Psychophysiology: Today and Tomorrow

BRAIN

BRAIN ORGANIZATION FOR LANGUAGE: Identification of Component Systems for Syntax, Verbal Memory, Focusing Attention and a System Common to Sequencing Motor Movements and Phonemic Discrimination

G.A. Ojemann,     Department of Neurological Surgery (RI 20), University of Washington, Seattle, WA 98195, USA

Publisher Summary

This chapter discusses brain organization for language. It also discusses a series of studies utilizing the electrical stimulation mapping technique during neurosurgical operations under local anesthesia where a variety of different language behaviors have been measured, including object naming, reading, short-term verbal memory, the control of single and sequential oral movements, and phonemic discrimination. In the medial central portions of ventral lateral thalamus, object naming can be disturbed by stimulation. It is suggested that this represents difficulty in the retrieval of names from long-term memory, a part of the same gating process of the specific alerting response. The naming task does not provide a sufficient variety of behavioral responses to classify the sites further, though one wonders if they might play a role in either retrieval from long-term memory or in some semantic aspect of language. The studies of naming in multilingual patients have indicated that there is a partial differential localization of cortex involved in naming in two languages. It remains to be determined whether these represent segregation of systems; for example, one might expect the syntactic system for the two languages to be differential, while the sequential movement–auditory discrimination system might be common to both languages.

An understanding of the physiological mechanisms used by the human brain for language must begin with anatomy, with the identification of what pieces of the brain play what role in language. From observations of language behaviour changes after strokes, the sites where stimulation changes naming, and more recently, the areas of brain that show evidence of increased work during language tasks, a traditional model has been developed of the brain areas for language. That model involves cortical structures in the dominant hemisphere, with an anterior zone just in front of the motor strip involved in motor, expressive aspects of language and a posterior zone in the region of the parietal-temporal junction involved in the receptive, understanding aspects of language. But there have always been problems with this traditional model. Most aphasic patients show both expressive and receptive deficits on careful testing (De Renzi and Vignolo, 1962). Sites of brain damage giving rise to a particular language disturbance often do not correspond to those predicted by the traditional model, particularly a lack of correlation between damage to the anterior language zone and the development of a motor aphasia (Mohr, 1976). And the traditional model cannot account for a number of language behaviours that are strongly lateralized to the dominant hemisphere, for example, short-term verbal memory (Albert, 1976) and the control of sequential motor movements (Mateer and Kimura, 1977). Nor does the traditional model of cortical language include the well confirmed evidence that subcortical, particularly thalamic lesions give rise to specific language disturbances (Fisher, 1958; Luria, 1977; Reynolds et al., 1978).

The present paper reviews a series of studies utilizing the electrical stimulation mapping technique during neurosurgical operations under local anaesthesia, where a variety of different language behaviours have been measured, including object naming, reading, short-term verbal memory, the control of single and sequential oral movements and phonemic discrimination. From these studies emerges a different model of what various regions of the dominant hemisphere do in relation to language. A limited region of premotor cortex in the dominant hemisphere is identified as a final common motor pathway for speech. The remainder of dominant hemisphere peri-Sylvian cortex is a brain region common to a sequential motor and auditory discrimination system. This includes not only frontal but also superior temporal and parietal regions. Cortex surrounding this both frontally and parieto-temporally is part of a system for short-term verbal memory. Interlaced between these two systems are specific cortical sites identified with control of syntax. Ventro-lateral thalamus in the dominant hemisphere contains a mechanism involved in controlling and maintaining attention on verbal material, a mechanism that is active in both language and short-term verbal memory. Although there is considerable individual variability in the exact cortical regions involved in each system, the relative relations between these systems in dominant hemispheres is quite constant.

MATERIALS AND METHODS

msec total duration biphasic square wave pulses from a constant current stimulator, using stimulation trains that last through the particular sample of language behaviour, usually 4 seconds. Electrode location at subcortical sites is recorded on X-rays that also show the anterior and posterior commissures as standard radiologic landmarks. Cortical localization is obtained from photographs of the cortical surface by the relation to the cortical veins; stimulation sites are then reconstructed on venograms.

Four different language behaviour tests have been used in this study. The first test measures object naming and short-term verbal memory. It is published in Ojemann, Blick and Ward (1971). This is a visually presented test consisting of a series of slides, four to each trial, the entire test consisting of 60 consecutive trials. Within each trial the first slide is a measure of object naming: a picture of an object whose name is a common word with the words ‘This is a’ printed above it; the patient is trained to say ‘This is a’ and give the name of the object aloud. This is then followed by a distractor slide, a two-digit number greater than 30, which the patient is trained to read aloud and then count backwards from it by three’s aloud. Following this are two output slides for a single item test of post-distractional short-term verbal memory patterned after Peterson and Peterson (1959) with naming as input to memory and counting as a distractor during which the name must be stored in short-term memory. The first is output from memory by a cued recall, a slide with the word ‘recall’ on it appearing and the patient giving back the name of the object pictured on that trial. The second is output from memory by word recognition, a slide with four words appearing; one word is the name of the object on this trial, one the name of the object on the immediately preceding trial, and two other names of objects pictured elsewhere in the test. The patient reads the name of the object aloud. Stimulation occurs during the naming slide on some trials, the distractor slide on other trials, the cued recall slide on still other trials, the naming and cued recall slides together on still other trials and interspersed are trials with no stimulation which provide a measure of control performance. Multiple blocks of trials containing each of these test conditions are obtained at each site of stimulation. This test was used for the entire series of thalamic stimulation and the initial series of cortical stimulation as a measure of object naming and short-term verbal memory.

More recently it has been modified, replacing the distractor slide with an 8-9 word sentence which the patient reads aloud, the sentence being phrased in the future tense. The recognition memory output slide has been dropped from this more recent form of the test. As these tests are ordinarily used the naming and retrieval slides are each shown for 4 seconds, the distractor for six seconds in the earlier form of the test and 8 seconds in the more recent form.

A third test is a measure of the patient’s ability to mimic single and sequential oral movements. A slide with either 3 pictures of the same simple oral movement, such as puckering the tongue or 3 different simple movements, for example, puckering the tongue, moving it to the right and sticking it out straight is shown on the screen and the patient has been instructed to mimic these movements. The patient’s oral facial movements are recorded by a television camera on video tape for later analysis, comparing trials with stimulation to those without stimulation. Phonemic discrimination has been measured using taped live voice presentation of stop consonants /b/, /p/, /g/, /k/, /d/, /t/, imbedded in the carrier phrase ae___ma. The phrase is presented for two seconds, followed by a two-second interval for the patient to respond with identification of the imbedded consonant. Stimulation occurs only during the presentation, not during the response.

The effects of thalamic stimulation during the first test of naming and short-term verbal memory have been observed in 37 thalamotomies, 20 in right brain and 17 in left. These data have been extensively published (see, for example, Ojemann, 1975). The effects of cortical stimulation on this same test have been obtained in six patients undergoing dominant hemisphere craniotomy for resection of epileptic foci (Ojemann, 1978). The more recent modification of this test that measures naming, reading and short-term verbal memory as well as the phonemic discrimination and oral movement tasks have been measured during stimulation of the dominant cortex in four additional patients, and non-dominant cortex in one. (Dominance in each of these cases has been determined preoperatively by intracarotid amytal testing). All the subjects in these studies have had preoperative IQ’s within the normal range.

RESULTS

Several component systems within human language cortex have been identified within this patient series:

1. A final motor pathway for speech. In the cortex this is characterized by an arrest of naming, reading and output from short-term memory and interference with all types of movement, whether repetitive or sequential. Sites within face motor cortex of either right or left hemisphere show this change, but in left brain only it is also seen from sites in the immediate premotor cortex of the third frontal convolution, particularly that vertical strip of the third frontal gyrus that runs parallel to the face motor cortex. This is the only site within the dominant hemisphere where language changes were found in every patient with cortical stimulation. At a thalamic level, similar arrests in speech can be evoked from the lateral portions of ventral lateral thalamus and adjacent internal capsule of either right or left brain. Extending further within left but not right ventral lateral thalamus are sites where stimulation has evoked other motor changes, including an overall slowing of the rate of speech (Mateer, 1978) and inhibition of respiration in expiration (Ojemann and Van Buren, 1967).

2. A system for both sequencing motor movements and phonemic discrimination. This system has been identified in periSylvian cortex of the dominant hemisphere of four patients, at sites in frontal, superior-temporal and parietal lobes as indicated in the Figure. The characteristics of these sites are an interference with sequential but not repetitive oral movements. At 9 of these 10 sites and at no other sites,

Location of component systems for language in dominant cortex.

Sites of stimulation in the left (dominant) lateral periSylvian cortex of 4 patients undergoing craniotomy under local anaesthesia for resection of an anterior temporal lobe epileptic focus. Each patient contributed 10-15 sites scattered throughout the periSylvian cortex. At sites identified by larger circles stimulation effects on naming, reading, short-term verbal memory, single and sequential oral movements and phonemic discrimination were determined. At sites identified by small circles, stimulation effects on only naming, reading and short-term verbal memory were measured. Shading indicates sites with naming and/or reading changes. Sites identified by numbers can be related to various component systems for language as described in the text: 1) final common motor pathway; 2) sequential motor-phonemic discrimination system; 3) short-term verbal memory system; 5) system for syntax. Open circles — no stimulation effects on any of the language functions tested at that site.

disturbance of phonemic discrimination also occurred. It thus appears that there is common cortex for sequencing movement and auditory speech discrimination. Naming or reading functions were altered at 8 of these 10 sites. At present we do not know what (if any) thalamic role there may be in this system.

3. A system for short-term verbal memory. In the cortex this system is always separate but adjacent to the system common to sequential motor control and phonemic discrimination as illustrated in the Figure. It seldom overlaps with any sites related to naming, though occasionally does with those related with reading. In parietal and temporal cortex it is stimulation during the input and particularly the storage phases of the memory task that interferes with short-term verbal memory; output stimulation there seldom alters memory. In frontal and occasionally parietal cortex, stimulation during the output phase of the task (but not input or storage phases) alters short-term verbal memory. None of these cortical sites shows any pattern of short-term verbal memory changes like that seen from the dominant thalamus. The finding of changes with stimulation during the storage phase suggests that these portions of cortex in parietal and temporal lobe surrounding the areas concerned with naming and sequential motor movements may be the site of the active storage portion of short-term memory.

4. A lateral thalamic verbal alerting attention system identified by the highly characteristic thalamic short-term verbal memory changes evoked by stimulation. When a lateral thalamic stimulating current is applied during the input to short-term verbal memory, overall recall error rate from memory is decreased to about half control levels. The same currents at the same thalamic sites applied at the time of output increase the error rate. Combining stimulation during input and output on the same trial has the algebraic sum of these effects and is indistinguishable from control conditions (Ojemann, 1975). In contrast to cortex, stimulation of the thalamus during storage has no effect on short-term verbal memory tasks. Output stimulation at smaller currents accelerates the rate of memory processes. Based on these data we have proposed a model for the left thalamic role in short-term verbal memory, the ‘specific alerting response’. Left thalamic stimulation activates this system that focuses attention on verbal aspects of external environment. The characteristics of this system are such that when attention is directed to the external environment, already internalized material cannot be retrieved from short-term or long-term memory. Thus this system acts as a gate controlling access to or from short-term verbal memory at any point in time. Elsewhere we have presented evidence that a similar system exists in the right thalamus for visual-spatial information (Ojemann, 1977a), and that when the inappropriate system is activated, that is the left thalamic system with only visual-spatial information present in the environment or vice versa, the verbal thalamic alerting system is clearly dominant over the visual-spatial one. The left thalamic specific alerting system also modulates the ease with which incoming verbal information will be retrieved from both short and long-term memory (Ojemann, 1975, 1976, 1977a, 1977b).

It appears that this same system has a role in language processes. In the medial central portions of ventral lateral thalamus, object naming can be disturbed by stimulation. It is suggested that this represents difficulty in retrieval of names from long-term memory, part of the same gating process of the specific alerting response. Stimulation sites in the posterior lateral thalamus, in the anterior superior lateral corner of pulvinar show more of the output stimulation interference with memory and less of the input stimulation enhancement of memory than is seen more anteriorally in ventrolateral thalamic nucleus (Ojemann and Fedio, 1968; Fedio and Van Buren, 1975). This suggests that the input and output parts of the lateral thalamic stimulation effects of memory involve two anatomically separate but overlapping systems.

5. A cortical system that seems to be specifically involved in the control of syntax. This has been identified in the reading task in 3 patients, at frontal, temporal and parietal sites as illustrated in the Figure. Reading errors are made at some sites that are part of the sequential motor-auditory discrimination system, and also some sites that are part of the memory system. At other sites only reading errors are made, with no errors in naming, short-term verbal memory, oral-facial movements or phonemic discrimination. These two regions of reading errors can be discriminated by the kind or error made. Errors made at sites where there are also disturbances of oral-facial movements or short-term memory are of a jargon type, that is, the patient makes up new words. But the errors at the isolated sites where only reading is disturbed most commonly are errors in grammar, as indicated by incorrect verb forms, or omission of prepositions and conjunctions. These errors then involve the syntactic structure of the language, indicating that there are specific cortical sites involved in this function, sites which seem to lie between the motor discrimination and memory systems. Jargon errors are seldom made at these sites — the semantic content of language seems to be intact there.

The exact sites involved in each of these systems, except for the final motor pathway and the thalamic specific alerting system, have been somewhat variable from one patient to another, but the relationships between each of these subsystems have been quite uniform. The magnitude of this individual variability in the cortical localization of naming for the patient population that is the subject of this study has been determined (Ojemann and Whitaker, 1978a; Ojemann, 1979).

DISCUSSION

Establishment of specific relationships between different parts of the dominant hemisphere of man and language component systems has a number of major consequences for the understanding of normal language physiology and development. First, these relationships indicate what kind of language behaviour one would expect to have reflected in physiological processes at a given brain site. With that information, experimental design of such physiological studies can be optimized, for example, identifying event-related potential or single neuron firing pattern changes occurring during a specific language behaviour in the area of brain concerned with that language system, compared with nearby areas that are not part of that system. Thus one would seek the active neuronal processes in short-term verbal memory in cortex in parietal arid temporal lobe which seems to be involved in the storage aspects of this system, while neuronal processes related to the sequential movements of language and decoding of phonemes would seem to center in periSylvian cortex committed to that system. The finding of considerable individual variability in localization of these functions, though, suggests that these experiments must be carried out under conditions where there is individual mapping of the localization in the particular subject. It does not appear that one can rely on general maps of localization of language cortex, outside of the immediate premotor area (Ojemann, 1979). What, if any, relation exists between the individual pattern of language localization and that person’s overall verbal abilities is not known, but there is a hint that such a relationship exists (Ojemann and Whitaker, 1978a).

Secondly, the identification of these systems provides a basis for search for the evolutionary beginnings of language processes in lower animals. Those evolutionary beginnings should be reflected in the appearance of lateralized systems for sequencing movements, short-term verbal memory and focusing attention. And, indeed, there is some evidence for a lateralized short-term memory system in monkeys (Dewson, 1977).

Third, the finding that there are common sites to sequencing oral movements and auditory phonemic discrimination provides confirmatory evidence for the motor theory of speech perception (Liberman et al., 1967). For our finding indicates that there is common cortex involved in both sequencing motor movements and in the decoding of auditory input. Liberman et aZ.’s proposal is that an internal model of speech production is used for phonemic analysis. This proposal is based on observations indicating that phonemic discrimination is more closely correlated with the phoneme’s articulation than its acoustics. Our finding provides a common area of cortex for the phoneme’s perception and articulation. Of course this association of sequential motor movements and speech perception may have developed the other way around, with the common area of cortex initially being involved in detecting meaningful sounds, and then matching sequential oral movements to those sounds as speech output