INTERACTION BETWEEN TRANSCALLOSAL AND THALAMOCORTICAL EXCITATION UDC 621.822.3.087

V. L. Bianki

The view is argued that the transcallosal flow of excitation performs three basic and closely interconnected functions: modulation of the size, concentration, and displacement of the thalamocortical flow of excitation. To express the situation in its general form, this amounts to filtration of the afferent flow. It is done by means of a mosaic of functional units, consisting mainly of a constellation of neurons with facilitatory center and depressing periphery, converting the ascending flow into a special kind of "funnel." KEY WORDS: integrative activity of the cortex; interaction between transcallosal and thalamocortical excitation; visual, auditory, and motor cortex; corpus callosum; callosotomy; general anesthesia.

The question of the role of horizontal and vertical flows of excitation and interaction between them occupies an important place in the problem of cortical integrative activity. At different stages of development of the problem the role either of intercortical connections (for example, classical associative psychology) or of subcortico-cortical pathways (in particular, views on the recticular formation) has been mainly emphasized. This problem still remains a matter for debate in modern neurophysiology also. However, as Adrianov [1] rightly observes, it is evident that the association systems are closely linked and interact with the projection systems; moreover, each of them evidently is represented by several channels, similar in structure but not functionally equivalent. It is important to note that when the problem of interaction between projection and association pathways is examined, the latter term is usually taken to mean only intrahemispheric association connections, and it completely disregards interhemispheric commissural systems. In this way the brain is deprived of its "third dimension." Nevertheless neocortical commissures and, in particular, the corpus callosum, contain very many fibers from all conducting tracts of the CNS [18]. It seems likely that the normal integrative activity of the cortex is effected through interaction between excitation spreading along projection, association, and commissural connections. In this context a fact described by Iontov et al. [8] is very important. They showed that an area of cortex in which callosal afferents, projection fibers from the lateral geniculate body, and association fibers from the visual areas are concentrated is located in the caudal part of the middle suprasylvian fissure of the cat on the boundary between areas 22, 2 I, and 7. It is natural to postulate an important role for this area in the processing of visual information. The question of interaction between transcallosal and thalamocortical flows of excitation has so far been investigated completely inadequately. The effect of callosal activity on other cortical systems is apparently highly complex. It has been shown that during interaction between transcallosal and thalamocortical excitation both facilitatory and depressing effects may be observed. The type of effect depends to some extent on the interval between stimuli [17, 19], on their order [ 17, 20], on the relations between these parameters [13], and also on whether the stimulated point of the cortex is homoor heterotopical [ 15 ]. In the investigation described below interaction between transcallosal and thalamocortical flows of excitation in the visual, auditory, and motor cortex of the cat was studied. METHOD

Experiments were carried out on 70 cats by the technique of functional topography of evoked potentials [3-5 ]. Weak anesthesia, induced with pentobarbitol alone or in conjunction with chloralose, was used. Bilateral and unilateral stimuli (flashes, clicks, electrical stimulation of nerves of the fore- or hindlimbs) were applied. Bilateral and unilateral applied under diotic conditions, i.e., they consisted of two equal unilateral components, with strict verification of the identity of the parameters of the unilateral components. Stimuli of near-threshold and high intensity (for the focus of maximal activity) were used. Evoked potentials were recorded by a monopolar technique by scanning symmetrical cortical points by means of two electrodes with tips about 40/1 in diameter. The electrodes were moved successively in steps of 1 mm over the surface of the cortex. In the visual region (mainly areas 17, 18, and 19) evoked potentials were derived from 200-270 points, in the auditory cortex (areas AI, AII, and EP) from 246 points, and in the motor cortex (areas 3, 4, and 6) Laboratory of Physiology of Behavior, Biological Institute, Leningrad University. Translated from Fiziologicheskii Zhurnal SSSR imeni.I.M. Sechenova, Vol. 65, No. 4, pp. 481-491, April, 1979. Original article submitted April 20, 1978.

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0097-0549/81/1104- 0328 $07.50 9 1982 Plenum Publishing C o r p o r a t i o n

from 170 points. A map of a particular region of the cortex was thus produced, after which the corpus callosum was divided, and the map of evoked potentials was recorded a second time. The results were processed as follows. Averaged and individual maps of the distribution of evoked potentials and of callosal influences were drawn. When the averaged maps of distribution of evoked potentials were compared, data for all animals and all hemispheres tested in the given series were pooled. Amplitudes of evoked potentials or their components were ranked in four classes. Ranking was independent before and after division of the corpus callosum. Class I included amplitudes varying between 100 and 76%, II between 75 and 51%, III between 50 and 26%, and IV between 25 and 0%. The term "focus of maximal activity" was used to describe ranking in class I. When the averaged maps of callosal influences were drawn, data obtained on all animals of the given series were pooled. The character and degree of change of amplitude of the evoked potentials and their components at the same points of the cortex as a result of division of the corpus callosum were compared. The increase in amplitude of the evoked potentials after callosotomy was taken as an indicator of the existence of depressing interhemispheric influences under normal conditions, whereas a decrease was taken as an indicator of facilitatory influences. To characterize the degree of caUosal influences values of differences in amplitudes of evoked potentials before and after division of the corpus callosum were ranked by the method described below. Besides the averaged maps, individual maps of distribution of evoked potentials and callosal influences also were drawn in the same way. All data were subjected to statistical analysis and the results of the operations were verified morphologically. EXPERIMENTAL RESULTS Functions of the Transcallosal Flow of Excitation The experiments showed that division of the corpus callosum causes changes in the size of the focus of maximal activity in the visual, auditory, and motor cortex in response to afferent stimulation. The following general rule was observed: A small focus of maximal activity (FMA) was increased as a result of callosotomy, a large FMA, on the other hand, was reduced in size. This relationship between the size of the FMA and the character of its changes after division of the corpus callosum is clearly visible in the averaged maps of distribution of evoked potentials obtained during bilateral stimulation at different intensities (Figs. 1, 2, 3). In the visual cortex (Fig. 1, I, A, B; II, A, B) FMA narrowed with the strength of stimulation being increased. Division of the corpus callosum caused a decrease in the size of a large focus by 1.5 times and an increase in the size of a small FMA by 1.2 times. In the motor cortex (Fig. 3, I, A, B; II, A, B) the FMA increased in size with an increase in the strength of stimulation of nerves to the hind limbs. Division of the corpus callosum led to an approximately threefold increase in the size of a small focus and a decrease on average by 1.2 times in the area of a large focus. All t~le influences described above were exhibited to the positive and negative components of the evoked potentials. The same rule also was reflected in fragments of individual maps of interhemispheric relations recorded during bilateral stimulation (Figs. 1, 2, 3). A small FMA in the visual, auditory, and motor cortex was widened after division of the corpus callosum (Fig. i, V, A, C; Fig. 2, V, B; Fig. 3, IV, B) whereas a large FMA was narrowed (Fig. 1, V, B; Fig. 2, V, C; Fig. 3, IV, C). Similar results were obtained on the motor cortex during stimulation of nerves to the forelimbs [5 ], during a study of the effect of callosotomy on the FMA in the visual, auditory, and motor cortex produced by unilateral stimuli [3-5, 14], and also separately in each area of the visual cortex during binocular stimulation [3]. In the last case the effect of widening of the focus of maximal activity as a result of section of the corpus callosum was most marked in area 18, which is known to receive the largest number of callosal afferents [10]. The facts stated above are evidence that one of the basic functions of the transcallosal flow of excitation in the intact brain is modulation of the size of the FMA, namely a decrease in the size of a small focus and an increase in the size of a large focus. It is interesting to compare the frequency and abundance of these two effects of division of the corpus callosum widening and narrowing of the FMA - in the visual, auditory, and motor cortex. It has been found that both during bilateral (Figs. 1, 2, 3) and during unilateral [3-5, 14] stimulation the effect of widening of the FMA under the influence of division of the corpus callosum was found more than twice as often and was approximately twice as intensive as the narrowing effect. In some cases widening of the FMA under these circumstances was accompanied by its breaking up into several smaller foci. Hence it follows that the other basic function of the transcallosal flow of excitation in the intact brain consists of concentration (limitation) of the FMA of thalamocortical excitation. Analysis of the location of the FMA in the visual, auditory, and motor cortex before and after division of the corpus callosum showed that callosotomy as a rule caused some displacement of the focus, mainly in the oral-caudal direction (Figs. 1, 2, 3) [3-5, 14]. During weak stimuli the foCus in the visual and auditory cortex was shifted mainly in the caudal direction, but with an increase in the strength of stimulation it moved in the oral direction. In the motor cortex, 329

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Fig. 1. Maps of distribution of evoked potentials and of callosal influences in visual cortex during binocular stimulation. I, II) Averaged maps; I) weak, II) strong stimuli; I, A, B and II, A, B) maps of distribution of evoked potentials; I, C, D, and II, C, D) maps of callosal influences. Legend to shading for I, II: 1) class I, 2) class II, 3) class III, 4) class IV of ranking of amplitude of evoked potentials. III-V) Fragments of individual maps of callosal influences: III, A, B, C, D) callosal influences with facilitatory center and depressing periphery; IV, A, B, C, D) callosal influences with depressing center and facilitatory periphery; V, A, B, C) effect of division of corpus callosum. Legend to shading for III-V: 1) FMA, 3) depressing, 5) facilitatory callosal influences; broken line - outlines of FMA after division of corpus callosum. on the other hand, during an increase in the strength of stimulation displacement mainly in the oral direction gave way to caudal displacement. A shift of the FMA of thalamocortical excitation mainly in the oral and caudal directions is thus seen to be the third basic function of the transcallosal flow of excitation. The direction of displacement in this case corresponds to the caudo-rostral principle of distribution of thalamic projections to the neocortex [ 1 ].

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Fig. 2. Maps of distribution of evoked potentials and of callosal influences in auditory cortex during binocular stimulation. III, A, B, C) Callosal influences with facilitatory center and depressing periphery; III, D and IV, A, B, C) callosal influences with depressing center and facilitatory periphery; IV, D, and V, A, B, C) effect of division of corpus callosum. Remainder of legend as in Fig. 1.

Properties of the Transcallosal Flow of Excitation Averaged ranked maps of facilitatory and depressing callosal influences in the visual, auditory, and motor cortex during afferent stimulation are given in Figs. 1, 2, 3: I, C, D; II, C, D. They were drawn for the intact brain and they reflect changes in amplitude of evoked potentials taking place after division of the corpus callosum. To some extent they have the same meaning as maps of distribution of transcallosal evoked potentials. The figures show that zones of facilitatory and depressing callosal influences are characterized by a concentric structure and a rather elongated shape. In the center of each zone the corresponding influences are usually most strongly expressed, and they gradually weaken toward the periphery. As a rule facilitatory and depressing zones make contact with one another in their regions of weakest intensity. The dynamic character of the facilitatory and depressing zones will be noted (Figs. 1, 2, 3: I, C, D; II, C, D). With an increase in the strength of stimulation the size of the depressing zones in the visual and auditory cortex increased whereas the size of the facilitatory zones decreased, and this was accompanied by a change in their location and configuration. In the motor cortex an increase in the strength of stimulation led to the opposite results.

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Fig. 3. Maps of distribution of evoked potentials and callosal influences in motor cortex during bilateral stimulation of sciatic nerves. IV, A) Callosal influences with depressing center and facilitatory periphery; IV, B, C) effect of division of corpus callosum. Remainder of legend as to Fig. 1. Analysis of the location of foci of maximal activity in the corresponding zones was undertaken by projecting them on maps of callosal influences. It was shown that normally the FMA could lie completely or mainly in a facilitatory (visual and motor cortex) or a depressing zone (auditory cortex). After division of the corpus callosum, however, its variable part was even more strictly localized: The widened area lay in the depressing zone and the narrowed part in the zone of facilitation. These rules could be studied in more detail on individual maps of callosal influences in the visual, auditory, and motor cortex. Altogether 140 such maps were analyzed. Characteristic fragments are shown in Figs. 1, 2, and 3. Influences with a facilitatory center and depressing periphery were among the most frequent type of callosal influences encountered. The depressing periphery under these circumstances could surround the center of all four sides (Fig. 1, III, A; Fig. 2, III, A; Fig. 3, III, A) or could lie on three, two, or one side of it (Fig. 1, III, B, C, D; Fig. 2, III, B, C; Fig. 3, III, B, C, D). Influences with a depressing center and facilitatory periphery were a much less frequent type of transcallosal influence. The facilitatory periphery in this case either surrounded the center of all four sides (Fig. 1, IV, A; Fig. 2, III, D) or could lie on three, two, or one of its sides (Fig. 1, IV, B, C, D; Fig. 2, IV, A, B, C; Fig. 3, IV, A).

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Fig. 4. Scheme of interaction between transcallosal and thalamocortical flows of excitation. I) Modulation of small, II, III) of large FMA. A) FMA, B) Callosal influences, C) interaction between transcallosal and thalamocortical flows of excitation. I) FMA, 2) depressing, 3) facilitatory callosal influences. Essentially the FMA as a rule was located in the central part of the callosal influences, usually closer to the border, and sometimes extending beyond its limits. It must be emphasized that with an increase in the strength of stimulation a certain tendency was observed for the number of callosal influences with depressing center and facilitatory periphery to increase. Within each cortical region tested several functional units of callosal influences could be observed, and sometimes they could belong to different types. All the general principles described above were reflected in both components of the evoked potentials.

DISCUSSION Three basic functions, closely interconnected, of transcallosal excitation were described above: modulation of the size, concentration, and displacement of the thalamocortical flow of excitation. Modulation of the size of the thalamocortical flows consisted of a decrease in the size of the small and an increase in the size of the large flow, leading to greater contrast of the differences between them, and so evidently facilitating the analysis of their intensity. Concentration of thalamocortical excitation probably serves the purpose of its filtration. Displacement of the thalamocortical flow of excitation evidently helps to direct it into a particular "channel." As an example the role of callosal influence in the concentration and direction of excitation into the zone of representation of the hindlimbs (area 4) and in widening of the flow and its direction into area 6, stimulation of which induces globally organized movements of muscle groups [5 ], can be mentioned. During the study of the properties of the transcallosal flow of excitation two types of callosal influences were found: those with a facilitatory center and depressing periphery and those with a depressing center and facilitatory periphery. A constellation of neurons with facilitatory center and depressing periphery can be regarded as the main functional unit of callosal influences. Similar results were obtained by the writer previously in a' study of interaction between the callosal and extracallosal systems [6]. The same principle also is realized at the neuronal level. It has been shown that during transcallosal stimulation the central zone of excitation, surrounded by a zone of inhibition, arises in the symmetrical area of cortex [9, 15 ]. This similarity in the organization of callosal influences and receptive fields of neurons in the visual cortex and lateral geniculate body will also be evident [121. To some extent it can be understood if callosal fibers are regarded as the continuation of projection pathways [7]. How does the transcallosal flow of excitation organize its own basic functions? The following facts must be borne in mind: 1) An FMA of thalamocortical excitation was localized in the zone of facilitatory or depressing callosal influences. 2) Part of the focus widened as a result of division of the corpus callosum was located in the zone of depressing, and the narrowed part in the zone of facilitatory callosal influences. It was shown previously that facilitatory interhemispheric interactions take place through summation of transcallosal and thalamocortical excitation, whereas depressing interactions take place through reciprocal influences [2]. Consequently, narrowing of the focus in the intact brain takes place on account of reciprocal interhemispheric influences, whereas it is widened on account of a summation process.

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Fig. 5. Isometric reconstruction of evoked potentials to bilateral stimulation. Averaged data: I) visual, II) auditory, III) motor cortex. II) Weak, I, III) strong stimuli. A) Before, B) after division of corpus callosum. Two main models of transcallosal modulation of thalamocortical excitation can be suggested (Fig. 4). The first of them is based on the existence of two types of callosal influences: those with a facilitatory center and depressing periphery and those with a depressing center and facilitatory periphery. It will be clear from Fig. 4, I, II that narrowing of the small FMA can take place on account of a reciprocal inhibition of its edges, whereas widening of a large FMA can take place on account of summation of transcallosal and thalamocortical excitation around its edges. In the last case sometimes a small "hole" is observed in the center of the focus (Fig. 3, II, A). The second model is based on the existence of variations in the relative size of the facilitatory and depressing zones in the case of callosal influences with excitatory center and depressing periphery. It will be clear from Fig. 4, I, II, that narrowing o f a small FMA takes place when the facilitatory center is smaller than the focus and that it occurs on account of reciprocal inhibition of its edges, whereas widening takes place when the facilitatory center is larger than the focus on account o f the summation of excitation around its edges. Functions of modulation of the size and concentration of thalamocortical excitation can take place by the methods described above. The function of displacement of the thalamocortical flow, on the other hand, is realized simultaneously, evidently because of noncongruence of the configurations of the flow and zones of callosal influences. All functions of transcallosal excitation are thus performed by a complex, dynamic mosaic of neuronal constellations, consisting o f units with different values of center and periphery. The general results of the process of interaction between transcallosal and thalamocortical excitation can be seen in a very demonstrative form in Fig. 5, which is an isometric reconstruction of the topography of evoked potentials in the visual, auditory, and motor cortex. Clearly in animals with an intact corpus callosum the relief of the evoked potentials was much sharper and more contrasted than in the absence of interhemispheric connections. The role of inhibition, of what

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Ukhtomskii [ 11 ] calls the "sculptor's chisel" shaping the block of stimuli, can be clearly seen here. Some time ago Bdkrsy [ 16] postulated that at different levels of the CNS a filtration process takes place, limiting and directing excitation by means of its intensification through summation and the weakening of its periphery through inhibition, which creates a unique sort of "funnel" from this excitation. This process lowers the absolute and raises the differential threshold and increases the signal to noise ratio, thereby improving stimulus localization. The similarity between these regular features and the data obtained by the study of interaction between transcallosal and thalamocortical flows of excitation will easily be seen. In this particular case it is the transcallosal flow which converts thalamocortical excitation into a "funnel." Previous investigations in the writer's laboratory also showed that the removal of transcallosal excitation by division of the corpus callosum leads to raising of the absolute threshold of light discrimination [ 10], to lowering of the differential threshold discrimination of three-dimensional visual and acoustic stimuli [2], and also to worsening of the signal to noise ratio in the case of binaural acoustic stimuli [ 14]. The results described above thus demonstrate the important role of interaction between projection and commissural pathways in the cortex in integrative brain activity - a role which in its most general form consists of filtration of afferent excitation. LITERATURE CITED 1. O.S. Adrianov, On the Principles of Organization of Integrative Brain Activity [in Russian], Meditsina, Moscow (1976). 2. V.L. Bianki, Evolution of the Paired Function of the Cerebral Hemispheres [in Russian], Leningrad University Press, Leningrad (1967). 3. V.L. Bianki and V. A Kurochkin, "Transcallosal modulation of a focus of maximal activity in the visual cortex," Fiziol. Zh. SSSR, 6_!1,No. 11, 1605 (1975). 4. V.L. Bianki and V. A. Kurochkin, "Callosal influences on a focus of maximal activity in the visual cortex during nearthreshold stimulation," Nauch. Dokl. Vyssh. Shkol., Biol. Nauki, No. 9, 76 (1976). 5. V.L. Bianki and I. A. Makarova, "Transcallosal modulation of a focus of maximal activity in the motor cortex," Fiziol. Zh. SSSR, 6_33,No. 10, 1376 (1977). 6. V.L. Bianki, V. A. Shramm, and E. V. Kharitonov, "Interaction between callosal and extracallosal systems," Fiziol. Zh. SSSR, 65, No. 2, 173 (1979). 7. M. Gazzaniga, The Bisected Brain, Plenum Press (1970). 8. A.S. Iontov, V. A. Otellin, E. E. Granstrem, and F. N. Makarov, Outlines of Morphology of Connections in the Central Nervous System [in Russian], Nauka, Leningrad (1972). 9. A.B. Kogan and G. A. Kuraev, "Organization of responses of the sensomotor cortex to stimulation of symmetrical points of the other hemisphere," Fiziol. Zh. SSSR, 6___22,No. 1, 56 (1976). 10. V.A. Kurochkin, "Effect of division of the corpus callosum on thresholds of visual stimulation," Vestn. Leningr. Gos. Univ., Noo 9, 155 (1972). 11. A. A. Ukhtomskii, The Dominant Focus [in Russian], Nauka, Moscow-Leningrad (1966). 12. D. Hubel, The Visual Cortex. Perception. Mechanisms and Models [Russian translation], Nit, Moscow (1974), pp. 169-184. 13. L.M. Chuppina, "Electrophysiological characteristics of convergence of transcallosal and somatosensory excitation in the somatosensory area of the rabbit cortex," Byull. t~ksp. Biol. Med., 74, No. 9, 8 (1972). 14. G.G. Shurgaya, V. I. Galunov, I. V. Koroleva, and A. A. Fedorov, "Functional interhemispheric asymmetry in the auditory cortex of the cat," in: Functional Asymmetry and Adaptation in Man [in Russian], Meditsina, Moscow (1976), pp. 296-297. 15. H. Asanuma and O. Okuda, "Effects of transcallosal volleys on pyramidal tract cells activity of cat," J. Neurophysiol., 2_55, 192 (1962). 16. G. B~krsy, Sensory Inhibition, Princeton University Press, Princeton, New Jersey (1967). 17. F. Bremer, J. Brihaye, and G. Andre-Balisaux, "Physiologic et pathologie du corps calleux," Arch. Suisses Neurol. Psychiat., 78, 31 (1956). 18. H.T. Chang, "Cortical response to callosal volleys," J. Neurophysiol., k6, No. 2, 117 (1953). 19. B. Grafstein, "Organization of callosal connections in suprasylvian gyms of cat," J. Neurophysiol., 22, 504 (1959). 20. W.M. Landau, G. H. Bishop, and M. H. Clare, "The interactions of several varieties of evoked response in visual and association cortex of the cat," Electroencephalogr. Clin. Neurophysiol., 1_33,43 (I 961).

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