**2. Printed stereotactic atlases**

The history of human brain atlases begins in 1947, when the surgeons noticed that it was possible to adapt mechanical devices used in animals to navigate precisely the human brain. Therefore, it was mandatory to generate maps with coordinates of the uncertain territory in order to plan the best routes to avoid even minimal collateral damage and to focus the targets with high precision. Printed stereotactic atlases were considered to supply blueprints to neurosurgeons for intracerebral navigation.

#### **2.1 Stereoencephalotomy ( thalamotomy and related procedures), part I: methods and stereotaxic atlas of the human brain (Spiegel & Wycsis, 1952)**

The first stereotactic human brain atlas was entitled *Stereoencephalotomy.* It was developed to solve the lack of accuracy of referenced systems based on cranial references and to allow the stereotaxic surgery to be performed in humans. It should be noted that since 1973 the term "stereotactic" is used for surgery in humans, whereas "stereotaxic" is used exclusively for neurosurgery in animals.

In 1947, Spiegel and Wycsis described the first human stereotactic instrument used routinely in subcortical surgery. It is based on the use of intraoperative radiographs, allowing the visualization of cerebral references. After the emergence of the technique of interventricular instillation of air (ventriculography), anatomical structures including the foramen of Monro (FM) and the calcification of the pineal gland could be used for localization of intracranial targets. With the advent of new contrast media it was possible to use new landmarks in the brain, such as the anterior commissure (AC), the posterior commissure (PC) and the intercommissural line (ICL).These new references are much more reliable than the former ones, as verified by Talairach (Talairach et al., 1957).With these new reference points at hand, the indication for neurosurgical interventions could be extended, since new targets appear within the coordinates of the stereotactic apparatus. Spiegel and Wycsis' (1952) atlas consisted of photographs of a series of coronal brain, sliced at regular intervals in relation to the posterior commissure and the midline, with a reference graph located at the edges of each section. Using this parameter, the surgeon was able to assess distances in millimeters in depth and laterality of subcortical targets with a known distance of the posterior commissure. Coordinates for many targets were derived from this concept, and neuroablative procedures became reality. These studies were the basic guidelines for targets used in pallidotomy for treatment of abnormal movements and mesencephalotomy for treatment of refractory chronic pain, published in 1950 by Spiegel and Wycis.

Prefrontal lobotomies were frequently performed in the days before the emergence of appropriate psychotropic medication. At the time of the development of stereotactic surgery, Spiegel hoped to refine this procedure to avoid the unwanted complications and deficits frequently associated with these procedures. With this in mind, the first use of the stereotactic apparatus was the coagulation of the dorsal median nucleus of the thalamus in patients with severe psychiatric disorders, seeking a less traumatic intervention than a lobotomy. Around the same time the use of stereotaxy for interruption of pain pathways, surgical treatment of abnormal movements, and drainage of fluid from pathological cavities, - , for instance, cystic tumors -, had also been proposed.

Initially, their reference coordinate system was the Cp-PO line (posterior commissure-pons line). This coordinate system was not simple and was not widely used. In their next work in 1962, Spiegel and Wycsis (Spiegel & Wycsis, 1962) assumed the intercommissural line as

The history of human brain atlases begins in 1947, when the surgeons noticed that it was possible to adapt mechanical devices used in animals to navigate precisely the human brain. Therefore, it was mandatory to generate maps with coordinates of the uncertain territory in order to plan the best routes to avoid even minimal collateral damage and to focus the targets with high precision. Printed stereotactic atlases were considered to supply blueprints

**2.1 Stereoencephalotomy ( thalamotomy and related procedures), part I: methods and** 

The first stereotactic human brain atlas was entitled *Stereoencephalotomy.* It was developed to solve the lack of accuracy of referenced systems based on cranial references and to allow the stereotaxic surgery to be performed in humans. It should be noted that since 1973 the term "stereotactic" is used for surgery in humans, whereas "stereotaxic" is used exclusively for

In 1947, Spiegel and Wycsis described the first human stereotactic instrument used routinely in subcortical surgery. It is based on the use of intraoperative radiographs, allowing the visualization of cerebral references. After the emergence of the technique of interventricular instillation of air (ventriculography), anatomical structures including the foramen of Monro (FM) and the calcification of the pineal gland could be used for localization of intracranial targets. With the advent of new contrast media it was possible to use new landmarks in the brain, such as the anterior commissure (AC), the posterior commissure (PC) and the intercommissural line (ICL).These new references are much more reliable than the former ones, as verified by Talairach (Talairach et al., 1957).With these new reference points at hand, the indication for neurosurgical interventions could be extended, since new targets appear within the coordinates of the stereotactic apparatus. Spiegel and Wycsis' (1952) atlas consisted of photographs of a series of coronal brain, sliced at regular intervals in relation to the posterior commissure and the midline, with a reference graph located at the edges of each section. Using this parameter, the surgeon was able to assess distances in millimeters in depth and laterality of subcortical targets with a known distance of the posterior commissure. Coordinates for many targets were derived from this concept, and neuroablative procedures became reality. These studies were the basic guidelines for targets used in pallidotomy for treatment of abnormal movements and mesencephalotomy for

treatment of refractory chronic pain, published in 1950 by Spiegel and Wycis.


Prefrontal lobotomies were frequently performed in the days before the emergence of appropriate psychotropic medication. At the time of the development of stereotactic surgery, Spiegel hoped to refine this procedure to avoid the unwanted complications and deficits frequently associated with these procedures. With this in mind, the first use of the stereotactic apparatus was the coagulation of the dorsal median nucleus of the thalamus in patients with severe psychiatric disorders, seeking a less traumatic intervention than a lobotomy. Around the same time the use of stereotaxy for interruption of pain pathways, surgical treatment of abnormal movements, and drainage of fluid from pathological cavities,

Initially, their reference coordinate system was the Cp-PO line (posterior commissure-pons line). This coordinate system was not simple and was not widely used. In their next work in 1962, Spiegel and Wycsis (Spiegel & Wycsis, 1962) assumed the intercommissural line as

**2. Printed stereotactic atlases** 

neurosurgery in animals.

to neurosurgeons for intracerebral navigation.

**stereotaxic atlas of the human brain (Spiegel & Wycsis, 1952)** 

standard reference system. The second part was a textbook and revised atlas updated from the first version. This atlas is currently out of print (Coffey, 2009).

*Main lines for spatial orientation are the mediosagittal Cp-Po line that connects the posterior commissure (Cp) with the bulbopontine sulcus. The h 0, a horizontal line (perpendicular to the Cp-Po-line) which crosses the Cp-Po-line at the level of the posterior commissure. The h1 line emerges in an acute angle at the crossing point of the Ch and the Cp and runs in a rostral direction. Cran.1 and cran.2 can be considered as ancillary lines. Cran.1 is perpendicular to h1 and forms an acute angle of 4° (-i) with the CP-PO-line, cran.2 like cran.1 leaves the Cp-Poline with an inclination of 4°, however, posterior to the Cp-Po-line (+i).* 

Fig. 1. First intracerebral reference system proposed by Spiegel & Wycsis in 1952.

#### **2.2 Atlas d'anatomie stéréotaxique: Repérage radiologique indirect des noyaux gris centraux des regions mésencéphalo-sous-optique et hypothalamique de l'homme (Talairach et al., 1957)**

The most important contribution of this publication is the use of AC and PC as reliable intracerebral stereotactic markers and their stable relationship to deep brain structures. From this work, came the concept of Talairach's space. The Talairach's space is a coordinate system based on AC and PC as pivotal landmarks. Using the distance between them and the orthogonal plans erected, it is possible to compare the location of brain structures in two different brains, independent from individual differences. Because of the individual variations in the three dimensions of human brains, the distances measured in millimeters are applicable only to one individual. This becomes increasingly true with greater distance from the basal lines. Talairach concluded that dimensions given in millimeters can apply only in a general population to the gray central nuclei, whose dimensional variations remain moderate. For this reason they presented later the three-dimensional proportional grid system ( Talairach & Tournoux, 1988).

Review of Printed and Electronic Stereotactic Atlases of the Human Brain 149

Since the beginning of stereotactic surgery, the main concern of the neurosurgeons was precision. The authors noted that all the previously presented atlases were based on very few specimens and even in the Schaltenbrand's atlas, despite the high total number of brains, only 7 out 111 were comprehensively studied. It was concluded that the stereotactic coordinates of subcortical nuclei were inadequately established, and that the variations would be so great that the procedures could not be reliably done with these

The authors thus presented a variability study, aiming to compensate for this lack of precision. They studied nineteen brains, and focused on thalamic nuclei variability. Besides the thalamus, the atlas includes adjacent basal ganglia, and medial temporal lobe structures. It consists of statistical analysis of the data, with probability tables and distances to important ventricular reference points such as the foramen of Monro (FM), PC and midcommisural plane. It was surely an important work to define variability patterns in pre-

They used the FM-PC line and the total thalamic length (TthL) as reference system instead of

**2.5 Variations and connections of the human thalamus (Van Buren & Borke,1972)**  These authors, together with Schaltenbrand and Talairach, published one of the most important atlases of that time. The atlas is the result of a meticulous work on this challenging structure of the human brain, and it comprises a detailed cytoarchitectonic description of the individual thalamic nuclei. The literature on the connections of each nucleus is also reviewed. A special section of the book is dedicated to present the primary lesions (intervention) and secondary thalamic degeneration in fifty-four patients due to stereotactic procedures. The authors care about questions such as correcting differential shrinkage with computational tools, and variation of the position of thalamic nuclei in

**2.6 The human somesthetic thalamus with maps for physiological target localization** 

In this work Tasker and Emmers have presented a detailed map for electrical stimulation of the thalamus, with 2mm interval stimulation. During stereotactic procedures performed with awake patients, the distribution of somesthetic responses elicited by electrical stimuli was projected into the templates and used to build a three-dimensional homunculus of the somesthetic thalamus. Tasker emphasized that physiologically defined anatomy rather than blind obedience to atlas coordinates should determine how to conduct functional

**2.7 Atlas for stereotaxy of the human brain with accompanying guide (Schaltenbrand** 

According to the preface of the second edition of their atlas the first one was "an exploration of a new field of clinical anatomy." The latest edition concentrates on clinically relevant issues. The authors emphasized the importance of the myelin sections and reduced the

the Talairach's space, although they have measured the AC-PC distance as well.

relation to midline, anterior, and posterior commissures.

**during stereotactic neurosurgery (Emmers & Tasker, 1975)** 

**2.4 A stereotaxic atlas of the human thalamus and adjacent structures: A variability** 

**study (Andrew et al.,1969)** 

coordinates.

CT/MRI era.

stereotactic operations.

**& Wahren,1977)** 

Several brains were studied, but the atlas was based on a single specimen. Talairach used his double-grid stereotactic instrument to create perforations in the craniocerebral specimen filled with air in the ventricular system. It was mounted on a stereotactic apparatus and metal probes were introduced. Radiographs were taken in profile and the brain was then removed and sectioned. The paths of the probes in the brain were used to establish the directional planes. Accurate coordinate measurements and profiles were derived for deep cerebral nuclei, subnuclei, and tracts.The stereotactically marked brains were cut in either parasagittal or frontal sections along Talairach's standard planes.

*The principal line for intracerebral orientation is the AC-PC line (also called the intercommissural line or ICL) that connects the superior edge of the anterior commissure with the inferior edge of the posterior commissure. Two perpendicular lines cut the AC-PC-line, the VAC, that runs through the center of the anterior commissure and the VPC, that runs through the center of the posterior commissure. Transformation of the ICL, VAC and VPC lines into planes yield the intercommissural plane (ICP), the anterior verticofrontal plane (VACp) and the posterior the verticofrontal plane, (VPCp) respectively.* 

Fig. 2. Talairach's stereotactic references.

The three-dimensional profiles of the thalamic nuclei and other structures were mapped on millimeter-ruled diagrams. The reference line was the intercommissural line. This line is widely used even to the present day. This atlas is currently out of print.

#### **2.3 Introduction to stereotaxis with an atlas of the human brain (Schaltenbrand & Bailey, 1959 )**

Schaltenbrand and Bailey published the most comprehensive and detailed stereotactic atlas. They studied 111 brains that were sectioned in the coronal, sagittal, and horizontal planes. Variability diagrams were based on seven specimens. Hassler and Wahren completed profound studies of nuclear structures in coronal and parasagittal sections. Akert, Bucy, Walker, Snider, and Hassler contributed with detailed chapters on the physiology and pathophysiology of deep structures of the human brain. Nearly forty years later, this atlas also contributes immensely to functional neurosurgeons, and it could be the most used atlas in the pre-CT era. Even today, the expanded 1977 edition with the most useful features of this work is used world-wide. Their coordinate system appears to be derived from Talairach's space, but shows slight differences.

Several brains were studied, but the atlas was based on a single specimen. Talairach used his double-grid stereotactic instrument to create perforations in the craniocerebral specimen filled with air in the ventricular system. It was mounted on a stereotactic apparatus and metal probes were introduced. Radiographs were taken in profile and the brain was then removed and sectioned. The paths of the probes in the brain were used to establish the directional planes. Accurate coordinate measurements and profiles were derived for deep cerebral nuclei, subnuclei, and tracts.The stereotactically marked brains were cut in either

*The principal line for intracerebral orientation is the AC-PC line (also called the intercommissural line or ICL) that connects the superior edge of the anterior commissure with the inferior edge of the posterior commissure. Two perpendicular lines cut the AC-PC-line, the VAC, that runs through the center of the anterior commissure and the VPC, that runs through the center of the posterior commissure. Transformation of the ICL, VAC and VPC lines into planes yield the intercommissural plane (ICP), the anterior verticofrontal plane (VACp) and the posterior the* 

The three-dimensional profiles of the thalamic nuclei and other structures were mapped on millimeter-ruled diagrams. The reference line was the intercommissural line. This line is

Schaltenbrand and Bailey published the most comprehensive and detailed stereotactic atlas. They studied 111 brains that were sectioned in the coronal, sagittal, and horizontal planes. Variability diagrams were based on seven specimens. Hassler and Wahren completed profound studies of nuclear structures in coronal and parasagittal sections. Akert, Bucy, Walker, Snider, and Hassler contributed with detailed chapters on the physiology and pathophysiology of deep structures of the human brain. Nearly forty years later, this atlas also contributes immensely to functional neurosurgeons, and it could be the most used atlas in the pre-CT era. Even today, the expanded 1977 edition with the most useful features of this work is used world-wide. Their coordinate system appears to be derived from

**2.3 Introduction to stereotaxis with an atlas of the human brain (Schaltenbrand &** 

widely used even to the present day. This atlas is currently out of print.

parasagittal or frontal sections along Talairach's standard planes.

*verticofrontal plane, (VPCp) respectively.* 

**Bailey, 1959 )** 

Fig. 2. Talairach's stereotactic references.

Talairach's space, but shows slight differences.

#### **2.4 A stereotaxic atlas of the human thalamus and adjacent structures: A variability study (Andrew et al.,1969)**

Since the beginning of stereotactic surgery, the main concern of the neurosurgeons was precision. The authors noted that all the previously presented atlases were based on very few specimens and even in the Schaltenbrand's atlas, despite the high total number of brains, only 7 out 111 were comprehensively studied. It was concluded that the stereotactic coordinates of subcortical nuclei were inadequately established, and that the variations would be so great that the procedures could not be reliably done with these coordinates.

The authors thus presented a variability study, aiming to compensate for this lack of precision. They studied nineteen brains, and focused on thalamic nuclei variability. Besides the thalamus, the atlas includes adjacent basal ganglia, and medial temporal lobe structures. It consists of statistical analysis of the data, with probability tables and distances to important ventricular reference points such as the foramen of Monro (FM), PC and midcommisural plane. It was surely an important work to define variability patterns in pre-CT/MRI era.

They used the FM-PC line and the total thalamic length (TthL) as reference system instead of the Talairach's space, although they have measured the AC-PC distance as well.

### **2.5 Variations and connections of the human thalamus (Van Buren & Borke,1972)**

These authors, together with Schaltenbrand and Talairach, published one of the most important atlases of that time. The atlas is the result of a meticulous work on this challenging structure of the human brain, and it comprises a detailed cytoarchitectonic description of the individual thalamic nuclei. The literature on the connections of each nucleus is also reviewed. A special section of the book is dedicated to present the primary lesions (intervention) and secondary thalamic degeneration in fifty-four patients due to stereotactic procedures. The authors care about questions such as correcting differential shrinkage with computational tools, and variation of the position of thalamic nuclei in relation to midline, anterior, and posterior commissures.

#### **2.6 The human somesthetic thalamus with maps for physiological target localization during stereotactic neurosurgery (Emmers & Tasker, 1975)**

In this work Tasker and Emmers have presented a detailed map for electrical stimulation of the thalamus, with 2mm interval stimulation. During stereotactic procedures performed with awake patients, the distribution of somesthetic responses elicited by electrical stimuli was projected into the templates and used to build a three-dimensional homunculus of the somesthetic thalamus. Tasker emphasized that physiologically defined anatomy rather than blind obedience to atlas coordinates should determine how to conduct functional stereotactic operations.

#### **2.7 Atlas for stereotaxy of the human brain with accompanying guide (Schaltenbrand & Wahren,1977)**

According to the preface of the second edition of their atlas the first one was "an exploration of a new field of clinical anatomy." The latest edition concentrates on clinically relevant issues. The authors emphasized the importance of the myelin sections and reduced the

Review of Printed and Electronic Stereotactic Atlases of the Human Brain 151

*The reference lines of Afshar et al. are confined to brainstem and cerebellar structures. The ventral HBG line runs in a rostro-caudal direction tangentially to the floor of the IVth ventricle. The parallel dorsal YFX line passes the tip of the fastigium. A line perpendicular to YX and HG goes likewise through the tip of the fastigium. Its* 

However this variation is proportional for each brain, and they propose to divide the brain

Each hemisphere is divided in twelve parts (1-12) in its supero-inferior (z) axis, in nine parts (A-I) in its anteroposterior (y) axis and in four parts (a-d) in the laterolateral (x) axis. Each voxel has the following dimensions: x: one-fourth of the distance between midline and the most lateral point of the parietotemporal cortex, named a-d ; y: The voxels located anterior to AC have ¼ from the distance from AC to the frontal pole(named A-D). The voxels located posterior to PC have ¼ of the distance from PC to the occipital pole (named F-I), and finally the AC/PC distance is the 9th voxel (named E) and can be divided in thirds, called "minivoxels"; z: the voxels located above the IC line have 1/8 of the distance between IC line and the highest point of the parietal cortex (called 1-8) and the voxels located below the IC line have ¼ of the distance between the IC line and the most inferior point of the temporal cortex (named 9-12). This voxels are fixed for every brain, allowing the normalization between two different subjects having in mind these proportions and not absolute distances in millimeters. The proportional grid system is the greatest contribution given by this work.It allows us to warp our atlases to the patient's MRI using this proportionality. The term "warping" is used in neuroimaging to describe the process of distorting an image (e.g.,

*intersection with YX defines F ; the one with HG defines B.* 

Fig. 3. Coordinate system proposed by Afshar et. al., 1978.

in proportional voxels or "orthogonal parallelograms."

number of macroscopical sections that proved to be of less interest. Thus the material could be condensed into a single and more practical volume. Some of the modifications took into account promising procedures at that time, such as operations on the small nuclei of the hypothalamus to treat deviant sexual behavior and vegetative disorders. They also added electroanatomical observations on the localization of important trigger points and radioanatomical observations in more than 300 patients.

The 111 brains, ranging in age from neonate to 86 years used in the preparation of this atlas were collected at the University of Würzburg, University of Lund (Germany) and the Sodersjuhuset in Stockholm (Sweden). They have considered to use Reid's plane (the plane that extends from the lower margin of the orbit to the center of the external acustic foramen) as reference, however the examination of the macroscopic series did not reveal consistent spatial relations between points on the outer surface of the skull and the subcortical structures, and they chose the AC-PC axis and the perpendicular line erected on the middle point of the two commissures as the basis for their system of reference.

The extremely careful work with great histological sections through the most clinically relevant structures inserted in a consensual reference system made this atlas one of the most consulted until the present day. This atlas is still in print, due to its practical value and use in functional neurosurgical procedures. Many other authors used this work to construct a computational tool for stereotactic surgery.

#### **2.8 Stereotaxic atlas of the human brainstem and cerebellar nuclei: A variability study (Afshar et al., 1978)**

In the early '70s, strategies for the treatment of spasticity due to cerebral palsy and other disturbances of muscle tone and posture by ablation of the dentate nucleus of the cerebellum were developed. In this context, Afshar focused on the cerebellar nuclei and brainstem structures involved in muscle tone disturbances and pain.

Thirty brains were studied using positive-contrast ventriculography and stereotactic marking of the specimens *in situ*. Their atlas comprises a variability and probabilistic study comparable to their previous study in 1969. They present a coordinate system based on the fastigium-floor line (FFL), and orthogonal to the ventricular-floor plane.

#### **2.9 Co-planar stereotaxic atlas of the human brain: Three-dimensional proportional system: An approach to cerebral imaging (Talairach & Tournoux, 1988)**

This work can be considered one of the most important in the field of brain mapping. Its focus is less on histology and architectonic and more on presenting the concept of proportionality and a new coordinate system, the so called Talairach space.

The Talairach's proportional grid system is based on the three dimensions (length, height, and width) of the human brain. The reference planes are defined as: the midline, defining the sagittal plane; the intercommissural plane that is obtained from the line that passes through the superior edge of the AC and inferior edge of PC, defining the horizontal plane; and two verticofrontal planes that intersect the anterior and posterior commissures (named VACp and VPCp). The authors state that direct distance coordinates vary widely from one brain to another and the variation is greater considering points far from the midline.

number of macroscopical sections that proved to be of less interest. Thus the material could be condensed into a single and more practical volume. Some of the modifications took into account promising procedures at that time, such as operations on the small nuclei of the hypothalamus to treat deviant sexual behavior and vegetative disorders. They also added electroanatomical observations on the localization of important trigger points and

The 111 brains, ranging in age from neonate to 86 years used in the preparation of this atlas were collected at the University of Würzburg, University of Lund (Germany) and the Sodersjuhuset in Stockholm (Sweden). They have considered to use Reid's plane (the plane that extends from the lower margin of the orbit to the center of the external acustic foramen) as reference, however the examination of the macroscopic series did not reveal consistent spatial relations between points on the outer surface of the skull and the subcortical structures, and they chose the AC-PC axis and the perpendicular line erected on the middle point of the two commissures as the basis for their system of

The extremely careful work with great histological sections through the most clinically relevant structures inserted in a consensual reference system made this atlas one of the most consulted until the present day. This atlas is still in print, due to its practical value and use in functional neurosurgical procedures. Many other authors used this work to construct a

**2.8 Stereotaxic atlas of the human brainstem and cerebellar nuclei: A variability** 

brainstem structures involved in muscle tone disturbances and pain.

fastigium-floor line (FFL), and orthogonal to the ventricular-floor plane.

**system: An approach to cerebral imaging (Talairach & Tournoux, 1988)** 

proportionality and a new coordinate system, the so called Talairach space.

In the early '70s, strategies for the treatment of spasticity due to cerebral palsy and other disturbances of muscle tone and posture by ablation of the dentate nucleus of the cerebellum were developed. In this context, Afshar focused on the cerebellar nuclei and

Thirty brains were studied using positive-contrast ventriculography and stereotactic marking of the specimens *in situ*. Their atlas comprises a variability and probabilistic study comparable to their previous study in 1969. They present a coordinate system based on the

**2.9 Co-planar stereotaxic atlas of the human brain: Three-dimensional proportional** 

This work can be considered one of the most important in the field of brain mapping. Its focus is less on histology and architectonic and more on presenting the concept of

The Talairach's proportional grid system is based on the three dimensions (length, height, and width) of the human brain. The reference planes are defined as: the midline, defining the sagittal plane; the intercommissural plane that is obtained from the line that passes through the superior edge of the AC and inferior edge of PC, defining the horizontal plane; and two verticofrontal planes that intersect the anterior and posterior commissures (named VACp and VPCp). The authors state that direct distance coordinates vary widely from one brain to another and the variation is greater considering points far from the

radioanatomical observations in more than 300 patients.

computational tool for stereotactic surgery.

**study (Afshar et al., 1978)** 

reference.

midline.

*The reference lines of Afshar et al. are confined to brainstem and cerebellar structures. The ventral HBG line runs in a rostro-caudal direction tangentially to the floor of the IVth ventricle. The parallel dorsal YFX line passes the tip of the fastigium. A line perpendicular to YX and HG goes likewise through the tip of the fastigium. Its intersection with YX defines F ; the one with HG defines B.* 

Fig. 3. Coordinate system proposed by Afshar et. al., 1978.

However this variation is proportional for each brain, and they propose to divide the brain in proportional voxels or "orthogonal parallelograms."

Each hemisphere is divided in twelve parts (1-12) in its supero-inferior (z) axis, in nine parts (A-I) in its anteroposterior (y) axis and in four parts (a-d) in the laterolateral (x) axis. Each voxel has the following dimensions: x: one-fourth of the distance between midline and the most lateral point of the parietotemporal cortex, named a-d ; y: The voxels located anterior to AC have ¼ from the distance from AC to the frontal pole(named A-D). The voxels located posterior to PC have ¼ of the distance from PC to the occipital pole (named F-I), and finally the AC/PC distance is the 9th voxel (named E) and can be divided in thirds, called "minivoxels"; z: the voxels located above the IC line have 1/8 of the distance between IC line and the highest point of the parietal cortex (called 1-8) and the voxels located below the IC line have ¼ of the distance between the IC line and the most inferior point of the temporal cortex (named 9-12). This voxels are fixed for every brain, allowing the normalization between two different subjects having in mind these proportions and not absolute distances in millimeters. The proportional grid system is the greatest contribution given by this work.It allows us to warp our atlases to the patient's MRI using this proportionality. The term "warping" is used in neuroimaging to describe the process of distorting an image (e.g.,

Review of Printed and Electronic Stereotactic Atlases of the Human Brain 153

They could observe the distribution of immunostaining among the thalamic groups and

One interesting technical aspect of this atlas is the correction for shrinkage factors. It was done by means of preoperative MRI from two patients who underwent medial thalamotomy for cancer-related neurogenic pain and who died later from their disease. Intercommissural distances were measured post-mortem at the end of histological processing, and an additional distortion factor was taken into account for coordinates between sections, by measuring the distance between two coronal sections intersecting the centers of the two commissures. The most valuable contribution of this atlas is though the presentation of a

This atlas consists of printed sections and digital media, making it especially easy to use. The first section is a topographic and topometric atlas, in which *in vivo* and *in vitro* MRI scans are compared to whole head sections in horizontal, coronal and sagittal plans. The myeloarchitectonic atlas is based on serial coronal sections through a single hemisphere from a 24-year-old male. Although the templates give detailed information about cytoarchitectonic fields, it is hard to imagine how they could have been segmented from the sections presented on the book, since the staining allows very good contrast between gray and white matter; however, it is hard to define cytoarchitectonic borders with this method. It is a comprehensive study, and its most interesting features are the *in vivo* and *in vitro* MRI comparison to the cadaveric slices, and the user-friendly interface in the

**2.12 Stereotactic atlas of the human thalamus and basal ganglia ( Morel, 2007)** 

In 2007, Morel presented this atlas with the main objective to combine high anatomical resolution (taking advantage of new staining methods) and stereotactic precision. This paper presents a collection of diagrams of the human thalamus, basal ganglia, and adjoining structures, consisting of a series of maps in the three stereotactic planes, and comparisons between brains with similar and differing intercommissural distances. This work, like the previously presented one ten years before, examines the distribution of different neurochemical markers in the thalamus and basal ganglia for comparison with non-human

Fiber tracts leading to the thalamus are also described, and there is a correlation between histological maps with MRI images. They compare also the individual representations,

This atlas is especially useful in functional neurosurgery for research purposes to those who want to understand the connections and plan new targets for neurosurgical interventions in

To give a better overview of various details, ranging from the number of cases studied to the reference coordinate systems, a table will summarize the salient features concerning

**2.13 Summary of materials and methods used in the preceding publications** 

correlate specific markers to functional units.

chemoarchitectonic organization of the human thalamus.

**2.11 Atlas of the human brain (Mai et al.,1998, 2003)** 

digital version.

primate data.

giving an idea of variability.

materials and methods applied.

diseases involving the thalamus and basal ganglia.

atlases) to fit other similar images (e.g. MRI). When two brains are normalized using this proportional system a " Talairach transformation" is performed.

Even with some known disadvantages, such as inter-slice distances variable between 2 and 5 mm, inconsistencies of orthogonal planes and assuming left/right symmetry, this atlas is widely used by neurosurgeons while planning interventions.

#### **2.10 Multiarchitectonic and stereotactic atlas of the human thalamus (Morel et al., 1997)**

Morel's et al. (1997) atlas is based on standard as well as histochemical and immuniohistochemical methods. Advanced neurochemical markers were used to further characterize thalamic nuclei and delimit subterritories of functional significance for stereotactic explorations. The objective was to improve the anatomical definition and precision of thalamic targets.

*The principal Talairach planes (ICp, VACp, VPCp) can be further parcelated by nine coronal planes (A-I), by four sagittal planes (a-d), and by twelve horizontal planes (1-12). Independent of individual hemispheric sizes, each hemisphere will consist of a total of 9x12x4 = 432 voxels. The coronal plane E, based on the AC-PC distance, represents a kind of core structure. Its dimensions are directly measured from the MRIs. The relative voxel sizes of A to D, F to I, a-d and 1-12 are a matter of convenience. They are derived from the maximal lobar extensions rostral, caudal, and lateral from VAC and VPC, and ventral from the AC-PC plane. They are expressed as fractions of the respective plane (1/4 in the coronal plane rostral and caudal to E, ¼ in the sagittal plane corresponding to a – d, 1/8 in horizontal planes dorsal to the AC-PC plane, and ¼ in horizontal planes ventral to the AC-PC plane).* 

Fig. 4. Hemisphere inserted in Talairach's space

atlases) to fit other similar images (e.g. MRI). When two brains are normalized using this

Even with some known disadvantages, such as inter-slice distances variable between 2 and 5 mm, inconsistencies of orthogonal planes and assuming left/right symmetry, this atlas is

Morel's et al. (1997) atlas is based on standard as well as histochemical and immuniohistochemical methods. Advanced neurochemical markers were used to further characterize thalamic nuclei and delimit subterritories of functional significance for stereotactic explorations. The objective was to improve the anatomical definition and

*The principal Talairach planes (ICp, VACp, VPCp) can be further parcelated by nine coronal planes (A-I), by four sagittal planes (a-d), and by twelve horizontal planes (1-12). Independent of individual hemispheric sizes, each hemisphere will consist of a total of 9x12x4 = 432 voxels. The coronal plane E, based on the AC-PC distance, represents a kind of core structure. Its dimensions are directly measured from the MRIs. The relative voxel sizes of A to D, F to I, a-d and 1-12 are a matter of convenience. They are derived from the maximal lobar extensions rostral, caudal, and lateral from VAC and VPC, and ventral from the AC-PC plane. They are expressed as fractions of the respective plane (1/4 in the coronal plane rostral and caudal to E, ¼ in the sagittal plane corresponding to a – d, 1/8 in horizontal planes dorsal to the AC-PC plane, and ¼ in horizontal planes ventral to* 

**2.10 Multiarchitectonic and stereotactic atlas of the human thalamus (Morel et al.,** 

proportional system a " Talairach transformation" is performed.

widely used by neurosurgeons while planning interventions.

**1997)** 

precision of thalamic targets.

*the AC-PC plane).* 

Fig. 4. Hemisphere inserted in Talairach's space

They could observe the distribution of immunostaining among the thalamic groups and correlate specific markers to functional units.

One interesting technical aspect of this atlas is the correction for shrinkage factors. It was done by means of preoperative MRI from two patients who underwent medial thalamotomy for cancer-related neurogenic pain and who died later from their disease. Intercommissural distances were measured post-mortem at the end of histological processing, and an additional distortion factor was taken into account for coordinates between sections, by measuring the distance between two coronal sections intersecting the centers of the two commissures. The most valuable contribution of this atlas is though the presentation of a chemoarchitectonic organization of the human thalamus.

#### **2.11 Atlas of the human brain (Mai et al.,1998, 2003)**

This atlas consists of printed sections and digital media, making it especially easy to use. The first section is a topographic and topometric atlas, in which *in vivo* and *in vitro* MRI scans are compared to whole head sections in horizontal, coronal and sagittal plans. The myeloarchitectonic atlas is based on serial coronal sections through a single hemisphere from a 24-year-old male. Although the templates give detailed information about cytoarchitectonic fields, it is hard to imagine how they could have been segmented from the sections presented on the book, since the staining allows very good contrast between gray and white matter; however, it is hard to define cytoarchitectonic borders with this method. It is a comprehensive study, and its most interesting features are the *in vivo* and *in vitro* MRI comparison to the cadaveric slices, and the user-friendly interface in the digital version.

#### **2.12 Stereotactic atlas of the human thalamus and basal ganglia ( Morel, 2007)**

In 2007, Morel presented this atlas with the main objective to combine high anatomical resolution (taking advantage of new staining methods) and stereotactic precision. This paper presents a collection of diagrams of the human thalamus, basal ganglia, and adjoining structures, consisting of a series of maps in the three stereotactic planes, and comparisons between brains with similar and differing intercommissural distances. This work, like the previously presented one ten years before, examines the distribution of different neurochemical markers in the thalamus and basal ganglia for comparison with non-human primate data.

Fiber tracts leading to the thalamus are also described, and there is a correlation between histological maps with MRI images. They compare also the individual representations, giving an idea of variability.

This atlas is especially useful in functional neurosurgery for research purposes to those who want to understand the connections and plan new targets for neurosurgical interventions in diseases involving the thalamus and basal ganglia.

#### **2.13 Summary of materials and methods used in the preceding publications**

To give a better overview of various details, ranging from the number of cases studied to the reference coordinate systems, a table will summarize the salient features concerning materials and methods applied.

Review of Printed and Electronic Stereotactic Atlases of the Human Brain 155

Orientation of sections and interval

(1)19 cor.,5 sag., 6 horiz.from 1 brain, and 4 from another; (2) 20 cor., 17 sag.and20 horiz.

(1)54 plates, 1mm thick ;(2) 12 cerebellar plates

36 sagittal (1- 4mm int.); 38 frontal (5mm int); 27 horizontal (5mm int)

3 blocks sagittal, 4 horizontal and 2 coronal

17 horizontal;15 coronal and 8 sagittal; (2) 69 coronal sections

Range of Slices Coordinate

(1)57 mm ant. - 44 mm post. to AC; 0 - 22mm from midline; 18 above-20mm below ICL; 5-28mm below ICL; (2)16.5 mm ant.- 16.5mm post midcom. line 1.5-27.5 mm lat. Midline 16.0mm above to 9.5mm below ICL

(1)23mm rostral to 30mm caudal to FFL; 1mm rostral to 10mm caudal to FFL

Right: 18 sec 0- 62mm ;Left:18 sec 0-61mm ;0-65mm ant. To VAC; 0- 100mm post VAC;0-6.5 mm above ICL;0- 4.1mmbelow ICL

Region of interest: thalamus

(2) 60mm ant.AC-100 mm post. AC (100µm)

System MRI

No

No

Preopera tive MRI of 2 patients

Yes for the macroser ies

ICP MSP McomP

VFP FFL Fastigial point

> ICP MSP

ICP MSP VAC

ICP MSP VAC

VAC Yes

Reference

Schaltenbrand &Wahren, 1977

Afshar et

Talairach& Tournoux,1988

> Morel et al.,1997

Mai et al.,1998,2003

Nr. of brains and sections

34 sec. for macro and 57 sec.for microseries (frozen sec. 30µm) Paraffin used to brainstem and cerebellum

al.,1978 30 brains Myelin-stained

1 brain cut sagittaly, frontal and horizontal sections were interpolated

9 thalamic frozen blocks cut in 40µm thick slices from 5 brains

6 brains – macroseries (frozen, 1 cm thick) and 1 hemisphere for Microseries (paraffin)

Staining and other investigative tissue methods

Unstained(1), myelin-stained and Nissl (2)

Anatomic sections, that are drawn as a result of tracing the sections

Nissl, myelin and Immunohystoc hemestry parvalbumin (PV), calbindinD-28K (CB), and calretinin (CR)

(1)Sudan red or Sudan Black B (2)Hematoxyli n- or sudan black B for myelinated fibers


Orientation of sections and interval

(1)cor.,sag., horiz.and oblique through brainstem (5mm int.) (2)cor. (2-4 mm) and oblique through brainstem (5mm)

(1)16 coronal (1- 4 mm) and 18 sagittal (0.5 to 2.5 mm);(2)20 horizontal

21 coronal (1 mm) and 17 sagittal (1mm)

10 sagittal (0.5 to 4mm); 8 horizontal (3.5mm) ; 10 coronal sections

5 sag. and 5 cor. plates; 10 sag. and cor. whole brain sections

Range of Slices Coordinate

16.5 mm ant. to AC and 16.5 mm post.to PC;2.0 - 27.5mm lat. to midline;16mm above to 9.5mm below midcom. pt.

1-21 mm behind FM;3-20 mm from midline; includes thalamus, basal ganglia, and medial temporal lobes.

2-25mm lat.to midline parallel to ICP; 17mm above to 8.1 mm below IC; 23.4 mm ant. PC - 47mm post. PC

Cut at 9, 11,13.5,16 and 18 mm lat. to midline; 8.5, 10 , 11, 12.5 mm post. to the midcom. point

System MRI

MSP No

No

No

PC-PO line

ICP, MSP, VACp , VPCp

> ICP MSP McomP

FM-PC line

ICP MSP

ICP MSP VAC

TthL No

VAC No

No

Reference

Spiegel & Wycsis,1952

Talairach et al.,

Schaltenbrand & Bailey,1959

Andrew et al.,

Van Buren &Borke, 1972

Emmers& Tasker, 1975

<sup>1969</sup>19 brains

Nr. of brains and sections

1 brain (30 sections)

1957 1 brain Unstained and

111 brains (7 brains for variability study)

6 brains individual profiles and 25 hemisph. for gross anatomy variability

2 brains: 1 for macroseries 1 for microseries

Staining and other investigative tissue methods

Unstained (1) and myelinstained (2)

Myelin-stained

Unstained (1) and myelin – stained (2)

Nissl and myelin stained from 1 brain

Cresyl-violet, myelin and Golgi preparations

Electrical stimulation at 2mm intervals and mapping of the somesthetic responses elicited in awake patients; results projected into the templates


Review of Printed and Electronic Stereotactic Atlases of the Human Brain 157

**3.1 Creation of a three-dimensional atlas by interpolation from Schaltenbrand-Bailey's** 

In 1987 Yoshida proposed the creation of a 3D atlas of the human brain based on the interpolation of the 2D templates of the Schaltenbrand-Bailey's atlas. Although the rendering resulted in great three-dimensional incoherency due to the lack of correction of the linear and non-linear tissue distortions present at the original sections, this atlas is important as the first of its kind and of the concept of referring to a volume instead of

**3.2 Multiple brain atlas database and atlas-based neuroimaging system (Nowinski et** 

Nowinski and his collaborators started in 1997 a project in which four previously published atlases were digitized, enhanced, segmented (color coded or contoured), labeled, aligned, and organized into volumes for the purpose of developing an atlas-based neuroimaging system for analysis, quantification, and real-time manipulation of cerebral structures in two and three dimensions. A software was developed that is available in a CD-ROM called "Electronic Clinical Brain Atlas-ECBA." It is impressive in terms of three-dimensional visualization of the structures; however, due to some inaccuracies inherent in the original print atlases, three dimensional structures reconstructed from Schaltenbrand & Wahren atlas are often convoluted and displayed in unrealistic shapes. As noticed and discussed by the authors in this paper, a given point in the stereotactic space may have up to three different labels on the Talairach & Tournox atlas, due to inconsistent orthogonal plates. Nevertheless, important questions about the 3D accuracy of the most-used atlases were

**3.3 Automated atlas integration and interactive three-dimensional visualization tools** 

The authors created a deformable volumetric atlas of the basal ganglia and thalamus from the Schaltenbrand and Wahren atlas (SW atlas) to help neurosurgeons navigate through MRI-invisible structures. They developed also a visualization platform that permits manipulation of the merged atlas and MRI data set in two- and three-dimensional views. A really interesting and new method of correction of errors was developed by this group. After digitizing the sections and the transparent overlays from the SW atlas, they aligned and segmented the nuclear contours based on the overlays and performed an interpolation to create a 3D volume. The alignment was based on the original grid, and they noted that the grid structure present in the atlas was placed on the cryotome images subsequent to photography, and so even precise alignment with respect to the grid is no guarantee that the underlying slices were not themselves distorted during the slicing process. However, they developed a methodology for matching automatically the slices with the 3D model. The atlas is registered point-to-point (250 homologous landmarks identified by a neuroanatomist) to a model MRI or standard reference volume. Even though any MRI could be chosen, they opted by the Colin27 that is the result of an average of 27 MRI scans of the same subject. As they have a labeled MRI based on the SW atlas, an algorithm called ANIMAL (Automated Nonlinear Image Matching and Anatomical Labeling) computes a nonlinear transformation to register the patient's MRI with the pre-labeled

**for planning and guidance in functional neurosurgery (St-Jean et al., 1998)** 

confining exclusively on two-dimensional representations of the neural tissue.

**atlas (Yoshida, 1987)** 

**al., 1997)** 

evidenced.


*Definitions: PC-PO line: connects the center of posterior commissure (PC) to the ponto-medullary sulcus (posterior border of the pons) and the midsagittal plane (MSP); ICL- intercommissural line: line that passes through the superior edge of the anterior commissure (AC) and inferior edge of PC; ICP- intercommissural plane: plane obtained from the ICL, defines the horizontal plane; MSP-Midsagittal plane: obtained from midline; VACp:Verticofrontal plane is formed by VAC line, that is a vertical line traversing the posterior margin of the AC: VPCp is the verticofrontal plane perpendicular ICL crossing it at PC; MComP: Midcommissural plane is erected from the midcommissural point, that is the midpoint of the ICL;The FM-PC line is the distance between the posterior inferior margin of the foramen of Monro (FM) to the midpoint of the ventricular surface of PC;The total thalamic length (TthL) is the distance between the FM and the top of the pulvinar;The ventricular-floor plane (VFP) is the plane defined by the floor of the fourth ventricle. Perpendicular to this plane and reaching the fastigium (apex of the roof of the fourth ventricle) is the fastigium-floor line(FFL).* 

Table 1. Printed stereotactic atlases based on number of cases studied, histological protocols, planes of section, coordinate systems, and reference to neuroimaging.
