Brain and Language 74, 238–259 (2000) doi:10.1006/brln.2000.2339, available online at http://www.idealibrary.com on
Language Representation in the Human Brain: Evidence from Cortical Mapping Subhash C. Bhatnagar Department of Speech Pathology and Audiology, Marquette University
George T. Mandybur Department of Neurosurgery, University of Mississippi Medical Center, Jackson
Hugh W. Buckingham Linguistics Program, Louisiana State University, Baton Rouge, LA
and Orlando J. Andy† Department of Neurosurgery, University of Mississippi Medical Center, Jackson The manner in which the human brain processes grammatical-syntactic and lexical-semantic functions has been extensively debated in neurolinguistics. The discreteness and selectivity of the representation of syntactic-morphological properties in the dominant frontal cortex and the representation of the lexical-semantics in the temporo-parietal cortex have been questioned. Three right-handed adult male neurosurgical patients undergoing left craniotomy for intractable seizures were evaluated using various grammatical and semantic tasks during cortical mapping. The sampling of language tasks consisted of trials with stimulation (experimental) and without stimulation (control) from sites in the dominant fronto-temporo-parietal cortex The sampling of language implicated a larger cortical area devoted to language (syntactic-morphological and lexical-semantic) tasks. Further, a large part of the fronto-parieto-temporal cortex was involved with syntactic-morphological functions. However, only the parieto-temporal sites were implicated with the ordering of lexicon in sentence construction. These observations suggest that the representation of language in the human brain may be columnar or multilayered. 2000 Academic Press
We thank Dr. Herman Kolk for his comments on an earlier version of the paper. Address correspondence and reprint requests to Subhash C. Bhatnagar, Ph.D., P.O. Box 1881, Marquette University, Milwaukee, WI 53201-1881. † Deceased. 238 0093-934X/00 $35.00
Copyright 2000 by Academic Press All rights of reproduction in any form reserved.
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Acquired disorders of language have long been of interest to scholars from different disciplines, who hold similar interests in psycho-cognitive properties of linguistics and their neurological correlates. Investigators concerned with the functional organization of the brain have used lesion-evidence from neurological patients to explain the selectivity of linguistic representation in the human brain and have related the linguistic functions with the underlying neuroanatomical underpinnings (Benson & Geschwind, 1985; Caplan, 1987, 1992; Ellis, 1987; Geschwind, 1965, 1974, 1985; Schachter & Devinsky, 1997; Goodglass & Geschwind, 1976; Marshall, 1986; McClelland & Rumelhart, 1986; Shallice, 1988; Whitaker, 1969). The explanations provided by these researchers over the past century have, for the most part, corroborated the classical brain-behavior model (Broca, 1861; Wernicke, 1874). Deriving most of its evidence from stroke patients with static lesions, the classical model assigns language functions to two regions in the left hemisphere, the inferior frontal region and the temporoparietal region. Injuries in the general boundaries of these cortical areas have resulted in clinically and linguistically different aphasic syndromes, referred to as agrammatic (Kean, 1985) and paragrammatic (Pick, 1931; Kleist, 1916; Heeschen, 1985; Butterworth & Howard, 1997) deficits. The agrammatic clinical picture associated with the anterior brain lesion is marked by awkward and halting articulation, effortful speech quality, aprosody, syntactically fragmented sentences, and attenuated use of syntactic and morphological markers (Goodglass, 1976a; Buckingham, 1998; Kean, 1985; Menn & Obler, 1990). Representing a breakdown of the semantic-syntactic organization, paragrammatism is characterized by sentences that are semantically empty and incorrectly formulated, intact grammatical structure, disrupted lexicon, impaired comprehension, and poor self-monitoring. Although patients speak fluently using long word strings with natural prosody as well as a variety of complex syntactic structures, they employ many of the grammatical words erroneously. This affects sentence meaning by altering the categorical (thematic) relations of lexicon to verbs (Bhatnagar, 1980). This lexical-semantic disintegration is often manifested by inappropriate and erroneous usage of semantic markers (subcategorization abnormalities), paraphasic substitutions, semantically empty verbalizations, and frequent jargon utterances (Buckingham & Kertesz, 1976). While there is a general consensus that agrammatic and paragrammatic deficits clinically represent two different patterns of grammatical breakdown and its manifestations, the manner in which the human brain regulates these grammatical constructs has been the subject of intense debate and research in the past. Since the linguistic breakdown in paragrammatism occurs on multilevels
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and involves multiple linguistic components, it has been difficult to characterize the exact nature of the deficit in patients with a posterior lesion. As a result, there have been fewer investigations of the syntactic/semantic breakdown among patients categorized as Wernicke’s aphasics. The selectivity of grammatical loss seen in patients with agrammatism of Broca’s aphasia (Broca, 1861) has, however, been actively investigated, debated, and validated since the seventies (Caplan, 1991). Many linguistic theories/explanations have been advanced to account for the reduced proficiency of grammar in patients with agrammatism, and each theory has provided a different perspective with regard to the hypothesized deficit and related underlying processes. The unresolved debate began with the argument over whether the deficit in agrammatism was central or whether it was modality-specific. Accounting for the loss of grammar as a modality-specific deficit, Goodglass (1976a) argued that agrammatic patients tend to omit small grammatical/functional words because such words lack saliency and are normally unfooted, when they initiate an utterance. This unfooted status of the utterance initiating article (as opposed to an article within the sentence) is what causes it to be deleted so often. Arguing for agrammatism as a central syntactic deficit, Caramazza and Zurif (1976) and Zurif and Caramazza (1976) demonstrated a parallelism between the production and comprehension of grammar. In between, many other explanations of limited scopes have been advanced. For example, Kolk (1978) attributed agrammatism to processing-economy, proposing that agrammatic output represents a patient’s strategy for adapting to the slowness in computing or retrieving grammatical morphemes. Schwartz et al. were intrigued by their observations of patients’ experiencing difficulty in forming declarative sentences, specifically where the agent was not the subject and the patients’ impaired performance in comprehending order dependent word-strings (Schwartz, Saffran, & Marin, 1980a, 1980b). Based on their meticulous analysis of the data, they described the agrammatical loss as the impaired knowledge of word-ordering since the patients had difficulty in determining the meaning of word strings dependent on the ordering of words. Grodzinski (1984, 1986, 1995, 2000) argued that the agrammatical deficit resulted from the patient’s inability to retain certain types of traces of elements that were moved within or between sentences; the processing of sentences with transformed word orders such as the passive structure posed additional problems for agrammatic patients. Moreover, recent lexical decision studies of semantic priming (Prather et al., 1997) have suggested that the online syntactic comprehension disorder of Broca’s aphasics is due to a neural lethargy. This slows the access to the lexicon, thereby disrupting normal sentence parsing routines, which require very fast lexical selection for thematic role processing, co-referential indexing, gap-filling and other types of grammatical processes. Based on linguistic investigations spanning three decades, the general un-
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derstanding is that grammatical functions are discretely represented. The programming of the articulatory-motor units and the selective processing of syntacto-morphological units (auxiliaries, verbal conjugations, inflections, and articles) are mediated in the frontal language cortex. The posterior temporo-parietal cortex is involved with language formulation, semantic schema arrangement, lexical selection, and comprehension of language. This commonly accepted tenet of two neurolinguistic loci continues to be limited by lacunae in our knowledge of the neurological underpinnings related to these grammatical functions. The presence of symptom-variability among similar aphasics (Goodglass & Menn, 1985) has called into question the anterior and posterior dichotomy of grammatical representation in the human brain. The observations of different clinical pictures in patients categorized similarly have further raised concerns about the perceived separation of cortical representation. In addition, the locations of lesions have not always been confirmed in the agrammatic patients selected for these neurolinguistic studies. In the majority of these investigations, a clinical fallacy has occurred, whereby the site of a lesion has been conjectured based on the clinical symptomatology based on the assumption that a lesion of another location than the presumed one would not have produced such a clinical picture of grammatical breakdown. Furthermore, there are additional limitations regardless of the technique used—static or dynamic—in examining the neurolinguistic properties in the brain (Ojemann, 1983). One limitation is related to the degree of refinement afforded by each technique in ‘‘measuring human behavior’’ and its ‘‘sensitivity to lesion’’ (Ojemann 1983), a view reiterated by Lesser at al. (1994b). The anatomical evidence obtained from autopsies in stroke patients is perhaps the most limited in scope because of its indeterminate nature regarding the exact boundary of the lesion and its inability to reveal any induced distant effects. Further, the lesion evidence is not sensitive to functional reorganization during natural recovery. The evidence obtained from modern techniques is comparatively more revealing though still limited. For example, the CT and MRI each provide a clearer anatomical picture of the lesion site, but their measurements do not include any distant effects of the lesion (Naeser et al., 1982; Binder et al., 1996). The small numerical ear advantage in processing two sets of competing verbal stimuli in the dichotic listening paradigm has been found to be more pertinent to attention-related processes than to true cerebral dominance (Ojemann, 1983; Bhatnagar et al., 1987, 1989, 1990). Furthermore, dynamic metabolic techniques, such as rCBF, SPECT, and PET, succeed in demonstrating the true extent of the participation of nuclei by measuring cellular metabolic changes. They do not, however, reveal the exact nature of nuclei functioning—inhibitory or excitatory. On the other hand, focal electrical stimulation of the brain, also partially limited by the preexisting brain pathology, has proved to be a more refined technique in the measurement of brain–behavior relationships, largely be-
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cause of its transient impact. With no subsequent kindling effect, the focal cortical stimulation eliminates the probability of cortical reorganization. It also has been used for mapping the sensorimotor cortex and the area responsible for language functions and memory in patients with intractable epilepsy (Andy & Bhatnagar, 1983, 1985, 1992; Ajmone-Marson, 1980; Fedio & Van Buren, 1974; Godring & Gregore, 1984; Laxer, Needlebaum, & Rosenbaum, 1984; Lesser, Hahn, Luders, Rothner, & Erenberg, 1981, Lesser et al., 1987; Ojemann, 1983, 1989; Ojemann & Whitaker, 1978; Penfield & Jasper, 1954; Penfield & Perot, 1963; Penfield & Roberts, 1959; Rapport, Tan, & Whitaker, 1983; Rasmussen & Milner, 1977; Van Buren et al., 1975, 1978). Recently, focal stimulation has also been used during surgery to remove tumors and correct arteriovenous malformations with no indication of any permanent tissue damage. The external focal electrical stimulation provides perhaps the most discrete evidence for localizing language. The purpose of this study was to examine the anatomical localization of grammatical properties in the human brain using externally applied focal electrical stimulation. More specifically, the goal was to examine whether or not the focal stimulation mapping of the human cortex provided any support for the classical separation of the differential grammatical (agrammatic and paragrammatic) functions into the anterior and posterior language areas of the brain. TECHNIQUES OF FOCAL ELECTRIC BRAIN STIMULATION
Focal external electric stimulation is based on early observations by Fritsch and Hitzig (1870) and Bartholow (1874) that externally applied electric current to the exposed brain altered sensorimotor functions in animals and in humans (Walker, 1957; Brazier, 1957). Cushing (1909) was the first to observe the stimulation-based sensorimotor mapping involving the human cortex in a conscious patient. After the safety and reliability of focal stimulation were established, stimulation mapping became a standard part of surgical treatment for medically intractable epilepsy and was used to map the somatosensory cortex and to chart the human brain for memory and language at the Montreal Neurological Institute (Penfield & Jasper, 1954; Penfield & Roberts, 1959; Penfield & Perot, 1963; Penfield & Jasper, 1963). Completed under local anesthesia while the patients remained awake, focal stimulation was used first to determine the stimulation threshold that produced after discharges and second to determine if the diseased part of the brain was critical for language and sensorimotor functions. Since many language functions can be located around the diseased part of the brain, mapping of language in and around the area of pathology helps neurosurgeons determine if it is safe to remove the diseased cortical tissues without any unacceptable loss of primarily higher mental functions (speech, language, and memory) and secondarily of sensorimotor functions. This mapping also helps determine the size and
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extent of the tissue that can be safely resected. As a rule of thumb, no tissue resection is undertaken from the somatosensory area in the fronto-parietotemporal cortex, unless there is a preexisting hemiplegia or the diseased tissue is not involved with language. In the post-Penfield era this technique has been extensively used by Dr. George Ojemann and his colleagues (Ojemann, 1983, 1989; Ojemann & Whitaker, 1976; Rappart, Tan, & Whitaker, 1983) to treat patients with epilepsy and also to manage other conditions, such as tumor surgery and the surgical management of arteriovenous malformations. Providing the best defense in support of the focal stimulation, Ojemann (1983) argued that focal stimulation acts like a reversible lesion of a very short duration on the brain ranging from 4 to 8 s; its interruption lasts only the duration of the applied current. Further, the stimulation-induced interruption provides the most precise details about functional localization, since the extent of the lesion is only several millimeters in diameter ranging from 0.5 to 3.00 mm. Also, it is not known to leave any lingering effect and/or postoperative aphasia. Carefully controlled stimulation parameters pose no safety concern to patients, cause no injury to the examined brain tissue, and produce no evidence of acute inflammation to the mapped region of the brain. Another advantage of focal stimulation is that its effects on a particular site are repeatable and at times qualitatively different from others evoked from sites in near proximity. Further, stimulation mapping does not require a separate control population for comparison, since nonstimulation trials serve as the control performance. Multiple samples of a single behavior from a single site allow for the necessary statistical analysis and can help to determine if the evoked linguistic errors are significant. The interpretation of the physiologic effects of focal stimulation is based on the interference it produces during ongoing activity. For example, if stimulation at a cortical site disrupts ongoing naming or speaking, the cortical area in question is considered to be functional for the task. If the stimulation does not block or alter the naming/speaking process, the stimulated area would not be considered to be involved in the ongoing activity. While evoking distant effects of the applied stimulation remains a possibility, the low current levels (below sensorimotor threshold) rule out any distant propagation of the current. The short time duration of the applied current-trains to the brain, however, is the only limitation of the technique. The time-constraint issue of focal stimulation, however, has been improved upon by technical advances involving the surgical implantation of a flexible grid with subdural multiple electrodes on gyri and sulci surfaces in the specified cortical regions. These electrodes can be left in the brain for varying time periods ranging from hours to days and weeks intraoperatively, thus allowing for neurolinguistic testing when the patient is rested, out of the surgery, and is in a more natural environment (Lesser et al., 1981, 1984a,b, 1994 a,b; Luder et al., 1982; Morris et al., 1984).
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Previous Studies Using Stimulation Mapping The first and the most comprehensive series of a stimulation mapping based study was undertaken at the Montreal Neurological institute by Wilder Penfield and his colleagues (Penfield & Jasper, 1954; Penfield & Roberts, 1959; Penfield & Perrot, 1963; Penfield & Jasper, 1963), who mapped either the right or the left hemispheres of over 110 patients. Using naming as a measure of language, they identified a large lateral area essential for language in the left fronto-parieto-temporal cortex (Whitaker, 1993), and reported a limited number of evoked errors of misnaming, omission, number confusion, and dysfluency. However, these investigators did not differentiate between the evoked errors of speech and language. Also using naming as a measure of language, Fedio and Van Buren (1974) differentiated between the errors of language and speech. Studying language localization in 19 patients, they evoked naming changes at sites from the lateral cortex far larger in range than previously implicated. They also noted that the stimulation of the frontal and temporal sites evoked differential effects on the input and output phases of short term verbal memory. Again using naming to map language cortex in 11 neurosurgical patients, Ojemann and Whitaker (1978) noted a discrete localization of language in the human lateral cortex, though homologous areas were differentially committed to language in 50–80% of the patients sampled. Only a narrow region of the posterior-frontal lobe rostral to the motor strip was implicated in all patients, thus rendering that region as the most essential for language, if the 100% evoked rate of response is a significant consideration. Later in a series of investigations, Ojemann and associates (1983, 1989) examined short-term verbal memory, facial mimicry, auditory discrimination, and syntactic morphology and found evidence in favor of an overlapping representation of language, which contradicted the traditional model. The important observation of Ojemann and his colleagues was the discrete representation of language involving the sites in two cortical areas, the frontal and temporoparietal, in mosaics of 1 to 2 cm 2. There was substantial individual variability reflecting patients’ verbal intelligence and possibly gender categorization. They also found that sites more frequently implicated with evoked naming errors were more essential to language than ones with lesser frequency of errors, an issue that remains to be debated. Besides the frontal lobe, the stimulation of sites scattered in the parieto-temporal regions evoked omissions and substitution of syntactic markers as well as naming errors. This led them to suggest that the dichotomy of frontal and temporoparietal cortex based on differential grammatical properties was not fully substantiated. Using focal stimulation through subdural grids of electrodes on patients performing reading, syllable discrimination, comprehension, and naming related tasks, Lesser et al. (1981, 1984a, b, 1987) found support for the classical
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TABLE 1 Patient-Related Information Sex/Age
Male/31 Male/31 Male/28
8 9 10
14 14 3
Right Right Right
Left Left Left
85 86 95
neuroanatomical correlates of language. However, they also observed substantial representational variability. METHODS AND PROCEDURES
Subjects Stimulation based mapping of the language cortex was performed on three male subjects with a history of medically intractable seizures, who elected cortical ablation of the epileptogenic tissue as the treatment (Table 1). Each of the subjects had a long history of seizure disorder and had been on two or more anticonvulsant medications. The study protocol included the assessment of handedness, preoperative IQ, auditory-verbal language, and cerebral dominance. Handedness was assessed with a questionnaire based on Crovitz and Zener (1962). All three subjects were identified as being right-handed. Intelligence was assessed using the Weschler Adult Intelligence Scale. All three subjects were found to be within low-normal to normal range with IQ scores ranging from 85 to 95. Wada’s sodium amytal infusion test (Wada & Rasmussen, 1960) revealed a left-hemispheric dominance for language in all subjects. All the subjects had 8 to 10 years of education and had worked independently until they were incapacitated by the intractable seizures. Two of the subjects had a seizure disorder for 14 years, and the third subject had experienced 3 years of seizures. During EEG recordings, abnormal electrophysiological spikes were identified in the left temporal area in all three patients.
Language Testing In order to test language during the surgery, a set of achromatic slides was used. The language testing included four tasks that represented different degrees of language complexity (Table 2). Task A involved sentence construction: patients were given a set of words, including one transitive verb and two or three associated thematic arguments (with the first noun always being the argument in subject position). They were required to construct an acceptable sentence in a canonical word order using correct grammatical/syntactic structures. Task B involved sentence completion, where patients were presented with a grammatically incomplete sentence and were required to provide the missing syntactic-grammatical marker(s) while reading aloud. Task C involved standard object naming. The patients were presented with a carrier phrase (‘‘This is a . . .’’ or ‘‘Here is a . . .’’) with a pictured object and were asked to name the depicted object, such as car, comb, book, table, and chair. Task D was designed to assess the patient’s ability to supply a pronoun. The patients were presented with an incomplete sentence and were required to provide the missing pronoun that coreferred to the subject of the sentence. In order to control the nonstimulation rate of errors, the patients had practiced the tasks prior to the surgery and they were familiar with language testing and procedures.
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TABLE 2 Language Tasks A. Sentence construction Cook (Mary, chicken) Open (John, door, key) Know (Bill, history) B. Sentence completion be closed tomorrow. The school she were the president. Mary wish the president. Bill wishes he Two four. Two C. Object Naming Here is a . . . or This is a . . . (pictured object) D. Pronominalization was sick. John said were the president. Susan wishes
Stimulation Procedures Standard neurolinguistic testing procedures which have been discussed elsewhere were followed (Andy & Bhatnagar, 1984; Bhatnagar & Andy, 1983; Ojemann, 1983a, b, 1989; Ojemann & Whitaker, 1978; and Penfield and Roberts, 1959). The left fronto-parieto-temporal cortex was exposed under general anesthesia, while the patient lay on the right side facing the investigator. The evaluation of language functions and stimulation mapping of the language cortex was performed on the exposed brain under local anesthesia. The exposed cortex was kept moist with saline for proper electrophysiologic contact during stimulation mapping. At the outset, focal stimulation was first used to identify the sensorimotor cortex by recording the evoked experiences of sensation and motor movements, and second to identify the focus of epilepsy by examining the presence of after discharges. The current vollies during stimulation were delivered through bipolar electrode (with a 3-mm interelectrode difference) using a constant current biphasic square wave pulse 200 Usp. 50 Hz, 6–9 mamp of 4–8 s duration. The specific parameters selected with each patient were below the threshold for after epileptogenic discharges and the threshold for the observed sensorimotor responses (Table 3). After calibrating the stimulation parameters to insure they were below the threshold for after-discharges and properly calibrated for mapping the sensorimotor cortex, focal stimulation was used for functional mapping on various randomly selected sites in the exposed area of TABLE 3 Stimulation Parameters a Number of sites stimulated Subject 1 28 Subject 2 39 Subject 3 25
Stimulations per site
Current in mamp
Base error rate
2.6 2.3 2.4
6–7 mamp 9 mamp 7 mamp
0% 9% anomia* 0%
a A current of 50–60 Hz, 200 Usp. was delivered from a constant current stimulator. * Errors were considered significant only if their probability of chance occurrence on a binominal single sample was less than .05.
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the brain. The stimulation intervals varied and two sequential stimulations at the same site were avoided. The stimulation was initiated as the slide was presented and terminated as the slide was changed. Duration of the current delivery ranged from 4 to 8 s, depending on the tasks. After each stimulation, a sterile numbered ticket was placed on the exposed cortex to record the evoked behavior from the stimulated site. A note was also made of each behavior whether evoked or unchanged during the stimulation. The experimental (stimulation) trials were mixed with the controlled (nonstimulation) trials. Testing was done to obtain multiple samples of behaviors from particular and multiple cortical sites in each patient to determine the statistical significance of the small number of stimulationevoked errors. Only the sites involved with the evoked errors of morphosyntax (omission or inappropriate selection of grammatical markers) and lexical-semantics (lexical omission, misnaming, pronominal disturbances, and word-order interferences) have been considered in this study. The sites associated with the evoked responses of speech interference and dysfluency (hesitation, distortion, speech arrest, and word/syllable repetition representing motor-speech interruptions) have been excluded. In total, we sampled 28 sites from the exposed temporo-parieto-frontal region in patient one (WT); 12 out of 28 sites were found to have interfered with language processing. Total sites sampled in patient two (RP) were 39; 13 of those sites were associated with evoked errors of language. In patient three (JH), 10 out of 25 sampled sites were found to be associated with language functions. At the end of the functional mapping, a photograph was taken of the stimulated areas tagged with sterile numbers. The gyral, sulcal, and vascular patterns of the photograph, along with the identified sensorimotor cortex, were used to construct a diagrammatic illustration of the stimulated sites of the exposed brain. The sites implicated with language are indicated in the attached diagrams, and the nature of each evoked response from each of the sites is described in the accompanying legend.
Evoked errors of syntactic morphology, word order (reflecting semantic roles), and naming were evoked from the reported sites stimulated in each of the patients. The occurrence of error for each task ranged from 50 to 75% at these sites, implicating all of the previously reported sites with language on 75–100% of the stimulation trials. Each stimulation site was statistically examined using the binomial single sample test of probability (as discussed by Ojemann, 1983a, b; Siegle, 1956) with a very small error rate on nonstimulation trials (in patient two). The evoked errors were considered to be significant only if their chance probabilities were found to be less than .05%. Illustrated in Fig. 1 are the temporo-parieto-frontal sites in patient one implicated with the stimulation evoked errors on different language functions. Naming (omission, misnaming, and pronominal deletion) was the only function to be altered from stimulation of each of the depicted sites in the figure. A triangle marks the sites associated with naming error alone. The errors of grammatical markers along with anomia were elicited from a smaller number of sites, identified with squares. These omissions and/or inappropriate selection of morphological-syntactic marker occurred when the patient was either required to supply the words while reading an incomplete sentence or asked to formulate a sentence using the provided lexicon. Circles
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FIG. 1. Diagrammatic representation of cortical sites implicated with evoked errors of language functions in patient one (TW). Stimulation at the triangles in the fronto-parietotemporal cortex resulted in evoked errors of naming (omission/misnaming) alone ranging from 50 to 100%: sites 5 and 9 (misnaming 50%); sites 6,10, 15, and 16 (omission 50%); site 8 (omission 100%). Squares in the frontal lobe are the sites associated with errors of naming (33%) and syntactic morphology (66%) in sentence completion and sentence construction tasks. Circles in the temporal lobe were implicated with errors of naming (20%), syntacticmorphological markers (40%), and word-ordering (40%). Some of these sites were also implicated with motor speech problems, which are not considered in this study.
are the sites involved with the evoked errors (omission and substitution) of grammatical markers, the errors of word-order, and naming (Table 3). Illustrated in Fig. 2 are the temporo-parieto-frontal sites associated with evoked linguistic errors in patient two. The sites implicated with the evoked errors of naming are marked with triangles. The squares were the sites associated with the evoked errors of naming and morphosyntactic markers, which occurred while the patient was required either to complete a written sentence or to formulate a sentence using a given set of one verb and two/three nouns. The circles represent the sites associated with the evoked errors of grammatical markers (omissions and misnamings), word order, and naming. Figure 3 illustrates the sites in the temporo-parieto-frontal cortex implicated with evoked linguistic errors in the third patient. The naming errors were evoked from sites scattered throughout the exposed brain (triangles). In contrast to the two other patients, only one frontal site in this patient was involved with grammatical errors, which otherwise had occurred from the stimulation of sites in the parietal and temporal lobes (squares). The errors of word order in this patient occurred from the anterior temporal sites alone (circles). A large lateral region of the cortex was found to be involved with language processing; it extended beyond the limits of the traditional language cortex. The resulting anatomical representation emphasizes two points: selective localization and multilevel columnar representation where some, but not all, language functions are overlaid on the areas of the brain that also serve other
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FIG. 2. Diagrammatic representation of cortical sites implicated with evoked errors of language functions in patient two (RP). Triangles are the sites associated with the evoked errors of naming (omission/misnaming) alone: site 4 (omission 100%), site 8 (misnaming 100%), site 29 (misnaming 50%), site 32 (misnaming 100%), and site 35 (omission 66%). Squares indicate the sites implicated with errors of naming objects and using correct syntacticmorphology in tasks of sentence completion and sentence construction ranging from 33 to 100%: sites 1 and 3 (anomia 33% and errors of syntactic-morphological marker 66%), sites 20 and 24 (anomia 25% and omission of syntactic-morphological markers 75%). Circles mark sites involved with errors of naming, syntactic-morphology, and word ordering; site 22 (anomia 20%, omission of syntactic-morphological markers and word-order errors 80%), site 23 (pronominal anomia 20% and errors of syntactic-morphological markers and word-order errors 80%), sites 25 and 39 (anomia 33% and errors of syntactic-morphological markers and wordordering errors 66%).
functions. Simpler language functions, such as naming and others that have been traditionally considered to be basic language tasks seem to involve a large area of cortical tissue (Fig. 4). Functions involving linguistically complex processing appeared to be multitiered and were restricted to limited, though distinct, brain regions. The selection of appropriate syntactic morphology involved fewer sites; these were restricted to a limited region in the frontal, parietal, and temporal cortex (Fig. 5). The errors of canonical word order assignment along with grammatical function, though, were mostly mediated by sites exclusively in the temporal and parietal cortex (Fig. 6). The anatomic relationship between sites with word-order errors displays a unique dissociation, since it was served only by the sites in the temporoparietal cortex, which had also mediated syntactic morphology and naming. The sites in the frontal cortex implicated with syntactic-grammatical morphology were not involved with the word-ordering aspect of sentence formation in any patient. This cerebral dissociation mirrors the separate functional processes of (1) matrix construction (syntactic frame) and (2) the selection and placement of lexical contentives into those frames (i.e., into the slots). That is, ‘‘frame’’ vs ‘‘content’’ in sentence production appears to fall out along the frontal-
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FIG. 3. Diagrammatic representation of cortical sites implicated with evoked errors of language functions in patient three (JH). Triangles indicate cortical sites associated with evoked errors of naming (omission/misnaming) alone: site 5 (anomia 66 %), site 7 (anomia 66%), and sites 13 and 27 (anomia 100%). Squares indicate the fronto-parieto-temporal sites implicated with the evoked errors of naming and syntactic-morphological markers during completion and construction of sentence: sites 1, 15, and 16 (anomia 50% and errors of syntacticmorphological markers 50%). Circles mark sites associated with evoked errors of syntacticmorphology, naming, and word-ordering in sentence construction: site 21 (anomia 20% and errors of syntactic morphological markers and word-ordering 80%), sites 22 and 25 (anomia 50% and errors of syntactic-morphological markers and word-ordering 50%), and site 26 (anomia 25% and errors of syntactic-morphology and word-ordering 75%).
FIG. 4. Composite representation of the language cortex implicated with errors of naming (omission and misnaming). This function makes up much of the cortical area committed to language. Triangles (patient one), circles (patient two); squares (patient three).
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FIG. 5. Composite representation of the language cortex implicated with errors of naming (omission and misnaming) and omissions or substitutions of the syntactic-morphological markers in three subjects: triangles (patient one); circles (patient two); squares (patient three).
posterior axis of the left hemisphere peri-sylvian region (see MacNeilage, 1998, for a ‘‘frame’’ and ‘‘content’’ analysis at the articulatory level in terms of segments and syllables). Morphosyntactic processes are involved with the construction of frames (comprised of labeled slots for grammatical contentives with functional morphemes in place), while lexical selection and positioning are involved with supplying content to the labeled grammatical category slots in the matrices. Errors of word positioning into morpho-syntactically well-formed frames give rise to paragrammatic language. Morphosyntactic derailments, on the other hand, give rise to agrammatic language. This, therefore, would not directly accord with lexical decision theories of
FIG. 6. Composite representation of the language cortex implicated with errors of naming, syntactic-morphology, and word-ordering. Errors of word ordering were restricted to the temporal-parietal cortex alone: triangles (patient one); circles (patient two); squares (patient three).
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agrammatic comprehension that claim that lexical access lethargy seems to arise from a lesion in the frontal speech regions (Prather et al., 1997). DISCUSSION
Psycholinguistic theories have provided a description of autonomous, though operationally interconnected, linguistic components and language processes (Geschwind, 1965, 1974; Garrett, 1984; Blumstein, 1973, 1998; Buckingham, 1992; Patterson, Marshall, & Colthart, 1985; Goodglass, 1976a; Caramazza & Zurif, 1976; Schwartz & Saffran, 1982). The concern in neurolinguistics has been whether these linguistic functions and processes are reducible to neurological parallels. Despite technological limitations and our inability to read micromolecular level functioning of the brain, notable advances have been made. Each technique has provided a different insight into the brain behavior relationship, such as focal cortical mapping (Ojemann, 1983; Andy & Bhatnagar, 1983; Lesser et al., 1994a, b; Gordon, 1990), regional cerebral blood flow and cellular metobolism measured by positron emission tomography (Damasio 1988; Martin et al., 1996), and functional magnetic imaging resonance (Binder et al., 1996). The emerging neurolingusitic evidence has suggested that while there is some truth to the selectivity of functional localization in the brain, a consistent variability in the size and extent of the localization is common, and an overlapping of functions within a given cortical area is a notable property of the functional organization in the human brain. Growing evidence from focal brain mapping (Ojemann, 1983a, b, 1989) has suggested that the classical model of language localization based on the dichotomy of production and comprehension is no longer supported by the available evidence. Evidence has emerged for a multilayered or columnar representation of some language functions, implying that some language functions are overlaid in a commmon perisylvian region, an area that is also common to the sequencing of motor movements, verbal memory, and phonemic identification (Ojemann, 1983a, b, 1989). Situated within or at the interface of these areas are the specialized cortical sites which mediate different language functions. For example, the temporal lobe is the site for syntactic functions, the posterior temporal lobe is associated with naming functions, and the frontal site is involved with motor-speech functions. Interestingly similar to our findings, Ojemann (1983a, b) also observed multiple frontoparieto-temporal sites implicated with the errors of syntactic-morphology on reading tasks (Ojemann, 1993). Accounting for the evocation of similar errors from different cortical regions, Ojemann (1983a, 1989) argued that the evidence obtained from focal stimulation may reflect the interruption at different processing levels of language function. For instance, the errors of syntax (frame construction) from
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the frontal cortex reflect an interruption in the retrieval phase of syntax (content word concatenation), and the errors of syntax from the temporoparietal cortex reflect an interruption in the storage and in the selection process itself. Our observations of evoked language errors have supported a tiered language representation model within the discrete limits of the perisylvian language brain, with variable commitment of brain tissue to different functions. For example, functional localization was noted to be the most diffuse for lexical processing, suggesting that the entire language cortex had mediated the processing of message ideation into lexicon and pronominal processes. However, morpho-syntactic processing appears to be less diffuse, since its errors were evoked only from a few sites of the temporo-parieto-frontal cortex. The functional representation of the processes regulating the lexical order related to the semantic/thematic roles in meaningful utterances was found to be the least diffused and was confined to the temporoparietal cortex. The frontal lobe was not implicated as had been previously discussed (Saffran, Schwartz, & Marin, 1980). Our observations, somewhat similar to those implied by Ojemann (1983a, 1989), seem to imply some form of microgenesis of language representation (Hanlon, 1991), where language, as a development of a mental phenomena, evolves through qualititatively different stages before its behavioral manifestations emerge (Harrington, 1991). Since similar observations were repeated by stimulation of the same sites, the evoked interruptions can relate to the progressive unfolding of mental representation in general time, though not necessarily in microseconds. By the same token observations of different behavioral symptoms from stimulation of the same site also related to the different progressive unfolding of mental representation in time These findings seem to suggest that the evolution of language formation proceeds from a deeper, discretely localized level to a diffuse cortical representation. The involvement of this deep processing level would produce a diffuse, multilevel, and multi-componential symtomatology emphasizing the important strategic location of the lesion, whereas the breakdown in the latter/peripheral and diffusely located levels of grammar and language would most likely produce isolated componential disorder. Since the effect of stimulation is so transient and repeatable, our observations might not have captured all the progressive unfoldings of language in microseconds, but rather seem to illustrate the true (though rudimentary) nature of the momentary in-time participation of cortical tissue in language functions, which would have varied a few microseconds before and after the point in time. REFERENCES Ajmone-Marson, C. (1980). Depth electrography and electrocorticography. In M. Aminoff (Ed.), Electrodiagnosis in clinical neurology (pp. 167–196). New York: Churchill Livingston.
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