A Combined MRI and Histology
Atlas of the Rhesus Monkey Brain in Stereotaxic Coordinates
This book is dedicated to Shanaz Saleem Farzana Saleem Rizwana Saleem
A Combined MRI and Histology
Atlas of the Rhesus Monkey Brain in Stereotaxic Coordinates
Kadharbatcha S. Saleem The Riken Brain Science Institute, Wako-shi, Japan; Washington University School of Medicine, Missouri, USA
and
Nikos K. Logothetis Max Planck Institute for Biological Cybernetics, Germany
AMSTERDAM • BOSTON • HEIDELBERG • LONDON • NEW YORK • OXFORD PARIS • SAN DIEGO • SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier
Academic Press is an imprint of Elsevier 84 Theobald’s Road, London WC1X 8RR, UK 30 Corporate Drive, Suite 400, Burlington, MA 01803, USA 525 B Street, Suite 1900, San Diego, California 92101-4495, USA First edition 2007 Copyright © 2007 Elsevier Ltd. All rights reserved No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone (44) (0) 1865 843830; fax (44) (0) 1865 853333; e-mail:
[email protected]. Alternatively you can submit your request online by visiting the Elsevier web site at http://elsevier.com/ locate/ permissions, and selecting Obtaining permission to use Elsevier material Notice No responsibility is assumed by the published for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library Library of Congress Catalog Number: 2006934165 ISBN–13: 978-0-12-372559-2 ISBN–10: 0-12-372559-3 For information on all Academic Press publications visit our web site at http://books.elsevier.com Typeset by Charon Tec Ltd (A Macmillan Company), Chennai, India www.charontec.com Printed and bound in China 07
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Contents
Preface About the Authors Acknowledgments
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Chapter 1
Introduction, Methods and Presentation of Data Introduction Materials and Methods Presentation of Illustrations in this Book References
1 1 1 4 6
Chapter 2
Cytoarchitectonic and Chemoarchitectonic Organization of Cortical and Subcortical areas: Sources and References Temporal Cortex Prefrontal Cortex Premotor and Motor Cortex (Agranular Frontal Cortex) Cingulate and Retrosplenial Cortex Postcentral Gyrus, Parieto-Occipital Cortex, and Nearby Cortex Other Cortical Areas Hippocampus Subcortical Structures References
13 13 18 19 21 21 22 22 23 24
Chapter 3
Horizontal Series MRI, Photomicrographs and Drawings in Horizontal Plane
29 29
Chapter 4
Coronal Series MRI, Photomicrographs and Drawings in Coronal Plane
125 125
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Contents
Chapter 5
Selected Cortical and Subcortical Areas in three Different MRI Planes Selected Cortical Areas Selected Subcortical Areas
Index of Abbreviations
279 281 282
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Preface
A combined MRI and Histology: Atlas of the Rhesus monkey brain in stereotaxic coordinates is designed to provide an easy to use resource/reference for anatomical, physiological, and functional imaging (fMRI, PET and MEG) studies in primates. We hope that this book will serve as a valuable guide for the neuroscientists. The key features: 1. The first combined MRI and histology maps of the cortical and subcortical areas of any non-human primate species. 2. The first detailed delineations of the cortical and subcortical areas in both horizontal and coronal planes in the same animal using five different staining methods (Nissl and immunohistochemistry for parvalbumin, calbindin, calretinin, and a non-phosphorylated epitope of a neurofilament protein [SMI-32]). 3. The dorsoventral extent of the left hemisphere is shown in 47 horizontal MRI and photomicrographic sections matched with 47 detailed diagrams (Chapter 3). 4. The rostrocaudal extent of the right hemisphere is illustrated in 76 coronal MRI and photomicrographic sections, and 76 corresponding drawings (Chapter 4). 5. Selected cortical and subcortical areas are shown in three different MRI planes (horizontal, coronal, and sagittal MRI planes) (Chapter 5). 6. The stereotaxic grid was derived from the in-vivo MR image, so it is free from shrinkage. 7. Shrinkage in the histological sections and drawings was corrected by comparison with the corresponding in-vivo MR images.
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About the Authors
K.S. Saleem, Ph.D. Dr. Kadharbatcha S. Saleem received his B.Sc., M.Sc., and Ph.D in Life Sciences (Zoology/ Neuroanatomy) from the University of Madras, India. Subsequently he conducted research on the anatomical organization and connections of visual cortical areas, and the medial temporal lobe memory regions in primates at RIKEN Brain Science Institute in Japan. He also conducted research on the neuronal circuitry in the basal ganglia and cortex using MRI-visible contrast agent. Since 2001, he has been at Washington University School of Medicine, St. Louis. Dr. Saleem’s main interest is the study of functionally less explored regions in the brain, particularly the prefrontal cortex and the temporal cortex. N.K. Logothetis, Ph.D. Dr. Nikos K. Logothetis is director of the department of Physiology of Cognitive Processes at the Max Planck Institute for Biological Cybernetics, in Tuebingen, Germany. He received a B.S. in Mathematics from the University of Athens, a B.S. in Biology from the University of Thessaloniki, and his Ph.D. in Human neurobiology from the Ludwig-Maximilians University in Munich. After research at Massachussetts Institute of Technology he joined the faculty of the Division of Neuroscience at Baylor College of Medicine in Houston. Since 1997 he has been at the Max Planck Institute for Biological Cybernetics. He works on the physiological mechanisms underlying visual perception and object recognition. His recent work includes the application of functional imaging techniques to monkeys and measurement of how the functional magnetic resonance imaging signal relates to neural activity. Dr. Logothetis is a recipient of the DeBakey Award for Excellence in Science, the Golden Brain Award of the Minerva Foundation, the 2003 Louis-Jeantet Prize of Medicine, and the Zülch-Price for Neuroscience.
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Acknowledgments
This work was supported by the Riken Brain Science Institute, Japan and Max-Planck Society, Germany. We thank Dr. Tsutomu Hashikawa (Riken Brain Science Institute, Japan) for the continuous support on this project. We thank Prof. G. Luppino (Universita di Parma, Italy) for the valuable comments and suggestions on the architectonic subdivisions of the agranular frontal cortex (premotor and motor cortex), and the parietal cortex, and Profs. Joseph L. Price and Andreas Burkhalter (Washington University) for the critical comments on Chapters 1 and 2. We thank Mark Augath (Max-Planck Institute) for the tremendous support on the MRI data collection and analysis, and Asiyabegum for technical (histological) assistance. Finally, we thank anonymous reviewers for the support, comments and useful suggestions on the proposal of this project.
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Chapter 1 Introduction, Methods and Presentation of Data
INTRODUCTION To understand the anatomical localization of functional activity in different cortical areas, we need an accurate map of the architectonic areas with reference to MR images in the same animal. In this study, we mapped the detailed architectonic subdivisions of the cortical and subcortical areas in the rhesus monkey (Macaca mulatta) using high-resolution MR images and the corresponding histological sections in the same animal. The map of cortical and subcortical areas was derived from both horizontal and coronal sections using five different staining methods (see below). In fMRI studies, the horizontal plane of section is often the preferred plane because multiple functionally active areas can be visualized simultaneously. This is the first detailed map of the macaque monkey brain that links cytoarchitectonic areas with MR images in the horizontal plane as well as in coronal plane (see other brain maps by Szabo and Cowan, 1984; Paxinos et al., 2000). The combined MRI and histology atlas can be used as a reference for the anatomical and physiological studies in macaque monkeys, and the functional imaging studies in human and non-human primates using fMRI and PET.
MATERIALS AND METHODS A male rhesus monkey (D99; Macaca mulatta; 4 years old), weighing 4.9 kg was used. The high-resolution T1 weighted MRI data was collected several times in this animal. Following the MRI scanning, the animal was perfused and the brain was processed for histology (see details below). All studies were in full compliance with the guidelines of the European community (EUVD 86/609/EEC) for the care and use of laboratory animals.
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MRI data collection The MRI data collection was done under general anesthesia. After the premedication with glycopyrolate (I.M. 0.01 mg/kg) and ketamine (I.M. 15 mg/kg), anesthesia was induced by intravenous injection of fentanyl (3 µg/kg), thiopental (5 mg/kg), and succinylcholine chloride (3 mg/kg). Following the intubation of the trachea, the lungs were ventilated using a Servo Ventilator 900 C (Siemens, Germany), maintaining an end-tidal CO2 of 33 mm Hg and oxygen saturation of 95%. Balanced anesthesia was maintained with end-tidal 0.35% (0.23 MAC for macaques) isoflurane in air and fentanyl (3 µg/kg/hr). Muscle relaxation was achieved with mivacurium (5 mg/kg/h). The body temperature, ECG, NIBP, CO2, and SpO2 were monitored throughout the experiment (Logothetis et al., 1999). The above protocol is established as optimal for imaging without discomfort to the animal. Prior to MRI scanning, the animal was placed in a custom-made restraining device mounted on the MRI chair, which held the animal’s head. The MRI scanning was done in a vertical 4.7 T (200 MHz) scanner with a 40 cm diameter bore (Biospec 47/40v, Bruker Medical, Ettlingen, Germany). The animal was imaged using a 120 mm-wide, custom-made linear homogeneous volume (saddle) coil (Logothetis et al., 2002). A linear birdcage-type resonator with an inner diameter of 198 mm (Bruker Medical, Ettlingen, Germany) was also used that delivered superior homogeneity over the entire brain volume. We used a Modified Driven Equilibrium with Fourier Transform (3D-MDEFT) method to obtain T1 weighted anatomical images. The imaging sequence used 180° and 90° adiabatic RF pulses for spin preparation (excitation flip angle 20°) and a segmented gradient-echo acquisition (Tau 800 ms; TR 14.9 ms; TE 4.0 ms). We collected five averages and four segments for an image acquisition time of 3 h 50 min to obtain 256 256 240 matrices at FOV 12.8 cm 12.8 cm 12.0 cm. All scans achieved an isotropic voxel resolution of 0.53 mm3. All horizontal MRI slices were aligned parallel to the horizontal plane passing through the interaural line and the infraorbital ridge (Ear Bar Zero or EBZ). The coronal MRI slices were aligned parallel to the vertical plane passing through the interaural line (EBZ).
Histological processing After the MRI scanning, the animal was deeply anesthetized with a lethal dose of sodium pentobarbital and perfused transcardially with warm heparinized saline followed by 1 liter of 1% paraformaldehyde in 0.1 M phosphate buffer (PB; pH 7.4, 4°C), 2 liters of 4% paraformaldehyde in 0.1 M PB (pH 7.4, 4°C) and finally 1 liter of 4% paraformaldehyde and 10% sucrose in 0.1 M PB (pH 7.4, 4°C). The flow rate of the fixative solution was adjusted so that the perfusion with paraformaldehyde took approximately 45 min. The brain was removed from the skull, photographed and carefully blocked in the stereotaxic plane (corresponding to MRI planes),
Introduction, Methods and Presentation of Data
and then postfixed for 6 hours in the last fixative-sucrose solution. Finally, these blocks were stored in 20% and 30% sucrose in 0.1 M PB at 4°C until they sank. We prepared four blocks from the two hemispheres: two blocks from the left hemisphere for horizontal slices, and two from the right hemisphere for coronal slices. Frozen sections were cut in horizontal and coronal planes at 40 m and 50 m thickness, respectively. Five parallel series of sections were stained for Nissl substance or with antibodies against parvalbumin, calbindin, calretinin, and a nonphosphorylated epitope of a neurofilament protein (SMI-32).
Immunohistochemical procedures Details of the antibodies used are given in Table 1.1. The calcium binding proteins parvalbumin, calbindin and calretinin have been shown previously to stain subpopulations of non-pyramidal neurons (GABAergic) in the neocortex, and to label different types of neurons in subcortical structures (Jones and Hendry, 1989; Jones, 1998; current study). The SMI-32 antibody recognizes a non-phosphorylated epitope of neurofilament H (Sternberger and Sternberger, 1983; Goldstein et al., 1987). The antibody has been shown to stain a subpopulation of pyramidal cells in the neocortex (e.g. Campbell and Morrison, 1989; Hof and Morrison, 1995); the pattern of staining seen in this study corresponds to well established patterns from previous studies. Free-floating sections were preincubated in the phosphate buffered saline (PBS), containing 0.5% Triton-X 100 and 5% normal serum (normal horse serum for parvalbumin, calbindin, and SMI-32, or normal goat serum for calretinin) and 2% bovine serum albumin (BSA) for 60 minutes at room temperature. The sections were then incubated in PBS containing 0.3% Triton-X 100, 3% normal serum, 1% BSA, and the primary antibody for 2 days at 4°C. After washing with PBS, sections were incubated in PBS containing 0.3% Triton-X 100, normal serum, 0.5% BSA, and the biotinylated horse antimouse IgG (for parvalbumin, calbindin, and SMI-32), or biotinylated goat antirabbit IgG (calretinin) for 90 minutes at room temperature. After washing with PBS, sections were reacted and stained in a solution containing 0.05 M tris buffer (pH 7.2–7.4), 0.05% diaminobenzidine (DAB) and 0.003% hydrogen peroxide (H2O2). The sections were then mounted on the glass slides, air-dried, dehydrated, and coverslipped with Entellan. Table 1.1 Antibody
Source
Catalog #
Species
Dilution
Parvalbumin Calbindin Calretinin SMI-32
Sigma Sigma Swant Sternberger Monoclonals
P-3171, Clone PA-235 C-8666, Clone CL-300 7698 (7699/4) SMI-32
Mouse Mouse Rabbit Mouse
1:2000 1:2000 1:2000 1:2000 or 1:5000
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Data analysis The sections were observed with a light microscope under bright field illumination. To make the figures, the horizontal and coronal histology sections were scanned, using a Nikon Film Scanner (LS-4500AF), and the scanned images were processed in Adobe Photoshop. Although we blocked and cut the left and right hemispheres in the stereotaxic plane (corresponding to MRI planes), the processed histological sections did not match exactly with the corresponding MR images. To correct this mismatch, we rotated and digitally resliced the MRI volume at the appropriate rostrocaudal and dorsoventral extent using the MEDx program. This procedure resulted in a perfect match of sulci and other anatomical landmarks in both MR images and histological sections (see images in Chapters 3 and 4). The final plane of the sections is therefore very slightly different from the stereotaxic plane (i.e. the horizontal plane passing through the interaural line and the infraorbital ridge).
PRESENTATION OF ILLUSTR ATIONS IN THIS BOOK
Presentation of photographs and drawings in horizontal series (Chapter 3) An example of the format in which photographs and drawings of the sections in the horizontal series are presented is shown in Figure 1.2 (‘How to read the horizontal series’). In brief, we illustrate the horizontal MR image sampled at 1 mm intervals and the matched histological sections stained for Nissl, Parvalbumin, and SMI-32 on the left side of the page. To help with the orientation of the section, we have labeled a few cortical and subcortical regions (e.g. somatosensory cortex, putamen, etc.). The dorsoventral position of the MR image with reference to the horizontal plane passing through the interaural line (Ear Bar Zero or EBZ) is marked on the rendered brain image of the corresponding hemisphere, made using the Analyze program. We marked 1, 2, etc. if the position of the slice is dorsal to the EBZ, and 1, 2 etc., if the position of the slice is ventral to the EBZ. Figure 1.1A shows other details. The detailed architectonic subdivisions of cortical and subcortical areas are illustrated in the corresponding line drawing of the section on the right side of the page. The drawings were made from Nissl or parvalbumin stained sections using Canvas software 8.0 (Deneba). The borders between different cortical and subcortical areas illustrated in the drawings were based on the observations from Nissl, Parvalbumin, SMI-32, calbindin and calretinin stained sections. We also relied on some of the observations based on the other publications
Introduction, Methods and Presentation of Data
(see Chapter 2). The stereotaxic grid and the exact position of the EBZ (interaural) illustrated with the drawing are based on the MR image shown at the bottom left. It should be noted that we corrected the shrinkage in the histology sections by comparing them with the corresponding MR images, and enlarging the drawings of the histology sections to fit. Thus, the final size of our horizontal and coronal drawings matches the in-vivo MR images. We estimated that the shrinkage of the histology sections due to the fixation procedures was approximately 11%. For other details see Figure 1.2.
Presentation of photographs and drawings in coronal series (Chapter 4) An example showing the presentation of photographs and drawing of the section in the coronal series is illustrated in Figure 1.3 (‘How to read the coronal series’). In brief, we illustrate the coronal MR image sampled at 1 mm intervals, and the matched histological sections stained for Parvalbumin and SMI-32 are on the left side of the page. The rostrocaudal position of the MR image with reference to the vertical plane passing through the interaural line (EBZ) is marked on the rendered brain image of the corresponding hemisphere. We marked 1, 2 etc., if the position of the slice is rostral to the EBZ, and 1, 2 etc., if the position of the slice is caudal to the EBZ (see Figure 1.1B). The other details are the same as before. Note that we lost a few histological sections at the end of each block due to the physical damage to the sections. We made drawings of these missing sections from the corresponding MR images (see Figures 39–41 and 104–108), and the mapping of the architectonic areas were interpolated from the adjacent histological sections or the corresponding regions of the opposite hemisphere.
Presentation of selected cortical and subcortical areas in different MRI planes (Chapter 5) In this chapter, we illustrated the location of selected cortical and subcortical areas in three different MRI planes: coronal, horizontal, and sagittal planes. The locations of these areas are schematically illustrated on the lateral, medial, and ventral views of the brain superimposed on the flatmap of the monkey cerebral cortex. The architectonic structure of these areas is illustrated in Chapters 3 and 4. The flatmaps were created using the Brain Voyager program (provided by Zoe Kourtzi, Max-Planck Institute and University of Birmingham), and the Caret program (provided by John Harwell and David Van Essen, Washington University, St. Louis).
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REFERE NCES Campbell, MJ and Morrison, JH. (1989) Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J. Comp. Neurol. 282:191–205. Goldstein, ME, Sternberger, LA and Sternberger, NH. (1987) Varying degrees of phosphorylation determine microheterogeneity of the heavy neurofilament polypeptide (Nf-H). J. Neuroimmunol. 14:135–148. Hof, PR and Morrison, JH. (1995) Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: a quantitative immunohistochemical analysis. J. Comp. Neurol. 352:161–186. Jones, EG. (1998) The thalamus of primates. In: Handbook of Chemical Neuroanatomy: The primate nervous system. Part II (Bloom, FE, Bjorklund, A and Hokfelt, T, eds). Vol. 14, pp. 1–298. New York: Elsevier. Jones, EG and Hendry, SHC. (1989) Differential calcium binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. Eur. J. Neurosci. 1:222–246. Logothetis, NK, Guggenberger, H, Peled, S and Pauls, J. (1999) Functional imaging of the monkey brain. Nat. Neurosci. 2:555–562. Logothetis, N, Merkle, H, Augath, M, Trinath, T and Ugurbil, K. (2002) Ultra high-resolution fMRI in monkeys with implanted RF coils. Neuron. 35:227–242. Paxinos, G, Huang, XF and Toga, AW. (2000) The Rhesus Monkey Brain in Stereotaxic Coordinates. San Diego: Academic Press. Sternberger, LA and Sternberger, NH. (1983) Monoclonal antibodies distinguish phosphorylated and non-phosphorylated forms of neurofilaments in situ. Proc. Natl Acad. Sci. 80:6126–6130. Szabo, J and Cowan, WM. (1984) A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis). J. Comp. Neurol. 222:265–300.
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Chapter 2 Cytoarchitectonic and Chemoarchitectonic Organization of Cortical and Subcortical areas: Sources and References
In the current study, we delineated the cytoarchitectonic and chemoarchitectonic characteristics of lateral and media temporal cortical areas based on our previous studies (see Saleem and Tanaka, 1996; Kondo et al., 2003, 2005; Saleem et al., 2006). We also distinguished architectonic subregions in the frontal, parietal, and occipital cortex, and many subcortical areas using Nissl, parvalbumin, SMI-32, calbindin, and calretinin staining that are mainly based on other published studies. These studies are briefly described under different subheadings as follows.
TEMPOR AL CORTEX
Medial temporal lobe (Perirhinal and Parahippocampal cortex, and Entorhinal cortex), Inferotemporal cortex (area TE) and Temporal pole (area TG) Perirhinal cortex (areas 35 and 36) This region was initially described in human by Brodmann (1909), who distinguishes area 35 as perirhinal cortex and area 36 as ectorhinal cortex (see Garey, 1994, Fig. 86, p. 110). In monkeys, Brodmann (1909) did not include either area 35 or 36 in his map of the cercopithicid monkey (guenon) cortex (see Garey, 1994, Fig. 91, p. 131), although he illustrated a section from a rhesus monkey that shows well developed areas 35 and 36 (Garey, 1994, Fig. 26, p. 43). More recently, both areas 35 and 36 have been recognized in monkeys, but it has been common to refer to both of them as the “perirhinal cortex”, and the term “ectorhinal” has been dropped.
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Area 35 is a narrow strip of agranular cortex located within in the lateral fundus and bank of the rhinal sulcus, between the entorhinal cortex (area 28) medially and area 36 laterally (see Figure 2.1B and C). Area 36 is a dysgranular or weakly granular cortex situated between area 35 medially, and area TEav laterally. Based on the architectonic characteristics, we divide area 36 into 3 subregions caudorostrally. They are areas 36c, 36r, and 36p (caudal, rostral and temporal-polar subregions of area 36, respectively). For architectonic details of these areas see Saleem et al., 2006. It should be noted that in our description, the perirhinal cortex does not extend into the temporal pole.
Parahippocampal cortex (areas TH and TF/TFO) This cortex is located in the posterior parahippocampal gyrus (Van Hoesen, 1982), and consists of two distinct cytoarchitectonic regions: areas TF and TH (von Bonin and Bailey, 1947). Area TH is a relatively small agranular cortical region that extends caudal to the entorhinal cortex and medial to area TF (Figure 2.1G). We found consistent rostrocaudal differences in the architectonic characteristics of area TF, especially in layers IV, V, and VI (Saleem et al., 2006). Based on these variations, and on differences in connections between rostral and caudal parts, we separated the caudal region from area TF and termed it “area TFO”, following a similar designation by Blatt et al. (2003; see also Saleem et al., 2006). However, our area TFO corresponds to areas THO and TLO of Blatt et al. (2003), but does not include more lateral area that they label TFO. While area TF is dysgranular, area TFO has a prominent layer IV, and can be considered granular cortex. The architectonic features of area TFO closely resemble those of the caudally adjacent visual area V4.
Entorhinal cortex (area 28) The cytoarchitectonic and chemoarchitectonic delineations of area 28 are similar to that of Amaral et al. (1987), and Pitkanen and Amaral (1993b).
Area TE Lateral to the perirhinal and parahippocampal cortex is the inferotemporal cortex area TE (von Bonin and Bailey, 1947). This area has been divided into four subregions: areas TEad, TEav, TEpd, and TEpv (Yukie et al., 1990; Saleem and Tanaka, 1996; Saleem et al., 2006). Areas TEad and TEav were located lateral to the perirhinal cortex, and areas TEpd and TEpv were found lateral to the parahippocampal cortex (Figure 2.1). These subregions have distinct architectonic characteristics (see Saleem et al., 2006), and connections with the cortex of the superior temporal sulcus, the hippocampus, amygdala, and the entorhinal, perirhinal, and parahippocampal cortex (Yukie et al., 1990; Saleem and Tanaka, 1996; Cheng et al., 1997; Saleem et al., 2000; Yukie, 2000). Caudal to the area TE (TEpd and TEpv) is area TEO. The border between area TE and TEO follows the electrophysiological mapping of Boussaoud et al. (1991) and is placed at the rostral limit of the posterior middle temporal sulcus (pmts).
Fig. 2.1 Chemoarchitectonic subdivisions of the perirhinal and parahippocampal cortex in macaque monkeys (adapted from Saleem et al., 2006). A–F: A series of color-coded images of parvalbumin stained sections through the medial and lateral temporal cortex, including the perirhinal cortex (areas 35 and 36), the parahippocampal cortex (areas TH, TF, and TFO), and areas 28 and TE (and its subdivisions) of a rhesus monkey (M. mulatta), made with the “MapAnalyser densitometry system”. Denser immuno-staining, corresponding primarily to neuropil staining, was coded as red, and weak staining as blue. The white lines normal to the surface mark boundaries between areas. Note that there is a clear decrease in the density of parvalbumin staining in areas 35, 36 (A-C), TF (D), and to a lesser extent TFO (E). G–H: Unfolded map and ventral brain surface of a cynomolgous monkey (M. fascicularis), illustrating the perirhinal cortex (blue and purple), parahippocampal cortex (light and dark orange), area 28 (red), the subdivisions of area TE, and area V4 (both yellow). The overall architectonic organization of perirhinal and parahippocampal cortex in rhesus monkey is similar to that of the cynomolgous monkey. The dashed lines in the map indicate the lips of the sulci (amts, ots, rs, and sts), and the solid lines show the borders between different subdivisions of the perirhinal and parahippocampal cortex. The red line indicates the boundary between dorsal and ventral TE. The solid lines with arrows at the sides of the unfolded map show the approximate location of parvalbumin stained sections (A–F). Scale bar in A 5 mm (also applies to B–F); 5 mm in G.
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Area TG We used terminology for the temporal pole similar to that used by Kondo et al. (2003). The temporal pole was designated area TG, following the commonly used terminology of von Bonin and Bailey (1947), and was subdivided into six regions: granular and dysgranular areas in the dorsal temporal pole (TGdg and TGdd, respectively), granular and dysgranular areas in the ventral temporal pole (TGvg and TGvd, respectively), a granular area around the rostral tip of the superior temporal sulcus (TGsts), and an agranular area on the medial side of the temporal pole (TGa). These subregions have distinct architectonic characteristics (see Kondo et al., 2003; Saleem et al., 2006), and connections with the orbital and medial prefrontal cortex (Kondo et al., 2003).
Auditory cortex and Superior temporal gyrus (STG) The terminology and architectonic criteria used in this study for the auditory cortex were based on the descriptions by Kaas and his colleagues (Hackett et al., 1998; Kaas and Hackett, 2000), with one modification. They subdivided macaque monkey auditory cortex into core areas (AI, R, and RT), which were surrounded by the lateral (RTL, AL, ML, and CL) and medial (RTM, RM, CM) belt areas. These areas were located in the ventral bank and the lip of the lateral sulcus. They also distinguished parabelt areas (RPB and CPB) adjacent to the lateral belt areas, approximately in the caudal and mid-portion of the superior temporal gyrus. Area STGr was recognized in the rostral part of the superior temporal gyrus, including the temporal pole. In the current study, we did not use the designations RPB and CPB. Instead, we recognized rostral and caudal subdivisions of the superior temporal gyrus (areas STGr and STGc, respectively). Our area STGr corresponds approximately to STGr and rostral part of RPB, while STGc corresponds to caudal part of RPB and CPB of Hackett et al. (1998). Core and belt areas are distinguished by a strong to moderate concentration of parvalbumin stained fibers and terminal plexus in the middle cortical layers (see photomicrographs in both the horizontal and coronal series). This pattern of labeling is essentially the same as that described by Hackett et al. (1998; see also Jones et al., 1995). The core and belt regions are also characterized by sparse to moderate concentration of SMI-32 labeled pyramidal neurons and their processes (dendrites) in layer III and V/VI. The sparse concentration of SMI-32 labeled neurons is mostly observed in the rostrotemporal (RT) areas of the auditory cortex (Figures 75–78). It should be noted that the area AI can be distinguished from areas R and RT based on the differential laminar distribution of SMI-32-immunoreactive pyramidal neurons. In “AI” these pyramidal neurons are distributed in 3 separate layers (III, V and VI) while in “R and RT” SMI-32-stained neurons are mainly found in layer III (compare Figures 86 and 91).
Cytoarchitectonic and Chemoarchitectonic Organization of Cortical and Subcortical areas
We also found dense parvalbumin stained fibers and terminals in the ventral bank of the lateral sulcus at the temporal pole region. This region is directly continuous with the parvalbumin-rich auditory core area RT, and it appears to represent the rostral end of this strip. We have termed this area RTp (“p” polar; Saleem et al., 2006). We distinguished RT from RTp in the coronal series, but in the horizontal series, these areas were difficult to distinguish, and we labeled only RT.
Superior temporal sulcus (STS) The terminology used for the regions within the dorsal and ventral banks, and the fundus (floor) of the STS was based on the study by Seltzer and Pandya (1978), except for the caudal part of the STS. They delineated areas TPO and TAa in the dorsal bank; areas TEa and TEm in the ventral bank; area IPa in the fundus, and area PGa at the dorsal bank/fundus junction of the STS. Multiple visual areas have been distinguished in the caudal part of the STS based on the anatomical and electrophysiological methods (Zeki, 1974; Van Essen et al., 1981; Desimone and Ungerleider, 1986; Boussaoud et al., 1990). These are areas MT, MST, FST, and V4t. Areas V4 and TEO were also distinguished in the ventral bank of the STS (Desimone and Ungerleider, 1986) that extended laterally into the prelunate and inferotemporal gyri. We delineated these areas in the current study based on the differential distribution of parvalbumin staining in the middle cortical layers, and SMI-32 labeled pyramidal neurons and their processes in layers III and V/VI (see the photomicrographs in chapters 3 and 4), similar to that described by Hof and Morrison (1995), Cusick et al. (1995) and Lewis and Van Essen (2000). It should be noted that the architectonic distinction between TEa and TEm in the ventral bank of the STS was not clear in most of our histology sections. Therefore, we did not indicate the border between these areas in our horizontal and coronal maps.
Insula The insular cortex (Jones and Burton, 1976; Mesulam and Mufson, 1982) is divided into 3 subregions: agranular (Ia), dysgranular (Id) and granular (Ig) insula. The agranular insula lacks layer IV in the Nissl stained section, and has weak parvalbumin and SMI-32 staining (see the photomicrographs). In contrast, the granular insula has prominent layer IV coupled with strong parvalbumin staining in layer IV, and moderate SMI-32 labeling in layer III (see Chapters 3 and 4). The dysgranular insula has weak layer IV and weak to moderate staining in sections stained for parvalbumin and SMI-32. See also Carmichael and Price (1994) for the subdivisions within agranular insula in the posterior orbital prefrontal cortex (see Figure 2.2).
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PREFRONTAL CORTEX
Orbitomedial prefrontal cortex (OMPFC) In the OMPFC, the architectonic maps of Carmichael and Price (1994) were used (Figure 2.2). See also Kondo et al. (2003, 2005) for the complimentary networks within OMPFC (“orbital” and “medial” networks), and the connections between these networks and the temporal cortex.
Fig. 2.2 Architectonic subdivision of the orbital (right) and medial (left) prefrontal cortex (OMPFC) in the macaque monkey. An imaginary cut line is made on the temporal pole (dashed line, right) to expose the caudal orbital surface (areas Ial, Iai, and Iapm).
Dorsolateral and ventrolateral prefrontal cortex In the current study, the overall extent and architectonic structure of areas 8, 8B, 9, 10, 12, 44, 45, and 46 in the dorsolateral and ventrolateral prefrontal cortex are closely matched with that of Petrides and his colleagues (Petrides and Pandya, 1999, 2002; Petrides, 2005). We also distinguished subdivisions within areas 8B, 9, 10, 12, and 46 based on the architectonic analysis, and other studies. The approximate correspondence between the prefrontal areas shown in the current study and other studies are indicated in Table 2.1.
Cytoarchitectonic and Chemoarchitectonic Organization of Cortical and Subcortical areas
Our subdivisions of areas 10 (10m and 10o), and 12 (12r, 12m, and 12l) are based on Carmichael and Price (1994; see Figure 2.2 opposite page), and subdivisions of area 8B (8Bd and 8Bm) and area 9 (9d and 9m) are similar to that of Preuss and Goldman-Rakic (1991a). Area 8B is also extended into the dorsal bank of the upper limb of arcuate sulcus, and we delineated this subdivision as area 8Bs (“s” stands for sulcus).
Table 2.1 Current study
Petrides (2005)
Walker (1940)
8A 8Bd, 8Bm, and 8Bs 9d and 9m 10m and 10o 12r, 12m, and 12l 44 45 46d and 46v
8Ad and 8Av 8B 9 10 47/12 44 45A and 45B 46, 9/46d, and 9/46v
8A and part of 45 8B 9 10 12 — 45 and 46 46
PREMOTOR AND MOTOR CORTEX (AGR ANUL AR FRONTAL CORTEX) We used the subdivisions of the agranular frontal cortex in our horizontal and coronal sections similar to that shown by Matelli et al. (1985, 1991), Luppino and Rizzolatti (2000), Geyer et al. (2000), and Rizzolatti and Luppino (2001). These subdivisions were based on the architectonic and functional properties of various sectors of the motor cortex (Figure 2.3A). For comparison, we also include in our maps the cytoarchitectonic and myeloarchitectonic subdivisions of premotor cortex shown by Barbas and Pandya (1987), and functional subdivisions illustrated by Luppino and Rizzolatti (2000; see also Tanji et al., 1996; Wise, 1997) (Figure 2.3B, C; Table 2.2). For example, we illustrated the premotor areas in our maps as follows (see Table 2.2 next page): F1 (4) F2 (6DR/6DC) F3 (SMA) F4 (4C/6Va/6Vb) F5 (6Va/6Vb) F6 (PreSMA) F7 (6DR)
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Table 2.2 Matelli et al., 1985; 1991 Luppino and Rizzolatti, 2000
Barbas and Pandya, 1987
Modern functional subdivision
F1 F2 F3 F4 F5 F6 F7
4 6DR/6DC 6DC (medial part)/MII 4C/6Va/6Vb 6Va/6Vb MII 6DR
M1 (Primary motor cortex) PMdc (dorsal premotor cortex, caudal) SMA (supplementary motor area) PMv (ventral premotor cortex) PMv (ventral premotor cortex) PreSMA (presupplementary motor area) PMdr (dorsal premotor cortex, rostral)
Fig. 2.3 Architectonic and functional subdivisions of the agranular frontal cortex (motor and premotor cortex).
Cytoarchitectonic and Chemoarchitectonic Organization of Cortical and Subcortical areas
CINGUL ATE AND RETROSPLENIAL CORTEX The architectonic subdivisions of the cingulate (areas 23a, b, c and 24a, b, c) and retrosplenial cortex (areas 29 and 30) follow Vogt et al. (1987), as slightly modified recently by Vogt et al. (2005) on the subdivisions of cingulate cortex. We distinguish these subregions, including few other subregions (24a’, b’, and c’ and v23a, b) in our maps based on Vogt et al. (2005).
POSTCENTR AL GYRUS, PARIETO-OCCIPITAL CORTEX, AND NEARBY CORTEX The terminology and architectonic criteria used in this study for the postcentral gyrus, parietooccipital cortex and adjacent cortical areas (1, 2, 3a/b, 5, 7a, 7b, 7m, LIPd/v, VIP, AIP, MIP, PIP, LOP, PO, V3, V3A, including areas V1, V2, and V4) were based on several previous studies (Brodmann, 1909; Jones et al., 1978; Pons et al., 1985; Colby et al., 1988; Andersen et al., 1990; Preuss and Goldman-Rakic, 1991b; Hof and Morrison, 1995; Lewis and Van Essen, 2000; see also Zeki and Sandeman, 1976; Zeki, 1978, 1980; Gattass et al., 1988).
Parietal cortex (lateral and media part) Areas 7a, 7b, and 7m These areas overlap with PF, PFG, PG, Opt, and PGm of Pandya and Seltzer (1982). In the SMI-32 stained sections, areas 7a and 7b are characterized by sparse to moderate distribution of lightly stained pyramidal neurons in layers III and V (Chapter 4, Figures 100, 101). Area 7a is clearly distinguished from adjacent area MST in the dorsal bank and fundus of the caudal superior temporal sulcus that shows denser band of SMI-32 labeled pyramidal neurons in layers III and V (Figures 100, 101). Area 7m contains more SMI-32 labeled pyramidal neurons than in areas 7a and 7b.
Area 5 This area is located in the lateral and medial part of the parietal cortex, including the medial bank of the intraparietal sulcus that overlaps with areas PE, PEa, and PEc of Pandya and Seltzer (1982). Area 5 is characterized by the dense concentration of SMI-32 positive pyramidal neurons in layers III and V.
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Parietal cortex (intraparietal sulcus) Areas LIPd/v and VIP Area LIP has been divided into dorsal and ventral subregions based on the myeloarchitectonic analysis (Blatt et al., 1990). In the SMI-32 stained sections, the area LIPd is characterized by sparse to moderate distribution of pyramidal neurons in layers III and V, while area LIPv is distinguished by dense concentration of pyramidal neurons in these layers. Our observation is consistent with Lewis and Van Essen (2000). We did not distinguish chemoarchitectonic subdivisions within area VIP in the current study.
OTHER CORTICAL AREAS We identified few other areas in the rostrocaudal extent of the lateral sulcus, in addition to auditory cortex and insular cortex. These areas are known or thought to be involved in somatosensory-related and gustatory functions. We used the criteria described by Jones and Burton (1976), and Friedman et al. (1986) for areas SII (secondary somatosensory area), Pi (parainsular area), and Ri (retroinsula); and those of Preuss and Goldman-Rakic (1991b) for areas 7op (parietal operculum), Tpt (temporo-parietal), and PrCO (precentral opercular area). We found strong parvalbumin positive fiber and terminal plexus in gustatory cortex (area G), and this pattern of labeling is essentially the same as that described by Carmichael and Price (1994). Two subdivisions can be distinguished with area SII based on the parvalbumin and SMI-32 staining. One subdivision located deep inside the lateral sulcus, close to granular insula (Ig) contains a dense concentration of parvalbumin stained fibers and terminals, and moderate to dense distribution of SMI-32 labeled pyramidal neurons. The other subdivision, lateral to the first subregion contains sparse to moderate distribution of parvalbumin stained fibers and terminals, and SMI-32 labeled pyramidal neurons (see Chapters 3 and 4).
HIPPOCAMPUS The terminology and architectonic criteria used for subdividing the hippocampal formation were based on the descriptions by Lorente de No (1934) and Rosene and Van Hoesen (1987).
Cytoarchitectonic and Chemoarchitectonic Organization of Cortical and Subcortical areas
SUBCORTICAL STRUCTURES
Amygdala The nuclear subdivisions of the amygdaloid complex follow Price et al. (1987), as slightly modified by Amaral and Bassett (1989) and Pitkanen and Amaral (1998). In brief, the deep nuclei of amygdala are divided into lateral (L), basal (B), accessory basal (AB), and paralaminar (PL) nuclei. The lateral nucleus is further subdivided into dorsal, dorsal intermediate and ventral subdivisions (Pitkanen and Amaral, 1998). Based on the parvalbumin staining, we did not recognize the dorsal intermediate subdivision of the lateral nucleus, but distinguished two other subdivisions of lateral nucleus in our maps. The basal nucleus is subdivided into magnocellular, intermediate, and parvicellular subdivisions (Bmc, Bi, and Bpc, respectively), and the accessory basal nucleus is subdivided into magnocellular and parvicellular subdivisions (ABmc and ABpc, respectively). The other subdivisions of the amygdala include the cortical nuclei, and anterior amygdaloid area, the central nucleus, the intercalated nuclei, and the amygdalohippocampal area. We found differential distribution of parvalbumin stained fibers and terminal plexus, and neurons in these subregions similar to that described by Pitkanen and Amaral (1993a) (see Chapters 3 and 4).
Thalamus and Hypothalamus We adapted the terminology and cytoarchitectonic subdivisions of the thalamic nuclei similar to that of Olszewski (1952). The parvalbumin, calbindin, and calretinin staining are also very useful in delineating different thalamic nuclei, as illustrated in the current study (see Chapters 3 and 4; calbindin and calretinin sections are not shown). The staining pattern is consistent with that shown by Jones and his colleagues (Jones and Hendry, 1989; Jones, 1998), although the terminology used in the latter studies is slightly different from that of Olszewski (1952). The hypothalamus consists of many subnuclei that are connected with the specific subregions of the orbitomedial prefrontal cortex (Ongur et al., 1998). The hypothalamic nuclei are distinguished in Nissl and SMI-32 stained sections but less so in parvalbumin stained sections (see the photomicrographs).
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Chapter 4 Coronal Series
MRI, PHOTOMICROGR APHS AND DR AWINGS IN CO RONAL PL ANE
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Chapter 5 Selected Cortical and Subcortical Areas in three Different MRI Planes
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Selected Cortical and Subcortical Areas in three Different MRI Planes
SELECTED CORTICAL AREAS
Temporal cortex Area TEad: Figure 124 Area TEav: Figure 125 Area TEO: Figure 126 AI (core region of the auditory cortex): Figure 127 R (core region of the auditory cortex): Figure 128 Entorhinal cortex (EC or area 28): Figure 129 Parahippocampal cortex (area TF): Figure 130 Perirhinal cortex (area 36): Figure 131
Prefrontal cortex Area 11m: Figure 132 Area 13l: Figure 133 Area 46d: Figure 134 Frontal eye field (area 8A): Figure 135 Gustatory cortex (area G): Figure 136
Somatosensory and Parietal cortex Area 3a/b: Figure 137 Area LIP: Figure 138 Area VIP: Figure 139 Area 7a/b: Figure 140 Area 5: Figure 141
Occipital cortex, and nearby cortex (including caudal STS) Area V1 (primary visual cortex): Figure 142 Area V4: Figure 143 Area MT: Figure 144
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Cingulate cortex Area 24b: Figure 145 Area 24c: Figure 146
SELECTED SUBCORTICAL AREAS Amygdala: Figure 147 Caudate nucleus: Figure 148 Putamen: Figure 149 Globus pallidus (external segment – GPe): Figure 150 Thalamus (VPL or VPM): Figure 151 Pulvinar (medial part – PM): Figure 152 Lateral geniculate nucleus (LGN): Figure 153 Medial geniculate nucleus (MGN): Figure 154 Superior colliculus: Figure 155 Inferior colliculus: Figure 156
Selected Cortical and Subcortical Areas in three Different MRI Planes
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Index of Abbreviations
Abbreviations are indicated in alphabetical order. Each abbreviation is followed by the name of that structure and the number of the figures on which the abbreviation appears.
Abbreviation
Structure
Figures
1-2 3a/b 3v 4 4C 5 6DC 6DR 6Va 6Vb 7a 7b 7m 7op 7t 8A 8Bd 8Bm 8Bs 9d 9m 10m 10o 11l 11m 12l 12m
somatosensory areas 1 and 2 somatosensory areas 3a and 3b third ventricle primary motor cortex premotor area 4C somatosensory area 5 (complex) dorsal premotor area 6, caudal subdivision dorsal premotor area 6, rostral subdivision ventral premotor area ventral premotor area visual area 7a visual area 7b area 7m in the medial parietal cortex area 7op (parietal operculum) transitional area 7 near the lip of ips area 8A area 8B, dorsal subdivision area 8B, medial subdivision area 8B in the arcuate sulcus (“s” stands for sulcus) area 9, dorsal subdivision area 9, medial subdivision area 10m area 10o area 11l area 11m area 12l area 12m
17–47, 74–96 18–45, 75–91, 137 78–95 27–46, 77–89 17–33, 72–77 35–47, 87–107, 141 32–45, 67–79 32–45, 62–79 17–33, 67–77 17–33, 67–77 33–45, 94–106, 140 28–40, 87–93, 140 29–43, 96–106 25–35, 88–97 33–37 27–34, 63–73, 135 32–35, 59–64 31–34, 59–61 30–32, 63–71 26–32, 52–59 26–34, 52–58 17–26, 48–66 17–22, 48–51 21–25, 51–60 18–22, 51–60, 132 15–23, 58–66 20–25, 56–60
317
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Index of Abbreviations
Abbreviation
Structure
Figures
12o 12r 13a 13b 13l 13m 14c 14r 23a 23b 23c v23a v23b 24a 24a’ 24b 24b’ 24c 24c’ 25 29 30 31 32 35 36c 36p
area 12o area 12r area 13a area 13b area 13l area 13m area 14c area 14r area 23a in posterior cingulate cortex area 23b in posterior cingulate cortex area 23c in posterior cingulate cortex area v23a in posterior cingulate cortex area v23b in posterior cingulate cortex area 24a in anterior cingulate cortex area 24a’ in anterior cingulate cortex area 24b in anterior cingulate cortex area 24b’ in anterior cingulate cortex area 24c in anterior cingulate cortex area 24c’ in anterior cingulate cortex area 25 area 29 (retrosplenial cortex) area 30 (retrosplenial cortex) area 31 in the posterior cingulate gyrus area 32 area 35 of the perirhinal cortex area 36 of the perirhinal cortex, caudal subregion area 36 of the perirhinal cortex, temporal-polar subregion area 36 of the perirhinal cortex, rostral subregion area 44 area 45 area 46, dorsal subdivision area 46, ventral subdivision
14–19, 61–67 22–25, 51–57 15–16, 66–68 17–20, 55–68 19–23, 61–67, 133 17–23, 61–68 16–18, 63–70 16–20, 52–63 31, 85–97 31–34, 85–97 32–40, 85–96 29–30, 97 22–30, 97–101 22–30, 63–71 31, 72–84 24–34, 60–71, 145 32–34, 72–84 24–33, 55–71, 146 33–34, 72–84 17–22, 67–71 25–30, 85–97 25–30, 85–97 31–39, 94–99 22–26, 55–65 3–4, 75–87 1–3, 82–88, 131 1–2, 75–76
anterior amygdaloid area accessory basal nucleus of amygdala accessory basal nucleus of amygdala, magnocellular
77–79 8–11, 82 12, 78–81
36r 44 45 46d 46v
1–2, 76–82 21–26, 67–71 20–28, 59–72 24–31, 50–69, 134 23–30, 50–69
A AAA AB ABmc
Index of Abbreviations
Abbreviation
Structure
Figures
ABpc AC AD AHA AHA AI AIP AL AM amts amy AON AONd AONl AONm apos aq Arh asl asu AV
accessory basal nucleus of amygdala, parvicellular anterior commissure anterior dorsal nucleus amygdalohippocampal area anterior hypothalamic areas auditory area I, core region of the auditory cortex anterior intraparietal area anterior lateral, belt region of the auditory cortex anterior medial nucleus anterior middle temporal sulcus amygdala anterior olfactory nucleus anterior olfactory nucleus, dorsal division anterior olfactory nucleus, lateral division anterior olfactory nucleus, medial division anterior parieto-occipital sulcus aqueduct arcuate hypothalamic nucleus arcuate sulcus lower limb arcuate sulcus upper limb anterior ventral nucleus
76–81 77–78 26–27, 82–86 6–8, 81–87 78 26–31, 89–94, 127 31–40, 87–90 16–26, 79–88 25, 80–83 1–4, 78–87 6–7, 147 14–16, 72 65–71 65–71 65–71 24–35 91–98 80–82 17–30, 68–73 31–34, 63–73 26–27, 80–85
basal nucleus of amygdala basal nucleus of amygdala, intermediate subdivision basal nucleus of amygdala, magnocellular subdivision basal nucleus of amygdala, parvicellular subdivision brachium of superior colliculus
8–10, 147 77–81, 147
93–95
CA1 subfield of hippocampus CA2 subfield of hippocampus CA3 subfield of hippocampus CA4 subfield of hippocampus capsule of the anterior nuclei calcarine sulcus
7–18, 82–98 7–19, 82–97 10–17, 82–98 8–16, 83–97 25–26, 83 25–39, 98–122
B B Bi Bmc Bpc bsc
11–12, 79–81, 147 77–81, 147
C CA1 CA2 CA3 CA4 can cas
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Abbreviation
Structure
Figures
cb CC cd cdc CE cif cim cis CL cl cla clc CM cnMD COa COp CP cs csl
cerebellum corpus callosum caudate nucleus central dorsocellular nucleus central nucleus of amygdala central inferior nucleus central intermediate nucleus cingulate sulcus caudal lateral, belt region of the auditory cortex central lateral nucleus claustrum central latocellular nucleus caudomedial, belt region of the auditory cortex centromedian nucleus anterior cortical nucleus posterior cortical nucleus cerebral peduncle central sulcus central superior lateral nucleus
6–24, 99–116 22–30, 62–96 12–29, 65–98, 148 22–25, 83 13, 81–82 85–87 23–24, 84–88 23–41, 51–100 30–31, 92–95 25–26, 87–91 8–24, 65–89 22, 81–82 22–31, 89–95 21–24, 87–91 13–14, 77–80 12 83–91 22–46, 81–91 86–89
dentate gyrus dorsolateral periaqueductal gray dorsomedial hypothalamic nucleus dorsomedial periaqueductal gray dorsal prelunate area dorsal raphe
8–19, 84–97 93–96 80–82 93–96 35–43, 103–108 94–96
entorhinal cortex, caudal division entorhinal cortex, caudal limiting division entorhinal cortex, intermediate division entorhinal cortex, lateral division (caudal part) entorhinal cortex, lateral division (rostral part) entorhinal cortex, olfactory division entorhinal cortex, rostral division
3–10, 83–87, 129 86–89 4–7, 80–82 80–82 76–79 3, 76–81 3–5, 76–79
fornix agranular frontal area F1
78–96 27–46, 77–89
D DG dlPAG DMH dmPAG DP DR
E EC ECL EI ELc ELr EO ER
F f F1
Index of Abbreviations
Abbreviation
Structure
Figures
F2 F3 F4 F5 F6 F7 fr FST
agranular frontal area F2 agranular frontal area F3 agranular frontal area F4 agranular frontal area F5 agranular frontal area F6 agranular frontal area F7 fasciculus retroflexus floor of superior temporal area
32–45, 67–79 31–43, 67–80 17–33, 72–77 17–32, 67–75 31–39, 62–66 35–39, 62–66 88–90 18–28, 94–99
gustatory cortex globus pallidus, external segment globus pallidus, internal segment
18–23, 71–75 16–21, 77–88, 150 16–19, 79–87
hippocampus hippocampal fissure habenular nucleus lateral habenular nucleus medial habenular nucleus
5–6 83–86 24–25 90–91 89–91
intercalated nucleus agranular insula intermediate agranular insula area lateral agranular insula area medial agranular insula area posterolateral agranular insula area posteromedial agranular insula area inferior colliculus internal capsule dysgranular insula granular insula third cranial nerve nuclei (oculomotor) oculomotor nerve (cranial nerve) inferior occipital sulcus area IPa (sts fundus) intraparietal sulcus fourth cranial nerve nucleus (trochlear)
13, 77–79 13–15, 76–78 13–20, 67–70 13–17, 70–75 69 14–16, 72–74 13–16, 70–74 98–99, 156 77–87 15–23, 75–87 21–26, 76–88 91–95 88–90 16–26, 97–117 8–18, 22–94 31–45, 84–108 96
G G GPe GPi
H HC hf Hi Hl Hm
I I Ia Iai Ial Iam Iapl Iapm IC ic Id Ig III IIIN ios IPa ips IV
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Abbreviation
Structure
Figures
lateral nucleus of amygdala lateral dorsal nucleus lateral nucleus of amygdala, dorsal subdivision lateral geniculate nucleus lateral hypothalamic area lateral intraparietal area lateral intraparietal area, dorsal subdivision lateral intraparietal area, ventral subdivision external medullary lamina lateral occipital parietal area lateral orbital sulcus lateral posterior nucleus lateral periaqueductal gray lateral sulcus lateral septum, dorsal part lateral septum, intermediate part lateral septum, ventral part lunate sulcus lateral nucleus of amygdala, ventral subdivision lateral ventricle
8–13 85–90 77–81 13–19, 87–93, 153 80–82 34–43, 91–104 91–103, 138 91–103 20–26, 82–95 35–40, 104–108 23, 55–65 22–24, 88–91 93–96 12–34, 74–100 73–77 73–77 73–77 23–44, 102–112 77–81 65–100
middle cerebellar peduncle medial dorsal nucleus, densocellular division mediodorsal nucleus, magnocellular division mediodorsal nucleus, multiform division mediodorsal nucleus, parvicellular division medial nucleus of amygdala medial geniculate nucleus medial intraparietal area medial lemniscus middle lateral, belt region of the auditory cortex molecular layer medial longitudinal fasciculus mammillary nucleus medial orbital sulcus medial preoptic area median raphe medial septum
92–99 92 22–26, 84–88 82–89 21–25, 84–91 12–13, 81–82 16–21, 91–93, 154 31–40, 98–107 94–96 26–29, 89–91 83–86 91–96 83–85 23, 50–65 76–78 94–96 73–77
L L LD Ld LGN LHA LIP LIPd LIPv Lme LOP los LP lPAG ls lsd lsi lsv lus Lv lv
M mcp MDdc MDmc MDmf MDpc ME MGN MIP ml ML ml mlf MN mos MPOA MR ms
Index of Abbreviations
Abbreviation
Structure
Figures
MST MT MTT
medial superior temporal area middle temporal area mammillo thalamic tract
29–37, 97–102 27–35, 98–102, 144 82
nucleus accumbens nucleus accumbens, core nucleus accumbens, shell nucleus basalis of Meynert nucleus of the lateral olfactory tract
14–17, 69–76 74–76 74–76 77–80 11, 77–80
optic chiasm olfactory tubercle optic tract occipitotemporal sulcus
78–79 14–17, 72–76 13–15, 80–87 4–18, 88–107
pulvinar paraventricular nucleus periamygdaloid cortex periamygdaloid cortex 2 periamygdaloid cortex 3 periamygdaloid cortex o periamygdaloid cortex, sulcal portion periaqueductal gray parasubiculum paracentral nucleus parafascicular nucleus area PGa inferior pulvinar parainsular area posterior intraparietal area piriform cortex lateral pulvinar paralaminar nucleus in amygdala medial pulvinar polymorphic layer posterior middle temporal sulcus
97 23–26, 81–88 5–10 76–77 78–81 75 76–81 91–98 8–18, 86–89 20–21, 81–86 20–21, 88–91 9–29, 76–96 16–19, 92–94 11–17, 76–82 31–34, 103–105 11–13, 72–76 18–27, 92–96 77–81 23–26, 92–96, 152 84–85 15–16, 97–101
N NA NAc NAsh NBM NLOT
O oc OT ot ots
P P Pa PAC PAC2 PAC3 PACo PACs PAG paraS Pcn Pf PGa PI Pi PIP Pir PL PL PM pm pmts
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Abbreviation
Structure
Figures
PN PO pos PrCO preS PreSMA proS ps pt pu pulo PVN
pontine nuclei parieto-occipital area parieto-occipital sulcus precentral opercular area presubiculum presupplementary motor area prosubiculum principal sulcus parataenial nucleus putamen pulvinar oralis nucleus paraventricular hypothalamic nucleus
92–98 30–41, 105–110 28–44, 100–116 13–16, 68–74 7–19, 83–97 31–39, 62–66 7–18, 82–98 23–30, 48–69 81–87 11–25, 68–90, 149 89–91 77–82
reticular nucleus rostral, core region of the auditory cortex reunions nucleus retroinsula rostromedial, belt region of the auditory cortex red nucleus rhinal sulcus rostrotemporal, core region of the auditory cortex lateral rostrotemporal, belt region of the auditory cortex medial rostrotemporal, belt region of the auditory cortex rostrotemporal (“p” refers to polar)
17–27, 81–95 14–25, 79–88, 128 20–21, 81–89 88–91 14–25, 79–88 87–89 3–11, 75–88 11–15, 76–78 12–16, 76–78
spur of the arcuate sulcus superior colliculus suprachiasmatic nucleus superior cerebellar peduncle substantia innominata secondary somatosensory area (S2) stria medullaris supplementary motor area substantia nigra substantia nigra pars compacta
73–77 18–22, 92–99 78–79 95–96 13 17–25, 75–88 27, 80–89 31–43, 67–80 90–91 84–89
R r R Re Ri RM RN rs RT RTL RTM RTp
12–13, 76–78 73–75
S sas SC SCN scp SI SII Sm SMA SN SNc
Index of Abbreviations
Abbreviation
Structure
Figures
SNr SON spcd spt STGc STGr STN sts Sub
substantia nigra pars reticulate supraoptic nucleus superior precentral dimple septum caudal superior temporal gyrus rostral superior temporal gyrus subthalamic nucleus superior temporal sulcus subiculum
84–89 78–79 76–80 72 18–29, 83–93 7–17, 74–82 16–18, 83–88 2–44, 72–106 7–21, 82–98
area TAa (sts dorsal bank) area TEa (sts ventral bank) dorsal subregion of anterior TE ventral subregion of anterior TE area TEm (sts ventral bank) area TEO dorsal subregion of posterior TE ventral subregion of posterior TE area TF of the parahippocampal cortex area TFO of the parahippocampal cortex agranular part of the temporal pole dorsal temporal pole dysgranular part of the dorsal temporal pole granular part of the dorsal temporal pole sts part of the temporal pole ventral temporal pole ventral dysgranular part of the temporal pole ventral granular part of the temporal pole area TH of the parahippocampal cortex habenular interpeduncular tract area TPO (sts dorsal bank) temporo-parietal area ventral tenia tectum
7–29, 75–93 4–18, 75–94 1–10, 76–87, 124 1–5, 74–87, 125 4–19, 75–92 9–28, 92–101, 126 6–18, 88–96 3–12, 88–96 4–12, 88–92, 130 11–16, 93–97 5–10, 72–75 70 6–11, 71–75 6–11, 71–73 2–7, 71–74 70 1–5, 71–74 1–2, 71–73 5–12, 89–92 88–90 7–32, 75–99 29–35, 93–99 69–70
ventricle visual area 1 (primary visual cortex) visual area 2
5–29 15–44, 101–123, 142 15–42, 96–120
T TAa TEa TEad TEav TEm TEO TEpd TEpv TF TFO TGa TGd TGdd TGdg TGsts TGv TGvd TGvg TH THI TPO Tpt TTv
V V V1 V2
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Abbreviation
Structure
Figures
v23a v23b V3A V3d V3v V4 V4t V4v VA VAmc vdb VIP VLc VLm VLo vlPAG VLps VMH VP VPI VPLc VPLo VPM VPMpc
area v23a in posterior cingulate cortex area v23b in posterior cingulate cortex visual area V3A visual area 3, dorsal part visual area 3, ventral part visual area 4 (dorsal part) V4 transitional area visual area 4, ventral part ventral anterior nucleus ventral anterior nucleus, magnocellular division nucleus of vertical limb of diagonal band ventral intraparietal area ventral lateral caudal nucleus ventral lateral medial nucleus ventral lateral oral nucleus ventrolateral periaqueductal gray ventral lateral postrema nucleus ventromedial hypothalamic nucleus ventral pallidum ventral posterior inferior nucleus ventral posterior lateral caudal nucleus ventral posterior lateral oral nucleus ventral posterior medial nucleus ventral posterior medial nucleus, parvicellular division
29–30, 97 22–30, 97–101 29–37, 104–108 25–38, 103–112 13–24, 96–111 24–43, 96–108, 143 28–36, 98–101 12–18, 96–106 20–25, 80–83 20–22, 81–83 73–76 30–35, 89–104 23–27, 83–87 83 21–22, 83–87 93–96 25–27, 89–91 80–82 77–78 18–19, 84–90, 139 18–24, 89–91, 151 20–21, 88, 151 20–24, 87–90, 151 85–89
zona incerta
83–87
Z zic
