Integration of Information Between the Cerebral Hemispheres
Transcription
Integration of Information Between the Cerebral Hemispheres
, Nl-MBPR I, FFBKl.'.XRY 1^98 ity in dichotic perception of vocal nonverbal . sounds. Canadian Journal of Psychology, 26,111116. Ladavas, E., Uimlta, C, & Ricci-Bitti, P.E. (YiW). Evidence for sex differences in righthemisphere dominance for emotions. Neuropsychologia, 18, 361-366. Landis, T., Assal, G., & Perret, E. (1979). Opposite cerebral hemispheric superiorities for visual associative processing of emotional facial expressions and objects. Nature, 278, 739-740. Lang, P,J., Bradley, M.M., & Cuthbert, B.N. (1990). Emotion, attention, and the startle reflex. Psychological Review, 97, 377-398. Ley, R., & Bryden, M.P. (1982). Hemispheric differences in processing emotions and faces. Brain and Language, 7, 127-138. MacLean, P.D. (1949). Psychosomatic disease and the "visceral hrain": Recent developments bearing on the Papez theory of emotion. Psychosomatic Medicine, 11, 338-353. sphere dysfunction in nonverbal learning disNitschke, J.B., Heller, W., & Miller, G.A. (in press). abilities: Social, academic, and adaptive funcThe neuropsychology of arwiety. In J.C. Borod tioning in adults and children. Psychological (Ed.), The neuropsychology of emotion. New York; Oxford University Press. Bulletin, 107, 196-209. Nitschke, J.B., Heller, W., Palmieri, P.A., & Miller, Spielberger, CD. (1968). Self-evaluation questionG.A. (1998). Contrasting patterns of brain activity naire. STAl Form K-2. Palo Alto, CA: Consultin anxious apprehension and anxious arousal. ing Psychologists Press. Manuscript submitted for publication. Suberi, M., & McKeever, W.F. (1977). Differential Papez, J.W. (1937). A proposed mechanism of right hemispheric memory storage of emoemotion. Archives of Neurological Psychiatry, 38, tional and non-emotional faces. Neuropsycholo725-743. gia, 15, 757-768. Robinson, R.G., Kubos, K.L., Starr, L.B., Rao, K., & Price, T.R. (1984), Mood disorders in stroke Tucker, D.M., Watson, R.T., & Heilman, K.M. patients: Importance of location of lesion. 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Davidson & K. Hugdahl (Eds.), Brain asymmetry (pp. 427\ 450). Cambridge, MA: MIT Press. Helhge, J.B. (1993). Chapter 6: Vari, eties of interhemisplieric interac, tion. In J.B. Hellige, Hemispheric asymmetry: Wfiat's right and what's left (pp. 168-206). Cambridge, MA: Harvard University Press. Lassonde, M., & Jeeves, M.A. (Eds.). (1994). Callosal agenesis: A natural split brain? New York: Plenum Press. Milner, A.D. (Ed.). (1995). Neuropsychological and developmental studies of the corpus callosum ' ISpecial lssuej % 921-1007 Neuropsyihologia, mation about how these two relatively distinct portions of the brain interact to provide the seamless behavior we all exhibit in everyday life. So striking are some of the demonstrations of lateralization of function in splif-brain patients (i.e., individuals in whom the corpus callosum, which connects the cerebral hemispheres, has been severed) that philosophers and neuroscientists alike have paused to consider whether humans might have two separate and unique consciousnesses, rather than a single mind. Recent work has helped to expand our understanding of the exquisite interplay between the hemispheres that provides us with unified thought. It has become clear that interhemispheric interaction has some unanticipated functions, such as playing a role in perceptually binding together disparate parts of an object or modulating attentional ability. Furthermore, in- l-'ublished by Cambridge University Press terhemispheric interaction appears to have emergent properties, in that under certain conditions, one cannot deduce how the hemispheres interact based solely on how each hemisphere operates in isolation. Researchers attempting to understand interhemispheric interaction have generally concentrated on two major lines of inquiry. The first examines how information is represented as it is transferred from one hemisphere to the other. Thought of differently, this line of inquiry attempts to understand the "language" that the hemispheres use to communicate with one another. The second line of inquiry examines how transfer between the hemispheres affects the brain's information processing capacities and strategies. Thaf is, this line of research attempts to understand what mental processes are modulated or influenced by interhemispheric interaction. Most interaction between the cerebral hemispheres occurs via a very large neural band of fibers known as the corpus callosum (see Fig. 1), which is composed of more than 200 million nerve fibers. Although there are other neural pathways by which information can be transferred between the hemispheres (see Fig. 1), the vast major- CURRi:\'T DIRIXTIONS SN PSYCHOiXXUCAL SCiFiNCB Hippocatnpal commissure Corpus callosum Habenular commissure Posterior commissure Anterior commissure Massa intermedia of the thalamus Collicular commissures Fig. 1. A view of the brain cut down the middle so that the inside-most regions of the right hemisphere are shown. Labeled in this figure are the various pathways through which information can be communicated between the hemispheres. Notice that the corpus callosum is by far the largest, and it is responsible for the vast majority of information transfer between the cerebral hemispheres. From Banich (1997). Copyright 1997 by Houghton Mifflin Company. Used with permission. ity of information is transferred via the callosum. As Reuter-Lorenz and Miller (this issue) discuss, only rudimentary information can be transferred without a callosum. Such information includes coarse visual information regarding motion but not visual form, binary information (yes/no, odd/even), general emotional tone (positive, negative), and information that allows for the automatic orienting of attention. HOW IS INFORMATION REPRESENTED WHEN IT IS TRANSFERRED BETWEEN THE HEMISPHERES? One of the guiding principles of interhemispheric interaction is that different types of information are transferred across different sections of the callosum. The callosum is organized topographically, with each section connecting nearby regions (i.e., the anterior callosum connects anterior brain regions; the posterior callosum connects posterior brain regions). Because each of the major types of sensory information (e.g., visual, auditory, tactile) is processed by a distinct brain region, and because different higher order representations of information (e.g., abstract visual form vs. meaning) are processed by different brain regions as well, one might expect that the callosum consists of channels, each of w^hich is responsible for transferring a distinct type of information. For the most part, this expectation seems to hold. For example, when a simple flash of light is directed to one hemisphere and the motor response is controlled by the other hemisphere, hoth sensory (i.e., visual) and motoric information are transferred. Electrophysiological recordings suggest that the motor signal is sent across middle portions of the callosum that connect motor regions of the brain, whereas the visual signal is sent across posterior portions of the callosum that connect visual regions of the brain (Rugg, Lines, & Milner, 1984). Furthermore, studies of patients with cailosal tumors or partial section of the callosum provide evidence that, for the most part. Copyright © 1998 American Psychological Society visual, auditory, and somatosensory information are transferred through different sections of the callosum (e.g., Risse, Gates, Lund, Maxwell, & Rubens, 1989). Intriguingly, there is evidence for an asymmetry in the speed of transfer of sensory information between the hemispheres: Such transfer is faster from the right hemisphere to the left than from the left hemisphere to the right (Marzi, Bisiacchi, & Nicoletti, 1991). Because not all information transferred between the hemispheres is sensory in nature, researchers have also attempted to determine how higher order (e.g., spatial, semantic) information is communicated. This task can be somewhat difficult because higher order information could be transferred between the hemispheres in a variety of ways. A word, for example, could be represented as a visual pattern, as a series of letters, as a series of sounds, or as a meaning. Hence, much of this research has focused not on the exact nature of information transferred, but rather on whether the representation of the information involved in interhemispheric communication is similar to or distinct from the representation employed by each hemisphere. A commonly utilized method in such endeavors is to com^pare the processing that occurs when information is directed to only one hemisphere with the processing that occurs when both hemispheres receive identical information. In the case of visual information, stimuli are presented to only one visual field (i.e., only to the left or right of fixation) on some trials and to both visual fields (i.e., to both sides of fixation) on other trials. Information presented to a given visual field is processed initially by the opposite hemisphere. Thus, information presented to the right visual field (RVF; i.e., to the right of fixation) is processed initially by VOLUME?, \'i;VIi3i.-R !, FEfiRLiARY Vm the left hemisphere, and information presented to the left visual field (LVF; i.e., to the left of fixation) is processed initially by the right hemisphere. The major finding of this line of inquiry is that the representation invoked when both hemispheres are involved in processing can vary across situations (see Hellige, 1993, chap. 6). In some cases, the representation employed when both hemispheres receive information is similar to the representation used by one hemisphere, but not the other. For example, Hellige, Jonsson, and Michimata (1988) asked individuals to differentiate two faces that varied by a single feature (hair, eyes, mouth, jaw), and examined performance as a function of which feature distinguished the two faces. One might presuppose that the representation employed when both hemispheres saw the faces (bilateral-visual-field, or BVF, trials) would be similar to the representation used by the hemisphere generally considered specialized for the task (in this case, the right hemisphere, because it is usually superior at face processing). However, that was not the case. The pattern of performance on BVF trials was identical to that observed on RVF (left-hemisphere) trials, but different from that for LVF (right-hemisphere) trials. In fact, the representation employed on BVF trials is frequently similar to that of the hemisphere less adept at the task. Perhaps when both hemispheres are involved, the more adept hemisphere has to "dumb down" to meet the other hemisphere's ability. In other cases, the nature of processing when both hemispheres are stimulated is a blend, or average, of the processing that takes place within each hemisphere. For example, when the task is naming consonant-vowel-consonant sequences, the pattern of errors varies by visual field. On LVF trials. errors are much more frequent on the third letter of the sequence than the first, whereas this difference is much reduced on RVF trials. The pattern of errors on BVF trials is intermediate between that of RVF and LVF trials (Luh & Levy, 1995). These findings suggest that both hemispheres contribute to performance so that the representation employed in the interchange of information is a blend of the different representations utilized by the two hemispheres. One of the m^ost interesting findings of such research is that the representation employed when both hemispheres receive information can be completely distinct from the representation employed by either hemisphere in isolation. In a series of studies, Karol and I instructed individuals to decide whether either of two probe words (which were positioned in the same visual field on some trials and in different visual fields on others) rhymed with a previously presented target word. We found that when a rhyme was present, performance on RVF trials, and to a lesser degree on BVF trials, was influenced by whether the meaning of the two probe words was identical (e.g., bee and bee) or different (e.g., bee and sea), an effect not observed for LVF trials. We then changed the task slightly, presenting the two words in different cases and fonts (e.g., BEE and bee, BEE and sea) so that they would no longer look identical. This manipulation did not affect performance on RVF and LVF trials, but changed the pattern for BVF trials (Banich & Karol, 1992, Experiments 4 and 5). Thus, the words' meaning and form interacted to affect performance on BVF trials, suggesting that the representation used when both hemispheres are involved in processing is one in which physical form and meaning are linked. In contrast, the fact that font and case did not affect either LVF or RVF performance I'liblished by Cambridge University Press suggests that the individual hemispheres employ a representation in which meaning and form are separable. HOW DOES INTERHEMISPHERIC INTERACTION MODULATE COGNITIVE PROCESSES? Researchers have also made some progress in understanding how interaction between the hemispheres influences the ways in which the brain processes information. Research with animals suggests that at least for the primary sensory areas of the brain (i.e., the region of the brain where information from sensor receptors, such as the eye, is first received), integration of information across the callosum allows for a unitary sensory world. Because the neural system is organized so that information on the left side of space goes to the right half of the brain, and vice versa, there is a need to fuse these two perceptual half-worlds. The callosum seems to play a critical role in this regard. Callosal connections in primary sensory areas are often limited to those regions of the sensory world that fall along the midline, such as where the RVF and LVF meet. Corroboration of the role of the callosum in sensory midline fusion comes from studies of individuals who were born without a callosum, a syndrome known as callosal 'agenesis. These individuals have interesting sensory difficulties, including a poor ability to discern which of two objects placed in central vision is closer or further away (an ability that relies on the brain computing slight differences in the retinal images received by the two eyes), a poor ability to determine whether two points touched on either side of the trunk are different or the same, and difficulties in localizing sounds in space (a skill that relies on the brain computing slight differences in the timing or intensity of sounds received by the two ears). All these difficulties rely critically on the comparison of information received separately by the two hemispheres, and hence require integration across the callosum (Lassonde, Sauerwein, & Lepore, 1995). Recently, it has been proposed that the pattern of activation across the callosum may help bind together different parts of the visual world into unitary objects. When stimuli on different sides of the visual midline move in tandem, cells in the two hemispheres fire synchronously. This synchrony relies specifically on the callosum, as it does not occur when the callosum is severed. Because parts of an object generally move together in the same direction and at the same speed, such temporal aspects of callosal firing may provide a mechanism for binding together parts of an object that appear on either side of the midline (Engel, Konig, Kreiter, & Singer, 1991). Because people typically move their eyes so that an object of interest falls in the center of gaze (and hence spans the midline), such callosal connections may be important for object recognition. Interaction between the hemispheres not only influences sensory processing, but also modulates the processing capacity of the brain. Belger and I (Banich & Belger, 1990) found that fhe ability of inferhemispheric interaction to facilitate performance increases as the computational complexity of the task, which we define as fhe number (and nature) of the steps involved, increases. For example, if it must be decided whether two digits add to 10 (summation task), performance is befter if one digit is presented to each hemisphere (so that the hemispheres musf interact to make a decision) than if both digits are presented to the same hemisphere (in which case, no interaction is required). In contrast, if the task is to decide whether two digits are identical (physicalidentity task), interhemispheric interaction does not yield a performance advantage. The summation task is more con:\plex because not only is perceptual processing of the digits required (as in the physicalidentity task), but then some identification and addition must be performed as well These results are consistent with others demonstrating thaf performance is better when operations are divided across the hemispheres (e.g., directing a digit to be added to a target to one hemisphere, while directing another digit to be subtracted from the target to the other hemisphere) than when bofh operations must be performed by the same hemisphere (Liederman, 1986). We believe this effect occurs because the computational power of the brain may be increased by dividing processing over as much neural space as possible (in this case, over the two hemispheres), much the way that computational power of computers is increased by dividing a task over many sysfems. Such a division is possible because for most tasks (with the possible exceptions of speech output and phonetic processing), specialization of the hemispheres is relative rafher than absolute. Thus, even though one hemisphere may do a particular task less capably or efficiently than the other, it nonetheless has the capacity to contribute (see also Beeman & Chiarello and Chabris & Kosslyn, this issue). As tasks get more difficulf, any cost overhead imposed by having to coordinate processing between the hemispheres is more than offset by the increased computational capacity provided by having both hemispheres involved. Indirect support for such an idea Copyright © 1998 American Psychological Society has been provided by the recent surge of brain-imaging studies. Although these studies are designed to examine specific cognitive processes (e.g., memory), the manipulations employed often vary in complexity (e.g., in how many items musf be retrieved from memory). As task demands are increased, often there is not only greater activation of the brain region specialized for that task, but greater activation over both hemispheres as well (e.g.. Braver et al., 1997). Such findings are consistent with the idea that as tasks get more difficult to perform, more resources are recruited from both hen:\ispheres. Interhemispheric interaction also seems to modulate fhe ability to select certain information for processing (e.g., the words on this page) while filtering out other information (e.g., the background noise that occurs while you are reading). Using three well-known paradigms, Alessandra Passarotti, Joel Shenker, Daniel Weissman, and I have demonstrated that interhemispheric interaction aids task performance when a high degree, but not a low degree, of selection is required. In one of these paradigms, the individual must pay attention to the overall shape (global form) of an item and ignore the small shapes (local form) of which it is composed (or vice versa); in another, individuals must decide if a pair of items matches, and that decision must be made by attending to one attribute of the pair (e.g., their shapes) but not another (e.g., their colors); and in the third paradigm, the Stroop paradigm, an individual must pay attention to (and name) the color of the ink in which a word is presented while ignoring the meaning of the word. When there is no interference between the two types of information and thus little need for selection, interaction between the hemispheres does not aid performance. For example, interhemispheric intefaction is not especially useful when the global and local form of an item are the same, when a pair of items have the same form and the same color, or when the color a word names is concordant with its ink color (e.g., "red" is printed in red ink). However, when there is conflicting information and individuals must select one type of information over another, the degree of interference engendered by the conflicting information can be reduced by interhemispheric interaction. For example, when an item's global and local shape lead to different responses, when items match in form but not color, and when the word "blue" is printed in red ink, interaction between the hemispheres leads to superior performance. Furthermore, these results, for the most part, are relatively independent of hemispheric asymmetries for the task, once again suggesting that interhemispheric interaction may affect processing in a manner independent of hemispheric specialization. THE IMPORTANCE OF INTERHEMISPHERIC INTERACTION FROM A CLINICAL OR LIFE-SPAN PERSPECTIVE The nature of interaction between the hemispheres may also be important in a number of neuropsychological syndromes, and may have implications for development and aging. For example, the corpus callosum seems especially vulnerable to damage caused by multiple sclerosis (e.g., Rao et al., 1989) and closed head injury (Gale, Johnson, Bigler, & Blatter, 1995), and the morphology and function of the corpus callosum are different in people with schizophrenia than in neurologically intact individuals (e.g., David, Minne, Jones, Harvey, & Ron, 1995). The implications of such findings remain unclear at present, but it is possible that some of the attentional difficulties observed in people with these syndronnes may be lir\ked to disrupted interhemispheric interaction. The interplay between the hemispheres may also be linked to changes in cognitive processing with development. During childhood, the speed with which information can be relayed between the hemispheres increases because the fatty insulation around neurons, called myelin, continues to increase in size around callosal neurons until some time during the late teen years. In essence, the hemispheres of young children are more functionally disconnected than those of adults. Children do not exhibit the same advantages of dividing processing across the hemispheres as observed in older individuals, but that changes as they grow older (Liederman, Merola, & Hoffman, 1986). Interhemispheric interaction may be disrupted in dyslexia (Markee, Brown, Moore, & Theberge, 1996), and may be atypical in attentional deficit disorder (Giedd et al., 1994). Future work is likely to be directed to more carefully explicating the nature of the relationship between interhemispheric interaction and certain developmental syndromes. CONCLUSION T In sum, the functionally distinct cerebral hemispheres appear to coordinate their performance in multiple ways via the corpus callosum, which allows for dynamic interchange of information. The nature of the representations used for such communication is not well elucidated at present, especially for higher order information. However, it is clear that to further understand the implications of later- Published by Cambridge University Press alization of function, it will be critical to understand interhemispheric integration, as research already suggests that the whole is more than the sum of its parts. Acknowledgments—Preparation of this article was supported by National Institute of Mental Health Grant ROl MH54217. I thank Mark Beeman, Christopher Chabris, Emanue! Donchin, and Wendy Heller for helpful comments. Note 1. Address correspondence to Marie T. Banich, Beckman Institute and Department of Psychology, University of Illinois at Urbana-Champaign, 405 N. 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APS's second journal, Current Directions in Psychological Science, consists of reader-friendly reviews of current research areas. It is available by subscription. For membership information and applications, contact the American Psychological Society, 1010 Vermont Avenue, NW, Suite 1100, Washington, DC 20005^907. Telephone: 202-783-2077; Fax: 202-783-2083; Internet: [email protected]. Copyright © 1998 American Psychological Society connection in multiple sclerosis: Relationship to atrophy of the corpus caJlosum. Archives of Neurology, 46, 918-920, Risse, G,L., Gates, J-, Lund, G,, Maxwell, R, & Rubens, A, (1989), Interhemispheric transfer in patients with incomplete section of the corpus callosum. Archives of Neurology, 46, 437-443, Rugg, M,D,, Lines, C.R, & Milner, A.D. (1984). Visual evoked potentials to lateralized visual stimuli and the measurement of interhemispheric transmission time. Neuropsychologia, 22, 215-225,