Basic Connectivity of the Cerebral Cortex and some Considerations on the Corpus Callosum

Basic Connectivity of the Cerebral Cortex and some Considerations on the Corpus Callosum

Neuroscience and Biobehavioral Reviews, Vol. 20, No. 4, pp. 567-570, 1996 Copyright Q 1996 Elsevier Science Ltd. All rights reserved Printed in Great ...

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Neuroscience and Biobehavioral Reviews, Vol. 20, No. 4, pp. 567-570, 1996 Copyright Q 1996 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0149-7634/96 $32.00 + .00

Pergamon

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0149-7634(95)00069-0

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microscopic sections (Fig. 2). This suggests that conduction times short enough to build up common activity in both hemispheres are given in some cases, but not in others. There is reason to assume that average conduction times across the corpus callosum are longer in large brains than in small brains. A comparison of the fibre diameters in the corpus callosum of mouse and monkey suggests that the thickness of the fibres does not increase sufficiently to fully compensate for the longer distances in larger brains. Although fibres in the monkey corpus callosum reach a thickness of 3 pm (Fig. 3), in some regions even about 9pm (12), such fibres are rare (Fig. 2). Preliminary measurements in cooperation with Jerison (11) indicate that the bulk of myelinated fibres in the two animals have diameters between 0.5 and 1 pm (Fig. 3). There are some open questions with regard to the unmyelinated fibres, the percentage of which may differ in different species. However, theoretical approaches also speak in favour of longer average conduction times in larger brains. Ringo et al. (19) showed that, if in brains of different sizes, average conduction times were to be kept constant, large brains would be much larger than is the case. as a result of the increased bulk of white substance

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FIG. 3. Measurements on the thickness of myelinated fibres in the corpus callosum of mouse and monkey. The upper graph shows the relative frequency, and the lower graph, the absolute frequency of fibres of the indicated thickness. All myelinated axons on the sample areas were measured. The myelin sheath is included in these measurements (same data as in (11)).

due to the thicker fibres. The authors pointed out that, in brains with a large number of neurons, much fibre mass can be saved by lateralization of those functions in which there is no obvious necessity for a co-operation between both hemispheres. Then, only a limited number of fibres has to be thick enough to compensate for the longer conduction times in larger brains. What might then be the task of the thin fibres in large brains? They might be involved in another important aspect of cortical information processing, the necessity of sequence formation. One possibility for the generation of sequences is the introduction of delays to cortical information flow. Such delays could be achieved by slow conduction velocity in long fibres such as are present in the corpus callosum (13). These fibres might thus be responsible for the successive ignition of cell assemblies located in different hemispheres. ACKNOWLEDGEMENTS

We are grateful to Valentin Braitenberg and Friedemann Pulvermuller for various discussions, to Monika Dortenmann for carrying out the measurements on fibre thickness and to Shirley Wiirth for correction of the manuscript.

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SCHUZ AND PREI13L REFERENCES

1. Aboitiz, F.; Scheibel, A. B.; Fisher, R. S.; Zaidel, E. Individual

12. LaMantia, A. S.; Rakic, P. Cytological and quantitative charac-

differences in brain asymmetries and fiber composition in the human corpus callosum. Brain Res. 598:154-161;1992. Blinkov, S. M.; Glezer, I. I. Das Zentralnervensystem in Zahlen und Tabellen. Jena: VEB Gustav Fischer; 1968. Braitenberg, V. Cell assemblies in the cerebral cortex. In: Heim, R.; Palm, G., eds. Theoretical approaches to complex systems. Lecture notes in biomathematics 21. Berlin: Springer; 1978: 171-188. Braitenberg, V.; Schiiz,A. Anatomy of the Cortex. Statistics and Geometry. Berlin: Springer; 1991. Caminiti, R.; Sbriccoli, S. The callosal system of the superior parietal lobule in the monkey. J. Comp. Neurol. 237:85-99; 1985. Cusick, C. G.; MacAvoy, M. G.; Kaas, J. H. Interhemispheric connections of cortical sensory areas in tree shrews. J. Comp. Neurol. 235:111-128;1985. Greilich, H. Quantitative Analyse der cortico-corticalen Femverbindungen bei der Maus. Thesis at the Faculty of Biology at the University of Tubingen; 1984. Hebb, D. O. Organization of behaviour. A neuropsychological theory. New York: Wiley and Sons; 1949(2nd ed. 1961). Horner, C. H. Plasticity of the dendritic spine. Progr. in Neurobiol. 41:281-321;1993. Innocenti, G. M. General organization of callosal connections in the cerebral cortex. In: Jones, E. G.; Peters, A. eds. Cerebral Cortex, Vol. 5, Sensory-motor areas and aspects of cortical connectivity. New York, London: Springer; 291–353;1986. Jerison, H. Brain size and the evolution of mind. 59th James Arthur Lecture. New York: Am. Mus. of Nat. Hist.; 1991.

teristics of four cerebral commissures in the rhesus monkey. J. Comp. Neurol. 291:52@537;1990. Miller, R. Representation of brief temporal patterns, Hebbian synapses, and the left-hemisphere dominance for phoneme recognition. Psychobiol. 15 (3):241–247;1987. Miller, R. Cortico-hippocampalinterplay and the representation of objects in the brain. Berlin: Springer; 1991. Miller, R. An interpretation, based on cell assembly theory, of the psychologicalimpairments followinglesions of the hippocampus and related structures. In: Delacour, J., ed. The memory system of the brain. Singapore:World Scientific;659–712;1994. Palm, G. Neural assemblies. An alternative approach to artificial intelligence. Berlin, Heidelberg: Springer, 1982. Palm, G. Associative networks and cell assemblies. In: Palm, G.; Aertsen, A., eds. Brain theory. Berlin: Springer; 211-228;1986. Palm, G. On the internal structure of cell assemblies. In: Aertsen, A., ed. Brain Theory. Spatio-temporal aspects of brain function. Amsterdam: Elsevier; 261-270;1993. Ringo, J. L.; Doty, R. W.; Demeter, S.; Simard, P. Y. Time is of the essence: A conjecture that hemispheric specialization arises from interhemispheric conduction delay. Cerebral Cortex 4:331-343(1047-3211/94);1994. Yorke, C. ‘H.; Caviness,’V. S. Jr. Interhemispheric neocortical connections of the corpus callosum in the normal mouse: A study based on anterograde and retrograde methods. J. Comp. Neurol. 164:233-246;1975. Zfiborsky, L.; Wolff, J. R. Distribution patterns and individual variations of callosal connections in the albino rat. Anat. Embryol. 165:213-232;1982.

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4. 5. 6. 7. 8. 9. 10.

11.

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13. 14. 15.

16. 17. 18. 19.

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