Microsurgical anatomy of the subthalamic nucleus: correlating fiber dissection results with 3-T magnetic resonance imaging using neuronavigation

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In Brief

Familiarity with the complex 3D anatomy of the STN and peri-subthalamic area is important for more effective targeting of the STN and better understanding of DBS side effects. The combination of meticulous anatomic dissections of the STN region and detailed discussions of pertinent anatomo-functional relationships in this paper will provide DBS practitioners with a more sophisticated understanding of this important brain region and empower them to improve the outcomes of STN DBS for their patients.

ABBREVIATIONS DBS = deep brain stimulation; GPe = globus pallidus externus; GPi = globus pallidus internus; GQI = generalized q-sampling imaging; IC = internal capsule; LGB = lateral geniculate body; MFB = medial forebrain bundle; SLF = superior longitudinal fasciculus; STN = subthalamic nucleus; ZI = zona incerta.

Article Information

Correspondence Necmettin Tanriover: Istanbul University, Istanbul, Turkey. nctan27@yahoo.com.

INCLUDE WHEN CITING Published online May 4, 2018; DOI: 10.3171/2017.10.JNS171513.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Lateral to medial fiber dissection of a left hemisphere to display the relations of the subthalamic region in a stepwise systematic manner. A: Identification of sulci and gyri on the lateral surface of the left hemisphere. B: The pyramid-shaped insula has been exposed by removing the cortical surface and underlying white matter along the frontoparietal and temporal operculi. C and D: Initially, the extreme capsule has been displayed through a decortication process along the insular cortex (C). The external capsule layer has been reached following the removal of the extreme capsule (D). Deeper external capsule layer contains dorsally located claustrocortical fibers and ventrally located inferior fronto-occipital and uncinate fasciculi. E and F: The putamen and globus pallidus, in addition to the IC, have been revealed by continuing the lateral to medial fiber dissection. Removing the ventral external capsule fibers exposed the putamen and, by removing this structure, the IC fibers and globus pallidus have been displayed. Ang. = angular; Ant. = anterior; Caps. = capsule; Cent. = central; Cor. = corona; Extr. = extreme; Fasc. = fasciculus; Fiss. = fissure; Front. = frontal; Glob. = globus; Gyr. = gyrus; IFOF = inferior fronto-occipital fasciculus; Inf. = inferior; Ins. = insular; Int. = interna, internal; Intrap. = intraparietal; Lim. = limiting; Lob. = lobule; Marg. = marginal; Mid. = middle; Operc. = opercularis; Orb. = orbitalis; Pall. = pallidus; Par. = parietal; Post. = posterior; Postcent. = postcentral; Precent. = precentral; Rad. = radiata, radiation; Sulc. = sulcus; Sup. = superior; Sylv. = sylvian; Temp. = temporal; Triang. = triangularis; Uncin. = uncinate. Copyright Necmettin Tanriover. Published with permission. Figure is available in color online only.

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    A: Further lateral to medial dissection. The anterior commissure has been exposed through further medial fiber dissection. The anterior commissure, passing just inferior to the middle base of the globus pallidus, has been shown, along with its temporal and occipital extensions. The division along the temporal stem is located near the temporal edge of the limen and proximal to the inferior limiting sulcus of insula. B: Retrolenticular and sublenticular parts of the IC, including the anterior part of the optic radiations, have been shown deep to the anterior commissure layer. Meyer’s loop consists of fibers arising from the lateral geniculate body, running anteriorly with a posterior curve at the temporal pole. C: Caudate nucleus medial to IC and thalamic radiations has been demonstrated by moving medially to the next step through the fiber dissection on the same hemisphere. C-shaped caudate nucleus, circling the anterosuperior and superior boundaries of the thalamus, has been exposed by removing the IC. D: The STN laterally, red nucleus inferomedially, and substantia nigra inferiorly have been identified by removing the posterior part of the thalamus in another left hemisphere. The ansa lenticularis, composed of pallidofugal fibers, lies between the globus pallidus and STN within the prerubral region. The STN, with its almond-like shape, is located superolateral to the red nucleus, medial to the GPi, and superior to the substantia nigra. E: The posterior part of the IC and thalamus have been removed to show substantia nigra and STN in relation to brainstem and cerebellum in another left hemisphere. Removing the transverse pontine fibers exposes medial lemniscus and cerebellar peduncles. The medial lemniscus runs from the gracile and cuneate tubercles to the ventral posterolateral nucleus of the thalamus and divides the brainstem into ventral and dorsal parts. The medial lemniscus fibers intermingle with substantia nigra and pass inferomedial to the STN before terminating in the thalamus. Corticospinal, corticobulbar, corticomesencephalic fibers have a close relationship with the lateral anterior and inferior borders of the STN throughout their descending path trajectory toward the pons within the IC. F: The ansa peduncularis and medial forebrain bundle have been exposed by removing the globus pallidus, IC fibers, and thalamus in another specimen on the left side. The medial forebrain bundle connects the lateral hypothalamus and the septal area with the ventral tegmental area. The medial forebrain bundle lies at the level of and just lateral to the red nucleus, lateral to the mammillothalamic tract, medial to the substantia nigra, and slightly inferomedial to the STN. Caud. = caudate; Cer. = cerebellar; CN = cranial nerve; Coll. = colliculus; Comm. = commissure; Diag. = diagonal; Epend. = ependyma; Ext. = externa; Gen. = geniculate; Hippo. = hippocampus; Innom. = innominata; Lat. = lateral; Lem. = lemniscus; Lent. = lenticularis; Mam. = mammillary; Med. = medial, medullaris; Nucl. = nucleus; Ped. = peduncle; Pedunc. = peduncularis; Subst. = substantia; Term. = terminalis; Thal. = thalami, thalamic; Tr. = tract; Vent. = ventricle. Copyright Necmettin Tanriover. Published with permission. Figure is available in color online only.

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    Medial to lateral fiber dissection of a left hemisphere to display the relations of the subthalamic region in a stepwise manner. A: Identification of sulci and gyri on the medial surface of the left hemisphere. B: Enlarged view of panel A, displaying the 3rd ventricular region. C: The fasciculus retroflexus, red nucleus, ZI, mammillothalamic tract, and postcommissural fornix have been displayed by removing the ventral part of the thalamus through a fiber dissection on the medial side of a left cerebral hemisphere. The fasciculus retroflexus lies between the habenula and interpeduncular nucleus just medial to the red nucleus. The red nucleus is visible medial and inferior to the ZI and posterior to the mammillothalamic tract. The ZI has been exposed under the thalamus and covers the STN on the dorsomedial side. D: The anterior part of the red nucleus has been removed during further medial to lateral dissection. The rostral part of the ZI extends over the dorsal and medial surfaces of the STN and its caudal part lies posteromedial to the nucleus. The substantia nigra spreads from the inferior part of the red nucleus to the inferior border of the ZI and STN. E: Fiber dissection of the subthalamic area in another left medial hemisphere. The ZI, superior part of the mammillothalamic tract, and transverse pontine fibers have been removed and the brainstem has been dissected to expose the STN and medial lemniscus. F: Enlarged view of panel E. Following the removal of the ZI, a biconvex-shaped STN has been exposed medial to the IC fibers. The STN is located superolateral to the red nucleus and superior to the substantia nigra. The IC fibers run from its inferior to anterolateral side. The medial lemniscus traverses the thalamus posterior to the corticospinal tract, before terminating in the thalamus. The medial lemniscus ascends posteroinferior to the STN and is located posterior to the nucleus at this level. Call. = callosum; Cing. = cingulate; Corp. = corpus; Cort. = cortico; Gl. = gland; Hypothal. = hypothalamic, hypothalamus; Mammillothal. = mammillothalamic; MLF = medial longitudinal fasciculus; Ped. = pedunculo; Pon. = pontine; Postcomm. = postcommissural; Retroflex. = retroflexus; Spin. = spinal. Copyright Necmettin Tanriover. Published with permission. Figure is available in color online only.

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    Superior to inferior fiber dissection of the subthalamic region in a stepwise manner. A: The brain has been cut at the level of the sylvian fissure to demonstrate a superior to inferior fiber dissection toward the subthalamic region. The anterosuperior parts of the caudate nuclei, parts of the fornix, the septum pellucidum, and callosal fibers have been exposed along the frontal horn, body, and atrium of the lateral ventricle. On the right side, the fornix and choroid plexus have been removed to show the anterolateral and posteromedial parts of the thalamus separated by the choroidal fissure. B: The fornix and choroid plexus along the choroidal fissure have been removed via further superoinferior dissection on both hemispheres and the tenia thalami has been removed on the right side. The respective thalamic nuclei, anterior thalamic nucleus, lateral dorsal nucleus, lateral posterior nucleus, medial nuclear group, and pulvinar, in addition to the stria terminalis and stria medullaris thalami, have been exposed. C: The thalamus has been removed on the left side to display the ZI and the red nucleus through further fiber dissection directed inferiorly. The ZI is located lateral and superior to the red nucleus. The ZI covers the STN dorsally and is located posterosuperior and slightly medial to the STN. D: The thalamus has been removed on both sides at this step of dissection. The red nucleus is located just lateral to the midline, posterior to the mammillary body, and the ZI lies between the IC and the red nucleus on the right side. The ZI has been removed on the left side to expose a biconvex-shaped STN, medial to the IC fibers. The STN is located superolateral to the red nucleus. Comparing fiber dissections on both hemispheres in this view places the STN ventral, anteroinferior, and slightly lateral to the ZI. Chor. = choroid; Dors. = dorsal; For. = forceps; Plex. = plexus; Prelem. = prelemniscal. Copyright Necmettin Tanriover. Published with permission. Figure is available in color online only.

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    Further superior to inferior dissection. A: The ZI has been dispatched on the right side and IC fibers have been removed on the left side. B: Enlarged view of Fig. 4E. The head of the caudate nucleus has been reflected superomedially on both sides to expose the IC fibers on the right side and the globus pallidus and putamen on the left side. The STN is located medial to the IC and globus pallidus. The pulvinar of thalamus and prelemniscal radiations are situated posterior to the STN. C: By proceeding with superior to inferior fiber dissection, the caudate nucleus has been removed on the left side, and the head has been preserved on the right. The GPi is located just lateral to the STN and the optic tract lies just under the GPi, inferomedial to the STN. D: Enlarged view of panel A. On the left hemisphere, the nucleus accumbens has been exposed under and extending beneath the head of the caudate nucleus. The substantia nigra spreads under the STN and red nucleus. The ansa lenticularis lies between the GPi and STN. Coll. = collateral, colliculus; Inf. = inferior. Copyright Necmettin Tanriover. Published with permission. Figure is available in color online only.

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    Inferior to superior fiber dissection of the subthalamic region in a stepwise manner. A: The brainstem has been cut at the level of the inferior colliculi. The medial geniculate body is located at the superior edge of the lateral mesencephalic sulcus, and the optic tract runs from the chiasm to the lateral geniculate body above the uncus. B: Enlarged view of panel A and a further stage on the inferior to superior fiber dissection of the diencephalic region. The substantia nigra, underneath the subthalamic and red nuclei, has been displayed by removing the transverse pontine fibers and the corticobulbar and corticospinal tracts. On the right side, portions of the red nucleus and substantia nigra were removed to better expose the STN with its oblique shape. Parahippo. Gyr. = parahippocampal gyrus. Copyright Necmettin Tanriover. Published with permission. Figure is available in color online only.

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    Axial, coronal, and sagittal anatomical sections of the diencephalon at different levels to display the STN and neighboring structures in the human brain. A: A midbrain axial cut through the upper edge of the superior colliculi has been performed to show the STN and its relationships. The STN is located anterolateral to the red nucleus and posteromedial to the corticospinal tract. The MFB is medial to the STN at this level. B: A coronal cut has been performed at the level of the central rolandic sulcus of the lateral cerebral hemisphere. The coronal cut corresponds to the anterior edge of the mammillary bodies medially. The STN is located between the ZI and substantia nigra with its almond-like shape just medial to the IC. The red nucleus is situated more posteriorly and cannot be seen at this section. C: A sagittal cut has been performed to show STN and its relationships. The ZI and substantia nigra spread to the posterior subthalamic region, from superior and from inferior, respectively. Interped. = interpeduncular. Copyright Necmettin Tanriover. Published with permission. Figure is available in color online only.

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    3D MRI reconstruction of neighboring anatomical structures associated with the STN and their correlations with the related white matter tracts through diffusion tensor imaging. A: Medial view; the STN (turquoise blue) is located superior to the substantia nigra (yellow), lateral to the red nucleus (orange), and medial to the IC and GPi. The IC fibers ascend from the inferior aspect of the STN and over its lateral surface and pass lateral to the caudate nucleus (green) at the level of the insula. B: Lateral view; the IC fibers ascend from the inferior aspect of the STN and over its lateral surface, medial to the globus pallidus (pink), and pass lateral to the caudate nucleus at the level of the insula. C: Medial 3D MRI view of the STN (turquoise blue), red nucleus (orange), ZI (green), substantia nigra (yellow), GPi (red), and GPe (pink). The red nucleus is located inferomedial to the STN with its spheroid shape. The ZI covers the superior surface of the STN and reaches its posterior border. The substantia nigra is located inferior to the red nucleus and the STN and also spreads toward the posterior territory of the STN. D: Lateral view of 3D MRI reconstruction of the STN (turquoise blue), red nucleus (orange), ZI (green), substantia nigra (yellow), and GPe (pink). The ZI extends from midline to the inferolateral border of the STN lying under the subthalamic and red nuclei. E: Anterior view of 3D MRI reconstruction of the STN (turquoise blue), red nucleus (orange), ZI (green), substantia nigra (yellow), GPi (red), and GPe (pink). The STN is surrounded by red nucleus posteromedially, by ZI (green) superiorly, and by substantia nigra inferoposteriorly. F: Posterior view of 3D MRI reconstruction of the STN (turquoise blue), red nucleus (orange), ZI (yellow), substantia nigra, GPi (red), and GPe (pink). The ZI from superior and substantia nigra from inferior extend to the posterior subthalamic area. Figure is available in color online only.

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    3D MRI reconstruction of neighboring anatomical structures associated with the STN and their correlations with the related white matter tracts through diffusion tensor imaging. A: Superior view of 3D MRI reconstruction of the STN (dark blue), red nucleus (orange), substantia nigra (yellow), caudate nucleus (green), and putamen (fuchsia). B: Inferior view of 3D MRI reconstruction of the STN (dark blue), red nucleus (orange), substantia nigra (yellow), GPi (red), GPe (pink), amygdala (dark blue), caudate nucleus (green), and putamen (fuchsia). C: Lateral view of 3D MRI reconstruction of the STN (turquoise blue) and tractography of the MFB (yellow), medial lemniscus (purple), and oculomotor nerve fibers (red). The medial lemniscus is located posterior to the STN. The MFB is located inferomedial to the STN and oculomotor nerve fibers are located inferomedial to the STN. D: Superior view of panel D. The medial lemniscus ascends posteroinferior to the STN. The oculomotor nerve fibers are medial to the STN. The medial forebrain bundle lies slightly inferomedial to the STN. E: Inferior view of panel D. F: Anterior view of panel D. G: Posterior view of panel D. Figure is available in color online only.

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    Demonstration of lead insertion to the STN from different angles. A: Coronal T1-weighted image obtained at the STN level with 3D STN modeling and depiction of a DBS lead insertion from 2 different angles in the coronal plane. Demonstration that changing the entry angle without changing the target can significantly alter the position of the implanted DBS contacts. Lead B would likely have excessively low thresholds for capsular side effects. B: Enlarged view of panel A. C: Sagittal T1-weighted image obtained at the STN level with 3D STN modeling and depiction of a DBS lead insertion from 2 different angles in the sagittal plane. Demonstration that changing the entry angle without changing the target can significantly alter the position of the implanted DBS contacts. Lead B would likely have excessively low thresholds for capsular side effects. D: Enlarged view of panel C. Dist. = distance. Figure is available in color online only.

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    Medial to lateral fiber dissection of the diencephalon on a silicone-injected cadaveric head with the aid of MR navigation. A: The ventral part of the thalamus and ventral tegmental area have been removed to expose the STN and red nucleus. The anterior part of the red nucleus has been removed to expose the substantia nigra. The navigation probe shows the superomedial part of the STN. The STN is located lateral to the red nucleus and superior to the substantia nigra. B: MRI-based stereotactic localization with the probe on the medial aspect of the STN on coronal, sagittal, and axial T2 MR sections of the same specimen. C: The navigation probe on the superomedial aspect of the red nucleus. The red nucleus is located posterior to the mammillothalamic tract and mammillary body, medial to the STN, and superior to the substantia nigra. D: Stereotactic localization of the superomedial aspect of the red nucleus. E: The navigation probe on the medial aspect of the substantia nigra. The substantia nigra lies ventral to the red nucleus and the STN. F: Stereotactic localization of the medial aspect of the substantia nigra. Nav. = navigation; Paraterm. = paraterminal. Panels A, C, and E: Copyright Necmettin Tanriover. Published with permission. Figure is available in color online only.

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