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Higher brain function, brain organization |
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N. Bechtereva
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Higher functions of the brain are rightfully believed to be uniquely characteristic of humans. The human brain alone enables its master (with the brain normally functioning as a humble servant) to learn to read, to do arithmetic, to finish school, and to earn specialized university degrees. From time immemorial, the establishment of comprehensive schools and universities has expressed the human brain's creativity and the urgent need for it. This specific activity of the brain has always resulted in, and will continue to result in, breakthroughs into the unknown with consequences for mankind that are favorable or ruinous.
Evolution of higher cerebral functions in humans has distinguished them from animals. Yet our experience with animals, such as the studies of higher nervous activity by I. P.Pavlov, as well as the teaching of some types of "language" communication to certain monkey species (pygmy chimpanzees), leaves no doubt that higher functions are not restricted to the human brain. The relationships of these functions in various species, in particular the question of commonality of principle, are not, however, clear, just as correlations between human and computer intelligence are unsatisfactory. A comprehensive evaluation of this problem is possible only when one studies the neurochemistry and neurophysiology of the human brain and compares the data obtained to that from animals.
Concepts of the cerebral maintenance of higher functions in the past have been on the correlation of anatomic and clinical psychological observations, which, as far back as the 19th century, defined the relationship between some cerebral areas, mainly of the left hemisphere, and speech. This "localizationist" approach was so "effective" that it resulted in structural and functional maps of the brain and, later, in maps of "brain centers." It provided a basis for diagnostic neurology, which served well until the advent of computerized tomography. A contrasting viewpoint has been that of "holism," according to which the brain maintains its functions as a whole, by means of the mass of cerebral substance.
However, all of the clinical psychological and anatomic data, especially those obtained through diagnostic stimulation of the brain, have always suggested that higher functions in the brain are maintained not by the brain centers or by brain mass but by systems of interacting components. The results obtained from point electrical stimulations during open and stereotactic neurosurgical operations (designed to influence deep cerebral formations), as well as from patients with brain electrodes implanted for diagnostic procedures and therapy, have revealed that higher cerebral functions are dependent on not one, but many, cerebral areas.
In parallel with genetically determined structural and functional neural formations providing for basic sensory, motor, and other activities, speech in most people is formed in such a way that its major structural and functional complexes are nearly always located in the same place in the brain in the course of the development of the individual. However, the most complicated cerebral functions are formed or shaped by many factors during the course of individual development. The organization of these functions involves both cortical and subcortical territories (where genetically predetermined monofunctionalism, such as that of primary sensory areas, does not exclude it).
Direct investigation of higher brain functions, as well as their dependence on multiple areas or systems, became possible only after methodological breakthroughs allowing simultaneous study of the various physiological processes taking place in the brain of subjects performing psychological tests designed to bring out particular emotional and mental processes. This entirely new level of research resulted from a comprehensive symbiosis involving physicians, physiologists, physicists, mathematicians, and engineers, each complementing the work of the others. The role of each (from that of the physicians, who determined the medical and ethical necessity of implanting electrodes and monitored the patient's well-being and progress, to that of the physicists, mathematicians, and engineers who were responsible for accurate signal extraction and analysis) was critical.
Physiological investigation of the brain during spontaneous and evoked emotional reactions in our laboratories has produced a number of basic results, including the fact that various infraslow physiological processes are most adequate for the investigation of emotional and other states of the brain and organism. Major findings have been as follows: (1) Rearrangements of infraslow physiological processes (ISPP, 0-0.5 Hz) accompanying emotions in the brains of emotionally balanced subjects develop only in a few structures that are essential for maintaining emotions. These are located principally in the mediobasal areas of the temporal lobe. We assume that similar rearrangements develop in the mediobasal areas of the brain-that is, the hypothalamic area-which is also essential to emotions but has not been investigated in humans. Neurochemical changes, which, dependent on the emotions, may affect the organism favorably or unfavorably, also occur in relation to the rearrangements and may eventually influence higher brain functions. (2) When the brain is emotionally out of balance or when an abrupt, severe emotiogenic factor appears, the physiological processes, as indicated by ISPP data, are rearranged in many (and not just a few) cerebral areas. The changes in brain functional state are so drastic and widespread that fulfillment of higher brain functions may suffer. Despite this, an affect may not occur. (3) More severe is the condition when, because of the initial state of the subject or the intensity of the emotiogenic factor, the ISPP dynamics resemble a "blast." Strong negative emotions correspond to the rapidly rising ISPP level primarily in the major emotiogenic cerebral areas.
What happens to the individual whose brain has developed this "storm" depends entirely on whether the physiological events in the brain are localized or propagate and what other ISPP changes occur in the brain. Affect, with all the consequences that follow, is inevitable if the dramatic changes in ISPP are similar in most major emotiogenic areas. However, there are intrinsic protective systems. If the increase in the ISPP level ("positivation") is accompanied by decreases ("negativation") in the adjacent areas (Figure 1), the "positivation-negativation" balance will be preserved and no affect will result (Bechtereva, 1988).
It is a well-known fact that violent emotional reactions of animals and humans can be accompanied by diverse changes in motor activity ranging from immobility to dramatic hyperactivity. In contrast to motor immobility, which may be ruinous to an individual, motor hyperactivity plays a protective role leading to the lowering of the intensity of emotions. For example, we have observed that speech activity involving both motor and semantic components reduces the likelihood of "blast" ISPP dynamics in response to an emotional stimulus. If speech is interrupted, the protective mechanism is lost, and "blast" ISPP dynamics develop. They can be so severe as to produce transient retrograde amnesia.
In summary, normal emotions in the emotionally balanced brain are physiologically economical. The associated physiological arrangements do not involve large cerebral territories but rather change the state of other areas through the finest neurochemical rearrangements. As such, they are an essential part of individual development and optimal brain function. Abnormal or severe emotionally induced (local or general) rearrangements, on the other hand, may result in nonoptimal conditions for higher brain function, with the severity of the effect dependent on the balance of the aggressive and protective mechanisms.
Before continuing on to the higher functions proper, we need to mention the neurophysiological "bridge" between emotions and thinking. Humans, as social and emotional beings, are affected not only by vital emotions but also by various events, which (arising primarily in the thinking) evoke emotions. To define the relationship between thoughts and the emotions they produce, we have used specially designed psychological tests stimulating positive emotions and recorded some extraordinary changes in neuronal discharge in areas such as Brodman field 4 (Figure 2), as well as in subcortical structures. These transient (about 1 sec) changes in neuronal discharge do not reflect the emotion itself but rather are the trigger for the rearrangements of the ISPPs, which do correlate with the emotion.
An effective line in investigation of the neurophysiological organization of mental function actually began when the recording of impulse activity of neurons and neuronal activity during psychological tests became a reality. As mentioned above, there were many requirements to make this possible. These included the ability to place multiple-contact electrode bundles precisely by computerized stereotaxis, to maintain stable brain contact, to design psychological tests providing analogous trials in sufficient numbers for adequate statistics, and to define new analytical methods capable of analyzing neuronal impulse activity and much more complex brain functions.
With these methods, it has been possible to demonstrate that reproducible changes in impulse activity occur during the psychological tests. Importantly, these occur in numerous cortical and subcortical areas. From these studies it is clear that the subcortex is involved not only in "energy supply" but also in information-processing mechanisms.
A second important finding is that there are both rigid and flexible links in the cerebral "system(?)." A given cortical or subcortical area may show reproducible activity (especially for maintenance of thinking processes) from trial to trial within a given test on a given day but respond differently on the same test hours or days later. The reproducibility of response may then appear in other cerebral areas instead. Still other areas, which are the rigid links, respond reproducibly irrespective of the day and hour of the investigation. For the flexible links, the ISPP is the neurophysiological actualization of these influences, and we know that both the so-called stable potential and waves in the decasecond range must be considered to understand or decode these processes (Bechtereva, 1978).
Why did a question mark (in parentheses) follow the word "system" in the paragraph above? One might conclude that existence of the "system" itself is proved by the fact that numerous cerebral areas, as opposed to one "center" or the "whole brain," are involved in maintaining higher function. However, the "system" we are defining requires not just the elements, but also the dynamic interactions between them. By using conventional (correlation analysis) and less traditional (spike coincidence) methods, we have shown that cerebral areas actively involved in maintaining thinking can be highly interrelated. This is manifested by clearly synchronous or, conversely, strictly asynchronous discharges within micro time intervals and by the interrelationships of many intermediate types of neural activity in adjacent and distant areas.These investigations demonstrate not only the system maintenance of higher cerebral functions but also the remarkable dynamic nature of the interactions of the links in the system. The type and dynamicity of rearrangements of the interactions between system links may correlate with specific activity in a given psychological trial. For example, when a subject is forced to do tedious, monotonous work (a variety of so-called corrective tests), connections between areas last only a few seconds. Against a background of external monotony, the brain appears to resist internal monotony (Medvedev, 1985).
Investigation of the impulse activity in the neuronal populations of the cortex and subcortical formations during psychological, emotional, motor, and other trials demonstrates reliable changes in the discharge rates of numerous neuronal populations, proving the polyfunctional capabilities of these areas. The range of functions maintained by a given cerebral area depends not only on the arrangement of the areas but also on their functional state, neurophysiologically expressed by the ISPP level. In addition to the modality-dependent polyfunctionality, we have observed a more subtle polyfunctionality (expressed as a variety of impulse dynamics in response to various, but always psychological, trials) in thalamic, striopallidal and cortical areas.
We have also observed cerebral areas that react mainly to one kind of activity in all the psychological tests. For example, in fields 1-4 of the left hemisphere and in field 4 of the right hemisphere, we have recorded neuronal populations that are detectors of correct sentence syntax (Figure 3). In the case shown, the left hemisphere reacted with a phasic increase of impulse activity to a grammatically correct phrase and a decrease to an incorrect phrase, while the right hemisphere showed decreased impulse activity consistently, though with varying latency.As another example, in field 7 of the left hemisphere, we have observed a neuronal population that responds selectively to counting. At the same time there is no response in area 6, and a pronounced but nonselective (control and trial) increase in the impulse activity in the lamella medialis caudalis, a subcortical area.
A still different set of neuronal populations are those showing no change in activity when the psychological test is performed correctly, but significant changes (frequently inhibition) when an error is made. These populations, which we have designated error detectors, have been found in some areas of the caudate nucleus, globus pallidus, and several other brain areas. The data enable the conclusion that an error-detection system (and not just a set of isolated areas with error-detection properties) exists (Bechtereva and Gretchin, 1968; Bechtereva, 1977, 2000).
What does the data that we collected enable us to say? Much remains to be done to define further the behavior of the various neuronal populations we have already studied in different types of trials. To date, we have performed a full battery of psychological tests specifically oriented to a variety of types of mental activity in a relatively small number of patients (compared with those in whom we have used a more limited battery of psychological tests), so more needs to be done here as well. What is clear, however, is that use of only a limited number of tests in combination with studies of the impulse activity concurrent with their presentation enables us not only to conclude that a given cerebral area is involved in a particular mental activity but also, on the basis of impulse activity dynamics alone, later on to say, "in this case the subject was counting" or in another case, "the subject was evaluating grammatical structure and the meaning of a sentence," etc.
To be more specific, if a person familiar with the principles of the research is shown a histogram of neuronal impulse activity that he or she has not seen before and is told when the task was presented, what can he say? To take a hypothetical example, the post-stimulus histogram could indicate that several uniform tasks involving the response of a specific cerebral area were involved. A short latency phasic reaction (60 to 100 msec) indicates that a given cerebral area reacts to the physical characteristics of the stimulus, whereas longer latency periods (200 to 300 ms) indicate that the area responds to the meaning of a signal. Even longer latency periods (more than 400 msec) may suggest preparation for a motor or speech-motor response and generally reflect the subject's motor response, provided that it coincides with the "answer." Reactions immediately after the "answer" may not be associated with the test itself but rather indicate the emotiogenic nature of the test.
What are the priorities and prospects for gaining further insight into the neurophysiological basis of thinking? It is hard to assign priorities because the tasks facing us are equally important, and, when solved, will supplement each other. One necessary task is the determination of the principal higher function of each area, thereby enabling the mapping of more and more of the brain. It is also important to determine the maintenance of related mental functions by the cerebral areas, a task which, when accomplished, will supplement the brain map mentioned above. The impulse activity analysis of each area separately, as well as multiple cerebral areas together, must be constantly improved to enable us to deal with the ability of the adult brain to recognize images, make decisions, etc., during just one recognition event. Finally there is a kind of "supertask"-the ability to (even tentatively) ascertain the type of ongoing mental activity by using neuronal population impulse activity data alone. The ability to achieve this goal depends both on modified and improved techniques as well as an enhanced understanding of the mechanisms underlying the activities of the cerebral systems.
The results of neurophysiological investigation into brain organization of thinking described here did have at least one intrinsic shortcoming. The technique we used permitted step-by-step regaining of unique knowledge about many tiny points of the brain, but it did not allow us to obtain data on the events happening simultaneously in the whole brain.
Overcoming these shortcomings became possible when creating new, noninvasive high technology, permitting us obtain simultaneously data on the functional state of all (or most) superficial and deep brain regions, cortex, subcortex and cerebellum. These new technologies created the basis for a new line revealing brain organization of different and especially of higher functions: brain mapping. In most cases, for brain mapping of higher brain functions, positron-emission tomography (PET) and functional magnetic resonance tomography (fMRT, recently fMRI) are used. With optimization of all of the technical aspects as well as of their intrinsic merits, electroencephalography (EEG) and magnetoencephalography (MEG) acquired a second life in the context of brain mapping.
In relation to the merits and shortcomings of different methodologies in future studies of the functional organization of the brain, the most complete data in this line can be obtained by the simultaneous use of different approaches, revealing different characteristics of physiological processes. Even now, simply comparing the data on functional anatomy of certain sites of the brain, obtained through different methodologies, could provide data answering not only the question of "where" but also of "how." In this regard, a group of American scientists working with PET on brain word and sentence processing registered a clear focus of activation (using oxygen-15) in the low anterior part of the left hemisphere in 7 of 10 volunteers. This focus proved to be active during sentence recognition. This permitted the investigators to identify it as kind of sentence recognition center. We did find practically the same in our PET investigations in volunteers. However, when processing neuronal impulse activity in a place bordering fields 46 and 10 (after Brodman) of the left hemisphere, we did find three points, 2 mm apart, that were clearly involved in sentence processing. The dynamic of impulse activity showed a differentiated decrease of the count rate. At one point, the post-stimulus histogram reflected the involvement of neurons in grammar; at the second point, it reflected their involvement in meaning processing; whereas the post-stimulus histogram of the third point could have been considered as a sum of both.
Among the investigations of the neurophysiology of higher functions involving the elucidation of functional anatomy, two main groups of work could have been determined: (1) investigation into the organization of particular (concrete) functions or activities of the organism, and (2) brain organization of the anatomy of physiological processes, maintaining function realization. In turn, the work related to the first group could be divided into subgroups depending on the kind of function or activity, the brain organization of which was studied.
The brain mapping era brought new light into the understanding of various kinds of emotions and emotional states. The investigation of emotions with modern technology is considered a rewarding though very complex field. It was shown that changes in amygdala, thalamus and other brain regions were reproducible in the classical fear induction paradigm, in high correlation with the emotiogenic stimuli applied. Brain activation prevailed in the left or right hemisphere (Mayberg and McGinnis, 2000). Some brain structures (thalamic, medial prefrontal regions) may participate in maintaining normal emotions unrelated to its type, while other regions-such as modality-specific sensory association areas and anterior temporal lobe regions-in the evaluation of the emotional significance of information, etc. (Reiman, 1997). It has been stated that anterior temporal pole activation and left amygdala activation are related to actual emotional memory retrieval (Dolan et al., 2000).
A large number of papers are dedicated to studies of brain organization of language and speech as the most important basis, though not the only basis, of thinking processes. A comprehensive study of brain activation during various language and speech tests was published in 1993 (Roland, 1993). As early as the beginning of the 1980s it was shown that auditory presentations of nouns evoked activation in the auditory cortex and nearby associative cortex of the left and right hemispheres, in temporal superior gyruses. At the same time in the left hemisphere, activation appears also in the upper posterior regions of the temporal lobe, in the region lying anterior to that mentioned above and in the cingulum as well. An interesting story evoked activation in transverse temporal gyrus, the left posterior mid-temporal region, the right mid-part of the midtemporal region, the left prefrontal cortex and the left posterior interior frontal region, as well as in the left and right thalamus (Mazziotta, 1982; Wise et al., 1991).
The brain organization of word production appears to be more complex than could have been predicted on basis of lesion data involving the middle frontal gyrus and perisylvian cortex (frontal and parietal opercules). Random number generation was associated with activation of the left dorsolateral prefrontal cortex, the anterior cingulate, the superior parietal cortex bilaterally, the right inferior frontal cortex, and the right and left cerebellar hemispheres. An increase in the rate of task fulfillment was associated with a significant decrease in activity (measured through regional cerebral blood flow, rCBI) in the left and right dorsolateral prefrontal cortex and the right superior parietal cortex (Jahanshahi et al., 2000). The role of inhibitory process facilitating the possibility of random number generation was not unique in these studies. These days more and more data are available on the evolvement of inhibitory processes of the cortex, which provides the possibility of more-precise decisions (Martin, 1998; Liddle et al., 2001; Bechtereva, 2000). Semantic processing was attributed by different authors to the left inferior frontal cortex (Pozner et al., 1988) and to the fusiform gyrus (Herbster et al., 1997; Murtha et al., 1999). Using a special psychological paradigm, one can change the fine course of events related to the fulfillment of the test (Munte, 1998). However, the moment authors began to analyze the brain organization of higher brain function, they emphasized the multicomponent aspects of these complex processes as well as their complex brain organization (Modayur et al., 1997). It is not a rare finding, therefore, that attempts are made to present data on an individual patient or on individual investigations.
Variations in the brain organization of language can depend on the priority of a given language, the plasticity of the brain, age-determined changes, etc. (Cabeza et al., 1997; Muller, 1977). One could suggest a priori that such a complex function as language would be not only genetically determined but would depend on individual evolution as well. This being the case, one is not surprised to see international differences in language brain mapping differences related to the type of alphabet used (Fujimaki et al., 1999). Data received by us confirm the statement above.
Investigations into anatomical variability in the cortical representation of first and second language showed that listening to stories in first language always activated a similar set of areas in the left temporal lobe clustered along the left superior temporal sulcus. Listening to stories in the second language activated a highly variable network of left and right temporal and frontal areas. Second language acquisition, sometimes restricted only to the right hemispheric regions, is not necessarily associated with a reproducible biological substrate, although the brain representation of the second language can be seen in the same structures as with the first language (Dehaene et al., 1997).
It is probably worth mentioning here that many of the authors, dealing with brain mapping of higher brain function as well as with its basic elements, are stressing the dynamicity of functional brain organization.
Of course, a very important role must be attributed to the psychological aspects of the studies (Petersen et al., 1988, 1990).
A significant difference in brain dynamics can be registered depending on whether a subject is listening to a number of words or a text or is generating words. For instance, listening to sentences activated the superior and middle temporal gyri bilaterally, with mean activation being stronger on the left. For sentence generation, activation was seen in the left middle and inferior temporal gyri (area 46, Muller et al., 1997).
In current studies of the brain organization of higher brain functions, the most complete data are obtained during brain mapping of language. An example of such results from the work of the Institute of the Human Brain are given in Vorobjev et al., 2000 (Figure 4).
A lot of papers also are dedicated to deciphering a more complex topic: the brain organization of thinking. It is probably difficult to separate this topic from investigations of memory, attention and even plasticity of the human brain. Plasticity is of course to be taken into account when studying the organization of a young brain, but it is of real importance in the theory and practice of brain science to remember that plasticity is present in the adult brain, slowly or very rapidly adjusting humans to the ever-changing environment. Many of these changes can be functional (reversible); however, some of them are limited and widespread structural phenomena (Chollet, 2001; Rapoport, 1999; Sugiura, 2001).
I am sure this volume will contain a special chapter dedicated to the neurophysiology of memory. This hopefully being the case, a few remarks on the topic nonetheless are warranted because of recent achievements. It is probably worth mentioning here that the signs of memory influence in the presentation of abstract words could be seen in the parieto-occipital region, whereas the same was found for concrete words obtained with a broad topographic distribution and in a late time interval at fronto-central recording sites. In some other papers, memory influence was registered through subliminal visual priming that was likely mediated by cortical areas such as anterior parts of the inferior temporal cortex.
Different kinds of thinking are correlated with a different mosaic of brain activation and the amount of factors of influence. These factors can produce quite different brain activation at seemingly similar thinking situation. However, as a "reward for investigators" there usually is a reproducible part in the brain activation pattern, which makes the inter-subject investigation worth trying.
Therefore one can find data showing that cognitive learning is correlated with activation in the gyri hippocampi, temporal pole, anterior insula, mediobasal thalamus, anterior cingulate cortex, and also the ventral striatum and orbitofrontal cortex (as well as some other places, depending on factors of influence and individual varieties [Roland, 1993-1997]). At the same time, it is difficult not to accept a kind of broader point of view that thinking simply has its own zones of activity-these being regions outside sensory, motor and immediate associative area, including many cortical and subcortical zones, depending on the type of thinking and topic involved. However, it is necessary to stress that there is no way yet to decipher the precise content of thinking. To solve this problem would require deciphering the brain code of thinking proper. We will return to this problem a bit later.
Some years ago most papers on brain mapping dealt with a simple paradigm. For instance, brain mapping was used to investigate whether only the observation of real objects (tools) activates premotor areas. Tool observation activated the left dorsal premotor cortex; in addition, silent tool naming increased the activity in this area and involved activation of the left ventral premotor cortex and the left supplementary motor area. Evidently quite rightfully, Grafton et al. (1997) concluded that the left premotor cortex has motor valence and is related to motor templates for object use. Other work showed that the right posterior parietal lobe, centered on the intraparietal sulcus, was activated during a mental rotation task (Harris et al., 2000). A review of related literature revealed that this area is involved in a variety of spatial transformations.
During simple calculation task activation in the medial frontal (cingulate guri, left dorsolateral prefrontal cortex, left anterior insular complex and right anterior insular cortex/putamen, left lateral parietal) cortex, the medial thalamus was registered. All of these structures form a network that maintains simple calculation, attention to this task, auditory and motor processing, the phonological store and articulate loop component of working memory. A very special role in the calculation task proper belongs to the parietal cortex (Cowell et al., 2000). Mental subtraction is mediated by a distributed system that includes predominantly the left prefrontal cortex and the inferior parietal cortex bilaterally (Barbaud et al., 1999).
The wide possibilities of modern technology have intrigued investigators, so much- more-complicated aspects of the problem of "brain thinking" have been raised and studied. The results of analyzing how humans understand at least some of the intentions of other human beings, predicting their actions, especially those having biological motion, have been presented (Blakemore and Decety, 2001). Of course, such an action needs the involvement of many brain structures; however, the role of the superior temporal sulcus was stressed as the most important one. The cerebellum is considered to be involved in the prediction of other people's intentions as well, storing representations of motor commands issued to make actions.
Studies of factors related to each other have revealed that activation in the rostral parts of the superior temporal cortex acts as an interface between the dorsal and ventral streams of visual impute processing, allowing the exploration of object-related and space-related information (Karnath, 2001).
A tendency is developing to go farther and farther into the investigation of brain maintenance of higher nervous activity. Results from finer brain mapping have provided a new understanding even of the brain lesion situation (Johnsrude et al., 2000). In describing the functional anatomy in brain lesion cases, Stuss and Alexander (2000) made statement on the physiology of the functions of the frontal lobe. Thus there is no unitary executive function; processes related to the frontal lobes contribute to a general concept of control functions. An important role of the frontal lobes lies in affective responsiveness, social and personality development, and self awareness.
In the study of syllogistic reasoning, the brain reaction to the presentation of sentences with or without content was performed. Content-based reasoning was performed by recruiting the left hemisphere temporal system, whereas the other activated a parietal system. The two systems were producing common activation sites in some other cortical and subcortical structures as well as in the right cerebellum (Goel et al., 2000).
Brain mapping technique was applied to distinguish brain regions related to deductive versus probabilistic reasoning (Osherson et al., 1998). Both probabilistic and deductive reasoning evoked activation bilaterally in medial frontal regions and in the cerebellum, although more thorough analysis showed the relation of probabilistic reasoning to the left dorsolateral frontal regions, whereas deductive reasoning was related to associative the occipital and parietal regions, with a right hemispheric prevalence. The results were considered a valid confirmation that reasoning about syllogisms engages distinct brain mechanisms, depending on the intention to evaluate them deductively or probabilistically. Guessing in a card-playing task, a test that can be considered not far from the test for which data are described above (though of course not nearly identical), evoked activation in the lateral prefrontal cortex (right more that left), right orbitofrontal cortex anterior cingulate, bilateral inferior parietal cortex and right thalamus (Elliott and Dolan, 1999). The orbitofrontal cortex was considered a very important part of this system, which probably reflects the requirements of dealing with uncertainty!
Even such a complex problem as consciousness was studied with the brain mapping technique (Martin, 1998), although the results till now do not of course elucidate the whole problem. They contribute to the general idea that complex mental operations (functions) rely on the coordinated activity of widely distributed brain regions that form a neural network.
So far only a few papers deal with a most intriguing aspect of the brain and mind problem: creativity proper. There are, however, some works that, though not using the term creativity, are actually very close to studying it. Some findings are consistent with the hypothesis that the anterior cingulate cortex is principally engaged in making and monitoring decisions (Liddle et al., 2001). Mapping the network for planning (with the help of the Tower of London task), a proposal was made that the dorsolateral prefrontal, lateral premotor, anterior cingulate and caudate areas form a network for the planning of movements (Dagher et al., 1999). In addition to what was said above about brain mapping of simple arithmetic performance, there is evidence that exact arithmetic is acquired in a language-specific format and recruits a network of word-association processes. Approximate arithmetic shows language independence and recruits bilateral areas of the parietal lobes involved in visuo-spatial processing. Mathematical intuition is supposed to result from the interplay of these brain systems.
How reliable are all these data presented above, in more or less sharp-focused concrete studies and in revealing complex relationships between the physiology of higher brain function and brain anatomy? In general, one can say that they are reliable in cases in which the possible mechanisms are easy to understand or are not yet clear, with partial differences in different papers, since there are nearly always commonalities in the results. Only future studies will determine the functional meaning of the divergences or reveal the randomness of some findings.
The level of studies in the "brain and mind" problem is in general such a high one that there is a scientific, physiological, moral and ethical justification to start studying the brain thinking mechanisms of a higher order-the creativity proper.
There are now only a few laboratories directly involved in the study of the brain organization of creativity (Bechtereva et al., 2000, 2001; Carlsson, 2000).
In studying the brain organization of creativity we are dealing with a process that opens new lines for brain activities, raises their potential, enlarges the possibilities of activities; it is the conditio sine qua non for obtaining completely new results, a process that will permit us to see "what never happened before." It is important to stress that in planning and performing these investigations, the role of the psychologist has become the first priority. One has to formulate tests in such a way that the result of following brain mapping could reliably reflect mostly the process of creativity proper, minimizing the interfering factors. The "eternal task" of finding the best interrelationship between the basic test (A) and control (B) in A-B PET methodology became a priority precisely when we began investigating creativity. Therefore, in contrast to the presentation of previous study data on language, thinking, etc., we will provide here not only conclusions but also some details of the psychological part of the test. The test consisted of four tasks presumably involving the creative form of thinking, each to a different extent. During each task, subjects were presented with a list of words (8 verbs and 8 nouns). In the first and second tasks, subjects were to present a short story with the word list of words respectively difficult or easy to link. The first condition involved more creative thinking, and therefore in this pair the second task could be considered a control to the first one, revealing a subtle difference in creativity with minimal inclusion of additional factors.
The results here that could have been considered as part of the system of brain maintenance of the creativity (Figure 5) revealed activation prevailing in the right frontal lobe (BA 10, 11, 45) (PET data were analyzed with SPM96 Software); registration of the cerebral blood flow was performed with radionuclide H2150. To control syntactic and memory-related aspects of the test, two more control tasks were added. One required composing a real narrative merely by changing word forms, and one required memorizing a list of words. The contrasts 1-3, 1-4, 2-4 and 2-3 demonstrated bilateral activation in the frontal cortex (BA 8, 9, 45, 47) as well as in the left temporal parietal (BA 21, 38, 39, 40) and left cingulate (BA 32) cortices.
Summarizing the above, one can speak about two main breakthroughs in the study of brain organization of higher functions in humans. The first breakthrough was due to the direct contact with the brain, being the result of invasive technique; the second breakthrough was the result of technological revolution-the creation of a new, noninvasive technique. Both of these breakthroughs were methodologically determined. Exactly on the basis of the methodological level, the human mind began to raise and solve new tasks as well as supertasks, not only permitting the most complete extraction of the information out of data but also using simultaneously various different methodologies-fMRI and multiunit activity, for instance (Logothetis, 2001; Drury and Essen, 1999; Liu et al., 1999). One can now see the increase in papers dealing with extremely fine brain correlates of activities, moving closer to brain codes proper. Experiments on animals have showed that the frequency and dynamics of discharges of cortical neurons over time reflect some behavioral states. Correlated fluctuations of discharges seem to warrant attention. Some signs reflecting the flow of information have been revealed as well. In another area, although the experiments were performed in insects, authors have discussed the possibility that transcient oscillatory activity evoked by an auditory stimulus could serve speech recognition (Salinas and Seinowski, 2001).
These works, however, are still very far from deciphering the fine code of thinking, from determining the fine brain rearrangements that correlate directly with the content of the word and not simply its acoustic or visual equivalent. This supertask needs a new breakthrough, a new technical solution. With the techniques we now possess, the attempt to solve this problem of first priority is immensely labor- and time-consuming, and the results are still not reliable enough (Bechtereva et al., 1977). Let us hope that the arrival of this super solution is not far away in our technological era.
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1. See also
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Cognition
Consciousness: neural basis of conscious experience
Prefrontal cortex
Emotional circuits in the brain
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2. Further reading
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Bechara A, Damasio H, Tranel D, Anderson SW (1998): Dissociation of working memory from decision making within the human prefrontal cortex. J Neurosci 18:428-437 [MEDLINE]
Bechtereva NP (1988): The Healthy and Diseased Human Brain 1988. Nauka - Moscow [MEDLINE]
Crozier S, Sirigu A, Lehericy S, van de Moortele PF, et al. (1999): Distinct prefrontal activations in processing sequence at the sentence and script level: an fMRI study. Neuropsychologia 37:1469-1476 [MEDLINE]
Gallagher HL, Happe F, Brunswick N, Fletcher PC, Frith U, et al. (2000): Reading the mind in cartoons and stories: an fMRI study of “theory of mind” in verbal and nonverbal tasks. Neuropsychologia 38:11-21 [MEDLINE]
Gill HS, O’Boyle MW, Hathaway J (1998): Cortical distribution of EEG activity for component processes during mental rotation. Cortex 34:707-718 [MEDLINE]
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4. Figures
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Figure 1
Dynamics of the ISPP level in the left (s) and right (d) amygdala (Amg) during the development of a spontaneous fear paroxysm. Vertical lines separate the period of clinical (behavioral) manifestations of the pathological emotion. Numbers near the curves mark the analyzed areas in the amygdala and correspond to the ordinal number in the electrode in a bundle. Abscissa, time (min); ordinate, ISPP level (mV).
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Figure 2
Dynamics of neuronal impulse activity discharge rate in cortical area 4 of the right hemisphere during the performance of a test for positive and negative emotions. In the upper part is a schematic representation of the trial. A fixation dot is being constantly projected on the screen and then replaced by one of the indicated slides. Exposure times (numbers above the slides) are given in milliseconds (ms). The pre-stimulus interval is introduced as a basis for subsequent statistical estimation of the response. S1, presentation of a figure. SR, verbal response trigger. S2, response quality mark; 5 means "good," 2 means "bad." Marks are given in random order unknown to the patient. On the left and below, peri-stimulus histograms of the neuronal discharge rate selectively averaged for trials with good (upper trace) and bad (lower trace) marks. Bin = 100 ms. Significant (p<0.05). Discharge rate deviations from the background level are filled with black. Thin vertical bars on the auxiliary time axes below the traces mark the bins where the discharge rate deviations were observed with p<0.05 (short bars), p<0.01 (intermediate bars), and p<0.001 (highest bars).
The axis labelled by M12 is used to mark time bins where significant differences were observed between the discharge rates for the two types of trials. On the right and below, averaged EMG of m. orbicularis oris. |
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Figure 3
Dynamics of neuronal impulse activity discharge rate during the performance of a test for detection of semantic and grammatical signs of speech. In the upper left corner, schematic representation of the trial. Four S1 slides represent different groups of trials (M1, M2, M3, M4). On the right, peristimulus histograms of the neuronal discharge rate averaged separately for each group of trials: a, left hemisphere (cortical area 1-4); b, right hemisphere (cortical area 4). Note that the significant excitatory reaction to presentation of the meaningful and grammatically correct phrase and the inhibitory reaction to meaningless phrases is not accompanied by significant discharge rate deviations from the background level (left hemisphere). In this area of the right hemisphere, one can see an inhibitory reaction in the first three types of trials, with an increase in the latency of reaction from M1 to M3. Other reaction in M1 as in Figure 2.
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Figure 5
Brain mapping of results of creativity study. First difficult (D) task minus second easy (E) task. |
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Copyright © 2004 Elsevier. All rights reserved.
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