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Psychopathology of early frontal lobe damage: Dependence on cycles of development

Published online by Cambridge University Press:  31 October 2008

Robert W. Thatcher*
Affiliation:
Veterans Administration Medical Center, and Departments of Neurology and Radiology, University of South Florida College of Medicine
*
Address correspondence and reprint requests to: Robert W. Thatcher, Ph.D., Neurology Service-151, Veterans Administration Medical Center, Bay Pines, FL 33504.

Abstract

A new theory of frontal lobe development is presented in which the role of the human frontal lobes during normal development and the psychopathological consequences of early frontal lobe injury are explored. Analyses of the development of human electroencephalograph (EEG) coherence indicate that there are oscillations and cyclic growth processes along the mediolateral and anterior-posterior planes of the brain. The cycles of EEG coherence are interpreted as repetitive sequences of increasing and decreasing synaptic effectiveness that reflects a convergence process that narrows the disparity between structure and function by slowly sculpting and reshaping the brain's microanatomy. This process is modeled as a developmental spiral staircase in which brain structures are periodically revisited resulting in stepwise increases in differentiation and integration. The frontal lobes play a crucial role because they are largely responsible for the selection and pruning of synaptic contacts throughout the postnatal period. A mathematical model of cycles of synaptic effectiveness is presented in which the frontal lobes behave as gentle synaptic “predators” whereas posterior cortical regions behave as synaptic “prey” in a periodic reorganization process. The psychopathological consequences of early frontal lobe damage are discussed in the context of this model.

Type
Articles
Copyright
Copyright © Cambridge University Press 1994

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References

Abbie, A. A. (1940). Cortical lamination in the monotremata. Journal of Comparative Neurology, 72, 429467.CrossRefGoogle Scholar
Ackerly, S. S. (1964). A case of prenatal bilateral frontal lobe defect observed for thirty years. In Warren, J. M. & Ackert, K. (Eds.), The frontal granular cortex and behavior (pp. 192218). New York: McGraw-Hill.Google Scholar
Ackerly, S. S., & Benton, A. L. (1947). Report of case of bilateral frontal lobe defect. Proceedings, Associations for Research in Nervous and Mental Disease, 27, 479504.Google Scholar
Bayer, S. A., & Altman, J. (1991). Neocortical development. New York: Raven Press.Google Scholar
Bendat, J. S., & Piersol, A. G. (1980). Engineering applications of correlation and spectral analysis. New York: John Wiley & Sons.Google Scholar
Berryman, A. A. (1981). Population systems: A general introduction. New York: Plenum Press. Berryman, A. A. (1990). Population dynamics: A workbook for POPSYS software. Pullman, WA: Ecological Systems Analysis.Google Scholar
Berryman, A. A., & Stenseth, N. C. (1984). Behavioral catastrophies in biological systems. Behavioral Science, 29, 127135.CrossRefGoogle Scholar
Blinkov, S. M., & Glezer, I. I. (1968). The human brain in figures and tables. New York: Plenum Press.Google Scholar
Bornstein, M. H. (Ed.). (1987). Sensitive periods in development: Interdisciplinary perspectives. Hillsdale, NJ: Erlbaum.Google Scholar
Bornstein, M. H. (1989). Sensitive periods in development: Structural characteristics and causal interpretation. Psychological Bulletin, 105, 179197.CrossRefGoogle Scholar
Braitenberg, V. (1978). Cortical architectonics: General and areal. In Brazier, M. A. B. & Petsche, H. (Eds.), Architectonics of the cerebral cortex. New York: Academic Press.Google Scholar
Carpenter, M. B., & Sutin, J. (1983). Human neuroanatomy. Baltimore, MD: Williams & Wilkins.Google Scholar
Case, R. (1985). Intellectual development: Birth to adulthood. New York: Academic Press.Google Scholar
Case, R. (1987). The structure and process of intellectual development. International Journal of Psychology, 22, 571607.CrossRefGoogle Scholar
Cicchetti, D. (1990). The organization and coherences of socioemotional, cognitive, and representational development: Illustrations through a developmental psychopathology perspective on Down syndrome and child maltreatment. In Thompson, R. (Ed.), Nebraska Symposium on Motivation: Socioemotional development (Vol. 36, pp. 259366). Lincoln: University of Nebraska Press.Google Scholar
Cicchetti, D. (1993). Developmental psychopathology: Reactions, reflections, projections. Developmental Review, 13, 471502.CrossRefGoogle Scholar
Cowan, W. M. (1979). The developing brain. In The brain (pp. 5669). San Francisco: Freeman.Google ScholarPubMed
Cragg, B. G. (1975). The development of synapses in the visual system of the cat. Journal of Comparative Neurology, 160, 147166.CrossRefGoogle ScholarPubMed
Dart, R. A. (1934). The dual structure of the neopallium: Its history and significance. Journal of Anatomy, 69, 319.Google ScholarPubMed
Diamond, M. C., Scheibel, A. B., & Elson, L. M. (1985). The human brain coloring book. New York: Barnes and Noble.Google Scholar
Eckhorn, R., Bauer, R., Jordan, W., Brosch, M., Kruse, W., Munk, M., & Reitboek, H. J. (1988). Coherent oscillations: A mechanism of feature linking in the visual cortex? Biological Cybernetics, 60, 121130.CrossRefGoogle ScholarPubMed
Epstein, H. T. (1980). EEG developmental stages. Developmental Psychobiology, 13, 629631.CrossRefGoogle ScholarPubMed
Eslinger, P. J., Grattan, L. M., Damasio, H., & Damasio, A. R. (1992). Developmental consequences of childhood frontal lobe damage. Archives of Neurology, 49, 764769.CrossRefGoogle ScholarPubMed
Feinberg, I. (1982). Schizophrenia: Caused by a fault in programmed synaptic elimination during adolescence. Journal of Psychiatric Research, 17, 319334.CrossRefGoogle ScholarPubMed
Finger, S., & Wolf, C. (1988). The “Kennard effect” before Kennard: The early history of age and brain lesions. Archives of Neurology, 45, 11361142.CrossRefGoogle Scholar
Fischer, K. W. (1980). A theory of cognitive development: The control and construction of hierarchies of skills. Psychological Review, 87, 477531.CrossRefGoogle Scholar
Fischer, K. W. (1983). Developmental levels as periods of discontinuity. In Fischer, K. W. (Ed.), Levelsand transitions in children's development (pp. 2345). San Francisco: Jossey-Bass.Google Scholar
Fischer, K. W. (1987). Relations between brain and cognitive development. Child Development, 57, 623632.CrossRefGoogle Scholar
Fischer, K. W., & Farrar, M. J. (1987). Generalizations about generalization: How a theory of skill development explains both generality and specificity. International Journal of Psychology, 22, 643677.CrossRefGoogle Scholar
Fischer, K. W., & Pipp, S. L. (1984). Processes of cognitive development: Optimal level and skill acquisition. In Sternberg, R. J. (Ed.), Mechanisms of cognitive development (pp. 4580). New York: Freeman.Google Scholar
Cause, G. F. (1934). The struggle for existence. Baltimore, MD: Williams & Wilkins.Google Scholar
Cause, G. F., & Witt, A. A. (1935). Behavior of mixed populations and the problem of natural selection. American Naturalist, 3, 596609.Google Scholar
Getz, W. M. (1984). Population dynamics: A percapita resource approach. Journal of Theoretical Biology, 108, 623643.CrossRefGoogle Scholar
Gilmore, R. (1981). Catastrophe theory for scientists and engineers. New York: John Wiley & Sons.Google Scholar
Glaser, E. M., & Ruchkin, D. S. (1976). Principles of neurobiological signal analyses. New York: Academic Press.Google Scholar
Gorbach, A. M., Tsicalov, E. N., Kuznetsova, G. D., Shevelev, I. A., Budko, K. P., & Sharaev, G. A. (1989). Infrared mapping of the cerebral cortex. Thermology, 3, 108112.Google Scholar
Grattan, L. M., & Eslinger, P. J. (1991). Frontal lobe damage in children and adults: A comparative review. Developmental Neuropsychology, 7, 283326.CrossRefGoogle Scholar
Grattan, L. M., & Eslinger, P. J. (1992). Long-term psychological consequences of childhood frontal lobe lesion in patient DT. Brain and Cognition, 20, 185195.CrossRefGoogle ScholarPubMed
Gray, C. M., Konig, P., Engel, A. K., & Singer, W. (1989). Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature (London), 338, 334337.CrossRefGoogle ScholarPubMed
Greenough, W., Black, J., & Wallace, C. (1987). Experience and brain development. Child Development, 58, 539559.CrossRefGoogle ScholarPubMed
Hanlon, H. W. (1994). Differences in female and male development of the human cerebral cortex from birth to age 16. Unpublished dissertation.Google Scholar
Holling, C. S. (1959). The components of predation as revealed by a study of small mammal predation of the European pine sawfly. The Canadian Entomologist, 91, 293320.CrossRefGoogle Scholar
Holling, C. S. (1966). The functional response of invertebrate predators to prey density. Memoirs of the Entomological Society of Canada, 48, 186.Google Scholar
Hudspeth, W. J., & Pribram, K. H. (1990). Stages of brain and cognitive maturation. Journal of Educational Psychology, 82, 881884.CrossRefGoogle Scholar
Hudspeth, W. J., & Pribram, K. H. (1991). Physiological indices of cerebral maturation. International Journal of Psychophysiology, 2, 1929.Google Scholar
Huttenlocher, P. R. (1979). Synaptic density in human frontal cortex: Developmental changes and effects of aging. Brain Research, 163, 195205.Google ScholarPubMed
Huttenlocher, P. R. (1984). Synapse elimination and plasticity in developing human cerebral cortex. American Journal Mental Deficiencies, 88, 488496.Google ScholarPubMed
Huttenlocher, P. R. (1990). Morphometric study of human cerebral cortex development. Neuropsychologia, 28, 517527.CrossRefGoogle ScholarPubMed
Huttenlocher, P. R., & de Courten, C. (1987). The development of synapses in striate cortex of man. Human Neurobiology, 6, 19.Google ScholarPubMed
Huttenlocher, P. R., de Courten, C., Carey, L., & Van der Loos, H. (1982). Synaptogenesis in human visual cortexs–Evidence for synapse elimination during normal development. NeuroscienceLetters, 33, 247252.Google ScholarPubMed
John, E. R. (1963). Mechanisms of memory. New York: Academic Press.Google Scholar
Kennard, M. A. (1936). Age and other factors in motor recovery from precentral lesions in monkeys. Journal of Neurophysiology, 1, 477496.CrossRefGoogle Scholar
Kolb, B. (1984). Functions of the frontal cortex of the rat: A comparative review. Brain Research Reviews, 8, 6598.CrossRefGoogle Scholar
Kolb, B. (1989). Brain development, plasticity and behavior. American Psychologist, 44, 12031212.CrossRefGoogle ScholarPubMed
Kolb, B., & Whishaw, I. Q. (1989). Plasticity in the neocortex: Mechanisms underlying recovery from early brain damage. Progress in Neurobiology, 32, 235276.CrossRefGoogle ScholarPubMed
Lilly, J. C., & Cherry, R. (1954). Surface movements of click responses from the acoustic cerebral cortex of the cat: The leading and the trailing edges of a response figure. Journal of Neurophysiology, 17, 521532.CrossRefGoogle ScholarPubMed
Lilly, J. C., & Cherry, R. (1955). Surface movements of figures in the spontaneous activity of anesthetized cerebral cortex: The leading and trailing edges. Journal of Neurophysiology, 18, 1832.CrossRefGoogle ScholarPubMed
Linas, R. R., & Ribary, U. (1992). Rostrocaudal scan in human brain: A global characteristic of the 40-Hz response during sensory input. In Basar, E. & Bullock, T. H. (Eds.), Induced rhythms in the brain (pp. 147154). Boston: Birkhauser.CrossRefGoogle Scholar
Lopes da Silva, F. (1991). Neural mechanisms underlying brain waves: From neural membranes to net-works. Electroencephalography and Clinical Neurophysiology, 79, 8193.CrossRefGoogle Scholar
Lopes da Silva, F., Pijn, J. P., & Boeijinga, P. (1989). Interdependence of EEG signals: Linear vs. nonlinear associations and the significance of time delays and phase shifts. Brain Topography, 2, 918.CrossRefGoogle ScholarPubMed
Lotka, A. J. (1925). The elements of physical biology'. Baltimore, MD: Williams & Wilkins.Google Scholar
Matousek, M., & Petersen, I. (1973). Frequency analysis of the EEG background activity by means of age dependent EEG quotients. In Kellaway, P. & Petersen, I. (Eds.), Automation of clinical eleclroencephalography (pp. 75102). New York: Raven Press.Google Scholar
Nicholson, A. J., & Bailey, V. A. (1935). The balance of animal populations. Proceedings of the Zoological Society of London, 3, 551598.CrossRefGoogle Scholar
Nunez, P. (1981). Electric fields of the brain: Theneurophysics of EEG. New York: Oxford University Press.Google Scholar
Nunez, P. L. (1989). Generation of human EEG by a combination of long and short range neocortical interactions. Brain Topography, 1(3), 199215.CrossRefGoogle ScholarPubMed
O'Leary, D. D. M. (1987). Remodelling of early axonal projections through the selective elimination of neurons and long axon collaterals. In Bock, G. & O'Connor, M. (Eds.), Selective neuronal death (pp. 113142). New York: John Wiley & Sons.Google Scholar
O'Leary, D. D. M., Stanfield, B. B., & Cowan, W. M. (1981). Evidence that the early postnatal restriction of the cells of origin of the callosal projection is due to the elimination of axon collaterals rather than to the death of neurons. Developmental Brain Research, 1, 607617.CrossRefGoogle Scholar
Otnes, R. K., & Enochson, L. (1972). Digital time series analysis. New York: John Wiley & Sons.Google Scholar
Pandya, D. N., & Barbas, H. (1985). Supplementary motor area structure and function: Review and hypotheses. Behavioral and Brain Sciences, 8, 595596.CrossRefGoogle Scholar
Pascual-Marqui, R. D. S. L., Valdes-Sosa, P. A., & Alvarez-Amador, A. (1988). A parametric model for multichannel EEG spectra. International Journal of Neuroscience, 125, 7386.Google Scholar
Purves, D. (1988). Body and brain: A trophic theory of neural connections. Cambridge: Harvard University Press.Google Scholar
Rabinowicz, T. (1979). The differentiate maturation of the human cerebral cortex. In Falkner, F. & Tanner, J. (Eds.), Human growth: Neurobiology and nutrition (pp. 97123). New York: Plenum Press.CrossRefGoogle Scholar
Rakic, P. (1985). Limits of neurogenesis in primates. Science, 227, 10541056.CrossRefGoogle ScholarPubMed
Rakic, P., Bourgeois, J., Eckenhoff, M., Zecevic, N., & Goldman-Rakic, P. S. (1986). Concurrent overproduction of synapses in diverse regions of primate cerebral cortex. Science, 232, 232234.CrossRefGoogle ScholarPubMed
Real, L. (1977). The kinetics of functional response. The American Naturalist, 111, 289300.CrossRefGoogle Scholar
Rogers, R. L., Baumann, S. B., Papanicolaou, A. C., Bourbon, T. W., Alagarsamy, S., & Eisenberg, H. M. (1991). Localization of the P3 sources using magnctoencephalography and magnetic resonance imaging. Electroencephalography and Clinical Neurophysiology, 79, 308321.CrossRefGoogle ScholarPubMed
Sanides, F. (1971). Functional architecture of motor and sensory cortices in primates in the light of a new concept of neocortex development. In Noback, C. R. & Montana, W. (Eds.), Advances inprimatology (pp. 137208). New York: Academic Press.Google Scholar
Schade, J. P., & Groeningen, V. V. (1961). Structural development of the human cerebral cortex. Acata Anatomica, 47, 79111.Google Scholar
Smart, I. H. M. (1983). Three dimensional growth of the mouse isocortex. Journal of Anatomy, 137, 683694.Google ScholarPubMed
Soloman, M. E. (1949). The natural control of animal population. Journal of Animal Ecology, 18, 135.CrossRefGoogle Scholar
Sroufe, L. A., & Rutter, M. (1984). The domain of developmental psychopathology. Child Development, 55, 1946.CrossRefGoogle ScholarPubMed
Thatcher, R. W. (1980). Neurolinguistics: Theoretical and evolutionary perspectives. Brain and Language, 11, 235260.CrossRefGoogle ScholarPubMed
Thatcher, R. W. (1989, 02). Nonlinear dynamics of human cerebral development. Paper presented at the First International Conference on Mechanisms on Mind, E. R. John (Organizer),Havana, Cuba.Google Scholar
Thatcher, R. W. (1991). Maturation of the human frontal lobes: Physiological evidence for staging. Developmental Neuropsychology, 7(3), 397419.CrossRefGoogle Scholar
Thatcher, R. W. (1992a). Are rhythms of human cerebral development “traveling waves”? Behavior and Brain Sciences, 14(4), 575.CrossRefGoogle Scholar
Thatcher, R. W. (1992b). Cyclic cortical reorganization during early childhood development. Brain and Cognition, 20, 2450.CrossRefGoogle Scholar
Thatcher, R. W. (1993, 03). Cyclic cortical morphogenesis: A nonlinear synaptic population model. Abstract presented at the biennial meeting of the Society for Research in Child Development,New Orleans.Google Scholar
Thatcher, R. W. (1994). Cyclic cortical reorganization: Origins of cognition. In Dawson, G. & Fischer, K. (Eds.), Human behavior and the developing brain (pp. 232268). New York: Guilford Press.Google Scholar
Thatcher, R. W., & John, E. R. (1977). Functional neuroscience: Foundations of cognitive processing. Hillsdale, NJ: Erlbaum.Google Scholar
Thatcher, R. W., Krause, P., & Hrybyk, M. (1986). Corticocortical association fibers and EEG coherence: A two compartmental model. Electroencephalography and Clinical Neurophysiology, 64, 123143.CrossRefGoogle ScholarPubMed
Thatcher, R. W., McAlaster, R., Lester, M. L., Horst, R. L., & Cantor, D. S. (1983). Hemispheric EEG asymmetries related to cognitive functioning in children. In Perecuman, A. (Ed.), Cognitive processing in the right hemisphere (pp. 125146). New York: Academic Press.CrossRefGoogle Scholar
Thatcher, R. W., Toro, C., Pflieger, M. E., & Hallett, M. (1993). Multimodal registration of EEG, PET and MRI: Analyses of neural network switching. Berkeley, CA: Society of Magnetic Resonance in Medicine: Functional MRI of the Brain.Google Scholar
Thatcher, R. W., Walker, R. A., & Giudice, S. (1987). Human cerebral hemispheres develop at different rates and ages. Science, 236, 11101113.CrossRefGoogle ScholarPubMed
Thatcher, R. W., Wang, B., Toro, C., & Hallett, M. (1994). Human neural network dynamics using multimodal registration of EEG, PET and MRI. In Thatcher, R., Hallett, M., Zeffiro, T., John, E., & Huerta, M. (Eds.), Functional neuroimaging: Technical foundations (pp. 269278). Orlando, FL: Academic Press.Google Scholar
Thorn, R. (1975). Structural stability and morphogenesis. Reading, MA: W. A. Benjamin.Google Scholar
Thompson, J., & Stewart, H. (1986). Nonlinear dynamics and chaos. New York: John Wiley & Sons.Google Scholar
Tucker, D. M., Roth, D. L., & Blair, T. B. (1986). Functional connections among cortical regions: Topography of EEG coherence. Electroencephalography and Clinical Neurophysiology, 63, 242250.CrossRefGoogle ScholarPubMed
van der Maas, H. L. I., & Molenaar, P. C. M. (1992). A catastrophe theoretical approach to stagewise cognitive development. Psychological Review, 99, 395417.CrossRefGoogle Scholar
Verzeano, M. (1972). Pacemakers, synchronization, and epilepsy. In Petsche, H. & Brazier, M. A. B. (Eds.), Synchronization of EEG activities in epilepsies (pp. 154188). New York: Springer-Verlag.CrossRefGoogle Scholar
Verzeano, M., & Negishi, K. (1960). Neuronal activity in cortical and thalamic networks. Journal of General Physiology, 43(Suppl.), 177.CrossRefGoogle Scholar
Verzeano, M., & Negishi, K. (1961). Neuronal activity in wakefulness and in sleep. In Wolstenholme, G. E. W. & O'Connor, M. (Eds.), The nature of sleep (pp. 108126). London: Churchill.Google Scholar
Volterra, V. (1926). Variazioni e fluttuaxioni del numero d'individui in specie animali conviventi. Memorial R. Academic Lincei Series, 6(2), 2643.Google Scholar
Weiss, P. (1961). Deformities as cues to understanding development of form. Perspectives in Biology and Medicine, 4, 660669.CrossRefGoogle ScholarPubMed
Weiss, P. (1969). The living system: Determinism stratified. In Koestler, A. & Smythes, J. (Eds.), Beyond reductionism (pp. 2536). Boston: Beacon Press.Google Scholar
Zigler, E., & Glick, M. (1986). A developmental approach to adult psychopathology. New York: Wiley.Google Scholar