- Email: [email protected]
Aphasia and the Lateralization of Language
APHASIA AND THE LATERALIZATION OF LANGUAGE D. Frank Benson (The Augustus S. Rose Professor of Neurology, UCLA School of Medicine, Los Angeles)
A major interest throughout the investigative career of Norman Geschwind concerned asymmetries of the cerebral hemispheres and the significance of these anatomical asymmetries for human behavior. The most dramatic functional example is, of course, human language, a phenomenon that occupied an important part of Geschwind's efforts. In this essay some contemporary investigations are viewed against the original conc~s of hemispheric specialization for language in an attempt to clarify our concepts of hemispheric asymmetries of language functions.
One of the most striking curiosities in all of biology concerns the strong hemispheric lateralization for language that is present in most humans - the dominance of the left hemisphere for language. It has been the study of aphasia, the loss or impairment of language caused by brain damage, that originally and still best demonstrates this striking curiosity. The data from clinical observations of aphasia patients is so overwhelming that no one questions the statement that the left hemisphere is crucial for language functions. On the other hand, recent research suggests that the right hemisphere is also capable of performing language functions; the left hemisphere is not alone in subserving language. Do we truly have language in both hemispheres? Is right hemisphere language function similar, modified, or distinct from left hemisphere language? Is the evidence from the study of aphasia biased? Have we· allowed the obvious language dysfunctions of aphasia to mislead us in considerations of the cerebral locus of language functions? The status of hemispheric specialization for language has been changing and the findings of aphasia investigation in this state of flux deserve reappraisal. Historical Background It can be truly stated that the correlation of hemispheric lateralization and aphasia stems from the work of Broca. Prior to Broca's initial presentation (1861), there had been serious scientific debate concerning Cortex (1986) 22, 71-86
72
D. Frank Benson
cerebral function but the disagreement revolved about whether the brain operated as a single, holistic unit (similar to the liver or the lungs) or with separate areas of the brain subserving separate mental functions. The phrenologist Gall (1810) had proposed a detailed breakdown of brain functions with separate areas of the brain cortex performing specific mental attributes. Gall's choice of focal mental functions is no longer acceptable and all agree that he was excessive in their localization; nonetheless, despite the exorbitance of his claims, Gall never went so far as to suggest that a given function was sub served by one hemisphere only. All proposed attributes were considered bilateral (Figure 1). Gall's proposal of localization of function within the brain produced disagreement in the early part of the 19th Century; some investigators supported the localization of psychological functions, including "speech", but most supported an holistic approach in which behavioral responses demanded action of the entire brain. Against this background, Broca (1861) demonstrated an individual who had lost "speech" and who, at post-mortem, had a focal brain lesion. Speech (language) appeared to be under the control of a limited area of the brain. While the controversy about the localization of language to a given segment of the brain was not settled, Broca's major contribution, the introduction of a new research tool in which observed behavioral abnormality was corelated with gross anatomical studies of brain lesions, was immediately accepted. Behavioral/ anatomical correlations could be conducted in many laboratories and were immediately undertaken. A major advance had occurred in neuroscience. Withinjust a few years many cases of language impairment had been correlated with focal brain lesions, some supporting the localization demonstrated by Broca, others in disagreement, but the occurrence of aphasia with focal brain damage had become well established. In this early excitement it was not immediately recognized that all of the language-impairing brain damage involved the left hemisphere. Hemispheric specialization for language was totally unanticipated and, in fact, was totally out.:of-step with prior biological observations. The human brain is a paired organ with the two hemispheres, at least to gross observation, being mirror images. There are many paired organs not only in humans but through all of biology. Eyes, ears, lungs, kidneys, arms, legs, etc. are all paired but in none of these paired organs is there evidence of a major function being performed by one and not by the other. There was no reason for the 19th Century neuroscientist to imagine that the function of language was an exception. With the accumulation of additional subject matter, by Broca and others, the importance of the frontal lobe for speaking was confirmed but a striking asymmetry appeared. In 1863 Broca reported eight cases that had suffered significant language output abnormality, each of whom had
Aphasia and the lateralization of language
73
Fig. 1 - Phrenology map demonstrating the bilateral symmetry of cerebral function suggested by the early supporters of brain localization.
left frontal damage at post-mortem. The novelty of these findings impressed Broca and he cautiously stated: "Here are 8 cases where the lesion is situated in the posterior portion of the third frontal convolution... and a most remarkable thing, in all of these patients the lesion is on the left side. I do not dare make a conclusion and I await new findings". Additional cases were soon available and by 1865 Broca stated flatly: "We speak with the left hemisphere". It has been suggested (Joynt and Benton, 1964) that Broca's absolute assertion was hastened by the appearance of a paper written many years earlier by Dax (1836, 1865; Joynt and Benton, 1964) but previously unpublished. Based on the observations that right hemiplegia was far more common than left hemiplegia in patients with acquired speech disturbance (aphasia), Dax had suggested that the left hemisphere was of particular importance for language function. This observation had been presented at a local medical meeting and the statement had gone unnoted for almost 30 years. When the findings of Broca and his colleagues became known, Dax's son found the original manuscript and had it published. Sufficient evidence had thus accumulated by 1865 and Broca clearly stated that the left hemisphere was of prime importance for language.
74
D. Frank Benson
Utilizing the technique of clinical/neuropathological correlation, a number of clinicians soon corroborated Broca's findings and demonstrated additional varieties of acquired language disturbance. They presented information concerning language disturbance and, in many instances, correlated the findings with specific areas of the brain in which pathology had been found. There were disagreements concerning the exact "sites" performing specific language functions but all agreed that all sites of damage that produced aphasia were located in the left hemisphere. By the end of the 19th Century the importance (dominance) of the left cerebral hemisphere for human language function was solidly established. In addition, Dax'x original observation that language impairment was associated with paralysis of the right (preferred) hand was generally confirmed, indicating an association between handedness and language dominance. By the late 19th Century it was widely held that: (1) the left hemisphere is crucial (dominant) for language in the right-handed individual; (2) the right hemisphere is similarly important for the left-handed individual. The importance of the left hemisphere for language was so broadly accepted that terms were developed to express this importance. Dominant and non-dominant were used for the left and right hemispheres, respectively, and other terms such as major and minor, active and passive, intimated that high level brain functions such as language were the function of the left hemisphere while, for these functions, the right hemisphere served primarily as a spare, an area of brain held in reserve. Early 20th Century Background
Ongoing research in the 20th Century has tended to confound and undermine the straightforward, simplistic 19th Century views concerning the lateralization of language. Studies in the first half of the century began to question the correlation of handedness and language function. Numerous studies of brain-injured soldiers from World War I and particularly World War II (Conrad, 1949; Goodglass and Quadfasel, 1954; Russell and Espir, 1961; Walker and Jablon, 1959, 1961) only partially confirmed the rules that had been laid down. Most civilian studies (Hecaen, 1959; Ohashi, 1962; Penfield and Roberts, 1959; Roberts, 1969) presented the same general figures. Table I presents a representative selection of these studies of handedness, aphasia and side of hemispheric damage. Among right-handed individuals who suffered left hemisphere damage, between 50 and 60 percent became aphasic while about one-third of those who claimed to be left-handed became aphasic after left hemisphere damage. Only a handful (usually 1 or 2 percent) of right-handers
Aphasia and the lateratization of language
75
who sustained right hemisphere damage became aphasic and fewer than 25 percent of those said to be left-handed developed a persistent language disturbance after right hemisphere lesion. These studies suggested that a majority of left-handed individuals had language dominance in the left hemisphere. As the vast majority of humans prefer the right hand (well over 90 percent) and have left dominance for language and even those who favor the left hand also appear to have left hemisphere language dominance, the importance of the left hemisphere for language functions became even stronger; conversely, the role of the right hemisphere receded further. While the early studies can be considered crude, technical refinements later in the century have only confused the picture further. It has become necessary to state that many humans have a mixed dominance for language if the newly acquired information is to be explained. Many now agree with Annett (1978) who insists that two conditions be noted: (1) right-handedness and non right-handedness (left-handedness and ambidexterity) are the appropriate terms for describing hand preference; (2) language function is sub served primarily by the left hemisphere in the right-handed whereas a mixture of right and left hemisphere loci of language functions is the rule in the non right-handers. The prevalence of mixed dominance in non right-handers was supported by the investigations of Gloning et al. (1969, 1977) who matched the brain abnormality in non right-handed individuals who came to autopsy with similar location and type of pathology in right-handed subjects. About 80 percent of the right-handed individuals with left hemisphere lesions had shown aphasic symptomatology prior to death; none of the right-handers who had suffered right hemisphere pathology has been considered aphasic. In contrast, in the "left handed" aphasia was reported during the clinical
TABLE I
Incidence of Aphasia with Unilateral Hemisphere Lesions Left hemisphere damage
Right hemisphere damage
Right handed Left handed Right handed Left handed
Conrad (1949) Penfield and Roberts (1959) Russell and Espir (1961) Walker and Jablon (1961)
175/338 121/175
10/19 10/48
11/249
11252 31221
7/18 2/12
66/312
9124 7127
17/286
4124 0120
548/1113 49%
36/118 30%
32/1008 3%
13174 18%
1861288
Modified from D.P. Benson, Language in the left hemisphere. In D.F. Benson and E. Zaidel (Eds.), The Dual Brain: Hemispheric Specialization in Humans. New York: The Guilford Press, 1985.
76
D. Frank Benson
course in approximately 80 percent regardless of whether the right or left hemisphere was involved. These findings imply bilaterality of language function in non right-handed individuals. Thus, by the 1970s a new general rule could be suggested: (1) the left hemisphere is crucial (dominant) for language in right-handed individuals; (2) non right-handers are less definite in cerebral locus of language with some having right hemisphere language dominance, some left hemisphere language dominance, but most showing mixed (bilateral) hemispheric dominance. Additional disagreement with the fixed rule of handedness/language dominance of the 19th Century stems from other clinical studies. One notable exception, frequently quoted, is crossed aphasia, an acquired language impairment in a right-handed individual following damage to the right hemisphere. While crossed aphasia had been reported through the years (Bramwell, 1899; Clarke and Zangwill, 1965), most published cases involved individuals who had either suffered brain trauma or surgical treatment of large intracranial masses (Boller, 1973). It appeared that both hemispheres had sustained injury in these cases so the early reports of crossed aphasia only weakly supported a right hemisphere dominance for language in right-handed individuals. Nonetheless, some cases that appear to be true crossed aphasia continue to be reported (Brown and Hecaen, 1976; Brown and Wilson, 1973; Henderson, Oken and Alexander, 1981; Hindson, Westmoreland, Carroll and Bodmer, 1984; Sweet, Panis and Levine, 1984; Yarnell, 1981). While uncommon, cases of crossed aphasia represent clear exceptions to the 19th Century rule concerning hemispheric dominance and handedness. A major impetus to the investigation of right hemisphere activity in language came from the investigations of split-brain patients. A number of techniques have been devised to probe for language function in the isolated right hemisphere following section of the corpus callosum (Gazzaniga, 1970; Sperry and Gazzaniga, 1967; Zaidel, 1976) and have successfully demonstrated that the isolated right hemisphere is capable of considerable language function. The degree and type of language functions sub served by the right hemisphere remain controversial, however. As the callosal section procedure was performed only on patients with intractable epilepsy, significant cerebral abnormality was present in all subjects studied; that this cerebral pathology influenced lateralization of language functions cannot be denied. In recent years ingenious techniques have been developed to present language materials to the right hemisphere only of normal subjects (Tsunoda, 1975; Zaidel and Peters, 1981). In general, these studies confirm the split-brain findings. The right hemisphere can recognize (decode) some printed and spoken words but its ability to present (encode) language material is extremely limited. The right hemisphere recognizes many nouns, some verbs and some adjectives
Aphasia and the lateralization of language
77
but grammatical structure is not handled; imageability appears to be a major factor. The normal right hemisphere is aphasic but the language limitation is not total. Both the split-brain and the specialized unilateral language studies demonstrate that the right hemisphere is capable of some language function. Another 20th century technique has produced additional evidence of right hemisphere language function. The removal of an entire cerebral hemisphere (hemispherectomy) has provided a few patients for intensive study (Smith and Burklund, 1966). Most hemispherectomies are performed in children with intractable seizure disorder secondary to a badly damaged hemisphere; it can be questioned whether language dominance was ever established in the damaged hemisphere in these subjects. A few have been performed on right-handed adults, however, as treatment for glioblastoma. In most instances the right hemisphere was removed and aphasia, at least in the classic sense, was not produced. In a few instances, however, a language dominant left hemisphere was removed (Smith and Sugar, 1975) producing a serious aphasia. In the few left hemispherectomy subjects that survived long enough to be carefully studied (Smith, 1966), considerable language recovery has been reported. In this instance the left cortex is totally absent; any language that can be demonstrated in the post-operative period must be produced by the right hemisphere. The language recovery demonstrated is far better for comprehension (both spoken and written) than for production; in fact, the language of these subjects resembles that demonstrated for the right hemisphere of the split-brain subjects. The hemispherectomy and split-brain experience supports a possibility suggested by clinical observation, that language function can be transferred from one hemisphere to another following serious unilateral brain damage. It has long been recognized that left hemisphere damage does not produce a long lasting aphasia in children. Zangwill (1960) labeled this phenomena an "equipotentiality" of the two hemispheres in that either could perform language functions during the early, developmental years so that a shift of language competency from one hemisphere to the other is easily accomplished at a young age. Even teenagers and young adults show better language recovery after an aphasia-producing lesion than do ol<;}er individuals; and even older subjects can develop some language competency in the opposite hemisphere (Cummings, Benson, Walsh and Levine, 1979). It is generally accepted that the language skills developed by the non-dominant hemisphere are not fully normal but innumerable technical difficulties make such comparisons questionable. One rarely noted aspect that may affect language dominance concerns the educational level of the subj ect. In a single well-studied case, Wechsler
78
D. Frank Benson
(1976) reported a right-handed illiterate who became aphasic following right hemisphere cerebral vascular accident and suggested that language had not lateralized as totally as in literate subjects. Cameron and colleagues (1971) studied 65 patients with known left hemisphere cerebral vascular accidents and divided them into three groups based on their premorbid ability to comprehend written language (read): literate, semiliterate (barely able to read at a sentence level) and fully illiterate. Seventy-eight percent of the literate group and sixty-four percent of the semi-literate group became aphasic with left hemisphere damage. In the totally illiterate group, on the other hand, the findings were reversed. Only 36 percent became aphasic; 64 percent did not become aphasic following left hemisphere vascular accident. These reports suggest that formal education, even to a minimum level of semi-literacy, may influence the laterlization of language function. On the other hand, Damasio et al. (1976) reported an illiterate who became aphasic following left hemisphere lesion. Modem data concerning aphasia in illiterates is too scanty to evaluate the postulation that literacy affects the establishment of dominance for language but it should be remembered that many of the subjects reported by the 19th Century aphasiologists were illiterate and the strong tendency toward hemispheric lateralization of language function developed at that time stemmed from study of illiterate subjects. Finally, the past two decades have seen many improvements in the study of language and the correlation of aphasia with anatomical damage. New approaches and new techniques in linguistics and psycholinguistics coupled with major advances in neuropsychology have provided important advances in the investigation of language and related behaviors. Simultaneously, new techniques for the study of neuroanatomy, neurophysiology and neurochemistry have appeared, providing additional knowledge of the structural . basis of the brain. The presentation and acceptance of Geschwind's disconnection theory (1965) provided a major advance in the ability to correlate observed behaviors with neuroanatomical findings. Finally, the radical advance brought about by the new brain imaging techniques (e.g., computerized tomography, positron emission tomography, magnetic resonance imaging, etc.) makes the study of brain/ behavior correlates both easier and more accurate. Combinations of these new techniques (e.g., psycholinguistic studies correlated with brain imaging) have already provided important new evidence and promise considerable hope for the future. All of this activity, however, has produced more questions than answers. Instead of providing a firm basis for the language dominance observations of the last century, the new studies have made this relationship far less exact. The left hemisphere is not the sole seat of human language.
Aphasia and the lateralization of language
7c)
Some Current Concepts
Although recent studies demonstrate that the relationship of language and the left hemisphere is not absolute, the presence of clinical aphasia still indicates that the left hemisphere has been damaged, at least in most individuals. The questions raised by current research activities do not so much reflect changes in hemispheric language functions as they reflect changes in the definitions used. A simple but long accepted definition for aphasia is the loss or impairment of language produced by brain damage (Benson, 1979; Eisenson, 1954). The key word in this definition, and the one most open to different meanings, is language. Broca used "speech" to define this function; later "verbal images" and finally "language" were used. None of these terms is precise. The current choice, language, has a number of diverse meanings. When used to define the brain function impaired in aphasia, language can be considered the ability to use (decode and encode) a system of communication that is common to a group of individuals in an attempt to express one's ideas (Jakob son, 1964; Kertesz, 1979). Language can be separated from speech which refers only to the neuro-mechanical aspect of communication output; while this distinction is commonly accepted at present, the precise borders of the separation are not always easy to observe. In addition, language can be separated from thought, the process that integrates sensory perceptions and fund of knowledge into ideas, the material to be communicated in language. To say the least, this is a difficult separation and is infrequently attempted and even less frequently accomplished. Failure to separate language from thought, however, has led to much of the confusion that currently surrounds the term language. Too often investigators (both clinical and academic) fail to define their meaning when describing studies of language and language dysfunction. Obviously, the key to any correlation of aphasia with hemispheric lateralization lies in the meanings given for the term language. Even when carefully separated from speech and thought, language represents a complex group of activities that can be subdivided into groups of separate activities (Jakob son, 1964; Ross, 1981). Some language activities are present in higher animals; others are uniquely human. An elementary division into four types of language can be presented; each can 'be considered a true language function but not all are left hemisphere functions. The four major divisions of language are: (1) gestural (motor) language (2) prosodic (vocal) language (3) semantic (definitional) language (4) syntactic (relational) language The first two types, gestural language and prosodic language, are
80
D. Frank Benson
present in much of the higher animal kingdom. A dog readily communicates its feelings through gesture and bodily appearance; the wagging of a tail indicates friendliness whereas the raising of the neck hairs and a tensing of the body suggests fright or anger. Similarly, dogs (and many other animals) can indicate feelings of happiness, apprehension, anger, etc. by different intonations of vocal output (e.g., barking). Similar forms of communication are present in the human. Both gesture and prosody are used consistently by humans to communicate ideas and feelings. They are legitimate forms of language that make up an important, although almost universally overlooked, aspect of human communication. The other two types, semantic and syntactic language, are not present to any significant degree in the animal kingdom. One minor exception would be those few higher apes that have been trained to use visual symbol systems or gestural sign languages. Some of these animals have demonstrated a limited competency in utilizing symbols for communication (Gardner and Gardner, 1969; Premack 1971); the apes' capacity for learning these language forms is limited, however, and most animals are totally incapable of learning any semantic or syntactic language functions. In general, the semantic and syntactic aspects of language can be considered uniquely human functions. Investigations of the past decade suggest that the right hemisphere is actually dominant for some language functions in the human. Ross and colleagues (Ross, 1981; Ross and Mesulam, 1979) suggest that the right hemisphere is dominant for that part of prosodic language that expresses emotion. Ross suggests that right posterior inferior frontal damage (the right hemisphere analogue of Broca's area) can lead to an inability to express emotion through either vocal melody or gesture, a process he.calls aprosodia (1981). He also suggests (1981) that the emotional quality of a vocalization cannot be comprehended if there is damage in the posterior temporal-parietal area of the right hemisphere. While Ross' observations have not been substantiated by any large controlled study, many agree that the right hemisphere is active in both prosodic and gestural language. It is well recognized, on the other hand, that the patient with left hemisphere damage also suffers abnormalities of gestqre (Goodglass and Kaplan, 1963), a tendency toward repetitive, stereotyped and decreased quantity of gesture. Changes in prosodic language (dysprosody) also occur with some left hemisphere lesions, particularly those producing an anterior aphasia. Prosody represents a complex of features, including melody, rhythm, inflection and timbre. The most striking feature of "motor aprosodia" patients is a monotonous verbal output, a lack of melody; melody appears to be a right hemisphere function in most humans. Conversely, rhythm appears to be more of a left hemisphere function and is severely disturbed in the aphasia produced by left anterior
Aphasia and the lateralization of language
81
brain damage. Right hemispheric dominance for melody and gesture is neither simple nor clear, however. That some or all of the prosodic attributes may be dependent upon subcortical rather than cortical activities deserves careful consideration. What is clear is that both gestural and prosodic languages are complex and multifactorial and neither of these language forms is totally controlled by left hemisphere structures. Investigations of semantic language are far more supportive of the traditional presentation of left hemisphere dominance but recent evidence shows that this is not absolute. While the ability to comprehend and to present meaningful names appears more dependent upon left posterior cortical structures (e.g., posterior temporal lobe, angular gyrus), there can be little question that the right hemisphere possesses some semantic language functions. This was clearly demonstrated in the hemispherectomy studies in which the left hemisphere was removed and is also noted in the studies of split-brain patients; in both situations considerable semantic language function can be demonstrated in the right hemisphere. Studies of semantic paralexia and deep dyslexia suggest, however, that the approach to word meanings used by the right hemisphere may be quite different from that used by the left hemisphere. Deep dyslexia (Coltheart, 1980; Marshall and Newcombe, 1966) is a relatively newly coined term used to describe a type of acquired reading disorder that features semantic paralexia, the insertion of an appropriate substitute for the actual word printed (e.g., "automobile" read as "car", "rifle" as "gun", etc.). A number of theories have been developed to explain this interesting but uncommon phenomenon; one of the strongest relates to the image ability of the printed word. It has been suggested (Benson, 1985) that the right hemisphere can interpret the printed word as a visual image and then, during a stage of language recovery, can name this image. In some instances the image will be given the printed name but in others a substitute name for the visualized image will be offered, producing a semantic paralexia. Imageability is a prime criterion of the words misread in deep dyslexia and words "read" by patients with the split-brain disturbance. If imageability is accepted as a key feature it could be postulated that the interpretation of the presented word is via a phonologic-semantic route in the left hemisphere and a visual imagesemantic route in the right hemisphere. Words that are not imageable the grammatic structures and abstract words including non-imageable nouns and verbs - would not be interpreted by the right hemisphere. Observations of the split-brain and hemispherectomy patients and data from the reported cases of deep dyslexia support this interpretation. Some portions of semantic language can be interpreted by both hemispheres but phonologic interpretation and response is almost exclusively a left hemisphere function.
D. Frank Benson
82
This brings us to a final type of language, the syntactic or relational aspect. All clinical accounts (hemispherectomy, split-brain, deep dyslexia) report that this language feature is handled little or not at all by the right hemisphere. Considerable research evidence also suggests that the right hemisphere does not handle the grammatical structures of language (Zaidel, 1985; Zaidel and Peters, 1981); in addition, there is good indication, although not truly proven, that sequences of verbal material are dependent upon an intact left hemisphere and may not be handled at all by the right hemisphere (Albert, 1972; Zaidel, 1978). It would appear that the syntactic aspect of language is the most clearly lateralized of the language functions and is almost totally an activity of the left hemisphere for most humans.
Aphasia and the Lateralization of Language Functions
The language functions associated with each of the two hemispheres, at least as understood from current evidence, are presented in a tabular form in Table II. Considerable language function is carried out by each hemisphere; the only strictly left hemisphere function concerns the syntactic elements of language. Nonetheless, there are dramatic differences in prosodic language dependent upon the hemisphere involved and even more striking differences in semantic language based on the hemisphere involved. On the basis of the observations listed in Table II, the position of aphasia (as defined earlier) and the lateralization of language can be discussed. TABLE II
Language Activities of Each Hemisphere Left hemisphere
Gestural Language Prosodic Language Rhythm Inflection Timbre Melody Semantic Language Verbal Meaning Concepts Visual Meaning Syntactic Language Sequencing Relationships Grammar
+
++ + + ++ +
++ ++ ++
Right hemisphere
+ + + ++
+ ++
Aphasia and the lateralization of language
83
Since 1865 a vast amount of evidence has demonstrated that the occurrence of aphasia indicates left hemisphere damage in a great majority of instances. From this unquestionable clinical observation it was natural to consider language to be a left hemisphere function. Delineation of language functions in recent years, however, suggests that this is not entirely true; language is carried out by both hemispheres, albeit in different ways. Either aphasia must be redefined, language redefined, or the role of language impairment in aphasia reinterpreted. These possibilities will be discussed in order. A clinical diagnosis of aphasia is based on a specific set of language impairments, combinations of disorders repeatedly demonstrated for over a century and fully accepted at present. The clinical findings that make up aphasia present a solid base for ongoing observations. Conversely, the language disturbances present following right hemisphere damage have not been called aphasia. It seems appropriate to continue to accept an association between the clinical term aphasia and left hemisphere damage, at least in the vast majority of human beings. If the definition of aphasia is to be altered, it should be by clarifying what is meant by language. The definition of language is far less certain and, as has been discussed above, has been altered in recent years. It is impossible to state that language consists only of those elements that are disturbed by left hemisphere damage. Rather, language, at least as defined in an overall view, can be disordered when damage occurs in either of the hemispheres. Language, then, represents a larger group of human capabilities, not just those affected by left hemisphere damage. If language impairment is to be used to define aphasia, it is imperative that the specific language actions under the command of one or the other of the hemispheres be isolated and the language disorders in what is generally accepted to be aphasia must be outlined. Table II outlines the language features most likely to be abnormal if the left hemisphere is involved. These include syntax (the grammatical and relational aspects of language), the phonological-meaning aspect of semantics (the ability to name and to interpret names), some portions of prosody, particularly rhythm but also the articulatory and timbre qualities, and gesture. Both the prosodic and gestural types of language also suffer following right hemisphere damage and probably following subcortical damage so abnormality in these functions cannot be accepted as proof of left hemisphere disturbance. Similarly, some semantic functions appear to be in the realm of the right hemisphere (quite possibly a major aspect); careful evaluation of semantic breakdown is essential before deciding that this problem represents left hemisphere damage. In summary: aphasia appears to be a condition in which some or all of
84
D. Frank Benson
the following problems are present: (1) a disturbance in the syntactical, relational aspects of language; (2) a disturbance in the phonologicalmeaning portion of semantic elements of language; (3) a disturbance of the rhythm of verbalization, possibly complicated by alterations in the timbre and articulatory clarity; (4) a decrease in the use of gesture. With this operational definition aphasia becomes a specific set of findings and would not be.used to represent all disturbances of the qualities that make up language. There appears little doubt that our knowledge of subdivisions of language will alter in the future; it also appears quite certain that aphasia, the loss or impairment of one or more of those aspects of language described above, will continue to be an indication of left hemisphere disturbance for the clinician.
REFERENCES
ALBERT, M. L. Auditory sequencing and left cerebral dominance for language. Neuropsychologia, 10: 245-248, 1972. ANNETT, M. Genetic and non-genetic influence on handedness. Behavioral Genetics, 8: 227-249, 1978. . BENSON, D. F. Aphasia, Alexia, and Agraphia. New York: Churchill Livingstone, 1979. BENSON, D. F. Alexia. In J. A. M. Frederiks (Ed.), Handbook of Clinical Neurology, Vol. 45: Clinical Neuropsychology, 2nd. Ed. Amsterdam: Elsevier Science Publishers B. v., 1985. BOLLER, F. Destruction of Wernicke's area without language disturbance. A fresh look at crossed aphasia. Neuropsychologia, 11: 243-246, 1973. BRAMWELL, B. On crossed aphasia and the factors which go to determine whether the "leading" or "driving" speech centers shall be located in the left or in the right hemisphere of the brain. Lancet, 1: 1473-1479. 1899. BROCA, P. Remarques sur Ie siege de la faculte du langage articule, suivies d'une observation d'aphemie. Bulletin - Societe Anatomique de Paris, 2: 330-357, 186l. BROCA, P. Localisation des functions cerebrales. Siege du langage articule. Bulletin Societe Anthropologie, 4: 200, 1863. BROCA, P. Sur la faculte du 1angage articule. Bulletin -Societe Anthropologie, 6: 337-393, 1865. BROWN, J. W., and HECAEN, H. Lateralization and language representation. Neurology, 26: 183-189, 1976. BROWN, J. W., and WILSON, F. R. Crossed aphasia in a dextral. Neurology, 23: 907-911, 1973. CAMERON, R. F., CURRIER, R. D., and HAERER, A.F. Aphasia and literacy. British J oumal of Disorders of Communication, 6: 161-163, 1971. CLARKE, B., and ZANGWILL, O. A case of "crossed aphasia" in a dextral. N europsychologia, 3: 81-86, 1965. COLTHEART, M. Deep dyslexia: A review of the syndrome. In M. Coltheart, K. Patterson and J.e. Marshall (Eds.), Deep Dyslexia, London: Routledge and Kegan Paul, 1980. CONRAD, K. Uber aphasische Sprachstorungen hirnverletzten Linkshander. Nervenarzt, 20: 148-154, 1949. CUMMINGS, J.L., BENSON, D.F., WALSH, M.J., and LEVINE, H.L. Left-to-right transfer of language dominance: A case study. Neurology, 29: 1547-1549, 1979.
Aphasia and the lateralization of language
85
DAMASIO, AR., CASTRO-CALDES, A., GROSSO, J.T., and FERRO, J.M. Brain specialization for language does not depend on literacy. Archives of Neurology, 33: 300-301, 1976. DAX, M. Lesions de la moitie gauche de l'encephale coincidant avec l' oubli des signes de la pensee. Paper presented in Montpe1lier, France, 1836. DAX, M. Lesions de la moite gauche de 1'encephale coincidant avec l'oubli des signes de la pensee (lu it Montpellier en 1836). Gazette hebdomadaire de Medecine et de Chirurgie, 33: 259, 1865. EISENSON, J. Examining for Aphasia. New York: Psychological Corporation, 1954. GALL, F., and SPURZHEIM, G. The Anatomy and Physiology of the Nervous System in General and the Brain in Particular. Vols. 1-4. Paris: F. Schoell, 1810-1819. GARDNER, R.A, and GARDNER, B. Teaching sign language to a chimpanzee. Science, 165: 664-672, 1969. GAZZANIGA, M.S. The Bisected Brain. New York: Appleton-Century-Crofts, 1970. GESCHWIND, N. Disconnexion syndromes in animals and man. Brain, 88: 237-294,585644, 1965. GLONING, K. Handedness and aphasia. Neuropsychologia, 15: 355-358, 1977. GLONING, I., GLONING, K., RAUB, G., and QUATEMBER, R. Comparison of verbal behavior in right-handed and non right-handed patients with anatomically verified lesion of one hemisphere. Cortex, 5: 43-52, 1969. GOODGLASS, H., and KAPLAN, E. Disturbance of gesture and pantomime in aphasia. Brain, 86 (Part IV): 703-720, 1963. GOODGLASS, H., and QUADFASEL, F.A Language laterality in left-handed aphasics. Brain, 77: 521-548, 1954. HECAEN, H. Dominance hemispherique et preference manuelle. Evolut. Psychiat., 1: 1-50, 1959. HENDERSON, V.W., OKEN, B., and ALEXANDER, M.P. Fluent crossed aphasia with crossed Gerstmann syndrome in a right-handed man. Annals of Neurology, 10: 102, 1981. (abstract). HINDSON, D.A, WESTMORELAND, D.E., CARROLL, W.A, and BODMER, B.A. Persistent Broca's aphasia after right cerebral infarction in a right-hander. Neurology, 34: 387389, 1984. JAKOBSON, R. Towards a linguistic typology of aphasic impairments. In AV.S. deReuck and M. O'Connor (Eds.), Disorders of Language. Boston: Little and Brown, 1964. JOYNT, R.J., and BENTON, AL. The memoir of Marc Dax on aphasia. Neurology, 14: 851-854, 1964. KERTESZ, A Aphasia and Associated Disorders. New York: Grune and Stratton, 1979. MARSHALL, J.e., and NEWCOMBE, F. Syntactic and semantic errors in paralexia. Neuropsychologia, 4: 169-176, 1966. OHASHI, H. Aphasia, apraxia, agnosia: The problem of cerebral dominance. Psychiatr. Neurol. Jap., 64: 890-896, 1962. PENFIELD, W., and ROBERTS, L. Speech and Brain-Mechanisms. Princeton: Princeton University Press, 1959. PREMACK, D. Language in the chimpanzee. Science, 172: 808-822, 1971. ROBERTS, L. Aphasia, apraxia and agnosia in abnormal states of cerebral dominance. In P.J. Vinken and G.W. Bruyn (Eds.), Handbook of Clinical Neurology, Vol. 4. Amsterdam: North Holland, 1969. Ross, E.D. The aprosodias: Functional-anatomic organization of the affective components of language in the right hemisphere. Archives of Neurology, 38: 561-569, 1981. Ross, E.D., and MESULAM, M.M. Dominant language functions of the right hemisphere? Prosody and emotional gesturing. Archives of Neurology, 36: 144-148, 1979. RUSSELL, W.R., and ESPIR, M.L.E. Traumatic Aphasia - A Study of Aphasia in War Wounds of the Brain. London: Oxford University Press, 1961. SMITH, A Speech and other functions after left dominant hemispherectomy. Journal of Neurology, Neurosurgery and Psychiatry, 29: 467-471, 1966.
86
D. Frank Benson,
SMITH, A., and BURKLUND, C.W. Dominant hemispherectomy. Science, 153: 1280, 1966. SMITH, A, and SUGAR, O. Development of above-normal language and intelligence 21 years after left hemispherectomy. Neurology, 25: 813-818, 1975. SPERRY, R.W., and GAZZANIGA, M.S. Language following surgical disconnection of the hemispheres. In F.L. Darley (Ed.), Brain Mechanisms Underlying Speech and Language. New York, Grone and Stratton, 1967. SWEET, E.W.S., PANIS, W., and LEVINE, D.N. Crossed Wernicke's aphasia. Neurology, 34: 475-479, 1984. TSUNODA, T. Functional differences between right and left cerebral hemispheres detected by the key tapping method. Brain and Language, 2: 152-170, 1975. WALKER, AE., and JABLON, S. A follow-up of head injured men of World War II. Journal of Neurosurgery, 16: 600-610, 1959. WALKER, AE., and JABLON, S. A follow-up study of head wounds in World War II. VA Medical Monograph. Washington, D.C., U.S. Government Printing Office, 1961. WECHSLER, A Crossed aphasia in an illiterate dextral. Brain and Language, 3: 164-172, 1976. YARNELL, P.R. Crossed dextral aphasia: a clinical radiological correlation. Brain and Language, 12: 128-139, 1981. ZAJDEL, E. Auditory vocabulary of the right hemisphere after brain bisection or hemidecortication. In P.H. Buser and A Rougeul-Buser (Eds.), Cerebral Correlates of Conscious Experience. Amsterdam: Elsevier, 1978. ZAJDEL, E. Right hemisphere language. In D.F. Benson and E. Zaidel (Eds.), The Dual Brain: Hemispheric Specialization in Humans. New York: The Guilford Press, 1985. ZAJDEL, E., and PETERS, AM. Phonological encoding and ideographic reading by the disconnected right hemisphere: Two case studies. Brain and Language, 14: 205-234, 1981. ZANGWILL, O.L. Cerebral Dominance and its Relation to Psychological Function Springfield, Illinois: Charles Thomas, 1960. D. Frank Benson, M.D., The Augustus S. Rose Professor of Neurology, UCLA School of Medicine, 710 Westwood Plaza, Los Angeles, CA. 90024, (213) 825-9873.
A major interest throughout the investigative career of Norman Geschwind concerned asymmetries of the cerebral hemispheres and the significance of these anatomical asymmetries for human behavior. The most dramatic functional example is, of course, human language, a phenomenon that occupied an important part of Geschwind's efforts. In this essay some contemporary investigations are viewed against the original conc~s of hemispheric specialization for language in an attempt to clarify our concepts of hemispheric asymmetries of language functions.
One of the most striking curiosities in all of biology concerns the strong hemispheric lateralization for language that is present in most humans - the dominance of the left hemisphere for language. It has been the study of aphasia, the loss or impairment of language caused by brain damage, that originally and still best demonstrates this striking curiosity. The data from clinical observations of aphasia patients is so overwhelming that no one questions the statement that the left hemisphere is crucial for language functions. On the other hand, recent research suggests that the right hemisphere is also capable of performing language functions; the left hemisphere is not alone in subserving language. Do we truly have language in both hemispheres? Is right hemisphere language function similar, modified, or distinct from left hemisphere language? Is the evidence from the study of aphasia biased? Have we· allowed the obvious language dysfunctions of aphasia to mislead us in considerations of the cerebral locus of language functions? The status of hemispheric specialization for language has been changing and the findings of aphasia investigation in this state of flux deserve reappraisal. Historical Background It can be truly stated that the correlation of hemispheric lateralization and aphasia stems from the work of Broca. Prior to Broca's initial presentation (1861), there had been serious scientific debate concerning Cortex (1986) 22, 71-86
72
D. Frank Benson
cerebral function but the disagreement revolved about whether the brain operated as a single, holistic unit (similar to the liver or the lungs) or with separate areas of the brain subserving separate mental functions. The phrenologist Gall (1810) had proposed a detailed breakdown of brain functions with separate areas of the brain cortex performing specific mental attributes. Gall's choice of focal mental functions is no longer acceptable and all agree that he was excessive in their localization; nonetheless, despite the exorbitance of his claims, Gall never went so far as to suggest that a given function was sub served by one hemisphere only. All proposed attributes were considered bilateral (Figure 1). Gall's proposal of localization of function within the brain produced disagreement in the early part of the 19th Century; some investigators supported the localization of psychological functions, including "speech", but most supported an holistic approach in which behavioral responses demanded action of the entire brain. Against this background, Broca (1861) demonstrated an individual who had lost "speech" and who, at post-mortem, had a focal brain lesion. Speech (language) appeared to be under the control of a limited area of the brain. While the controversy about the localization of language to a given segment of the brain was not settled, Broca's major contribution, the introduction of a new research tool in which observed behavioral abnormality was corelated with gross anatomical studies of brain lesions, was immediately accepted. Behavioral/ anatomical correlations could be conducted in many laboratories and were immediately undertaken. A major advance had occurred in neuroscience. Withinjust a few years many cases of language impairment had been correlated with focal brain lesions, some supporting the localization demonstrated by Broca, others in disagreement, but the occurrence of aphasia with focal brain damage had become well established. In this early excitement it was not immediately recognized that all of the language-impairing brain damage involved the left hemisphere. Hemispheric specialization for language was totally unanticipated and, in fact, was totally out.:of-step with prior biological observations. The human brain is a paired organ with the two hemispheres, at least to gross observation, being mirror images. There are many paired organs not only in humans but through all of biology. Eyes, ears, lungs, kidneys, arms, legs, etc. are all paired but in none of these paired organs is there evidence of a major function being performed by one and not by the other. There was no reason for the 19th Century neuroscientist to imagine that the function of language was an exception. With the accumulation of additional subject matter, by Broca and others, the importance of the frontal lobe for speaking was confirmed but a striking asymmetry appeared. In 1863 Broca reported eight cases that had suffered significant language output abnormality, each of whom had
Aphasia and the lateralization of language
73
Fig. 1 - Phrenology map demonstrating the bilateral symmetry of cerebral function suggested by the early supporters of brain localization.
left frontal damage at post-mortem. The novelty of these findings impressed Broca and he cautiously stated: "Here are 8 cases where the lesion is situated in the posterior portion of the third frontal convolution... and a most remarkable thing, in all of these patients the lesion is on the left side. I do not dare make a conclusion and I await new findings". Additional cases were soon available and by 1865 Broca stated flatly: "We speak with the left hemisphere". It has been suggested (Joynt and Benton, 1964) that Broca's absolute assertion was hastened by the appearance of a paper written many years earlier by Dax (1836, 1865; Joynt and Benton, 1964) but previously unpublished. Based on the observations that right hemiplegia was far more common than left hemiplegia in patients with acquired speech disturbance (aphasia), Dax had suggested that the left hemisphere was of particular importance for language function. This observation had been presented at a local medical meeting and the statement had gone unnoted for almost 30 years. When the findings of Broca and his colleagues became known, Dax's son found the original manuscript and had it published. Sufficient evidence had thus accumulated by 1865 and Broca clearly stated that the left hemisphere was of prime importance for language.
74
D. Frank Benson
Utilizing the technique of clinical/neuropathological correlation, a number of clinicians soon corroborated Broca's findings and demonstrated additional varieties of acquired language disturbance. They presented information concerning language disturbance and, in many instances, correlated the findings with specific areas of the brain in which pathology had been found. There were disagreements concerning the exact "sites" performing specific language functions but all agreed that all sites of damage that produced aphasia were located in the left hemisphere. By the end of the 19th Century the importance (dominance) of the left cerebral hemisphere for human language function was solidly established. In addition, Dax'x original observation that language impairment was associated with paralysis of the right (preferred) hand was generally confirmed, indicating an association between handedness and language dominance. By the late 19th Century it was widely held that: (1) the left hemisphere is crucial (dominant) for language in the right-handed individual; (2) the right hemisphere is similarly important for the left-handed individual. The importance of the left hemisphere for language was so broadly accepted that terms were developed to express this importance. Dominant and non-dominant were used for the left and right hemispheres, respectively, and other terms such as major and minor, active and passive, intimated that high level brain functions such as language were the function of the left hemisphere while, for these functions, the right hemisphere served primarily as a spare, an area of brain held in reserve. Early 20th Century Background
Ongoing research in the 20th Century has tended to confound and undermine the straightforward, simplistic 19th Century views concerning the lateralization of language. Studies in the first half of the century began to question the correlation of handedness and language function. Numerous studies of brain-injured soldiers from World War I and particularly World War II (Conrad, 1949; Goodglass and Quadfasel, 1954; Russell and Espir, 1961; Walker and Jablon, 1959, 1961) only partially confirmed the rules that had been laid down. Most civilian studies (Hecaen, 1959; Ohashi, 1962; Penfield and Roberts, 1959; Roberts, 1969) presented the same general figures. Table I presents a representative selection of these studies of handedness, aphasia and side of hemispheric damage. Among right-handed individuals who suffered left hemisphere damage, between 50 and 60 percent became aphasic while about one-third of those who claimed to be left-handed became aphasic after left hemisphere damage. Only a handful (usually 1 or 2 percent) of right-handers
Aphasia and the lateratization of language
75
who sustained right hemisphere damage became aphasic and fewer than 25 percent of those said to be left-handed developed a persistent language disturbance after right hemisphere lesion. These studies suggested that a majority of left-handed individuals had language dominance in the left hemisphere. As the vast majority of humans prefer the right hand (well over 90 percent) and have left dominance for language and even those who favor the left hand also appear to have left hemisphere language dominance, the importance of the left hemisphere for language functions became even stronger; conversely, the role of the right hemisphere receded further. While the early studies can be considered crude, technical refinements later in the century have only confused the picture further. It has become necessary to state that many humans have a mixed dominance for language if the newly acquired information is to be explained. Many now agree with Annett (1978) who insists that two conditions be noted: (1) right-handedness and non right-handedness (left-handedness and ambidexterity) are the appropriate terms for describing hand preference; (2) language function is sub served primarily by the left hemisphere in the right-handed whereas a mixture of right and left hemisphere loci of language functions is the rule in the non right-handers. The prevalence of mixed dominance in non right-handers was supported by the investigations of Gloning et al. (1969, 1977) who matched the brain abnormality in non right-handed individuals who came to autopsy with similar location and type of pathology in right-handed subjects. About 80 percent of the right-handed individuals with left hemisphere lesions had shown aphasic symptomatology prior to death; none of the right-handers who had suffered right hemisphere pathology has been considered aphasic. In contrast, in the "left handed" aphasia was reported during the clinical
TABLE I
Incidence of Aphasia with Unilateral Hemisphere Lesions Left hemisphere damage
Right hemisphere damage
Right handed Left handed Right handed Left handed
Conrad (1949) Penfield and Roberts (1959) Russell and Espir (1961) Walker and Jablon (1961)
175/338 121/175
10/19 10/48
11/249
11252 31221
7/18 2/12
66/312
9124 7127
17/286
4124 0120
548/1113 49%
36/118 30%
32/1008 3%
13174 18%
1861288
Modified from D.P. Benson, Language in the left hemisphere. In D.F. Benson and E. Zaidel (Eds.), The Dual Brain: Hemispheric Specialization in Humans. New York: The Guilford Press, 1985.
76
D. Frank Benson
course in approximately 80 percent regardless of whether the right or left hemisphere was involved. These findings imply bilaterality of language function in non right-handed individuals. Thus, by the 1970s a new general rule could be suggested: (1) the left hemisphere is crucial (dominant) for language in right-handed individuals; (2) non right-handers are less definite in cerebral locus of language with some having right hemisphere language dominance, some left hemisphere language dominance, but most showing mixed (bilateral) hemispheric dominance. Additional disagreement with the fixed rule of handedness/language dominance of the 19th Century stems from other clinical studies. One notable exception, frequently quoted, is crossed aphasia, an acquired language impairment in a right-handed individual following damage to the right hemisphere. While crossed aphasia had been reported through the years (Bramwell, 1899; Clarke and Zangwill, 1965), most published cases involved individuals who had either suffered brain trauma or surgical treatment of large intracranial masses (Boller, 1973). It appeared that both hemispheres had sustained injury in these cases so the early reports of crossed aphasia only weakly supported a right hemisphere dominance for language in right-handed individuals. Nonetheless, some cases that appear to be true crossed aphasia continue to be reported (Brown and Hecaen, 1976; Brown and Wilson, 1973; Henderson, Oken and Alexander, 1981; Hindson, Westmoreland, Carroll and Bodmer, 1984; Sweet, Panis and Levine, 1984; Yarnell, 1981). While uncommon, cases of crossed aphasia represent clear exceptions to the 19th Century rule concerning hemispheric dominance and handedness. A major impetus to the investigation of right hemisphere activity in language came from the investigations of split-brain patients. A number of techniques have been devised to probe for language function in the isolated right hemisphere following section of the corpus callosum (Gazzaniga, 1970; Sperry and Gazzaniga, 1967; Zaidel, 1976) and have successfully demonstrated that the isolated right hemisphere is capable of considerable language function. The degree and type of language functions sub served by the right hemisphere remain controversial, however. As the callosal section procedure was performed only on patients with intractable epilepsy, significant cerebral abnormality was present in all subjects studied; that this cerebral pathology influenced lateralization of language functions cannot be denied. In recent years ingenious techniques have been developed to present language materials to the right hemisphere only of normal subjects (Tsunoda, 1975; Zaidel and Peters, 1981). In general, these studies confirm the split-brain findings. The right hemisphere can recognize (decode) some printed and spoken words but its ability to present (encode) language material is extremely limited. The right hemisphere recognizes many nouns, some verbs and some adjectives
Aphasia and the lateralization of language
77
but grammatical structure is not handled; imageability appears to be a major factor. The normal right hemisphere is aphasic but the language limitation is not total. Both the split-brain and the specialized unilateral language studies demonstrate that the right hemisphere is capable of some language function. Another 20th century technique has produced additional evidence of right hemisphere language function. The removal of an entire cerebral hemisphere (hemispherectomy) has provided a few patients for intensive study (Smith and Burklund, 1966). Most hemispherectomies are performed in children with intractable seizure disorder secondary to a badly damaged hemisphere; it can be questioned whether language dominance was ever established in the damaged hemisphere in these subjects. A few have been performed on right-handed adults, however, as treatment for glioblastoma. In most instances the right hemisphere was removed and aphasia, at least in the classic sense, was not produced. In a few instances, however, a language dominant left hemisphere was removed (Smith and Sugar, 1975) producing a serious aphasia. In the few left hemispherectomy subjects that survived long enough to be carefully studied (Smith, 1966), considerable language recovery has been reported. In this instance the left cortex is totally absent; any language that can be demonstrated in the post-operative period must be produced by the right hemisphere. The language recovery demonstrated is far better for comprehension (both spoken and written) than for production; in fact, the language of these subjects resembles that demonstrated for the right hemisphere of the split-brain subjects. The hemispherectomy and split-brain experience supports a possibility suggested by clinical observation, that language function can be transferred from one hemisphere to another following serious unilateral brain damage. It has long been recognized that left hemisphere damage does not produce a long lasting aphasia in children. Zangwill (1960) labeled this phenomena an "equipotentiality" of the two hemispheres in that either could perform language functions during the early, developmental years so that a shift of language competency from one hemisphere to the other is easily accomplished at a young age. Even teenagers and young adults show better language recovery after an aphasia-producing lesion than do ol<;}er individuals; and even older subjects can develop some language competency in the opposite hemisphere (Cummings, Benson, Walsh and Levine, 1979). It is generally accepted that the language skills developed by the non-dominant hemisphere are not fully normal but innumerable technical difficulties make such comparisons questionable. One rarely noted aspect that may affect language dominance concerns the educational level of the subj ect. In a single well-studied case, Wechsler
78
D. Frank Benson
(1976) reported a right-handed illiterate who became aphasic following right hemisphere cerebral vascular accident and suggested that language had not lateralized as totally as in literate subjects. Cameron and colleagues (1971) studied 65 patients with known left hemisphere cerebral vascular accidents and divided them into three groups based on their premorbid ability to comprehend written language (read): literate, semiliterate (barely able to read at a sentence level) and fully illiterate. Seventy-eight percent of the literate group and sixty-four percent of the semi-literate group became aphasic with left hemisphere damage. In the totally illiterate group, on the other hand, the findings were reversed. Only 36 percent became aphasic; 64 percent did not become aphasic following left hemisphere vascular accident. These reports suggest that formal education, even to a minimum level of semi-literacy, may influence the laterlization of language function. On the other hand, Damasio et al. (1976) reported an illiterate who became aphasic following left hemisphere lesion. Modem data concerning aphasia in illiterates is too scanty to evaluate the postulation that literacy affects the establishment of dominance for language but it should be remembered that many of the subjects reported by the 19th Century aphasiologists were illiterate and the strong tendency toward hemispheric lateralization of language function developed at that time stemmed from study of illiterate subjects. Finally, the past two decades have seen many improvements in the study of language and the correlation of aphasia with anatomical damage. New approaches and new techniques in linguistics and psycholinguistics coupled with major advances in neuropsychology have provided important advances in the investigation of language and related behaviors. Simultaneously, new techniques for the study of neuroanatomy, neurophysiology and neurochemistry have appeared, providing additional knowledge of the structural . basis of the brain. The presentation and acceptance of Geschwind's disconnection theory (1965) provided a major advance in the ability to correlate observed behaviors with neuroanatomical findings. Finally, the radical advance brought about by the new brain imaging techniques (e.g., computerized tomography, positron emission tomography, magnetic resonance imaging, etc.) makes the study of brain/ behavior correlates both easier and more accurate. Combinations of these new techniques (e.g., psycholinguistic studies correlated with brain imaging) have already provided important new evidence and promise considerable hope for the future. All of this activity, however, has produced more questions than answers. Instead of providing a firm basis for the language dominance observations of the last century, the new studies have made this relationship far less exact. The left hemisphere is not the sole seat of human language.
Aphasia and the lateralization of language
7c)
Some Current Concepts
Although recent studies demonstrate that the relationship of language and the left hemisphere is not absolute, the presence of clinical aphasia still indicates that the left hemisphere has been damaged, at least in most individuals. The questions raised by current research activities do not so much reflect changes in hemispheric language functions as they reflect changes in the definitions used. A simple but long accepted definition for aphasia is the loss or impairment of language produced by brain damage (Benson, 1979; Eisenson, 1954). The key word in this definition, and the one most open to different meanings, is language. Broca used "speech" to define this function; later "verbal images" and finally "language" were used. None of these terms is precise. The current choice, language, has a number of diverse meanings. When used to define the brain function impaired in aphasia, language can be considered the ability to use (decode and encode) a system of communication that is common to a group of individuals in an attempt to express one's ideas (Jakob son, 1964; Kertesz, 1979). Language can be separated from speech which refers only to the neuro-mechanical aspect of communication output; while this distinction is commonly accepted at present, the precise borders of the separation are not always easy to observe. In addition, language can be separated from thought, the process that integrates sensory perceptions and fund of knowledge into ideas, the material to be communicated in language. To say the least, this is a difficult separation and is infrequently attempted and even less frequently accomplished. Failure to separate language from thought, however, has led to much of the confusion that currently surrounds the term language. Too often investigators (both clinical and academic) fail to define their meaning when describing studies of language and language dysfunction. Obviously, the key to any correlation of aphasia with hemispheric lateralization lies in the meanings given for the term language. Even when carefully separated from speech and thought, language represents a complex group of activities that can be subdivided into groups of separate activities (Jakob son, 1964; Ross, 1981). Some language activities are present in higher animals; others are uniquely human. An elementary division into four types of language can be presented; each can 'be considered a true language function but not all are left hemisphere functions. The four major divisions of language are: (1) gestural (motor) language (2) prosodic (vocal) language (3) semantic (definitional) language (4) syntactic (relational) language The first two types, gestural language and prosodic language, are
80
D. Frank Benson
present in much of the higher animal kingdom. A dog readily communicates its feelings through gesture and bodily appearance; the wagging of a tail indicates friendliness whereas the raising of the neck hairs and a tensing of the body suggests fright or anger. Similarly, dogs (and many other animals) can indicate feelings of happiness, apprehension, anger, etc. by different intonations of vocal output (e.g., barking). Similar forms of communication are present in the human. Both gesture and prosody are used consistently by humans to communicate ideas and feelings. They are legitimate forms of language that make up an important, although almost universally overlooked, aspect of human communication. The other two types, semantic and syntactic language, are not present to any significant degree in the animal kingdom. One minor exception would be those few higher apes that have been trained to use visual symbol systems or gestural sign languages. Some of these animals have demonstrated a limited competency in utilizing symbols for communication (Gardner and Gardner, 1969; Premack 1971); the apes' capacity for learning these language forms is limited, however, and most animals are totally incapable of learning any semantic or syntactic language functions. In general, the semantic and syntactic aspects of language can be considered uniquely human functions. Investigations of the past decade suggest that the right hemisphere is actually dominant for some language functions in the human. Ross and colleagues (Ross, 1981; Ross and Mesulam, 1979) suggest that the right hemisphere is dominant for that part of prosodic language that expresses emotion. Ross suggests that right posterior inferior frontal damage (the right hemisphere analogue of Broca's area) can lead to an inability to express emotion through either vocal melody or gesture, a process he.calls aprosodia (1981). He also suggests (1981) that the emotional quality of a vocalization cannot be comprehended if there is damage in the posterior temporal-parietal area of the right hemisphere. While Ross' observations have not been substantiated by any large controlled study, many agree that the right hemisphere is active in both prosodic and gestural language. It is well recognized, on the other hand, that the patient with left hemisphere damage also suffers abnormalities of gestqre (Goodglass and Kaplan, 1963), a tendency toward repetitive, stereotyped and decreased quantity of gesture. Changes in prosodic language (dysprosody) also occur with some left hemisphere lesions, particularly those producing an anterior aphasia. Prosody represents a complex of features, including melody, rhythm, inflection and timbre. The most striking feature of "motor aprosodia" patients is a monotonous verbal output, a lack of melody; melody appears to be a right hemisphere function in most humans. Conversely, rhythm appears to be more of a left hemisphere function and is severely disturbed in the aphasia produced by left anterior
Aphasia and the lateralization of language
81
brain damage. Right hemispheric dominance for melody and gesture is neither simple nor clear, however. That some or all of the prosodic attributes may be dependent upon subcortical rather than cortical activities deserves careful consideration. What is clear is that both gestural and prosodic languages are complex and multifactorial and neither of these language forms is totally controlled by left hemisphere structures. Investigations of semantic language are far more supportive of the traditional presentation of left hemisphere dominance but recent evidence shows that this is not absolute. While the ability to comprehend and to present meaningful names appears more dependent upon left posterior cortical structures (e.g., posterior temporal lobe, angular gyrus), there can be little question that the right hemisphere possesses some semantic language functions. This was clearly demonstrated in the hemispherectomy studies in which the left hemisphere was removed and is also noted in the studies of split-brain patients; in both situations considerable semantic language function can be demonstrated in the right hemisphere. Studies of semantic paralexia and deep dyslexia suggest, however, that the approach to word meanings used by the right hemisphere may be quite different from that used by the left hemisphere. Deep dyslexia (Coltheart, 1980; Marshall and Newcombe, 1966) is a relatively newly coined term used to describe a type of acquired reading disorder that features semantic paralexia, the insertion of an appropriate substitute for the actual word printed (e.g., "automobile" read as "car", "rifle" as "gun", etc.). A number of theories have been developed to explain this interesting but uncommon phenomenon; one of the strongest relates to the image ability of the printed word. It has been suggested (Benson, 1985) that the right hemisphere can interpret the printed word as a visual image and then, during a stage of language recovery, can name this image. In some instances the image will be given the printed name but in others a substitute name for the visualized image will be offered, producing a semantic paralexia. Imageability is a prime criterion of the words misread in deep dyslexia and words "read" by patients with the split-brain disturbance. If imageability is accepted as a key feature it could be postulated that the interpretation of the presented word is via a phonologic-semantic route in the left hemisphere and a visual imagesemantic route in the right hemisphere. Words that are not imageable the grammatic structures and abstract words including non-imageable nouns and verbs - would not be interpreted by the right hemisphere. Observations of the split-brain and hemispherectomy patients and data from the reported cases of deep dyslexia support this interpretation. Some portions of semantic language can be interpreted by both hemispheres but phonologic interpretation and response is almost exclusively a left hemisphere function.
D. Frank Benson
82
This brings us to a final type of language, the syntactic or relational aspect. All clinical accounts (hemispherectomy, split-brain, deep dyslexia) report that this language feature is handled little or not at all by the right hemisphere. Considerable research evidence also suggests that the right hemisphere does not handle the grammatical structures of language (Zaidel, 1985; Zaidel and Peters, 1981); in addition, there is good indication, although not truly proven, that sequences of verbal material are dependent upon an intact left hemisphere and may not be handled at all by the right hemisphere (Albert, 1972; Zaidel, 1978). It would appear that the syntactic aspect of language is the most clearly lateralized of the language functions and is almost totally an activity of the left hemisphere for most humans.
Aphasia and the Lateralization of Language Functions
The language functions associated with each of the two hemispheres, at least as understood from current evidence, are presented in a tabular form in Table II. Considerable language function is carried out by each hemisphere; the only strictly left hemisphere function concerns the syntactic elements of language. Nonetheless, there are dramatic differences in prosodic language dependent upon the hemisphere involved and even more striking differences in semantic language based on the hemisphere involved. On the basis of the observations listed in Table II, the position of aphasia (as defined earlier) and the lateralization of language can be discussed. TABLE II
Language Activities of Each Hemisphere Left hemisphere
Gestural Language Prosodic Language Rhythm Inflection Timbre Melody Semantic Language Verbal Meaning Concepts Visual Meaning Syntactic Language Sequencing Relationships Grammar
+
++ + + ++ +
++ ++ ++
Right hemisphere
+ + + ++
+ ++
Aphasia and the lateralization of language
83
Since 1865 a vast amount of evidence has demonstrated that the occurrence of aphasia indicates left hemisphere damage in a great majority of instances. From this unquestionable clinical observation it was natural to consider language to be a left hemisphere function. Delineation of language functions in recent years, however, suggests that this is not entirely true; language is carried out by both hemispheres, albeit in different ways. Either aphasia must be redefined, language redefined, or the role of language impairment in aphasia reinterpreted. These possibilities will be discussed in order. A clinical diagnosis of aphasia is based on a specific set of language impairments, combinations of disorders repeatedly demonstrated for over a century and fully accepted at present. The clinical findings that make up aphasia present a solid base for ongoing observations. Conversely, the language disturbances present following right hemisphere damage have not been called aphasia. It seems appropriate to continue to accept an association between the clinical term aphasia and left hemisphere damage, at least in the vast majority of human beings. If the definition of aphasia is to be altered, it should be by clarifying what is meant by language. The definition of language is far less certain and, as has been discussed above, has been altered in recent years. It is impossible to state that language consists only of those elements that are disturbed by left hemisphere damage. Rather, language, at least as defined in an overall view, can be disordered when damage occurs in either of the hemispheres. Language, then, represents a larger group of human capabilities, not just those affected by left hemisphere damage. If language impairment is to be used to define aphasia, it is imperative that the specific language actions under the command of one or the other of the hemispheres be isolated and the language disorders in what is generally accepted to be aphasia must be outlined. Table II outlines the language features most likely to be abnormal if the left hemisphere is involved. These include syntax (the grammatical and relational aspects of language), the phonological-meaning aspect of semantics (the ability to name and to interpret names), some portions of prosody, particularly rhythm but also the articulatory and timbre qualities, and gesture. Both the prosodic and gestural types of language also suffer following right hemisphere damage and probably following subcortical damage so abnormality in these functions cannot be accepted as proof of left hemisphere disturbance. Similarly, some semantic functions appear to be in the realm of the right hemisphere (quite possibly a major aspect); careful evaluation of semantic breakdown is essential before deciding that this problem represents left hemisphere damage. In summary: aphasia appears to be a condition in which some or all of
84
D. Frank Benson
the following problems are present: (1) a disturbance in the syntactical, relational aspects of language; (2) a disturbance in the phonologicalmeaning portion of semantic elements of language; (3) a disturbance of the rhythm of verbalization, possibly complicated by alterations in the timbre and articulatory clarity; (4) a decrease in the use of gesture. With this operational definition aphasia becomes a specific set of findings and would not be.used to represent all disturbances of the qualities that make up language. There appears little doubt that our knowledge of subdivisions of language will alter in the future; it also appears quite certain that aphasia, the loss or impairment of one or more of those aspects of language described above, will continue to be an indication of left hemisphere disturbance for the clinician.
REFERENCES
ALBERT, M. L. Auditory sequencing and left cerebral dominance for language. Neuropsychologia, 10: 245-248, 1972. ANNETT, M. Genetic and non-genetic influence on handedness. Behavioral Genetics, 8: 227-249, 1978. . BENSON, D. F. Aphasia, Alexia, and Agraphia. New York: Churchill Livingstone, 1979. BENSON, D. F. Alexia. In J. A. M. Frederiks (Ed.), Handbook of Clinical Neurology, Vol. 45: Clinical Neuropsychology, 2nd. Ed. Amsterdam: Elsevier Science Publishers B. v., 1985. BOLLER, F. Destruction of Wernicke's area without language disturbance. A fresh look at crossed aphasia. Neuropsychologia, 11: 243-246, 1973. BRAMWELL, B. On crossed aphasia and the factors which go to determine whether the "leading" or "driving" speech centers shall be located in the left or in the right hemisphere of the brain. Lancet, 1: 1473-1479. 1899. BROCA, P. Remarques sur Ie siege de la faculte du langage articule, suivies d'une observation d'aphemie. Bulletin - Societe Anatomique de Paris, 2: 330-357, 186l. BROCA, P. Localisation des functions cerebrales. Siege du langage articule. Bulletin Societe Anthropologie, 4: 200, 1863. BROCA, P. Sur la faculte du 1angage articule. Bulletin -Societe Anthropologie, 6: 337-393, 1865. BROWN, J. W., and HECAEN, H. Lateralization and language representation. Neurology, 26: 183-189, 1976. BROWN, J. W., and WILSON, F. R. Crossed aphasia in a dextral. Neurology, 23: 907-911, 1973. CAMERON, R. F., CURRIER, R. D., and HAERER, A.F. Aphasia and literacy. British J oumal of Disorders of Communication, 6: 161-163, 1971. CLARKE, B., and ZANGWILL, O. A case of "crossed aphasia" in a dextral. N europsychologia, 3: 81-86, 1965. COLTHEART, M. Deep dyslexia: A review of the syndrome. In M. Coltheart, K. Patterson and J.e. Marshall (Eds.), Deep Dyslexia, London: Routledge and Kegan Paul, 1980. CONRAD, K. Uber aphasische Sprachstorungen hirnverletzten Linkshander. Nervenarzt, 20: 148-154, 1949. CUMMINGS, J.L., BENSON, D.F., WALSH, M.J., and LEVINE, H.L. Left-to-right transfer of language dominance: A case study. Neurology, 29: 1547-1549, 1979.
Aphasia and the lateralization of language
85
DAMASIO, AR., CASTRO-CALDES, A., GROSSO, J.T., and FERRO, J.M. Brain specialization for language does not depend on literacy. Archives of Neurology, 33: 300-301, 1976. DAX, M. Lesions de la moitie gauche de l'encephale coincidant avec l' oubli des signes de la pensee. Paper presented in Montpe1lier, France, 1836. DAX, M. Lesions de la moite gauche de 1'encephale coincidant avec l'oubli des signes de la pensee (lu it Montpellier en 1836). Gazette hebdomadaire de Medecine et de Chirurgie, 33: 259, 1865. EISENSON, J. Examining for Aphasia. New York: Psychological Corporation, 1954. GALL, F., and SPURZHEIM, G. The Anatomy and Physiology of the Nervous System in General and the Brain in Particular. Vols. 1-4. Paris: F. Schoell, 1810-1819. GARDNER, R.A, and GARDNER, B. Teaching sign language to a chimpanzee. Science, 165: 664-672, 1969. GAZZANIGA, M.S. The Bisected Brain. New York: Appleton-Century-Crofts, 1970. GESCHWIND, N. Disconnexion syndromes in animals and man. Brain, 88: 237-294,585644, 1965. GLONING, K. Handedness and aphasia. Neuropsychologia, 15: 355-358, 1977. GLONING, I., GLONING, K., RAUB, G., and QUATEMBER, R. Comparison of verbal behavior in right-handed and non right-handed patients with anatomically verified lesion of one hemisphere. Cortex, 5: 43-52, 1969. GOODGLASS, H., and KAPLAN, E. Disturbance of gesture and pantomime in aphasia. Brain, 86 (Part IV): 703-720, 1963. GOODGLASS, H., and QUADFASEL, F.A Language laterality in left-handed aphasics. Brain, 77: 521-548, 1954. HECAEN, H. Dominance hemispherique et preference manuelle. Evolut. Psychiat., 1: 1-50, 1959. HENDERSON, V.W., OKEN, B., and ALEXANDER, M.P. Fluent crossed aphasia with crossed Gerstmann syndrome in a right-handed man. Annals of Neurology, 10: 102, 1981. (abstract). HINDSON, D.A, WESTMORELAND, D.E., CARROLL, W.A, and BODMER, B.A. Persistent Broca's aphasia after right cerebral infarction in a right-hander. Neurology, 34: 387389, 1984. JAKOBSON, R. Towards a linguistic typology of aphasic impairments. In AV.S. deReuck and M. O'Connor (Eds.), Disorders of Language. Boston: Little and Brown, 1964. JOYNT, R.J., and BENTON, AL. The memoir of Marc Dax on aphasia. Neurology, 14: 851-854, 1964. KERTESZ, A Aphasia and Associated Disorders. New York: Grune and Stratton, 1979. MARSHALL, J.e., and NEWCOMBE, F. Syntactic and semantic errors in paralexia. Neuropsychologia, 4: 169-176, 1966. OHASHI, H. Aphasia, apraxia, agnosia: The problem of cerebral dominance. Psychiatr. Neurol. Jap., 64: 890-896, 1962. PENFIELD, W., and ROBERTS, L. Speech and Brain-Mechanisms. Princeton: Princeton University Press, 1959. PREMACK, D. Language in the chimpanzee. Science, 172: 808-822, 1971. ROBERTS, L. Aphasia, apraxia and agnosia in abnormal states of cerebral dominance. In P.J. Vinken and G.W. Bruyn (Eds.), Handbook of Clinical Neurology, Vol. 4. Amsterdam: North Holland, 1969. Ross, E.D. The aprosodias: Functional-anatomic organization of the affective components of language in the right hemisphere. Archives of Neurology, 38: 561-569, 1981. Ross, E.D., and MESULAM, M.M. Dominant language functions of the right hemisphere? Prosody and emotional gesturing. Archives of Neurology, 36: 144-148, 1979. RUSSELL, W.R., and ESPIR, M.L.E. Traumatic Aphasia - A Study of Aphasia in War Wounds of the Brain. London: Oxford University Press, 1961. SMITH, A Speech and other functions after left dominant hemispherectomy. Journal of Neurology, Neurosurgery and Psychiatry, 29: 467-471, 1966.
86
D. Frank Benson,
SMITH, A., and BURKLUND, C.W. Dominant hemispherectomy. Science, 153: 1280, 1966. SMITH, A, and SUGAR, O. Development of above-normal language and intelligence 21 years after left hemispherectomy. Neurology, 25: 813-818, 1975. SPERRY, R.W., and GAZZANIGA, M.S. Language following surgical disconnection of the hemispheres. In F.L. Darley (Ed.), Brain Mechanisms Underlying Speech and Language. New York, Grone and Stratton, 1967. SWEET, E.W.S., PANIS, W., and LEVINE, D.N. Crossed Wernicke's aphasia. Neurology, 34: 475-479, 1984. TSUNODA, T. Functional differences between right and left cerebral hemispheres detected by the key tapping method. Brain and Language, 2: 152-170, 1975. WALKER, AE., and JABLON, S. A follow-up of head injured men of World War II. Journal of Neurosurgery, 16: 600-610, 1959. WALKER, AE., and JABLON, S. A follow-up study of head wounds in World War II. VA Medical Monograph. Washington, D.C., U.S. Government Printing Office, 1961. WECHSLER, A Crossed aphasia in an illiterate dextral. Brain and Language, 3: 164-172, 1976. YARNELL, P.R. Crossed dextral aphasia: a clinical radiological correlation. Brain and Language, 12: 128-139, 1981. ZAJDEL, E. Auditory vocabulary of the right hemisphere after brain bisection or hemidecortication. In P.H. Buser and A Rougeul-Buser (Eds.), Cerebral Correlates of Conscious Experience. Amsterdam: Elsevier, 1978. ZAJDEL, E. Right hemisphere language. In D.F. Benson and E. Zaidel (Eds.), The Dual Brain: Hemispheric Specialization in Humans. New York: The Guilford Press, 1985. ZAJDEL, E., and PETERS, AM. Phonological encoding and ideographic reading by the disconnected right hemisphere: Two case studies. Brain and Language, 14: 205-234, 1981. ZANGWILL, O.L. Cerebral Dominance and its Relation to Psychological Function Springfield, Illinois: Charles Thomas, 1960. D. Frank Benson, M.D., The Augustus S. Rose Professor of Neurology, UCLA School of Medicine, 710 Westwood Plaza, Los Angeles, CA. 90024, (213) 825-9873.