Edit rial Does Diaschisis Have Clinical Correlates? In this issue of the Proceedings (pages 357 to 364), Dr. Richard Caselli reports an interesting study. The article is concerned with the nature of bilateral impairments of somesthetically mediated object recognition due to unilateral cerebral lesions. He examined a group of 30 patients for deficits in primary sensation and also for secondary cortical interpretative sensation with use of a battery of neurologic tests that concentrated primarily on each patient's ability to recognize objects by feeling them. Testing also compared tactile with visual object recognition as well as discrimination of the weight, texture, shape, volume, and substance of objects. In addition, he examined two-point discrimination, double simultaneous stimulation, and the usual tests of primary somatosensory function. Test results were then correlated with findings on detailed neuroimaging of the brain with use of computed tomography and magnetic resonance imaging. The large sample of patients examined was divided into (1) those with large right cerebral hemispheric infarctions who had disabling left hemineglect, (2) those with large right cerebral hemispheric infarctions but with mild left hemineglect, (3) those with lacunar infarctions confined to the internal capsule with motor paralysis but without sensory loss, (4) those with unilateral thalamic infarctions, and (5) neurologically normal control subjects. Patients with dysphasia were excluded from the study. Results of the study showed that patients with either motor paralysis or primary sensory loss due to thalamic infarctions did not have as severe impairment of somesthetic recognition Address reprint requests to Dr. J. S. Meyer, Director, Cerebral Blood Flow Laboratory, Department of Veterans Affairs Medical Center, 2002 Holcombe Boulevard, Houston, TX 77211. Mayo Clin Proc 66:430-432,1991
of objects as did patients with right parietal cortical sensory loss and with persistent hemineglect. Bilateral impairments of somesthetic identification ofobjects, demonstrated by impairment on testing the right hand (ipsilateral to the right hemispheric lesions), were seen only in patients with extensive right hemispheric infarctions, all of which involved the parietal lobe. All these patients exhibited severe left-sided neglect. After careful consideration and rejection of other different and possible explanations, Caselli concluded that impairments of somesthetic recognition in the right hand (ipsilateral to the lesion) after severe right hemispheric infarction resulted from transcallosal depression ofthe function of the parietal cortex, contralateral to the infarct, which impaired arousal and attentional mechanisms by "transcallosal diaschisis." Is this explanation, implicating "diaschisis" as being responsible for the inattention of the contralateral hemisphere, scientifically acceptable, or is it merely substituting one unknown for another? In the light of recent studies of diaschisis that included the use of three-dimensional analysis of cerebral blood flow and metabolism, this explanation is certainly scientifically acceptable. The considerable data accumulated during the past 20 years about the nature of diaschisis support Caselli's explanation for his carefully documented clinical observations. Diaschisis-or a "splitting of function"-is a term that was originally proposed in 1914 by the Russian neurologist von Monakow to describe remote depressions of brain function that were noted at a distance from a circumscribed lesion of the brain. Von Monakow postulated that diaschisis was due to a severance of nervous connections or fiber tracts that connected the site of the cerebral lesion with other regions of the brain, causing their functional depression. Since then, several neurophysiologic studies, including measurements of regional cerebral blood flow and metabolism, have supported the hypothesis of von Monakow. Disconnections in
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the white matter tracts of the corpus callosum are known to be a frequent cause of diaschisis both in patients and in animal models; thus, infarctions ofthe ipsilateral hemisphere depress the function, perfusion, and metabolism not only of the ipsilateral but also of the contralateral hemisphere. 1 The most important single mechanism responsible for diaschisis, as judged by remote reductions of local cerebral perfusion and metabolism, is structural or functional deafferentation or disconnection of white matter fibers that connect one group of cerebral neurons to another. Close perusal of Figure 2 in Caselli's article shows that most of the right hemisphere, up to and including the right half of the corpus callosum, is indeed involved in the extensive right hemispheric infarction. Therefore, disconnections with the contralateral left (intact) hemisphere may reasonably be expected to result. Measurements of cerebral blood flow together with oxygen and glucose metabolism in many similar patients in this laboratory and others have shown that the contralateral (intact) hemisphere, including not only the parietal lobe and the second somatosensory cortical region (responsible for somesthetically mediated object recognition) but also the contralateral (intact) cerebellar hemisphere, exhibits decreased blood flow and metabolism. Thus, in cases of extensive right hemispheric infarctions, inattention in conjunction with impairments of somesthetic object identification in the ipsilateral hand may indeed be reasonably assumed to result. Investigators have substantiated that among patients with infarction of the parietal lobe, double simultaneous stimulation-or the use of other multiple sensory inputs-progressively impairs simpler unilateral test responses and may eventually result in a "catastrophic reaction" in which patients can no longer respond at all to such complex testing. Caselli's observations together with his diaschisis explanation lend validity to the concept of "impaired attention" that occurs in patients with parietal lesions and leads to a phenomenon termed "perceptual rivalry," a theoretical concept advanced by my-
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self, Denny-Brown, and Horenstein almost 40 years ago. 2 According to the concept of "perceptual rivalry," patients with infarction of the parietal lobe respond to simple tests but with impaired alertness and attention. Consequently, the more complex and bilateral the testing becomes, the more likely the attention will fail and some sensory stimuli will be neglected or ignored by the mutilated nervous system (that is, "sensory inattention"). The study by Caselli indicates how our understanding of behavioral neurology is likely to continue to be advanced with recent developments of three-dimensional brain imaging. 3 Caselli was able to study 30 living patients and to classify them into 6 carefully defined groups on the basis of the anatomic site oftheir cerebral infarctions, as determined by computed tomography and magnetic resonance imaging. Before the advent of neuroimaging, such an extensive study, conducted by one person, would have been impossible because autopsy confirmation of the site of the lesions in such a large series of patients would have been highly improbable. Combining three-dimensional computed tomographic imaging with local measurements of cerebral blood flow is now possible in most major hospitals by having patients inhale 27% xenon during serial computed tomographic scanning. 4 This procedure allows quantitative estimates of brain integrity and regional functional activity to be correlated with neurologic and cognitive test performance. In the limited number of research centers where scanning with positron emission tomography is available, measurements of local perfusion and metabolism have been correlated with the remote effects of capsular and thalamic lesions attributed to diaschisis or disconnection syndromes; thus, hypoperfusion and depressed metabolism of the overlying cortex and of the contralateral cerebral and cerebellar hemispheres have been demonstrated. 5 Studies such as these have made possible documentation of the neural networks used for motor recovery after hemiplegic stroke" and relearning speech during recovery from aphasia after stroke wherein pathways of the contralateral hemisphere were shown to facilitate
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functional recovery.I-" In the future, we hope to learn more about the brain and behavior in health and disease by using imaging of the brain in combination with meticulous neurologic and cognitive testing. John Stirling Meyer, M.D. Director, Cerebral Blood Flow Laboratory Department of Veterans Affairs Medical Center Professor of Neurology Baylor College of Medicine Houston, Texas
REFERENCES
1. Meyer JS, Hata T, Imai A: Clinical and experimental studies of diaschisis. In Cerebral Blood Flow: Physiological and Clinical Aspects. Edited by JH Wood. New York, McGraw-Hill Book Company, 1987, pp 481-502
2. Denny-Brown D, Meyer JS, Horenstein S: The significance of perceptual rivalry resulting from parietal lesion. Brain 75:433-471, 1952 3. Brooks DJ: PET: its clinical role in neurology (editorial). J Neurol Neurosurg Psychiatry 54:1-5, 1991 4. Meyer JS, Shinohara T, Imai A, Kobari M, Sakai F, Hata T, Oravez WT, Timpe GM, Deville T, Solomon E: Imaging local cerebral blood flow by xenon-enhanced computed tomography-technical optimization procedures. Neuroradiology 30:283-292, 1988 5. Pappata S, Mazoyer B, Tran Dinh S, Cambon H, Levasseur M, Baron JC: Effects of capsular or thalamic stroke on metabolism in the cortex and cerebellum: a positron tomography study. Stroke 21:519-524,1990 6. Chollet F, DiPiero V, Wise RJS, Brooks DJ, Dolan RJ, Frackowiak RSJ: The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol 29:63-71,1991 7. Meyer JS, Sakai F, Yamaguchi F, Yamamoto M, Shaw T: Regional changes in cerebral blood flow during standard behavioral activation in patients with disorders of speech and mentation compared to normal volunteers. Brain Lang 9:61-77, 1980 8. Yamaguchi F, Meyer JS, Sakai F, Yamamoto M: Case reports of three dysphasic patients to illustrate rCBF responses during behavioral activation. Brain Lang 9:145-148, 1980
of objects as did patients with right parietal cortical sensory loss and with persistent hemineglect. Bilateral impairments of somesthetic identification ofobjects, demonstrated by impairment on testing the right hand (ipsilateral to the right hemispheric lesions), were seen only in patients with extensive right hemispheric infarctions, all of which involved the parietal lobe. All these patients exhibited severe left-sided neglect. After careful consideration and rejection of other different and possible explanations, Caselli concluded that impairments of somesthetic recognition in the right hand (ipsilateral to the lesion) after severe right hemispheric infarction resulted from transcallosal depression ofthe function of the parietal cortex, contralateral to the infarct, which impaired arousal and attentional mechanisms by "transcallosal diaschisis." Is this explanation, implicating "diaschisis" as being responsible for the inattention of the contralateral hemisphere, scientifically acceptable, or is it merely substituting one unknown for another? In the light of recent studies of diaschisis that included the use of three-dimensional analysis of cerebral blood flow and metabolism, this explanation is certainly scientifically acceptable. The considerable data accumulated during the past 20 years about the nature of diaschisis support Caselli's explanation for his carefully documented clinical observations. Diaschisis-or a "splitting of function"-is a term that was originally proposed in 1914 by the Russian neurologist von Monakow to describe remote depressions of brain function that were noted at a distance from a circumscribed lesion of the brain. Von Monakow postulated that diaschisis was due to a severance of nervous connections or fiber tracts that connected the site of the cerebral lesion with other regions of the brain, causing their functional depression. Since then, several neurophysiologic studies, including measurements of regional cerebral blood flow and metabolism, have supported the hypothesis of von Monakow. Disconnections in
430
Mayo Clin Proc, April 1991, Vol 66
the white matter tracts of the corpus callosum are known to be a frequent cause of diaschisis both in patients and in animal models; thus, infarctions ofthe ipsilateral hemisphere depress the function, perfusion, and metabolism not only of the ipsilateral but also of the contralateral hemisphere. 1 The most important single mechanism responsible for diaschisis, as judged by remote reductions of local cerebral perfusion and metabolism, is structural or functional deafferentation or disconnection of white matter fibers that connect one group of cerebral neurons to another. Close perusal of Figure 2 in Caselli's article shows that most of the right hemisphere, up to and including the right half of the corpus callosum, is indeed involved in the extensive right hemispheric infarction. Therefore, disconnections with the contralateral left (intact) hemisphere may reasonably be expected to result. Measurements of cerebral blood flow together with oxygen and glucose metabolism in many similar patients in this laboratory and others have shown that the contralateral (intact) hemisphere, including not only the parietal lobe and the second somatosensory cortical region (responsible for somesthetically mediated object recognition) but also the contralateral (intact) cerebellar hemisphere, exhibits decreased blood flow and metabolism. Thus, in cases of extensive right hemispheric infarctions, inattention in conjunction with impairments of somesthetic object identification in the ipsilateral hand may indeed be reasonably assumed to result. Investigators have substantiated that among patients with infarction of the parietal lobe, double simultaneous stimulation-or the use of other multiple sensory inputs-progressively impairs simpler unilateral test responses and may eventually result in a "catastrophic reaction" in which patients can no longer respond at all to such complex testing. Caselli's observations together with his diaschisis explanation lend validity to the concept of "impaired attention" that occurs in patients with parietal lesions and leads to a phenomenon termed "perceptual rivalry," a theoretical concept advanced by my-
EDITORIAL
431
self, Denny-Brown, and Horenstein almost 40 years ago. 2 According to the concept of "perceptual rivalry," patients with infarction of the parietal lobe respond to simple tests but with impaired alertness and attention. Consequently, the more complex and bilateral the testing becomes, the more likely the attention will fail and some sensory stimuli will be neglected or ignored by the mutilated nervous system (that is, "sensory inattention"). The study by Caselli indicates how our understanding of behavioral neurology is likely to continue to be advanced with recent developments of three-dimensional brain imaging. 3 Caselli was able to study 30 living patients and to classify them into 6 carefully defined groups on the basis of the anatomic site oftheir cerebral infarctions, as determined by computed tomography and magnetic resonance imaging. Before the advent of neuroimaging, such an extensive study, conducted by one person, would have been impossible because autopsy confirmation of the site of the lesions in such a large series of patients would have been highly improbable. Combining three-dimensional computed tomographic imaging with local measurements of cerebral blood flow is now possible in most major hospitals by having patients inhale 27% xenon during serial computed tomographic scanning. 4 This procedure allows quantitative estimates of brain integrity and regional functional activity to be correlated with neurologic and cognitive test performance. In the limited number of research centers where scanning with positron emission tomography is available, measurements of local perfusion and metabolism have been correlated with the remote effects of capsular and thalamic lesions attributed to diaschisis or disconnection syndromes; thus, hypoperfusion and depressed metabolism of the overlying cortex and of the contralateral cerebral and cerebellar hemispheres have been demonstrated. 5 Studies such as these have made possible documentation of the neural networks used for motor recovery after hemiplegic stroke" and relearning speech during recovery from aphasia after stroke wherein pathways of the contralateral hemisphere were shown to facilitate
432
EDITORIAL
Mayo Clin Proc, April 1991, Vol 66
functional recovery.I-" In the future, we hope to learn more about the brain and behavior in health and disease by using imaging of the brain in combination with meticulous neurologic and cognitive testing. John Stirling Meyer, M.D. Director, Cerebral Blood Flow Laboratory Department of Veterans Affairs Medical Center Professor of Neurology Baylor College of Medicine Houston, Texas
REFERENCES
1. Meyer JS, Hata T, Imai A: Clinical and experimental studies of diaschisis. In Cerebral Blood Flow: Physiological and Clinical Aspects. Edited by JH Wood. New York, McGraw-Hill Book Company, 1987, pp 481-502
2. Denny-Brown D, Meyer JS, Horenstein S: The significance of perceptual rivalry resulting from parietal lesion. Brain 75:433-471, 1952 3. Brooks DJ: PET: its clinical role in neurology (editorial). J Neurol Neurosurg Psychiatry 54:1-5, 1991 4. Meyer JS, Shinohara T, Imai A, Kobari M, Sakai F, Hata T, Oravez WT, Timpe GM, Deville T, Solomon E: Imaging local cerebral blood flow by xenon-enhanced computed tomography-technical optimization procedures. Neuroradiology 30:283-292, 1988 5. Pappata S, Mazoyer B, Tran Dinh S, Cambon H, Levasseur M, Baron JC: Effects of capsular or thalamic stroke on metabolism in the cortex and cerebellum: a positron tomography study. Stroke 21:519-524,1990 6. Chollet F, DiPiero V, Wise RJS, Brooks DJ, Dolan RJ, Frackowiak RSJ: The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol 29:63-71,1991 7. Meyer JS, Sakai F, Yamaguchi F, Yamamoto M, Shaw T: Regional changes in cerebral blood flow during standard behavioral activation in patients with disorders of speech and mentation compared to normal volunteers. Brain Lang 9:61-77, 1980 8. Yamaguchi F, Meyer JS, Sakai F, Yamamoto M: Case reports of three dysphasic patients to illustrate rCBF responses during behavioral activation. Brain Lang 9:145-148, 1980
