INFLUENCE OF PULSE STIMULATION OF THE VISUAL CORTEX ON THE FUNCTION OF THE SUPERIOR COLLICULUS OF THE AWAKE RABBIT N. A. Gadzhieva, F. B. Kulieva, L. I~. Kul'gavin, and I~. I. Kuliev
UDC 612.825.54+612.826
It has been demonstrated in awake rabbits that stimulation of the visual cortex by a solitary pulse of electrical current leads to the formation of a short-latency response in the superior colliculus. The formation of this response is suppressed when a light stimulus precedes it. At the same time, a conditioning solitary electrostimulation of the visual cortex induces a short inhibition of the formation of the response to the test light stimulus. This fact suggests that the influences of the visual cortex on the functioning of the superior colliculus may be biphasic in character. When the adrenergic apparatus of the reticular formation is blocked this inhibitory influence bears a more pronounced and prolonged character. The stimulation of the reticular formation, on the other hand, by means of anodic polarization leads to the diametrically opposite effect: the inhibitory character of the influence of the cortex is replaced by a facilitatory one. The inference is drawn that the character and the directionality of the influence of the visual cortex on the functioning of the superior colliculus is determined to a significant degree by the initial functional state of nonspecific brain systems. It is known [4, 5, 8, 12] that visual information reaches the superior colliculus both along direct retinocoIlicular pathways and along inputs mediated through the visual area of the cerebral cortex. However, the cortical inputs to the superior colliculus which take their origin in layer V of the visual cortex [9,19] play not only a retransmitter role, but a regulatory role as well. In particular, it has been demonstrated [1, 3, 7] that constant stimulation (high-frequency electrical stimulation, the application of strychnine, etc.) or functional switching on of the visual cortex leads to perceptible changes in the formation ~f visual responses of the superior colliculus; this attests to the presence of tonic influences of the visual cortex on the function of this midbrain visual center. Investigations carried out in cats in acute experimental conditions [11] have made it possible to hypothesize that the influences of the visual cortex on the function of the superior colliculus may also be phasic in character. The fact that significant changes in the formation of evoked activity of neurons of the superior colliculus are observed in conditions of the conditioning pulse stimulation of the visual cortex serves as evidence of this. Despite the fact that the possibility of the activation of the neurons of this structure in rabbits evoked by stimulation of the visual cortex by a single pulse of current has been demonstrated [20], the presence of phasic influences of the visual cortex on the function of the superior colliculus of this animal has been denied [14]. It should be noted that the above-mentioned investigations were carried out on anesthetized rabbits; this could have influenced the final result to a significant degree. Thus, in particular, it is known [10] that the barbiturates facilitate the discharge of GABA from the synaptic cleft and the activation of extrasynaptic GABA-sensitive receptors. It is possible that even the electrical stimulation of the visual cortex may not elicit excitation of its neurons in these conditions, and, consequently, the possibility is lacking for the organization of phasic influences on the functioning of the superior colliculus. Taking into account the characteristics of the functional role of the superior colliculi, which are associated, in particular, with the effectuation of rapid oculomotor reactions, as well as the data concerning the existence of direct corticocollicular inputs from the visual (just as from the motor) region of the cortex [9, 18], it is difficult to agree with the assertion of the absence of phasic influences of the cortex on the functioning of the superior colliculus. The objective was set, on the basis of the above, of elucidating whether phasic influences of the cortex on the functioning of the superior colliculus of the awake rabbit exist, and if they exist, of elucidating theft character and directionality. The answer to this question may add a certain clarity to the problem of the character of the interactions of the visual cortex and superior colliculus; this in its turn will make it possible to formulate a clearer notion of the mechanism of the functioning of the midbrain visual center. Laboratory of Neurophysiology of Integrative Brain Activity, A. I. Karaev Institute of Physiology, Academy of Sciences, Baku. Department of Normal Physiology, State Medical Institute, Tyumen. Translated from Fiziologicheskii Zhurnal SSSR imeni I. M. Sechenova, Vol. 77, No. 5, pp. 26-34, May, 1991. Original article submitted July 2, 1990. 0097-0549/92/2205-0423512.50
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Fig. 1. Formation of the corticocollicular response under conditions of monomodal paired stimulation of the visual cortex. CCO-I, CCO-II, corticocollicular responses to solitary conditioning and test stimuli, respectively. Figures above the tracings, interstimulus intervals, msec. Calibration: for intervals from 0 to 150 msec, 50 gV, 20 msec; for intervals from 150 to 450 msec, 50 laV, 50 msec. Other explanations in the text. Fig. 2. Influence of a single light stimulation on the formation of the corticocollicular response. A) Responses to single stimuli; LIGHT) response to light stimulus; CCO) corticocollicular response; B) paired stimulation: figures above tracings, interstimulus intervals, msec. Calibration as in Fig. 1.
METHODS
The experiments were carried out on 12 awake rabbits in chronic experimental conditions. Nichrome wire monopolar electrodes, 0.3 mm in diameter, were implanted to record the evoked responses in the superior colliculus in accordance with the coordinates of the stereotaxic atlas [17]. Nichrome wire bipolar electrodes (interelectrode distance 1.5 mm), 0.35 mm in diameter, were implanted in the visual cortex. The indifferent electrode was fixed to the nasal bones of the skull.
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Fig. 3. Graph of relationship of the amplitude parameters of the corticocollicular response at the intervals between the conditioning and test stimuli. Along the abscissa: interstimulus intervals, msec; along the ordinate: amplitude, in percent of control. I) Presentation of monomodal cortical stimuli; 2) heteromodal stimuli: conditioning light, test - cortical.
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Fig. 4. Influence of a solitary pulse stimulation of the visual cortex on the formation of the response of the superior colliculus to a light stimulus in the norm (A) and in conditions of the action of aminazin (B). Remaining designations the same as in Fig. 2.
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Fig. 5. Influence of a solitary pulse stimulation of the visual cortex of a formation of the response of the superior colliculus to a light stimulus in the norm (A) and in conditions of the stimulation of the reticular formation (B). Remaining designations as in Fig. 2.
The recording of the EP was accomplished by means of a Medikor photostimulator (a single 1.4 J burst of energy was used), and the electrical stimulation of the visual cortex was accomplished by means of an t~SL-1 electrostimulator (a single pulse of 150-200 ~tA current lasting 0.3--0.5 msec). The change in the functional state of the brainstem reticular formation was achieved by means of the intravenous injection of aminazin (0.8 ml of a 2.5% solution) or by the creation in it of a focus of heightened excitability by means of anodic polarization (5-10 ~tA, 10 rain). The change in the functional state of the reticular formation was monitored on the basis of its evoked responses to the light flash. The statistical analysis of the data was carried out by means of the Student-Fisher t test and the Wilcoxon-Mann-Whitney U test [2] (p < 0.05). INVESTIGATION
RESULTS
The experiments showed (Fig. IA) that stimulation of the visual cortex by a single pulse of electrical current leads to the formation in the superior colliculus of short-latency (3 _+ 1 msec) responses of the EP type. This response, which we have termed the corticocollicular response, had a positive-negative configuration. The duration of the positive wave was 15 + 7 msec, the amplitude 164 + 20 p.V. The duration of the positive wave was 18 +_5 msec, the amplitude 50 + 10 IxV. The recovery cycles of the superior colliculus were investigated in order to more fully characterize the lability of its neuronal apparatus, which forms the corticocollicular response. The experiments showed that a prolonged blockade of the formation of the response to the second stimulus is observed in conditions of the presentation of paired cortical stimuli (Fig. 1B; Fig. 3). The response to the test stimulus is not formed at all in the intervals from 0 to 100 msec. The formation of a negative component of the corticocortical response which was decreased in amplitude (by 20 + 5%) was observed when the inter-
426
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Fig. 6. Graph of the relationship of the amplitude parameters of the visual response of the superior colliculus to intervals between the conditioning (cortical) and test (light) stimulus in the norm (1), in conditions of the action of aminazin (3), and against the background of the anodic polarization of the reticular formation (2). Remaining designations as in Fig. 3. stimulus interval reached 50 msec. The formation of a positive component began at an interval of 450 msec. Complete recovery of the response to the control values was not observed in the range of interstimulus intervals we investigated (from 0 to 450 msec). It is now known [12] that cortical and retinal fibers converge on the very same neurons of the superior colliculus. Consequently it can be hypothesized with a fair degree of confidence that the same neural elements participate in the generation of the corticocollicular response and of the visual response of the superior colliculus. If that is the case, the formation of the corticocollicular response in the circumstances of a light stimulus preceding it should be suppressed significantly and for a long period of time. This hypothesis is based on the previous demonstration of the formation of a prolonged IPSP of the neurons of the superior colliculus in response to a flash of light, an IPSP which induces a significant suppression of the formation of the response to a test light stimulus following it. Consequently, if the same neurons of the superior colliculi as participate in the formation of the response to light participate in the generation of the corficocoUicular response, blockade of the generation of the corticocollicular response should be observed in the circumstances of the formation of the IPSP induced by light stimulation. A series of experiments in which the influence of a conditioning light flash on the formation of the corticocollicular response was investigated was carried out in order to test this hypothesis. The experiments showed (Fig. 2B, Fig. 3) that a significant suppression of the formation of the corticocollicular response takes place under these circumstances. In the case of small intervals between the stimuli (from 0 to 30 msec) the response to the test cortical stimulus does not form at all. A corticocollicular response, substantially reduced in amplitude (to 30 _+5%) from the initial level, appears when the interval is increased to 50 msec. Complete recovery of the amplitude of the corticocollicular response to control values was not observed in the range of interstimulus intervals we investigated (from 0 to 450 msec). The formation of the corticocollicular response suggests that the visual cortex may exert on the function of the superior colliculus of the awake rabbit not only the previously described [1, 3, 14] tonic influence on its ongoing activity, but a phasic influence as well, associated with the formation of an intrinsic discharge focus. The next objective of the present investigation was the elucidation of the possible influence of the corticocollicular response on the formation of the response to the light stimulus. In other words, the formation of the visual response of the superior colliculus was tested in the circumstances of a conditioning single stimulation of the visual cortex.
427
As the investigations showed (Fig. 4A; Fig. 6), the formation of the visual response of the superior colliculus in the case of small intervals between the conditioning cortical and test light stimulus (from 0 to 20 msec) was somewhat inhibited. The amplitude of the response decreases by 20 + 5% in this case. Further increase in the intervals (from 30 to 50 msec) leads to the complete recovery of the formation of the visual response of the superior colliculus to control values. Since it known that the association of the visual cortex with the superior coUiculi is accomplished not only along direct corticocollicular connections but along connections mediated through the mesencephalic reticular formation [15, 16, 20], it can be hypothesized that the latter may play a specific role in the organization of the phasic influences of the visual cortex on the functioning of the superior colliculus. The recording of the responses of the superior colliculus induced both by a light flash and by stimulation of the visual cortex under the conditions of various states of the mesencephalic reticular formation was carried out in order to test this hypothesis. The experiments showed that changes are observed in the formation of both the visual response of the superior colliculus and the corticocollicular response in the circumstances of the blockade of the adrenergic substratum of the reticular formation by aminazin (Fig. 4B). Thus, the amplitude of the corticocollicular response increased in the process by 17 + 3%, and that of the visual response by 20 + 5%. An intensification of the inhibitory influence of the visual cortex on the functioning of the superior colliculus was observed simultaneously (Fig. 4B; Fig. 6). The creation of a focus of increased excitability in the mesencephalic reticular formation induced by anodic stimulation led to an insignificant decrease in the amplitude parameters of both the corticocollicular response and the visual response of the superior colliculus (by 7 + 2 and 8 + 3%, respectively) (Fig. 5B). A substantial change in the character of the influence of the cortical stimulus on the formation of the visual response was observed simultaneously (Fig. 5B; Fig. 6). Unlike the control, in this instance the phase of inhibition of the visual response in the case of small (from 0 to 20 msec) interstimulus intervals is lacking. Instead the phase of facilitation of the formation of the response to the test light stimulus begins immediately. DISCUSSION OF RESULTS The data obtained suggest that the stimulation of the visual cortex by a single pulse of current leads to the formation of a discharge focus in the superior colliculus which induces the generation of a corticocollicular response. Since it is known [13] that cortical and retinal fibers converge on the very same neurons of the superior colliculus, it can be hypothesized that the neurons responsible for the generation of the visual response of the superior colliculus participate in the formation of the corticocollicular response. This hypothesis is confirmed by our data, in which the suppression of the formation of the corticocollicular response was demonstrated, since it is known [3, 5] that a light stimulus induces a prolonged IPSP in neurons participating in the generation of the visual response of the superior colliculus. The possibility of the formation of the corticocollicular response, as well as of change in the formation of the visual response of the superior colliculus in the circumstances of a light stimulus preceding it, suggests that the visual cortex exerts not only the previously described [1, 3, 5, 7, 14] tonic influence, but a phasic influence as well. The latter is brief and inhibitory in character. Published data [13] regarding the presence of direct cortical inputs to the superior colliculus, as well as our own data (the quite short latent period of the corticocollicular response, 3 + 1 msec) and the relative stability of the formation of the corticocollicular response against the background of the blockade of the activity, or, on the contrary, of the activation of the reticular formation, make it possible to hypothesize that the phasic influences of the visual cortex on the functioning of the superior colliculus are accomplished along direct corticotectal fibers. The changes, on the other hand, in the character of this influence under the conditions of varied functional states of the mesencephalic reticular formation evidently attest to a modulating influence of the latter on the effectuation of cortical control of the functioning of the midbrain visual center. Since it is known [5] that the cortical and reticular inputs to the superior colliculus terminate in different layers of this structure, between which bilateral connections have not been established, the presence of an "intermediary" between the reticular formation and the superficial layers of the superior colliculus can be hypothesized. The reticular nucleus of the thalamus, which has connections both with the reticular formation and the superior colliculus (see review [5]) may be such an "intermediary". It is known ([6] and others) that a change in the functional state of one of the subdivisions of the reticular formation, the locus coeruleus, which sends adrenergic fibers to the reticular nucleus of the thalamus, induces shifts in the functional state of the latter, and this evidently leads to an attenuation or to an intensification of its influence on the functioning of the superior colliculus; this is reflected to a substantial degree in the achievement of cortical control of the functioning of the tectal neurons. 428
Thus, it can be concluded that the degree of manifestation of the phasic influence of the visual cortex on the functioning of the superior colliculus depends to a definite degree on the functional state of the nonspecific systems of the brain. LITERATURE CITED 1. 2. 3. 4. 5. 6.
7. 8. 9.
10. 11. 12. 13. 14. t5. 16. 17. 18. 19.
20. 21.
N.A. Gadzhieva, An Electrophysiological Investigation of the Central Regulation and Heterosensory Integration in the System of the Visual Analyzer [in Russian], Baku (1974). E.V. Gubler and A. A. Genkin, The Use of Nonparametric Statistical Tests in Medical-Biological Research [in Russian], Moscow (1973). E.I. Kambarly, Cortical and Reticular Regulation of the Superior Colliculi of the Corpora Quadrigemina in Varied Functional States of the Central Nervous System [in Russian], Baku (1978). Yu. G. Kratin, N. A. Zubkova, V. V. Lavrov et al., The Visual Pathways and Activation System of the Brain [in Russian], Leningrad (1982). A.M. Mass and A. Ya. Supin, Functional Organizalion of the Superior Colliculus of the Brain of Mammals [in Russian], Moscow (1985). S.P. Narikashvili, Z. I. Nanobashvili, and N. A. Khizanishvili, "The influence of stimulation of the locus coeruleus of the brain stem on the neuronal activity of the reticular nucleus of the thalamus of the cat," Izv. AN GSSR. Ser. Biol, 11, No. 1, 52-54 (1985). N.L. Pisareva, "Influence of the visual cortex on evoked potentials of the superior colliculus of the corpora quadrigemina in rabbits in early ontogenesis," Zh. Evol. Biokhim. Fiziol., 8, No. 5, 542-547 (1972). N.F. Podvigin, F. N. Makarov, and Yu. E. Shelepin, Elements of the Structural-Functional Organization of the Visual-Oculomotor System [in Russian], Leningrad (1986). A.V. Revishchin and A. Ya. Supin, "Sources of efferent fibers of the visual cortex of the rabbit, identified by the method of retrograde axonal transport of Evans blue and primuline," in: The Axonal Transport of Substances in Brain Systems [in Russian], Kiev (1981), pp. 133-136. F.N. Serkov, Cortical Inhibition [in Russian], Kiev (1986). V.L. Silakov, "The convergence of corticofugal impulse bursts in the neurons of the superior colliculi," Fiziol. Zh. SSSR, 65, No. 9, 1249-1255 (1979). H.M.J. Lawrence, "Retinal and visual cortical projections to the superior colliculus of the rabbit," Exp. Neurol., 57, No. 3,668-675 (1977). R.R. Mize, "Patterns of convergence and divergence of retinal and cortical synaptic terminals in the cat superior colliculus," Exp. Brain Res., 51, No. 1, 88-96 (1983). S. Molotchnikoff, P. Lashapelle, and D. Richard, "Latency distribution [sic] geniculate nucleus and superior colliculus of rabbits," Brain Res. Bull., 4, No. 3, 579-581 (1979). W . J . H . Nauta and H. G. Kuypers, "Some ascending pathways in the brain stem reticular formation," in: Reticular Formation of the Brain, Boston (1958), pp. 3-30. G.W. Pearce, "Some cortical projections to the midbrain reticular formation," in: Structure and Function of the Cerebral Cortex, Amsterdam, New York, London (1960), pp. 131-143. C.H. Sawyer, J. M. Everett, and J. D. Green, "The rabbit diencephalon in stereotaxic coordinates," J. Comp. Neurol., 101, No. 7, 801-824 (1954). T.S. Sotnichenko, "Convergence of the descending pathways of motor, visual and limbic cortex in the cat di- and mesencephalon," Brain Res., 116, 401-415 (1976). H.A. Swadlow and T. G. Weyand, "Efferent systems of the rabbit visual cortex: Laminar distribution of the cells of origin, axonal conduction velocities and identification of axonal branches," J. Comp. Neurol., 203, No. 6, 799-822 (1981). Y. Takachashi, T. Ogawa, T. Takimori, and H. Kato, "Intracellular studies of rabbit's superior colliculus," Brain Res., 123, No. 2, 170-175 (1977). F. Valverde, "Reticular formation of the albino rat brain stem. Cytoarchitecture and corticofugal connections," J. Comp. Neurol., 119, No. 1, 25-53 (1962).
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It has been demonstrated in awake rabbits that stimulation of the visual cortex by a solitary pulse of electrical current leads to the formation of a short-latency response in the superior colliculus. The formation of this response is suppressed when a light stimulus precedes it. At the same time, a conditioning solitary electrostimulation of the visual cortex induces a short inhibition of the formation of the response to the test light stimulus. This fact suggests that the influences of the visual cortex on the functioning of the superior colliculus may be biphasic in character. When the adrenergic apparatus of the reticular formation is blocked this inhibitory influence bears a more pronounced and prolonged character. The stimulation of the reticular formation, on the other hand, by means of anodic polarization leads to the diametrically opposite effect: the inhibitory character of the influence of the cortex is replaced by a facilitatory one. The inference is drawn that the character and the directionality of the influence of the visual cortex on the functioning of the superior colliculus is determined to a significant degree by the initial functional state of nonspecific brain systems. It is known [4, 5, 8, 12] that visual information reaches the superior colliculus both along direct retinocoIlicular pathways and along inputs mediated through the visual area of the cerebral cortex. However, the cortical inputs to the superior colliculus which take their origin in layer V of the visual cortex [9,19] play not only a retransmitter role, but a regulatory role as well. In particular, it has been demonstrated [1, 3, 7] that constant stimulation (high-frequency electrical stimulation, the application of strychnine, etc.) or functional switching on of the visual cortex leads to perceptible changes in the formation ~f visual responses of the superior colliculus; this attests to the presence of tonic influences of the visual cortex on the function of this midbrain visual center. Investigations carried out in cats in acute experimental conditions [11] have made it possible to hypothesize that the influences of the visual cortex on the function of the superior colliculus may also be phasic in character. The fact that significant changes in the formation of evoked activity of neurons of the superior colliculus are observed in conditions of the conditioning pulse stimulation of the visual cortex serves as evidence of this. Despite the fact that the possibility of the activation of the neurons of this structure in rabbits evoked by stimulation of the visual cortex by a single pulse of current has been demonstrated [20], the presence of phasic influences of the visual cortex on the function of the superior colliculus of this animal has been denied [14]. It should be noted that the above-mentioned investigations were carried out on anesthetized rabbits; this could have influenced the final result to a significant degree. Thus, in particular, it is known [10] that the barbiturates facilitate the discharge of GABA from the synaptic cleft and the activation of extrasynaptic GABA-sensitive receptors. It is possible that even the electrical stimulation of the visual cortex may not elicit excitation of its neurons in these conditions, and, consequently, the possibility is lacking for the organization of phasic influences on the functioning of the superior colliculus. Taking into account the characteristics of the functional role of the superior colliculi, which are associated, in particular, with the effectuation of rapid oculomotor reactions, as well as the data concerning the existence of direct corticocollicular inputs from the visual (just as from the motor) region of the cortex [9, 18], it is difficult to agree with the assertion of the absence of phasic influences of the cortex on the functioning of the superior colliculus. The objective was set, on the basis of the above, of elucidating whether phasic influences of the cortex on the functioning of the superior colliculus of the awake rabbit exist, and if they exist, of elucidating theft character and directionality. The answer to this question may add a certain clarity to the problem of the character of the interactions of the visual cortex and superior colliculus; this in its turn will make it possible to formulate a clearer notion of the mechanism of the functioning of the midbrain visual center. Laboratory of Neurophysiology of Integrative Brain Activity, A. I. Karaev Institute of Physiology, Academy of Sciences, Baku. Department of Normal Physiology, State Medical Institute, Tyumen. Translated from Fiziologicheskii Zhurnal SSSR imeni I. M. Sechenova, Vol. 77, No. 5, pp. 26-34, May, 1991. Original article submitted July 2, 1990. 0097-0549/92/2205-0423512.50
9
Plenum Publishing Corporation
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t.-..
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Fig. 1. Formation of the corticocollicular response under conditions of monomodal paired stimulation of the visual cortex. CCO-I, CCO-II, corticocollicular responses to solitary conditioning and test stimuli, respectively. Figures above the tracings, interstimulus intervals, msec. Calibration: for intervals from 0 to 150 msec, 50 gV, 20 msec; for intervals from 150 to 450 msec, 50 laV, 50 msec. Other explanations in the text. Fig. 2. Influence of a single light stimulation on the formation of the corticocollicular response. A) Responses to single stimuli; LIGHT) response to light stimulus; CCO) corticocollicular response; B) paired stimulation: figures above tracings, interstimulus intervals, msec. Calibration as in Fig. 1.
METHODS
The experiments were carried out on 12 awake rabbits in chronic experimental conditions. Nichrome wire monopolar electrodes, 0.3 mm in diameter, were implanted to record the evoked responses in the superior colliculus in accordance with the coordinates of the stereotaxic atlas [17]. Nichrome wire bipolar electrodes (interelectrode distance 1.5 mm), 0.35 mm in diameter, were implanted in the visual cortex. The indifferent electrode was fixed to the nasal bones of the skull.
424
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Fig. 3. Graph of relationship of the amplitude parameters of the corticocollicular response at the intervals between the conditioning and test stimuli. Along the abscissa: interstimulus intervals, msec; along the ordinate: amplitude, in percent of control. I) Presentation of monomodal cortical stimuli; 2) heteromodal stimuli: conditioning light, test - cortical.
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Fig. 4. Influence of a solitary pulse stimulation of the visual cortex on the formation of the response of the superior colliculus to a light stimulus in the norm (A) and in conditions of the action of aminazin (B). Remaining designations the same as in Fig. 2.
425
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Fig. 5. Influence of a solitary pulse stimulation of the visual cortex of a formation of the response of the superior colliculus to a light stimulus in the norm (A) and in conditions of the stimulation of the reticular formation (B). Remaining designations as in Fig. 2.
The recording of the EP was accomplished by means of a Medikor photostimulator (a single 1.4 J burst of energy was used), and the electrical stimulation of the visual cortex was accomplished by means of an t~SL-1 electrostimulator (a single pulse of 150-200 ~tA current lasting 0.3--0.5 msec). The change in the functional state of the brainstem reticular formation was achieved by means of the intravenous injection of aminazin (0.8 ml of a 2.5% solution) or by the creation in it of a focus of heightened excitability by means of anodic polarization (5-10 ~tA, 10 rain). The change in the functional state of the reticular formation was monitored on the basis of its evoked responses to the light flash. The statistical analysis of the data was carried out by means of the Student-Fisher t test and the Wilcoxon-Mann-Whitney U test [2] (p < 0.05). INVESTIGATION
RESULTS
The experiments showed (Fig. IA) that stimulation of the visual cortex by a single pulse of electrical current leads to the formation in the superior colliculus of short-latency (3 _+ 1 msec) responses of the EP type. This response, which we have termed the corticocollicular response, had a positive-negative configuration. The duration of the positive wave was 15 + 7 msec, the amplitude 164 + 20 p.V. The duration of the positive wave was 18 +_5 msec, the amplitude 50 + 10 IxV. The recovery cycles of the superior colliculus were investigated in order to more fully characterize the lability of its neuronal apparatus, which forms the corticocollicular response. The experiments showed that a prolonged blockade of the formation of the response to the second stimulus is observed in conditions of the presentation of paired cortical stimuli (Fig. 1B; Fig. 3). The response to the test stimulus is not formed at all in the intervals from 0 to 100 msec. The formation of a negative component of the corticocortical response which was decreased in amplitude (by 20 + 5%) was observed when the inter-
426
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Fig. 6. Graph of the relationship of the amplitude parameters of the visual response of the superior colliculus to intervals between the conditioning (cortical) and test (light) stimulus in the norm (1), in conditions of the action of aminazin (3), and against the background of the anodic polarization of the reticular formation (2). Remaining designations as in Fig. 3. stimulus interval reached 50 msec. The formation of a positive component began at an interval of 450 msec. Complete recovery of the response to the control values was not observed in the range of interstimulus intervals we investigated (from 0 to 450 msec). It is now known [12] that cortical and retinal fibers converge on the very same neurons of the superior colliculus. Consequently it can be hypothesized with a fair degree of confidence that the same neural elements participate in the generation of the corticocollicular response and of the visual response of the superior colliculus. If that is the case, the formation of the corticocollicular response in the circumstances of a light stimulus preceding it should be suppressed significantly and for a long period of time. This hypothesis is based on the previous demonstration of the formation of a prolonged IPSP of the neurons of the superior colliculus in response to a flash of light, an IPSP which induces a significant suppression of the formation of the response to a test light stimulus following it. Consequently, if the same neurons of the superior colliculi as participate in the formation of the response to light participate in the generation of the corficocoUicular response, blockade of the generation of the corticocollicular response should be observed in the circumstances of the formation of the IPSP induced by light stimulation. A series of experiments in which the influence of a conditioning light flash on the formation of the corticocollicular response was investigated was carried out in order to test this hypothesis. The experiments showed (Fig. 2B, Fig. 3) that a significant suppression of the formation of the corticocollicular response takes place under these circumstances. In the case of small intervals between the stimuli (from 0 to 30 msec) the response to the test cortical stimulus does not form at all. A corticocollicular response, substantially reduced in amplitude (to 30 _+5%) from the initial level, appears when the interval is increased to 50 msec. Complete recovery of the amplitude of the corticocollicular response to control values was not observed in the range of interstimulus intervals we investigated (from 0 to 450 msec). The formation of the corticocollicular response suggests that the visual cortex may exert on the function of the superior colliculus of the awake rabbit not only the previously described [1, 3, 14] tonic influence on its ongoing activity, but a phasic influence as well, associated with the formation of an intrinsic discharge focus. The next objective of the present investigation was the elucidation of the possible influence of the corticocollicular response on the formation of the response to the light stimulus. In other words, the formation of the visual response of the superior colliculus was tested in the circumstances of a conditioning single stimulation of the visual cortex.
427
As the investigations showed (Fig. 4A; Fig. 6), the formation of the visual response of the superior colliculus in the case of small intervals between the conditioning cortical and test light stimulus (from 0 to 20 msec) was somewhat inhibited. The amplitude of the response decreases by 20 + 5% in this case. Further increase in the intervals (from 30 to 50 msec) leads to the complete recovery of the formation of the visual response of the superior colliculus to control values. Since it known that the association of the visual cortex with the superior coUiculi is accomplished not only along direct corticocollicular connections but along connections mediated through the mesencephalic reticular formation [15, 16, 20], it can be hypothesized that the latter may play a specific role in the organization of the phasic influences of the visual cortex on the functioning of the superior colliculus. The recording of the responses of the superior colliculus induced both by a light flash and by stimulation of the visual cortex under the conditions of various states of the mesencephalic reticular formation was carried out in order to test this hypothesis. The experiments showed that changes are observed in the formation of both the visual response of the superior colliculus and the corticocollicular response in the circumstances of the blockade of the adrenergic substratum of the reticular formation by aminazin (Fig. 4B). Thus, the amplitude of the corticocollicular response increased in the process by 17 + 3%, and that of the visual response by 20 + 5%. An intensification of the inhibitory influence of the visual cortex on the functioning of the superior colliculus was observed simultaneously (Fig. 4B; Fig. 6). The creation of a focus of increased excitability in the mesencephalic reticular formation induced by anodic stimulation led to an insignificant decrease in the amplitude parameters of both the corticocollicular response and the visual response of the superior colliculus (by 7 + 2 and 8 + 3%, respectively) (Fig. 5B). A substantial change in the character of the influence of the cortical stimulus on the formation of the visual response was observed simultaneously (Fig. 5B; Fig. 6). Unlike the control, in this instance the phase of inhibition of the visual response in the case of small (from 0 to 20 msec) interstimulus intervals is lacking. Instead the phase of facilitation of the formation of the response to the test light stimulus begins immediately. DISCUSSION OF RESULTS The data obtained suggest that the stimulation of the visual cortex by a single pulse of current leads to the formation of a discharge focus in the superior colliculus which induces the generation of a corticocollicular response. Since it is known [13] that cortical and retinal fibers converge on the very same neurons of the superior colliculus, it can be hypothesized that the neurons responsible for the generation of the visual response of the superior colliculus participate in the formation of the corticocollicular response. This hypothesis is confirmed by our data, in which the suppression of the formation of the corticocollicular response was demonstrated, since it is known [3, 5] that a light stimulus induces a prolonged IPSP in neurons participating in the generation of the visual response of the superior colliculus. The possibility of the formation of the corticocollicular response, as well as of change in the formation of the visual response of the superior colliculus in the circumstances of a light stimulus preceding it, suggests that the visual cortex exerts not only the previously described [1, 3, 5, 7, 14] tonic influence, but a phasic influence as well. The latter is brief and inhibitory in character. Published data [13] regarding the presence of direct cortical inputs to the superior colliculus, as well as our own data (the quite short latent period of the corticocollicular response, 3 + 1 msec) and the relative stability of the formation of the corticocollicular response against the background of the blockade of the activity, or, on the contrary, of the activation of the reticular formation, make it possible to hypothesize that the phasic influences of the visual cortex on the functioning of the superior colliculus are accomplished along direct corticotectal fibers. The changes, on the other hand, in the character of this influence under the conditions of varied functional states of the mesencephalic reticular formation evidently attest to a modulating influence of the latter on the effectuation of cortical control of the functioning of the midbrain visual center. Since it is known [5] that the cortical and reticular inputs to the superior colliculus terminate in different layers of this structure, between which bilateral connections have not been established, the presence of an "intermediary" between the reticular formation and the superficial layers of the superior colliculus can be hypothesized. The reticular nucleus of the thalamus, which has connections both with the reticular formation and the superior colliculus (see review [5]) may be such an "intermediary". It is known ([6] and others) that a change in the functional state of one of the subdivisions of the reticular formation, the locus coeruleus, which sends adrenergic fibers to the reticular nucleus of the thalamus, induces shifts in the functional state of the latter, and this evidently leads to an attenuation or to an intensification of its influence on the functioning of the superior colliculus; this is reflected to a substantial degree in the achievement of cortical control of the functioning of the tectal neurons. 428
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