Complex Surgical Cases of the Limbic System Sepehr Sani, Mustafa K Baskaya, Richard W Byrne
Page numbers followed by f refer to figure.
Adult limbic system 1
Adult remnant of the hippocampus 2f
Alveus 2
Ambient cistern 18
Ammon's horn 1
Anaplastic astrocytoma 136
Anaplastic mixed oligoastrocytoma 136
Anterior choroidal artery 32, 47, 141
Anterior temporal lobectomy 35
Anterior temporal lobectomy with amygdalohip- pocampectomy 35
neocortical resection 35
positioning and equipment 35
resection of the hippocampus 45
resection of uncus and amygdala 38
Approaches to the mesial temporal lobe for epilepsy 26
surgical anatomy 26
Arachnoid villi 63
Arteriovenous fistulas (AVFs) 140
Arteriovenous malformations (AVMs) 71, 140
Bardeen chest 91
Basal ganglia 8
Basal vein of Rosenthal 34, 142
Brain mapping during surgery 107
epilepsy specific techniques in eloquent cortex 115
multiple subpial transections 115
responsive neurostimulation system 116
indications 107
integrating with functional imaging 108
preoperative preparation 108
anesthetic considerations 109
craniotomy considerations 110
equipment 109
preparations and positioning 110
stimulation mapping 110
stimulation pitfalls 114
subcortical stimulation mapping 114
surgical endpoints 114
Broca's area 107
Calcarine sulcus 88
Callosal sulcus 2f
Callosomarginal artery 100
Capillary telangiectasias 140
Central nervous system (CNS) 140
Choroidal fissure 31
Choroid plexus 18
Cingulate gliomas 136
Cingulate gyrus 2, 90, 99
surgical approaches 99
Cingulate gyrus tumors 130
anatomical classification and growth patterns 134
clinical features 134
histopathological characteristics 135
overview of anatomy 130
surgery 136
surgical approaches 136
surgical outcomes 136
Collateral sulci 57
Corpus callosum 2
Corticofugal fibers 88
Crura of fornix 4
Crus of the fornix 16
Deep venous drainage 143
Diagonal band of Broca 5
Diencephalon 1
Entorhinal cortex 48
Falx-occipital fissure 88
Fasciolar gyrus 33
Fimbria 1
Fimbriodentate fissure 4
Foramen of Monro 16, 33
Fornix 1
Frontoparietal lobes 6
Frontotemporal curvilinear incision 35
Fusiform gyrus 36
Giant limbic tumors 129
Grade I ganglioglioma 126
Grade II astrocytoma 126
Grade IV glioblastoma 126
Gyrus of Ebertaller 22
Habenula 8
Hemianopia 130
Heschl's gyrus 9, 72
Hippocampal fissure 1
Hippocampal tail 2
Hippocampus and the choroidal fissure 33
Indusium griseum 2, 33
Infralimbic gyrus 13
Insula 21
Internal carotid artery (ICA) 54
Internal cerebral veins 152
Intralimbic gyrus 30
Labbe and Sylvian veins 48
Lamina terminalis 142
Left anterosuperior insular low-grade glioma 75
history 75
surgery 76
Left frontal-cingulate grade II mixed olio-astrocytoma 100
history 100
surgery 100
Left insular-subfrontal low-grade glioma; combined transsylvian/subfrontal- transcortical approach 78
history 78
surgery 78
Left posterior insula cavernoma 82
history 82
surgery 84
Left uncus cavernous malformation 53
history 53
surgery 53
Lenticulostriate arteries 71
Level of limen insula 73
Limbic cavernous malformations 154
anatomic distribution 154
clinical features 154
surgery 155
surgical approaches and techniques 155
surgical outcomes 156
Limbic embryologic development 1
Limbic lobe 140
Limbic system 1
structure and development 1
amygdala 5
fornix and mammillary body 3
hippocampus 1
insula 5
parahippocampal gyrus 3
septal area 5
Limen insulae 13
Lingual gyrus 88
Low-grade glioma 32
Magnetoencephalography (MEG) 108
Malignant gliomas 136
Mammillary body 8
Mediobasal temporal tumors 123
clinical features 124
growth patterns and anatomical classifications 125
histopathological characteristics 126
overview of microsurgical anatomy 123
surgery 126
surgical approaches 126
surgical outcomes 129
Mesial pia 38
Mesial pia of the temporal horn 18
Metzenbaum scissors 93
Meyer's loop 33, 88, 146
Middle cerebral artery 54, 141
Mixed oligoastrocytoma 136
Motor evoked potential 100
Nasal cannula 110
Neocortical limbic structures 8
Neurolon sutures 93
Occipital interhemispheric approach 87
anatomy 87
contraindications 89
details of surgical approach 91
history 87
indications 89
risks and pitfalls 95
Occipitoparietal sulci 148
Occipitotectal fibers 17
Occipitotemporal gyrus 3
Ojemann cortical stimulator 111
Olfactory stria 5
Opaque arachnoid bands 152
Parahippocampal gyrus 31
Parietal-occipital sulcus 88
Pericallosal artery 100
Planum polare 9
Planum temporale 9
Postcentral gyrus 75
Posterior cerebral artery 141
Posterior communication (PCOA) artery 47
Posterior interhemispheric parafalx 148
Posterior pole of incisura 127
Quadrantanopia 130
Quadrigeminal cistern 65, 95, 152
Quadrigeminal segment 142
Responsive neurostimulation system (RNS) 116
Right-sided amygdala and hippocampus low grade glioma 48
history 48
surgery 51
Ringer's solution 109
Root of the zygoma 35
Schramm's series 126
Selective amygdalohip- pocampectomy 45
Sensorimotor stimulation 111
Septal nuclei 5, 8
Somatosensory cortex 111
Somatosensory evoked potential 100
Spetzler-Martin (SM) grading system 145
Splenium of the corpus callosum 88
Spontaneous hemorrhage 151
Stein's anatomical classification 148
Subcortical stimulation mapping (SSM) 114
Superior insular sulcus 21
Superior temporal gyrus 36
Supracerebellar transtentorial approach 57
anatomy 57
gross anatomy 57
vascular anatomy 58
contraindications 60
description of the approach 60
closure 69
dural opening and dissection 63
incision and craniotomy 61
preoperative evaluation and positioning 60
history 57
indications 58
risks and pitfalls 69
Supramarginal gyrus 73
Surgery for giant and unusual tumors 120
Surgery for vascular malformations of the limbic system 140
anatomical classifications 144
arteriovenous malformations 143
cavernous malformations 153
clinical features 145
surgical approaches 145
calloso-cingulate arteriovenous malformations 148
mediobasal temporal arteriovenous malformations 145
parasplenial arteriovenous malformations 148
surgical considerations 149
surgical outcomes 153
vascular anatomy of the limbic system 140
calloso-cingular area 142
mediobasal temporal region 141
Surgical anatomy of the insula 71
insular anatomy 72
operative approach 74
Sylvian fissure 21, 111
Sylvian fissure and opercular anatomy 24
Telencephalon 1
Temporal lobe 6, 9, 73
anatomy 9
amygdala 13
hippocampus 15
mesial surface 11
superior surface 9
temporal horn and choroidal fissure 17
uncus 11
histology 9
vascular relationships 18
anterior choroidal artery 19
internal carotid artery 18
middle cerebral artery 20
posterior cerebral artery 19
posterior communicating artery 18
Temporal stem 73
Tentorial incisura 58
Transcranial magnetic stimulation (TMS) 108
Transsylvian approach to amygdalohippocam- pectomy 47
Tumor resection in the anterior temporal lobe 47
Uncal gyrus 38
Uncal recess 47
Uncinate fasciculus 48
Uncohippocampal artery 142
Uncus and amygdala 32
Vagus nerve stimulation (VNS) 116
Vascular clips 63
Vein of Galen 58
Vein of Labbé 36, 65
Velum terminale 30
Venous anatomy 65
Vertex of the gyrus 116
Visual field defects (VFD) 153
Wernicke's area 107
Yasargil's series 126
Chapter Notes

Save Clear

EmbryologyCHAPTER 1

Sepehr Sani,
Joshua T Wewel,
Richard W Byrne
One of the most dramatic developmental changes of the central nervous system is that seen in the limbic system. Various structures of the adult limbic system encompass every lobe as well as the brainstem with interconnections via fiber tracks that at times travel almost circumferential distances. The embryologic development of the human limbic system is evolutionarily old and has remained remarkably consistent over time and across most mammalian species. The formation of various structures of the limbic system in conjunction with the surrounding brain development helps explain the form and function of the adult limbic system. A thorough understanding of the limbic embryologic development is critical to the neurosurgeon's ability to operate safely within its structures.
The limbic system extends from the medial surface of the frontal lobe to the temporal lobe, comprising a series of four C-shaped structures that are separated by sulci or remnants (Fig. 1.1). The outermost “C” arch is formed sequentially by the subcallosal area, cingulate gyrus, parahippocampal gyrus, and uncus. The inner arch is formed by the paraterminal gyrus, indusium griseum, tail of hippocampus, dentate gyrus, and Ammon's horn.1-4 A long sulcus between these two arches, the callosal sulcus and the hippocampal fissure, defines the third arch. The fourth and final arch is formed by the fimbria and fornix.2,4,5 The anatomic complexity of the limbic structures is reflected by their embryological development and an overview is presented in the following text.
Developmentally, the limbic system arises from the telencephalon and diencephalon.4-6 Examination of the gray matter architecture reveals that most structures have a three layered cortex. The dentate gyrus and Ammon's horn have a trilaminar type of cortex which gradually transitions to a neocortical six layer cortex in the entorhinal area of the parahippocampal gyrus.4,7
The hippocampus first appears at the dorsomedial wall of the cerebral hemisphere adjacent to the lamina terminalis at around day 37 of gestation4-6,8,9 and is the first cortical area to differentiate.8-10
zoom view
Fig. 1.1: Mesial surface of brain demonstrating the adult pathway of the four limbic arches. The outermost arch is formed by the cingulate gyrus, which merges with and becomes the parahippocampal gyrus. The inner arch is formed by the indusium griseum, which is the adult remnant of the hippocampus. This structure is continuous with the tail of hippocampus, dentate gyrus, and Ammon's horn. The callosal sulcus, which becomes the hippocampal fissure, defines the third arch. The fourth and final arch is formed by the fimbria and fornix (white arrowheads).
This structure forms a continuous bulge into the inferomedial wall of the lateral ventricle as it extends in crescent fashion into the temporal tip where the temporal lobe forms. At week 10 of gestation, the hippocampus forms a large part of the cerebral hemisphere.11
As the corpus callosum begins to develop around 14 weeks’ gestation, the anterior hippocampus regresses and the temporal portion remains as the most developed part.8,11 By 17 weeks, the paraterminal gyrus and indusium griseum are the only remnants of the anterior hippocampus. In the temporal lobe, the anterior tip of the hippocampus is separated from the developing amygdala by the uncal recess of the temporal horn. The body of the hippocampus forms the inferomedial border of the temporal horn with its subependymal superior surface covered by the alveus (Figs. 1.2A to D). The hippocampal tail extends around the splenium of the corpus callosum and forms the indusium griseum.3,12,13 The indusium griseum and its associated white matter bundles (medial and lateral longitudinal striae) are intimately applied to the surface of the corpus callosum.4,14 Anteriorly, the indusium griseum extends around the genu of the corpus callosum to merge with the paraterminal gyrus.3,4,13,15
The hippocampal fissure is first seen at about 55 days’ gestation but is not well formed until 10 weeks.8,16 It forms as a result of the differential growth of Ammon's horn compared to the dentate gyrus.10,11,16 By 15 weeks (Figs. 1.2A to D), the most developed part of the fissure is in the temporal lobe.8,11 With continued growth of the dentate gyrus, the hippocampal fissure deepens and eventually fuses together. A remnant cavity of this can be seen in 10% of the normal population in MRI studies.7,17 The medial hemispheric part of the fissure eventually becomes the callosal sulcus separating the indusium griseum from the cingulate gyrus.2,5 In the temporal lobe, the hippocampal fissure runs parallel to the choroidal fissure5 and merges into the uncal sulcus.17
3Parahippocampal Gyrus
The parahippocampal gyrus forms the inferomedial surface of the temporal lobe in the adult form. Developmentally, the hippocampal fissure forms the superior border of the parahippocampal gyrus. On the lateral side, the collateral sulcus separates it from the occipitotemporal gyrus. Beginning at 13 weeks and soon after, the parahippocampal gyrus undergoes rapid growth and expansion, essentially causing it to rotate in the inferomedial direction, covering the hippocampus and hippocampal fissure.
Fornix and Mammillary Body
The fornix is the main efferent fiber tract from the hippocampus. The majority of fibers arise from the subiculum and Ammon's horn,13,18 travel over the subependymal ventricular surface as the alveus and merge as the fimbria.
zoom view
Figs. 1.2A and B:
zoom view
Figs. 1.2A to D: Photographs and MRI images of the medial surface of the embryological cerebral hemispheres. (A) The medial surface of an approximately 14-week-old embryo. The hippocampus (H) extends from the temporal lobe to the frontal lobe (small arrows). The prominent hippocampal sulcus is readily visible (large arrowheads). The uncus (U) has an anterior position but has not fully turned to cover the hippocampus medially. (Th: Thalamus;*: Area affected by dissection) (B) Reformatted sagittal oblique MRI image of the same specimen demonstrating the hippocampus (H) and the hippocampal sulcus (small arrows). (C) The medial surface of an approximately 17-week-old specimen. The corpus callosum (CC) is partially formed and the hippocampal remnant along the sulcus of the corpus callosum (arrowheads) is visible along the frontoparietal region. The cingulate gyrus (CG) is now visible. The hippocampal sulcus (small arrows) is less visible as the uncus (U) assumes a more medial position. Early formation of the parahippocampal gyrus (PHG) is also seen at this time. (D) Sagittal MRI image of the same specimen. The hippocampal remnant is seen (arrows) along the forming sulcus of the corpus callosum.
The fimbria lies superior to the dentate gyrus and is separated from it by the fimbriodentate fissure. Posteriorly, the fimbria increases in thickness, becoming the crura of fornix. Anteriorly, the crura form a triangular sheet of fibers called the commissure of the fornix. The crura then join to from the body of the fornix, which continue on to becoming the columns of the fornix before dividing proximal to the anterior commissure 5to the precommissural and postcommissural fibers. The precommissural fibers terminate in the septal area, diagonal band of Broca, lateral preoptic area, and anterior hypothalamus. The postcommissural fibers terminate in the mammillary bodies.
The fibers of the fornix appear at 8 weeks’ gestation. The commissure of the fornix begins to appear around 10 weeks and by 13.5 weeks, the alveus is visible in the subependymal surface, and the fimbriodentate fissure is present.8 The fornix and hippocampus can be seen as separate entities after 16 weeks gestational age.14 The mammillary bodies, which are diencephalic in origin, arise as a single rounded protuberance from the floor of the hypothalamus. Around the 3rd month of gestation, the mammillary bodies are divided by a median furrow, forming the left and right sides.4-6
Septal Area
The septal area is an important part of the limbic system and serves as an area of interconnection for various anatomic nuclei. The area includes the subcallosal gyrus, paraterminal gyrus, septal nuclei, olfactory stria, and the diagonal band of broca.5,13,15 This region is located on the medial surface of the frontal lobe, inferior to the corpus callosum and anterior to the lamina terminalis.4,15
The septal area is a telencephalic structure that first appears at 37 days’ gestational age.8 The septal nuclei and some of the fiber connections can be identified at about 47 days’ gestation. By the 3rd month of gestation, the septal nuclei are well-developed and lie below the corpus callosum and anterior to the septum pellucidum near their adult anatomic position.8
The amygdala is an almond-shaped collection of nuclei that have both olfactory and limbic functions.19 Although in the adult brain, the uncus which encompasses the amygdala and the hippocampus has an intimate anatomic relationship, as will be explained here, the two structures are distinct and develop separately during gestation. The amygdala arises from the corpus striatum embryologically and remains directly connected to the putamen superiorly and the tail of the caudate nucleus that ends in the amygdala.4,5,13,18 The amygdala is divided into two major masses of nuclei: (1) the corticomedial and (2) basolateral nuclear group.
Developmentally, the amygdala is the first part of the corpus striatum to appear as a thickening next to the primitive hippocampal formation at about 35 days’ gestation. As it develops, the amygdala migrates from being directly posterior to the lateral ventricle to its ventral and anterior temporal location; and it rotates medially such that nuclei that were originally lateral become basal and ventral in position.8,20,21 This parallels the development of the temporal horn and medial rotation of the temporal pole. This development continues until the adult uncus assumes its anteromedial temporal position.
The sylvian fold and insular region begin to develop by gestation week 18. This is followed by the development of the central insular sulcus, which is visible on the surface before the temporal and frontal lobes fold.
zoom view
Fig. 1.3: Lateral surface of the embryological hemisphere at 19-week gestation age. The frontoparietal central sulcus (small arrows) is visible and is aligned with the developing central insular sulcus (arrowheads). As the temporal lobe continues to fold and join the frontotemporal opercula (large arrows), the insula assumes its adult hidden position.
The central insular sulcus corresponds to the location and development of the central sulcus of the frontoparietal lobes (Fig. 1.3). As development continues by 22 weeks’ gestation, the insula becomes narrower and less visible due to the posterior-to-anterior folding of the temporal lobe against the parietal and frontal opercula. The Sylvian fissure becomes anatomically visible and completely closed by 27 weeks gestation, at which point the insula is no longer visible.
The developmental anatomy of the limbic system is complex. A detailed understanding of the sequential development of various structures allows for an understanding of the adult structures including the four C-shaped arches, lying in an oblique sagittal plane and extending from the temporal pole to the medial surface of the frontal lobe.
  1. Duvernoy H. The Human Brain: Surface, Three Dimensional Sectional Anatomy and MRI. New York: Springer-Verlag;  1991.
  1. Mark LP, Daniels DL, Naidich TP, Borne JA. Limbic system anatomy: an overview. Am J Neuroradiol. 1993;14(2):349–52.
  1. Naidich TP, Daniels DL, Haughton VM, Pech P, Williams A, Pojunas K, et al. Hippocampal formation and related structures of the limbic lobe: anatomic-MR correlation. Part II. Sagittal sections. Radiology. 1987;162(3):755–61.
  1. Gray FRS, Wolff K, Winkelman R. Gray's Anatomy. Philadelphia: WB Saunders;  1980.
  1. Carpenter MB. Human Neuroanatomy, 8th edition. Baltimore: Williams & Wilkins;  1983.

  1. 7 O'Rahilly RR, F Müller. Human Embryology and Teratology. New York: Wiley-Liss;  1992.
  1. Bronen RA, Cheung G. MRI of the normal hippocampus. Magn Reson Imaging. 1991;9(4):497–500.
  1. Lemire RJ, Loeser JD, Leech RW, et al. Normal and Abnormal Development of the Human Nervous System. Hagerstown, MD: Harper & Row;  1975.
  1. O'Rahilly MF. The Embryonic Human Brain: An Atlas of Developmental Stages. New York: Wiley-Liss;  1994.
  1. Humphrey T. The development of the human hippocampal formation correlated with some aspects of its phylogenetic history. In: Evolution of the Forebrain: Phylogenesis and Ontogenesis of the Forebrain. New York: Plenum Press;  1967.
  1. Kier EL, Fulbright RK, Bronen RA. Limbic lobe embryology and anatomy: dissection and MR of the medial surface of the fetal cerebral hemisphere. Am J Neuroradiol. 1995;16(9):1847–53.
  1. Mark LP, Daniels DL, Naidich TP, et al, Borne JA. The hippocampus. Am J Neuroradiol. 1993;14(3):709–12.
  1. Naidich TP, Daniels DL, Haughton VM, Williams A, Pojunas K, Palacios E. Hippocampal formation and related structures of the limbic lobe: anatomic-MR correlation. Part I. Surface features and coronal sections. Radiology. 1987;162(3):747–54.
  1. Sitoh YY, Tien RD. The limbic system. An overview of the anatomy and its development. Neuroimaging Clin N Am. 1997;7(1):1–10.
  1. Mark LP, Daniels DL, Naidich TP, et al, Maas E. Anatomic moment. The septal area. Am J Neuroradiol. 1994;15(2):273–6.
  1. Humphrey T. The development of the human hippocampal fissure. J Anat. 1967;101(Pt 4):655–76.
  1. Hayman LA, Hinck VC. Adult cerebrum. In: Clinical Brain Imaging: Normal Structure and Functional Anatomy. St. Louis: Mosby-Year Book;  1992.
  1. Nieuwenhuys R, Voogd J, Van Huijzen C. The Human Central Nervous System: A Synopsis and Atlas, 3rd edition. New York: Springer-Verlag;  1988.
  1. Kretschmann H-J, W Weinrich. Cranial Neuroimaging and Clinical Neuroanatomy, 2nd edition. New York: Thieme;  1992.
  1. Humphrey T. The development of the human amygdala during early embryonic life. J Comp Neurol. 1968;132(1):135–65.
  1. Humphrey T. The development of the human amygdaloid complex. The Neurobiology of the Amygdala. New York: Plenum Press;  1972.