Neurosurgical Neuropsychology: The Practical Application of Neuropsychology in the Neurosurgical Practice

destiny."

Section I

Introduction

Outline

Chapter 1 The Historical Role of Neuropsychology in Neurosurgery

Chapter 2 Foundations of Contemporary Neuropsychology

Chapter 3 Components and Methods of Evaluating Reliable Change in Cognitive Function

Chapter 4 A Primer on Neuropsychology for the Neurosurgeon

Chapter 1

The Historical Role of Neuropsychology in Neurosurgery

Mairaj T. Sami and Paul J. Camarata,    Department of Neurosurgery, University of Kansas Medical Center, Kansas, United States

Abstract

Neuropsychology as the study of how the brain and its structures influence thought and behavior is arguably unique to the human brain. While the brain and nervous system have been studied by some in the past, it is only within the last century with advances in pioneering surgery on the brain that the field of Neuropsychology has bourgeoned. In this chapter, we highlight the major advances and those proponents who have truly developed the field into the robust discipline we know today.

Keywords

Neurosurgery; neuropsychology; history; cognition; memory; collaboration; epilepsy; language

The more we discover about the brain, the more clearly do we distinguish between the brain events and the mental phenomena, and the more wonderful do both the brain events and the mental phenomena become.

John C. Eccles.

Trephined skulls and ancient papyri testify to the fact that practitioners of what we now know as neurosurgery have existed for millennia. Similarly, since the earliest times humans have puzzled over how human behavior is produced. It is only within the last century or so that the two fields have begun to cooperate extensively, and it is this cooperation that has led to profound advances in the respective sciences. In this chapter, we will describe the early evolution of each field, and the fruits of that ever-increasing cooperation.

Origins of Neurosurgery

Brain surgery is a terrible profession. If I did not feel it will become different in my lifetime, I should hate it.

Wilder Penfield.

Where written records are lacking, the telltale signs of manmade surgery on the human skull are evident in the paleological record of most every continent. It can be determined that many of these skull perforations were placed before death; some perhaps for medical reasons, and others perhaps in warfare or injury. In a 1954 monograph on trephination, Graña concluded that many of the skull perforations were made for medical reasons, with evidence of brain tumors, fractured skulls, and cranial osteomyelitis (Grana & Rocca, 1954). However, the first written records regarding brain surgery date from about 3000 BC, where the writings from Imhotep, a physician priest of King Zoser, are detailed in what is now known as the Edwin Smith papyrus.

In this document which describes the wounds of 48 persons, 17 of them had injuries to the nervous system. He describes treating wounds of the head with underlying skull fractures by laying fresh meat upon the wound the first day, then afterward with grease, honey, and lint. However, if the dura were penetrated, it was an ailment not to be treated (Breasted, 1930).

In the time of Hippocrates, who lived from about 460 to 379 BC, physicians knew the brain to be the receptive organ for sensations and the source of all motor activity, but were unclear about how the brain communicated with the body. It was known, however, that in head wounds if the wound is on the left side of the head, convulsion seizes the right side of the body, and if the wound is on the right side of the head, convulsion seizes the left side of the body. There are some patients who also become apoplectic, and in this condition they die within 7 days in summer or 14 days in winter (Hanson, 1999). Aristotle, however, a near contemporary, believed that the heart was actually the seat of thinking and emotion, believing that the brain only served to cool the heart-generated heat (Benton & Sivan, 2007). Despite evidence to the contrary and perhaps somewhat surprisingly, this belief of a heart-centered mind had its proponents even through the 1600s. In the English language alone, we maintain vestiges of this belief in such aphorisms as learning by heart, a loved one has our heart, or someone with a heart of gold.

Perhaps the most outstanding early Christian physician was the Greek Galen who was born in AD 130. As a physician to the gladiators for 4 years, Galen undoubtedly witnessed many brain injuries. Much of his neurological writing was unavailable to the western world, and indeed it was lost from the 9th century until the 19th century when two Arabic translations were found (Walker, 1998). Galen made numerous studies in animals observing the brain and spinal cord in vivo, recognizing sensory and motor nerves of the spinal cord, and seven pairs of cranial nerves. It was not until the 17th century when the brain had clearly displaced the heart as the seat of the mind and sentience, and with it came certain concepts of cerebral localization subserving various neurologic functions. Thomas Willis (1621–73), a physician in Oxford and London, attracted a number of talented associates who performed exquisite anatomical dissections which helped him postulate on the various functions of different areas of the brain. He placed memory in the cerebral cortex. Others had other theories of localization—Francois La Peyronie (1678–1747) sited intelligence in the corpus callosum and Emmanual Swedenborg (1688–1772) placed intellectual functions in the cerebral cortex (Benton & Sivan, 2007).

Another major advance in the concept of neurophysiology that would impact surgery of the brain took place when Franz Joseph Gall (1758–1828) postulated that the human brain was an assemblage of organs that subserved a specific cognitive ability or trait. This stimulated detailed anatomical studies of the brain throughout the scientific community, such that by 1860 illustrations of the human cortical surface are essentially the same as those found in today’s texts. (Benton & Sivan, 2007, p. 143). Shortly thereafter, Paul Broca (1824–80) discovered that speech is primarily mediated by the left hemisphere. Though, as detailed earlier, Hippocrates had noted the contralateral control of extremities 2000 years earlier, the demonstration by Gustav Fritsch and Eduard Hitzig in 1870 that electrical stimulation of the precentral gyrus in a dog produced contralateral limb movement rocked the neuroscience community. This was the first time anyone had done any localized study regarding the brain and electric current.

Following shortly thereafter, in 1874, a Cincinnati physician, Roberts Bartholow, performed a similar experiment in one of his patients. A young woman dying of a malignant scalp lesion allowed him to insert insulated wires through the granulation tissue directly into the underlying cortex. When current was passed through the electrodes presumably placed in the left peri-Rolandic cortex, it elicited a pronounced contraction of the right arm, hand, and leg. With continued stimulation, he eventually produced a seizure. The woman died a few days later of overwhelming brain infection. His experiments were roundly criticized by scientists all over the world (Walker, 1998).

The work on cerebral localization and observations of eminent British Neurologist John Hughlings Jackson (1835–1911) set the stage for the nascent field of neurosurgery to remove brain tumors and treat focal causes of epilepsy. It was also occasioned by the introduction of antiseptic techniques and anesthesia. Sir Rickman John Godlee successfully removed a tumor from the right Rolandic cortex in 1884. When that was presented before the Medical and Chirurgical Society of London, Scottish physician William Macewen (Fig. 1.1A) related that he had removed a brain tumor in 1879. He is then largely regarded as the first surgeon to operate a brain tumor without any external clue that a tumor was present in the brain. It has since been learned that in Italy in 1883, Giacomo Novaro in Turin operated on a hyperostosing meningioma, and his colleague in Rome, Francesco Durante, removed an olfactory groove meningioma in a patient in 1885 (Guidetti, Giuffre, & Valente, 1985).

Figure 1.1 (A) Photo of William Macewan (first surgeon to operate brain tumor by intuiting its location) and (B) photo of Harvey Cushing.

Pioneer neurosurgical procedures were fraught with an extraordinarily high rate of complications with a mortality at times reaching 65%! It took the wiles and skills of an American, Harvey Williams Cushing (1869–1939) to essentially rescue neurosurgery from its rapid waning at the turn of the last century (Fig. 1.1B). Cushing taught himself to operate on the brain, and through his meticulous surgical technique, learned at the hand of surgeon William Halstead at the Johns Hopkins Hospital, he reduced the mortality to only 10%. These pioneers and others ushered in the neurosurgical advances of the last century.

Origins of Neuropsychology

If a man has lost a leg or an eye, he knows he has lost a leg or an eye; but if he has lost a self—himself—he cannot know it, because he is no longer there to know it.

Oliver Sachs.

The discipline of neuropsychology comprises the study of brain function as it relates to human behavior and thinking. Over the course of history, neuropsychology has enjoyed rich contributions from many disciplines including anatomy, physiology, pharmacology, biology, and philosophy. Today, neuropsychology is a dynamic profession which serves many practical clinical applications—lateralization and localization of brain lesions, diagnosis of neurobehavioral conditions, detection of cognitive deficits or brain damage, and the establishment of functional baselines for assessment of neuropsychiatric improvement or deterioration (Parsons, 1991).

Although neuropsychology is a relatively young field-achieving fruition primarily during the 20th century, the series of events that led to its emergence as a distinct science, and the very nature of its origin are often debated.

It is uncertain as to when the term neuropsychology first entered common scientific lexicon. In 1913, Sir William Osler used the term while addressing the Phipps Psychiatric Clinic of Johns Hopkins Hospital in order to underscore the biological aspect of psychiatric disease (Bruce, 1985). Hebb (1949) was the first to capture the term in physical text, when he published his book, The Organization of Behavior: A Neuropsychological Theory (Hebb, 1949). Karl Lashley used neuropsychology briefly in a 1936 presentation to the Boston Society of Psychiatry and Neurology (Bruce, 1985), as well as in later texts during the 1960s (Beach, Hebb, Morgan, & Nissen, 1960). Perhaps the most prominent use of the term, and the instance that gave neuropsychology its current meaning, was during a 1948 symposium presentation given by Hans-Lukas Teuber at the American Psychological Association (APA). During the symposium, which was aptly titled Neuropsychology, Teuber described procedures that he developed with his colleague, Morris Bender, to study the behavioral consequences of penetrating brain injuries (Benton, 1987). Teuber’s presentation at the APA is considered an influential work that led to widespread recognition of neuropsychology as an independent, separate field.

Numerous attempts have been made to attribute the creation of the field of Neuropsychology to a specific person or event. The history of neuropsychology is replete with such examples. The creation of Ward Halstead’s laboratory for psychological evaluation of brain damaged patients in 1935 was a significant contribution. Karl Lashley, considered one of the founders of neuropsychology, performed much of his seminal work in the physical manifestation of memory and neuroplasticity during the 1920s. Fritsch and Hitzig’s experiment detailing contralateral movement with electrical stimulation of the cortex heralded a golden age of cerebral localization where many subsequent studies aimed to define the functional purpose of every area of the cerebral cortex. The case could also be made that Broca’s discovery of hemispheric cerebral dominance in the 1860s, or Gall’s theory of the brain as an aggregate of specialized cortical areas rather than a single unitary organ, were also key in shaping the field of neuropsychology (Stringer & Cooley, 2002).

When these isolated events are viewed as a whole, it becomes apparent that the field of neuropsychology arose from evolution rather than revolution. There is no single inciting event or creator that is solely responsible for the precipitous existence of neuropsychology. It is a discipline that arose out of necessity, a tool developed to serve the clinical and intellectual curiosities of its many pioneers. Neuropsychology was born from vital contributions from seminal individuals, spanning many generations, avenues, and eras in time.

The Collaboration of Neurosurgery and Neuropsychology: A Mutually Beneficial Partnership

But a man does not consist of memory alone. He has feeling, will, sensibilities, moral being—matters of which neuropsychology cannot speak.

A.R. Luria.

In an autobiographical work, Karl Pribram describes an early illustrative example of the symbiotic relationship between neurosurgery and neuropsychology (Fig. 1.2) (Pribram, 2002). Pribram was intrigued by the recently published classic text, Physiology of the Nervous System, by John Fulton. After training in neurosurgery at Northwestern with Percival Bailey and Paul Bucy, and in Memphis with Eustace Semmes, Pribram was working as a neurosurgeon in Jacksonville, Florida when he first met Karl Lashley in 1946. Pribram and Lashley devised a plan to perform experiments on spider monkeys in order to settle a dispute. Pribram recalls: the issue between us was whether the brain was organized into systems, each of which served a separate psychological process. While Lashley agreed that localized systems could serve in sensory and motor tasks, he believed that higher order cognitive functions were distributed generally over the cerebral cortex. Drawing from clinical observations of his own patients with various agnosias, Pribram reasoned instead that higher order cognitive functions reside in specific areas of injured cerebral cortex.

Figure 1.2 Photo of Karl Pribram.

The ensuing collaboration between Pribram and Lashley was emblematic of how the distinct characteristics of neurosurgery and neuropsychology are ideally suited and complementary to one another. In approaching Pribram, Lashley sought biological techniques to investigate psychological processes. Conversely, Pribram was in pursuit of behavioral techniques to investigate the organization of brain processes. Pribram jokingly asserted that Lashley also required his aid because Lashley’s surgical skill and knowledge of aseptic technique left much to be desired. Pribram placed this sentiment in a larger context when he stated that physiological psychologists fared no better; their lack of surgical skill and anatomical naïveté made it common knowledge that no two experimenters ever obtained the same results. However, Pribram was quick to note that contemporary studies within neurosurgery and neurology were flawed as well. He felt that human clinical studies endured difficulty in identifying the site and extent of a lesion, and that there was a prevalent lack of sophistication in experimental design. In a 1954 paper titled Toward a Science of Neuropsychology, Pribram ultimately concluded that neuropsychology became a true science when the traditions and practices of clinical neurology and neurosurgery were mated with experimental psychology (Pribram, 1954).

Epilepsy

Pribram and Lashley serve as just one example of the many mutually beneficial partnerships between neurosurgery and neuropsychology found throughout history. Perhaps the earliest and most meaningful collaborations between neurosurgery and neuropsychology took place within the realm of epilepsy surgery. The collaborations we will mention are by no means the only such partnerships that flowered over the last 100 years.

The disciplines of neurosurgery and neuropsychology were each making independent progress toward treatment of epilepsy during the late 1800s. In 1870, British neurologist John Hughlings Jackson was the first to describe the origination of focal motor seizures from the contralateral cerebral hemisphere, rather than from the brainstem as previously believed (Eadie, 2007). Meanwhile, Sir Victor Horsely, was refining his surgical technique using animals as he would go on to perform the first epilepsy surgery in 1886. Horsely had been informed by Jackson’s theory that all epilepsy was focal, deducing that removal of the focal abnormality should result in a cure from seizures. In this case, Horsely’s 22-year-old patient, James B., suffered a skull fracture in a traffic accident and became seizure-free after a cortical scar had been surgically removed (Taylor, 1986).

While it had long been understood that uncontrolled epilepsy would lead to progressive neurological decline and dementia, the first formal studies of the effects of epilepsy on cognition were not performed until the late 19th and early 20th centuries. In a British psychology journal, Smith (1905) compared two groups of epilepsy patients to healthy controls using an array of tests that resemble those used in neuropsychology today. Word and picture tasks were used to assess memory. Smith found that epilepsy patients with dementia suffered from increased confusion with regard to old and new (Smith, 1905). The first study of cognition in epilepsy in the United States was published in 1912. Wallin used Binet–Simon intelligence scales to categorize patients with epilepsy into groups based on intelligence as reflected by mental age (MA). This study is remarkable for its use of a positive control group, as these epilepsy patients were then compared to feeble-minded institutionalized patients. Wallin found that patients with epilepsy had overall less cognitive impairment than feeble-minded patients based on intelligence according to MA (Wallin, 1912).

Collaboration between neurosurgery and neuropsychology at three major epilepsy centers gave rise to the modern era of epilepsy surgery. These centers include The University of Illinois, the University of London, and the Montreal Neurological Institute (MNI).

The epilepsy program at the University of Illinois was led by neurosurgeon, Percival Bailey. Bailey, whose former residents included Paul Bucy and Karl Pribram, avoided resection of the hippocampal apparatus during epilepsy surgery to prevent development of what has become known as the Kluver–Bucy syndrome. This is the likely explanation for poorer outcomes seen in the University of Illinois series of epilepsy patients in comparison to other similar institutions at the time. However, the University of Illinois epilepsy program enjoyed the advantage of being in close proximity to Chicago. Thus, Percival Bailey had all of his epilepsy patients evaluated pre- and postoperatively by Ward Halstead. Halstead employed a battery of neuropsychological tests and published his findings in 1958, noting that epilepsy surgery did not result in a generalized cognitive decline, and that most indicators actually demonstrated an improvement postoperatively. Patients showed no significant change in the Impairment Index. Halstead’s work was critical in showing that surgical treatment of epilepsy did not have to result in significant cognitive impairment (Halstead, 1958; Hermann & Stone, 1989).

Murray Falconer was the neurosurgeon in charge of epilepsy treatment at University of London. Unlike his contemporary, Percival Bailey, Falconer was known for en bloc resections of the temporal lobe and was keenly aware of hippocampal involvement in the pathological process and treatment outcomes related to epilepsy. Falconer worked closely with psychologists Victor Meyer and Aubrey Yates, and their findings regarding the effects of epilepsy surgery and hippocampal/temporal lobe dysfunction remain relevant to this day. Meyer and Yates concluded that operation in the dominant temporal lobe commonly results in a severe deficit of auditory–verbal learning (Mayer & Yates, 1955).

Nonetheless, the greatest contributions to the fields of epilepsy surgery and neuropsychology occurred at McGill University and the MNI. The epilepsy program was led by the renowned neurosurgeon from Hudson, Wisconsin, Wilder Penfield (Fig. 1.3), who cofounded MNI in 1934. Penfield’s early career was spent in a sort of neuroscience Grand Tour beginning with the aid of a Rhodes scholarship to study with the famous Oxford neurophysiologist Sir Charles Scott Sherrington. He also spent time in the Madrid laboratories of histopathologists Ramon y Cajal and Pio del rio Hortega. And finally, he spent time with the man who pioneered electroencephalography (EEG), Otfrid Foerster.

Figure 1.3 Neurosurgeon Wilder Penfield, Director of the Montreal Neurological Institute.

It is doubtless that Penfield’s pioneering work in epilepsy surgery, operating on awake human brains, was occasioned by his time with Sherrington. Charles Sherrington won the Nobel Prize for his contributions to the study of the neuron and synapses, and later became a mentor to three Nobel laureates. Sherrington later wrote about the connection between the mind and the brain in his work, Man: On His Nature (Sherrington, 1940), where he waxed eloquently on the relationship of the mind to the myriad of neural impulses.

the brain is waking and with it the mind is returning. It is as if the Milky Way entered upon some cosmic dance. Swiftly the head-mass becomes an enchanted loom where millions of flashing shuttles weave a dissolving pattern, always a meaningful pattern though never an abiding one;

Sir Charles Scott Sherrington (Sherrington, 1940).

He would spend the later years of his career trying to solve the mind–brain conundrum, and hence the relationship between psychiatry and neurophysiology…

In the training and in the exercise of medicine a remoteness abides between the field of neurology and that of mental health, psychiatry. It is sometimes blamed to prejudice on the part of the one side or the other. It is both more grave and less grave than that. It has a reasonable basis. It is rooted in the energy-mind problem. Physiology has not enough to offer about the brain in relation to the mind to lend the psychiatrist much help.

Sherrington in The Brain Collaborates With Psyche (1940).

One can see Penfield’s time with his mentor influencing his second career, when a year before his death he would remark, Throughout my own scientific career I, like other scientists, have struggled to prove that the brain accounts for the mind. But perhaps the time has come when we may profitably consider the evidence as it stands, and ask the question… Can the mind be explained by what is now known about the brain? (Penfield, 1975).

Penfield’s inspiration for surgical treatment of epilepsy was derived from the time he spent with Otfrid Foerster at the Brain Research Institute in Breslau, Germany. Penfield had received a grant to study with Foerster from the Rockefeller Foundation. Though not a surgeon by formal training, as a neurology consultant in World War I Foerster began operating on the wounded, especially those with peripheral nerve injuries. He described to Paul Bucy how he became a reluctant neurosurgeon…

I had to accompany the patient to the operating room. I had to tell Mickulz (a general surgeon) where to operate. When he got inside the skull, I had to tell him where the tumor was and what to do. And then the patients all died. I decided I could do no worse.

Bucy (1978) (Fig. 1.4).

Figure 1.4 Photo of Paul Bucy holding a light for surgeon Otfrid Foerster.

In 1928, Penfield spent 6 months with Foerster in Breslau, learning awake cortical stimulation techniques while performing surgery on many of the World War I veterans who suffered from posttraumatic epilepsy (Sarikcioglu, 2007). Though Hans Berger is credited with recording the first human electroencephalogram (EEG), Foerster was the first to record an actual intraoperative electrocorticogram in 1934.

Penfield returned from Germany, and with William Cone, a surgeon who had also spent time in Breslau, founded the MNI at McGill, aided by another grant from the Rockefeller Foundation. At MNI, Penfield championed a multidisciplinary approach that was unique for its time. Penfield recruited Herbert Jasper, a neurophysiologist, who claimed that he could localize epileptic foci by detecting abnormal brain rhythms outside of the skull. Through multiple shared patients, Penfield was able to confirm the merits of EEG in localizing epileptogenic lesions (Feindel, 1999).

As a visionary, Penfield also established the first clinical psychology service at a major hospital in 1938 at the MNI. Though at the time, the sciences of psychology and medicine were largely separate entities, Penfield understood the value and insight that neuropsychologists could provide. In progressive fashion, Penfield hired Molly Harrower, who was the only female staff in the entire hospital, as his first clinical neuropsychologist (Loring, 2010).

Over the remainder of his career at MNI, Penfield continued a tradition of collaboration between neurosurgery and what would come to be known as neuropsychology. Penfield relied on another prominent neuropsychologist, Donald Hebb, to successfully map eloquent cortex through stimulation language mapping. During dominant temporal lobe resections for treatment of epilepsy, it was Hebb who would often converse with awake patients through a wide range of topics (Almeida, Martinez, & Feindel, 2005).

Hebb’s most significant contributions to Penfield and MNI can be attributed to the innovative work he performed regarding the frontal lobes. Hebb showed that clinical frontal release signs were caused by frontal lesions and associated mass effect rather than large prefrontal lesions alone (Hebb, 1977). These findings afforded clinicians at MNI an opportunity to more rapidly diagnose and offer cognitive evaluation to these patients in comparison to their peers. In the course of his career, Hebb accrued a substantial series of patients with frontal lobe