Magnetic Resonance Imaging of the Temporal Lobe: Normal Anatomy and Diseases

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1 Canadian Association of Radiologists Journal 65 (2014) 148e157 Neuroradiology / Neuroradiologie Magnetic Resonance Imaging of the Temporal Lobe: Normal Anatomy and Diseases Alla Khashper, MD*, Jeffrey Chankowsky, MD, FRCPC, Raquel del Carpio-O Donovan, MD, FRCPC Department of Radiology, McGill University Health Center, Montreal, Quebec, Canada Abstract Objective: This pictorial essay will review the magnetic resonance imaging anatomy of the temporal lobes and describe the major pathologic processes of this complex area. Conclusions: Magnetic resonance imaging is an essential tool in the investigation of a patient with suspected temporal lobe pathology. Various conditions may affect this anatomic region, and, therefore, classification of imaging findings into specific groups may help provide a more focused differential diagnosis. Resume Objectif : Cet essai illustre a pour but de passer en revue l anatomie des lobes temporaux en imagerie par resonance magnetique et de decrire les principaux processus pathologiques qui touchent cette region complexe. Conclusions : L imagerie par resonance magnetique joue un r^ole essentiel dans l examen du patient que l on soupçonne de presenter une pathologie du lobe temporal. Diverses affections peuvent toucher cette region anatomique; c est pourquoi les resultats d imagerie doivent ^etre classifies selon des categories precises afin de favoriser l etablissement d un diagnostic differentiel cible. Ó 2014 Canadian Association of Radiologists. All rights reserved. Key Words: Temporal lobe; Magnetic resonance imaging anatomy; Magnetic resonance imaging findings; Temporal lobe pathology Throughout the history of medicine, the temporal lobe has been considered an enigmatic region. Presently, there is a well-described group of diseases that affect the temporal lobe. Common clinical presentations include seizures, dementia, and memory impairment, followed by a spectrum of behavioral disturbances. Technical improvements in diagnostic imaging have certainly improved our ability to make more-specific diagnoses. Computed tomography is often the initial examination; however, magnetic resonance imaging (MRI) is almost always required for further workup. MRI provides excellent spatial and soft-tissue contrast resolution that helps demonstrate normal anatomic landmarks and tissue abnormalities. This pictorial essay aims to * Address for correspondence: Alla Khashper, MD, Department of Radiology, McGill University Health Center, 1650 Cedar Avenue, Suite C5 118, Montreal, Quebec H3G 1A4, Canada. address: khashper@yahoo.com (A. Khashper). review normal imaging anatomy of the temporal lobes and demonstrate various pathologies that affect this region of the brain primary based on conventional MRI. Anatomy The upper surface of the temporal lobe is delimited from the frontal and parietal lobes by the sylvian fissure. No clear boundary is defined posteriorly, where it is separated from occipital and parietal lobes by an imaginary lateral parietotemporal line running downward from the posterior edge of the sylvian fissure (Figure 1). The medial border is delimited by a line that connects the inferior fork of the sylvian fissure to the superior-lateral aspect of the choroidal fissureetemporal horn complex [1]. The temporal lobe is composed of neocortex and mesial temporal lobe structures, including the uncus, parahippocampal gyrus, amygdala (located superiorly and anteriorly to hippocampal head), /$ - see front matter Ó 2014 Canadian Association of Radiologists. All rights reserved.

2 MRI findings in temporal lobe of the brain / Canadian Association of Radiologists Journal 65 (2014) 148e T1W inversion recovery sequence avoids partial volume averaging and provides high-contrast resolution between grey and white matter. Diffusion weighted images (DWI) are included in our routine temporal epilepsy protocol, which may provide information in the peri-ictal phase in patients with epilepsy [2]. Contrast enhancement is not routinely needed, unless tumour is suspected. Anatomic Variants and Developmental Abnormalities of Temporal Lobe Anatomical Variants Figure 1. Imaging anatomy of temporal lobe. The temporal lobe is delimited from the frontal (FL) and parietal lobes (PL) by the sylvian fissure (SF). The posterior border is delimited from the occipital lobe (OL) by the imaginary temporo-occipital line (white line). Superior (S), medial (M), and inferior (I) temporal gyri are divided by corresponding superior and inferior sulci. and hippocampus (composites of head, body, and tail) (Figure 2). Imaging Protocol This MRI protocol excludes quantitative MRI (hippocampal volumetry or T2 relaxometry) and functional (spectroscopy, perfusion) MRI, which are beyond the scope of this review. In our institution, sagittal T1-weighted (W) spin echo sequence is initially obtained to demonstrate gross brain anatomy and to ensure the optimal acquisition plane of the coronal oblique images perpendicular to the long axis of hippocampus. Coronal T2W and fluid attenuated inversion recovery (FLAIR) sequences oriented to the hippocampus reveal morphology and optimally demonstrate signal characteristics of the mesial temporal lobe. Thin, 1-mm, 3-dimensional, fast spoiled gradient-echo recalled (FSPGR) When temporal lobe asymmetry is recognized, the right side is usually larger than the left. Therefore, a smaller right temporal lobe is worth special attention in symptomatic patients [3]. Asymmetry of collateral white matter is uncommon but might be seen in normal individuals and should be considered a supportive finding rather than primary sign of hippocampal sclerosis [4]. Developmental Abnormalities Hippocampal developmental abnormalities are found in a high percentage of patients with congenital malformations. Arrest of the normal hippocampal inversion is found bilaterally in association with congenital malformations (ie, agenesis of the corpus callosum, lissencephaly, holoprosencephaly, or Dandy-Walker complex) (Figure 3). However, the presence of unilateral hippocampal abnormality should prompt a reader for searching of cortical disorder (ie, heterotopia, polymicrogyria, schizencephaly) located on the same side [5]. Focal thickening of cerebral cortex >4 mm is compatible with cortical dysplasia often associated with increased T2 signal in the abnormal cortex and underlying white matter [6]. Grey matter heterotopia is another well-recognized developmental abnormality, which reflects collections of dysplastic neurons in unusual locations. This arrested neuronal migration lies between the ependymal surface of the ventricles and subcortical fibers (Figure 4); heterotopias must parallel the signal intensity of grey matter on all MRI sequences. Figure 2. Imaging anatomy of temporal lobe. Coronal T2-weighted (A) and sagittal T1 3-dimensional inversion recovery (B) images, showing mesial temporal lobe structures: sylvian fissure (1); superior (2), medial (3), inferior (4) temporal gyri; parahippocampal gyrus (5); collateral white matter (6); uncus (U); amygdala (A); and head (H), body (B), and tail (T) of the hippocampus.

3 150 A. Khashper et al. / Canadian Association of Radiologists Journal 65 (2014) 148e157 Figure 3. Axial fluid attenuated inversion recovery image of patient with Dandy-Walker spectrum, revealing enlargement of IV ventricle (*) and agenesis of the cerebellar vermis in association with globular-shaped unfolded hippocampi (arrows). A 3-dimensional T1W high-resolution sequence is particularly helpful in demonstrating small areas of grey heterotopia or cortical dysplasia. Malformations of cortical development are usually associated with small hippocampi, otherwise grey matter heterotopia might directly invade mesial temporal structures [7,8]. Spontaneous encephalocele is defined as herniation of cerebral parenchyma and meninges through skull defects and represents a rare cause of intractable seizures, cerebrospinal fluid leak or possible meningitis [9]. Indeed, the entity is uncommon; however, surgical treatment might cure the patient (Figure 5). Figure 5. Coronal T2-weighted image, showing occult subtemporal meningoencephalocele (arrows) projecting into the sphenoid sinus medially from the inferomedial aspect of the right temporal lobe, which contains dysplastic brain parenchyma. Temporal Lobe Lesions Lesions in the temporal lobe may be classified into 3 groups according to their MRI features: (a) pathologies that demonstrate volume loss, (b) bilateral disease, and (c) space-occupying lesions (Table 1). Temporal Lobe Disease Associated With Volume Loss Volume loss can be seen with normal aging (Figure 6), old infarction, sequelae of remote trauma, or surgery, as well previous infection or inflammation. Therefore, knowledge of Figure 4. Heterotopic grey matter in an 18-year-old patient with seizures. Coronal 3-dimensional T1 fast spoiled gradient-echo replaced image, revealing a large heterotopic focus (arrows) in the right temporal lobe. Table 1 Imaging based classification of pathology that involves the temporal lobe Unilateral volume loss Mesial temporal sclerosis Old infarction Remote brain injury Prior surgery Bilateral pathology Alzheimer disease Fronto-temporal dementia Age-related volume loss Mesial temporal sclerosis (10%) Limbic encephalitis Postradiation changes Space-occupying lesions Cystic neoplasia Solid neoplasm Encephalitis Abscess Vascular malformations Acute infarction Acute trauma

4 MRI findings in temporal lobe of the brain / Canadian Association of Radiologists Journal 65 (2014) 148e Figure 6. A coronal T2-weighted magnetic resonance imaging, revealing age-related findings, including generalized volume loss, uniform dilatation of lateral ventricles, and hyperintense signal in the periventricular white matter. Hippocampi (arrows) are unremarkable. the medical history as well as comparison with previous imaging is crucial. The specific location of the volume loss is also very revealing. For example, posttraumatic encephalomalacia is commonly seen in anterior pole or posterior inferior aspect of the temporal lobe. Sequelae of herpes encephalitis classically involves the mesial temporal lobe and limbic system (Figure 7), which distinguishes poste herpetic encephalomalacia from infarction that involves particular vascular territories. Specific findings in Alzheimer disease include bilateral loss of hippocampal height and increased width of the choroidal fissure and temporal horn, associated with periventricular white matter hyperintensity (Figure 8). Figure 8. Coronal T1-weighted magnetic resonance imaging, demonstrating typical findings of symmetric bilateral mesial temporal atrophy in a patient with known Alzheimer disease, including increased width of the temporal horns and decreased height of the hippocampi (arrowheads). Frontotemporal dementia is characterized by frontotemporal volume loss, which allows differentiation from the temporoparietal volume loss seen in Alzheimer disease. Agerelated changes are usually characterized by diffuse widening of cerebral sulci and enlarged ventricles, which reflect cortical and central type of volume loss, respectively. This is commonly associated with chronic microvascular ischemic changes in white matter. Hippocampal atrophy is unusual with normal aging (Figure 6) [10]. Figure 7. Coronal T2-weighted image, revealing bilateral marked mesial temporal encephalomalacia compatible with sequelae of herpes encephalitis. Figure 9. Right mesial temporal sclerosis on coronal oblique T2-weighted magnetic resonance imaging. Classic volume loss and dysmorphic morphology of the right hippocampus, hyperintense signal abnormality (dashed arrow), and associated secondary enlargement of the right temporal horn (arrow).

5 152 A. Khashper et al. / Canadian Association of Radiologists Journal 65 (2014) 148e157 (Figure 9). The disease usually affects the entire hippocampus, but partial involvement may also be seen. Secondary signs include unilateral atrophy of the mammillary body or fornix, thinning of the collateral white matter bundle, and loss of grey-white demarcation in the ipsilateral anterior temporal lobe (Figure 10). Unilateral dilatation of the temporal horn represents a less reliable sign and might represent an anatomic variant when it is a mild and isolated finding [8]. Selective transcortical amygdalohippocampectomy is a possible surgical treatment for patients with refractory temporal epilepsy. In cases of persistent seizures after surgery, MRI might demonstrate residual sclerosis of hippocampal formation and lead to repeated surgical treatment (Figure 11). Bilateral Temporal Lobe Abnormalities Figure 10. Coronal oblique T2-weighted magnetic resonance imaging, showing secondary signs of mesial temporal sclerosis, including ipsilateral atrophy of fornix (arrow), mammillary body atrophy (arrowhead), temporal horn dilatation (dashed arrow), thinning of the collateral white matter (CWM) adjacent to the collateral sulcus (CS). Mesial temporal sclerosis (MTS) is the most common cause of complex partial seizures and is characterized histologically by pyramidal cell loss and gliosis in the hippocampal formation, amygdala, parahippocampal gyrus, and the entorhinal cortex. Key MRI features of MTS include hippocampal volume loss that is commonly associated with hyperintense T2W and FLAIR signal abnormality Figure 11. Coronal oblique fluid attenuated inversion recovery magnetic resonance imaging, showing remote right selective transcortical amygdalohippocampectomy (*). Residual right hippocampus (arrow) is atrophic and shows hyperintense signal compatible with sclerosis, potentially explaining persistent refractory seizures. The minor gliosis is seen along surgical tract. Note atrophy of the right fornix (arrowhead). Bilateral temporal lobe signal abnormalities may be seen in various clinical scenarios. Infectious diseases (herpes simplex virus, congenital cytomegalovirus infection) may involve the temporal lobes bilaterally. Cerebral autosomal dominant arteriopathy with subcortical infarctions and leukoencephalopathy is a hereditary small-vessel disease that affects young individuals who usually present with migraines and recurrent strokes that progress to subcortical dementia. MRI findings include focal lacunar infarctions and diffuse T2W hyperintensity in the white matter similar to chronic ischemic changes seen in the elderly. However, T2W hyperintensity specifically confined to the temporal poles is characteristic and diagnostic of cerebral autosomal dominant arteriopathy with subcortical infarctions and leukoencephalopathy (CADASIL) (Figure 12). Involvement of the external capsule, although less specific, may be seen in early stage disease [10,11]. In 3%-10% of cases, imaging findings of MTS are seen bilaterally, which represents a diagnostic challenge (Figure 13), which may place a patient in a nonsurgical category [12]. Subacute encephalitis is usually related to paraneoplastic syndrome with or without onconeural antibodies. A common clinical presentation includes memory loss and seizures, and it is often associated with cancers of the lung, testicle, and breast. Hyperintense T2W and FLAIR abnormality and focal enhancement of mesial temporal structures (Figure 14) may persist from months to years and result in focal volume loss approximately 1 year after onset of the disease [13]. Herpes simplex virus (HSV) is the most common cause of acute fatal sporadic encephalitis, with a particular predilection for the limbic system. Key imaging features include bilateral or unilateral signal abnormality in the temporal lobes that extends to the limbic system, early hemorrhagic changes, restriction on DWI, and abnormal enhancement (Figure 15). A typical clinical presentation includes systemic signs of acute infection, positive HSV serology and elevated viral titers. HSV encephalitis may be differentiated from acute infarction (Figure 16) based on the predominant

6 MRI findings in temporal lobe of the brain / Canadian Association of Radiologists Journal 65 (2014) 148e Figure 12. Cerebral autosomal dominant arteriopathy with subcortical infarctions and leukoencephalopathy (CADASIL) in a 38-year-old patient. Axial fluid attenuated inversion recovery (A) and T2-weighted (B) images, showing characteristic subcortical infarctions in the anterior temporal poles (A, arrows) and chronic ischemic changes in the basal ganglia and external capsules bilaterally. involvement of grey matter with relative sparing of white matter, extension towards cingulate gyrus and insula as well as its possible bilaterality. Temporal lobe necrosis represents a late-stage complication of radiotherapy in patients with nasopharyngeal cancer who are receiving radiotherapy. Due to the inclusion of the temporal lobes in the radiation field, high-dose treatment (>5000 cgy) may result in temporal lobe necrosis. T2W hyperintensity is typically seen in the inferomedial aspect of the temporal lobes, found bilaterally in approximately two-thirds of cases (Figure 17). In addition, the affected temporal regions may develop cystic changes, hemorrhages, or enhancement [14]. Findings usually remain stable over the long term, which allows for distinction from metastasis or primary brain neoplasm. In the immediate postictal phase, hippocampal oedema may hide underlying atrophy or mimic disease (encephalitis, neoplasm, etc). Postictal MRI abnormalities consist mainly of T2W and FLAIR hyperintensity (Figure 18) and restricted diffusion on DWI [8]. However, the clinical history and rapid resolution help to clarify the diagnosis. Figure 13. Coronal oblique T2-weighted magnetic resonance imaging, revealing small hyperintense hippocampi (arrows) and dilated temporal horns (arrowheads), which represent bilateral mesial temporal sclerosis. Figure 14. Limbic encephalitis in a 72-year-old patient who presented with memory impairment. Axial T2-weighted images, showing increased signal in both mesial temporal lobes (arrows).

7 154 A. Khashper et al. / Canadian Association of Radiologists Journal 65 (2014) 148e157 Figure 15. Herpes simplex virus encephalitis in a 56-year-old man with somnolence. Axial fluid attenuated inversion recovery image, revealing hyperintense signal (arrows) in the anterior and mesial portions of the right temporal lobe and along the gyrus rectus. Temporal Space-Occupying Lesions Focal temporal lobe lesions account for 10% of temporal lobe seizures [6]. Lesions may demonstrate specific imaging features, which allow one to narrow the differential diagnosis. Figure 17. Temporal lobe radiation necrosis 6 years after radiotherapy for nasopharyngeal carcinoma. Axial T2 image, showing signal abnormality in both inferior temporal lobes, right (arrow) greater than left. Sphenoid sinus mucosal thickening and right mastoid opacification reflect postradiation changes. Temporal Lobe Tumours True temporal parenchymal neuroglial cysts are rare, congenital epithelial-lined lesions. They are rounded, unilocular, follow cerebrospinal fluid signal in all sequences, and show no mass effect nor enhancement. The suppressed signal on FLAIR images helps to distinguish them from lacunar infarctions or cystic neoplasms. Dysembryoplastic neuroepithelial tumours, ganglioglioma, low-grade astrocytoma, and oligodendroglioma are commonly Figure 16. Acute infarction in a 55-year-old patient with acute onset of expressive aphasia. Axial fluid attenuated inversion recovery image, demonstrating a hyperintense signal in the right temporal lobe, which involves both white and grey matter, much more typical of infarction rather than herpes simplex virus infection. Figure 18. Subtle postictal changes a few hours after generalized seizure. Symmetric mild bilateral hyperintense T2 signal abnormality (arrows) is seen in the hippocampi. The findings resolved on follow-up examination.

8 MRI findings in temporal lobe of the brain / Canadian Association of Radiologists Journal 65 (2014) 148e Figure 19. Small low-grade astrocytoma in the right hippocampus (arrow) with an ill-defined increased T2-weighted signal, which remained stable over 10 years. seen in young patients (<35 years old). They usually are well demarcated and surrounded by minor oedema, if at all. However, these lesions often display no specific imaging features. Gliomas, most commonly astrocytomas (Figure 19), account for nearly 80% of primary neoplasms in patients who present clinically with seizures [8]. Dysembryoplastic neuroepithelial tumours (DNETs) are cortical-based tumours with occasional cysts and calcifications that show no enhancement (Figure 20). They may cause scalloping of the overlying bone and may mimic cortical dysplasias [6]. Predominantly solid tumours such as high-grade astrocytoma or glioblastoma multiforme show more aggressive Figure 20. Dysembryoplastic neuroepithelial tumour in a 21-year-old patient. T2-weighted image, revealing multicystic partially solid lesion (arrow) in the left hippocampus, which involves the cortex, without oedema or enhancement (not shown). features, including heterogeneous partially necrotic parenchyma, surrounding oedema, infiltrative margins, significant mass effect, and marked enhancement (Figure 21). Differentiation of metastatic lesion from primary brain tumour remains challenging and often requires advanced imaging techniques (perfusion, magnetic resonance spectroscopy). Infiltrative type of growth would favor primary brain tumour, whereas multiple lesions, significant vasogenic oedema, and mass effect out of proportion to tumour size are all typical for metastases (Figure 22). Brain abscesses demonstrate similar imaging features, including peripheral Figure 21. T2-weighted image (A), showing a right temporal glioblastoma multiforme surrounded by marked oedema and infiltrative tumour (A, arrows), which causes significant mass effect. The lesion demonstrates aggressive imaging features, including signal heterogeneity, ill-defined borders, necrotic centre, and peripheral enhancement on T1-weighted sequence (B, arrowheads).

9 156 A. Khashper et al. / Canadian Association of Radiologists Journal 65 (2014) 148e157 Figure 22. Solitary brain metastases in a 68-year-old woman with breast cancer. A small left inferior temporal lesion surrounded by significant vasogenic oedema (A) and showing peripheral enhancement on T1-weighted postcontrast image (B, arrow). enhancement, restricted diffusion on DWI, and surrounding vasogenic oedema (Figure 23). Clinical history and symptoms help with the correct diagnosis. Vascular Pathology Approximately 50% of patients with arteriovenous malformations and cavernomas experience seizures. Most developmental venous anomalies are clinically silent. However, they frequently accompany cavernomas [8]. On T2W sequence, cavernomas typically demonstrate hyperintense foci on T1W images and significantly hypointense rim outlining the lesion on T2W sequences due to the presence of blood products of different ages (Figure 24). Gradient echo T2W sequences are sensitive for the detection of blood products and blooming artifact that might pick up additional cavernomas compared to regular T2W images. Arteriovenous malformations appear as multiple flow voids (nidus) supplied by a feeding artery and is associated with a prominent draining vein (Figure 25). Figure 23. Toxoplasma abscess in a 57-year-old man known for having human immunodeficiency virus. Axial T2-weighted image, revealing a cortico-subcortical lesion (arrow) in the right posterior temporal lobe surrounded by marked oedema. Figure 24. Cavernoma in the left temporal lobe (arrow). Magnetic resonance imaging, showing a salt and pepper bright T2-weighted signal (due to slow-flowing blood and thrombosed vascular channels) surrounded by a rim of signal loss (due to hemosiderin deposition).

10 MRI findings in temporal lobe of the brain / Canadian Association of Radiologists Journal 65 (2014) 148e References Figure 25. A 35-year-old patient with a 5-cm arteriovenous malformation in the right temporal lobe; the central structure is compatible with nidus (*), supplied by right middle cerebral artery branches (arrow) and drainage into superficial and deep venous systems. Conclusion MRI is an essential tool in the investigation of a patient with suspected temporal lobe pathology. It may not only suggest the diagnosis but provide useful information concerning appropriate treatment and management. [1] DeFelipe J, Fernandez-Gil MA, Kastanauskaite A, et al. Macroanatomy and microanatomy of the temporal lobe. Semin Ultrasound CT MR 2007;28:404e15. [2] Szabo K, Poepel A, Pohlmann-Eden B, et al. Diffusion-weighted and perfusion MRI demonstrates parenchymal changes in complex partial status epilepticus. Brain 2005;128:1369e76. [3] Szabo CA, Xiong J, Lancaster JL, et al. Amygdalar and hippocampal volumetry in control participants: differences regarding handedness. Am J Neuroradiol 2001;22:1342e5. [4] Bronen RA, Cheung G. MRI of the temporal lobe: normal variations, with special reference toward epilepsy. Magn Reson Imaging 1991;9:501e7. [5] Sato N, Shinitsu H, Shimizu N, et al. MR evaluation of the hippocampus in patients with congenital malformations of the brain. AJNR Am J Neuroradiol 2001;22:389e93. [6] Castillo M. Metabolic, toxic, and degenerative disorders. In: The Core Curriculum: Neuroradiology. Lippincott, Williams & Wilkins; p. 79e116. [7] Montenegro MA, Kinay D, Cendes F, et al. Patterns of hippocampal abnormalities in malformations of cortical development. J Neurol Neurosurg Psychiatry 2006;77:367e71. [8] Gupta RG. Magnetic resonance imaging of temporal lobe epilepsy. Appl Radiol 2002;31:22e9. [9] Wind JJ, Caputy AJ, Roberti F. Spontaneous encephaloceles of the temporal lobe. Neurosurg Focus 2008;25:E11. [10] Sereka J, Jakkani RK. Clinico-radiological spectrum of bilateral temporal lobe hyperintensity: a retrospective review. Br J Radiol 2012;85:e782e92. [11] O Sullivan M, Jarosz JM, Martin RJ, et al. MRI hyperintensities of the temporal lobe and external capsule in patients with CADASIL. Neurology 2001;56:628e34. [12] Camacho DL, Castillo M. MR imaging of temporal lobe epilepsy. Semin Ultrasound CT MRI 2007;28:424e36. [13] Urbach H, Soeder BM, Jeub M, et al. Serial MRI of limbic encephalitis. Neuroradiology 2006;48:380e6. [14] Bharatha A, Yu E, Symons SP, et al. Early- and late-term effects of radiotherapy in head and neck imaging. Can Assoc Radiol J 2012;63:119e28.