive elucidating the functions of the insula. They have will develop into the insula, but the process is slower than
classified the insula as part of the paralimbic region, the development of surrounding cerebral lobes. The neo-
which is composed of mesocortex. Mesocortex is interca- cortical areas (opercula) gradually overlap and enclose the
lated between allocortex and isocortex, affording a subtle, insula, resulting in the formation of the periinsular sulci,
gradual transition from one to the other. The anteroinferi- which define the boundary of the insula. This whole de-
or portion of the insula is composed of the peripaleocorti- velopmental process subsequently leads to the formation
cal structure, the middle portion is composed of the pro- of the sylvian fissure, which does not completely evolve at
isocortical structure, and the posterior portion of the insula its most anterior portion until after birth.6,24,41
is composed of isocortical structure.20 Paralimbic struc- The anatomical variations of the sylvian fissure have
tures of the brain comprise the caudal orbitofrontal cortex, been elaborately described.22,24,32,37,43 In the current litera-
the insula, the temporal pole, the parahippocampal gyrus, ture, however, little attention has been directed toward the
and the cingulate complex. These five paralimbic areas insula, which is totally concealed beneath the surface of
form an uninterrupted girdle surrounding the medial and the brain on the medial aspect of the opercula. The rela-
basal aspects of each cerebral hemisphere. The limbic and tionship between the insula and opercula has also been
paralimbic zones of the cortex, together with the hypo- neglected. Considering the large number of surgical ex-
thalamus and the limbic components of the basal ganglia plorations that are undertaken in this region—in particu-
and thalamus, constitute the limbic system, which plays a lar, the opening of the sylvian fissure, which always ex-
crucial role in all aspects of memory, learning, and emo- poses the insula—there is a deficiency of knowledge in
tions.19,20 However, virtually no neurological deficit can, this particular field of neurosurgery. An analysis in which
with certainty, be attributed to underlying insular damage the relevance of the insula’s vital functions is defined and
because information on the functional specialization and a comprehensive study in which its anatomy, topography,
anatomical connections of this region is presently incom- and physiology are evaluated are lacking.
plete.20 A detailed illustrated description of the insula and A wide range of nomenclature is used to describe the
its connections as well as investigations related to its func- insular and opercular anatomy. We prefer to classify these
tion remain projects for future studies. areas with reference to the rami of the sylvian fissure and
The cerebral opercula comprise those portions of the according to the topography of the insula. Our nomencla-
frontal, temporal, and parietal lobes that overlap and cover ture also elucidates the embryological development of the
the insula and ultimately form the sylvian fissure. The insula, opercula, and the sylvian fissure. In studying the
opercula enclose areas that are vital not only for the per- literature, we found that the definitions applied to certain
ception of spoken language (posterior portion of Area 22 structures—for example, the sylvian stem, sylvian vallec-
and Area 39 on Brodmann’s chart), but also for motor ula, sylvian point, insular pole, insular apex, limen insula,
aspects of speech (Areas 44 and 45), for auditory function and ambient gyrus—differed in specific anatomical char-

J. Neurosurg. / Volume 90 / April, 1999 731


U. Türe, et al.

acteristics from publication to publication, and the termi- localize Broca’s area (Area 44, pars opercularis of F3), and
nology used to identify them varied depending on the the motor cortex (Area 4, precentral gyrus). Magnetic res-
author.7,8,10,16,24,29–32 Retzius29,30 used the terms “limen insu- onance imaging studies can demonstrate the sulcal and
la” and “insular pole” when referring to the same region. gyral anatomy in detail, but the application of this knowl-
Eberstaller12 and Cunningham,7,8 in describing the insular edge intraoperatively is difficult. The computer-assisted
apex, applied the term “pole.” In accordance with the re- stereotactic approach and frameless stereotactic equip-
sults of our detailed anatomical study, we have endeav- ment do not solve this problem because of inevitable intra-
ored to devise concise anatomical descriptions and to operative brain shifting. The ability to localize the pars tri-
evaluate and clarify the nomenclature with the aim of re- angularis of F3 and the anterior short insular gyrus is the
taining the most commonly used terminology. An excep- key to maintaining precise orientation during exploration
tion applies to the terms “circular sulcus,” “limiting sul- of the sylvian region. The pars triangularis is located
cus,” “circuminsular sulcus,” and “insular sulcus,” which between the horizontal and ascending rami of the sylvian
are all used to describe the sulcus separating the insula fissure and always covers the anterior short insular gyrus.
from its opercula.7,8,12,14,29,30,42–45 We suggest the term “peri- The subtriangular gyrus constitutes the medial surface of
insular sulcus,” which precisely describes its anatomical the triangular gyrus. The detailed anatomy of the insula
location, demarcating the anterior, superior, and posterior and opercula and their complex interrelationships can be
portions of the insula. precisely defined in each individual patient by a careful
The fiber dissection technique allowed us to demon- study of transverse, coronal, and sagittal magnetic reso-
strate connections of insula with the surrounding opercula nance images, which are essential preoperative investiga-
and with the massive short-fiber bundles. This technique tions.
was essential to our study and led to an integral under-
standing of the three-dimensional anatomy of the insular
region, deep nucleus, and association fibers of the brain Conclusions
(Figs. 9 and 10). The topographic anatomy of the insula and its relation-
A pterional approach, or a modification of this ap- ship to the opercula has been studied in detail and de-
proach, combined with a transsylvian exposure offers a scribed. A practical terminology for gyral and sulcal pat-
“gateway” to many regions of the brain. Opening the syl- terns that are of surgical significance has been suggested.
vian stem is essential to achieving adequate access to, and Applying this detailed knowledge of anatomy to preoper-
successful exploration of, the circle of Willis, the sellar ative planning and to the techniques and skills required to
and parasellar areas, and the mediobasal temporal region. explore the insula will contribute to more precise and
Extensive opening of the posterior ramus of the sylvian effective surgery for the complete removal of epileptic
fissure ensures access to specific lesions, such as epileptic foci, tumors, and vascular malformations in this region,
foci, tumors, and vascular lesions, that involve the insula, without causing damage to vital neural structures.
its opercula, or the periinsular regions. Applying this same
technique will also create an approach to deep lesions
Acknowledgments
located in the basal ganglia or in the lateral ventricle.43–45
A transsylvian–transinsular approach will access lesions The authors thank Ching Hearnsberger, R.N., for helping prepare
(for instance, cavernomas or hematomas) in the putamen. the manuscript and Ron M. Tribell for original artistic work.
The anterior insular point is the landmark that can be
readily identified and will indicate the direction that References
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