(95) T. V. ORLOVA, V. G. SIDYAKIN, A. M. KULICHENKO and V. B. PAVLENKO. Frunze State University, Simferopol, Ukraine
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1 Pergamon Biophysics, Vol. 40, No. 5, pp , 1995 Copyright 1996 Elsevier Science Ltd Printed in Great Britain. Allrightsreserved /95 $ (95) ACTIVITY OF THE NEURONS OF THE PARIETAL- ASSOCIATIVE CORTEX AND THE REGION OF THE SUBSTANTIA NIGRA OF THE CAT ON EXPOSURE TO MAGNETIC FIELDS OF FREQUENCY 8 Hz* T. V. ORLOVA, V. G. SIDYAKIN, A. M. KULICHENKO and V. B. PAVLENKO Frunze State University, Simferopol, Ukraine (Received 2 March 1994) In experiments on alert cats the authors have studied the impulse activity of the neurons of the parietal-associative cortex linked with voluntary self-initiated movement and the background rhythmics of the cells of the region of the substantia nigra on brief (6 min) exposure to magnetic fields with a frequency of 8 Hz and induction of 20 jxt. The neurons of the cortex were found to show enhancement of the reactions of inhibition appearing in the planning phase of voluntary movement. In the region of the substantia nigra the frequency and stability of background impulse activity of the neurons increased, especially in the presumed dopaminergic cells. Such changes in the activity of the neurons of the neocortex and stem structures may underlie the behavioural effects of the action of weak magnetic fields. Based on extensive statistical and experimental material, it has been established that the background geomagnetic fields closely related to solar activity are an important ecological factor [1,2]. Investigations of weak (non-thermal) artificial variable magnetic fields of ultralow frequency simulating natural geomagnetic disturbances have shown the sensitivity to them of the behavioural reactions of organisms. The biological activity of the magnetic fields with a frequency of 8 Hz close to the fundamental frequency of the ionospheric waveguide is particularly emphasized. Experiments have shown that such fields produce changes in conditioned reflex activity of experimental animals and disturbances in their adaptive behaviour [1]. The neuronal mechanisms of these effects have been insufficiently studied. Therefore, the present work seeks to study the influence of weak magnetic fields of frequency 8 Hz on the reaction of individual neurons of the parietal-associative region of the cortex linked with the performance of voluntary movement and also on the neurons of the region of the substantia nigra of the midbrain. The choice of parietal-associative region as test object was dictated by the importance of its contribution to the shaping of behaviour as a poly sensory structure involved in programming and triggering goal-directed movements in experimental space [3, 4], As for the substantia nigra, it possesses bilateral links with the parietal-associative region and the frontal cortex in the cat [5], in it lie dopaminergic (DA) neurons influencing the higher integrative processes in the neocortex [6]. * Biofizika, 40, No. 5, ,
2 978 T. V. Orlova et al MATERIALS AND METHODS OF INVESTIGATION The experiments were conducted on alert cats. The discharges of the neurons after modifying the known technique [7] were recorded extracellularly with a microelectrode from a silver tip-pointed microlead (diameter of lead 12 jxm, insulation 70 xm). The activity of the cells was analysed with a personal computer and an original package of programs. The magnetic fields were established with the aid of Helmholtz rings placed in a screened chamber (attenuation of the external magnetic fields at a frequency of 8 Hz was 25 db). The sinusoidal field frequency was 8 Hz, the voltage in the region of the animal head 20 JULT and exposure 6 min. We compared the indices of the activity of the neurons before exposure to the magnetic field and in the period beginning after the first 3 min of exposure (test group) or its shamming (control group). The degree of change in the indicator under the influence of the factor (or its sham) was expressed as a percentage of the initial level. The significance of the inter-group differences was evaluated as a function of the normality of the distribution of the data using the Student and Wilcoxon criteria. In the first series of experiments run on three cats, we analysed the reactions of the neurons of the parietal-associative region (anterior part of the midsupra Sylvian gyrus) of the left hemisphere linked with the execution of the self-initiated movement. The animals were trained to raise in voluntary rhythm the right paw from the support platform and to press a pedal by which means they were rewarded with food. Peristimulus histograms were plotted and the changes in impulse activity preceding the start of movement evaluated. We determined the strength of the reaction the ratio of the number of action potentials in the period of the reaction to the level of background impulse activity of the given neuron for the corresponding time (for the inhibitory phase of the reaction the opposite ratio). In the second series run on two cats we analysed the background impulse activity of the neurons in the region of the compact part of the substantia nigra and determined the mean frequency, the standard deviation of the length of the interpulse intervals and the coefficient of packet group activity (explosive activity the ratio of the number of impulses following with an interval less than 10 ms to the total number of impulses). The analysis of background impulse activity lasted 3 min. The cells with a low frequency of impulsation and a longer action potential were assigned to presumed dopaminergic neurons [8] and the others to non-da nerve cells. RESULTS AND DISCUSSION In the first series of the experiment we investigated the activity of 135 parietal-associative region neurons in 88 of which reactions were established associated with movement. The most characteristic pattern of the reaction (identified in 75 neurons) was inhibition beginning ms before the start of movement often followed (in 32 cells) by excitatory reactions appearing ms before the movement. Less often (in 13 cells) the excitatory reactions began ms before the movement. In the neuronal processes anticipating movement the existence of two phases is postulated: early and late. The first begins 1-2 s before the movement and corresponds to planning and programming of the movement, the second appears in 0.4 s and is connected with its triggering [9]. Thus, to the phase of planning of the movement corresponded, as a rule, inhibitory reactions and to the phase of its initiation mostly excitatory reactions. To analyse the impact of an e.m.f., we selected the most stable reactions 30 excitatory and 60 inhibitory divided into equal control and test groups. The strength of the inhibitory phases of
3 Activity of Neurons of Cat on Exposure to Magnetic Fields 979 the reactions in the test group increased and was ± 7.4% (here and hereafter the mean and its error are indicated) in relation to the initial level (Fig. 1). In the control group this magnitude was somewhat lower at 95.6 ± 4.5%. The differences between these values are statistically significant (p 0.03). No significant changes were found in the strength of the excitatory phases of the reactions. Thus, the reactions of inhibition appearing in the early phase of determination of movement are sensitive to the magnetic fields with the parameters used. The activity of the neuronal chains linked with unstable and quite lengthy processes of planning is modified, whereas the trigger chains taken over by induction of the motor act are relatively insensitive to the action of the magnetic field. In the second series we studied the activity of 29 neurons of the substantia nigra region selected on the basis of a discharge stable over a long time. The entire population was divided into two groups presumed DA cells (14) and non-da neurons (15). Each of the cells was tested both on exposure to the magnetic field and for its sham (exposure and the sham were alternated in random fashion with an interval between them of not less than 30 min). Exposure to the magnetic field led to a rise in the mean frequency of the background impulse activity of the whole neuronal population accompanied by enhanced explosive activity (Table 1). Considerable changes in background impulse activity were noted for the DA neurons (Fig. 2). They showed a particularly considerable increase in the frequency of the background impulse activity with reduced standard deviation of the length of the interpulse interval, i.e. the activity became more stable. Characteristic of the non-da cells to a high degree was passage to explosive activity. Thus, the neurons of the substantia nigra region including the presumed DA cells are sensitive to the magnetic fields studied. It is known that DA neurons control the activity of the pyramidal and inhibitory neurons of the neocortex [10]. Enhancement of their activity may, it is thought, disturb the processing of sensory information and motor activity [11, 12]. Fig. 1. Peristimulus histograms of the reactions associated with self-initiated movement of the neuron of the parietal associative cortex before (a) and after (b) exposure to the magnetic field. The start of movement is taken as 0, n = number of impulses in the bin; N=20 (number of recordings). 1 s
4 980 T. V. Orlova et al Table 1. Change (%) in the background impulse activity of the neurons of the region of the substantia nigra in the control series (C) and on exposure to a magnetic Held (m.f.). Type of experiment Frequency of discharge Standard deviation of the interimpulse interval Explosive activity Whole population of neurons C 102,8±4,4 118,7±12,7 U0,3±15,0 m.f. 129,2±9,2 101,9±Î3,1 156,1 ±20,6 p - 0,01 Dopaminergic neurons C 105,3±7,5 123,8±13,8 123,5±29,3 m.f. 140,7±10,6 77,2±20,4 148,9±28,3 p - 0,01 p - 0,03, Non-dopaminergic neurons C 100,5±5,2 114,0±21,5 97,1 ±7,3 m.f. 118,4±14,6 125,0±23,1 163,3±31,0 p - 0, ms Fig. 2. Histogram of the distribution of inter-impulse intervals of the background activity of the presumed dopaminergic neuron before (a) and after (b) exposure to the magnetic field; a, n 692, x = 3.8 s _1 ; 8 = 0.48 s; b, n 1300; x 7.2 s" 1 ; 8 = 0.27 s (n is number of inter-impulse intervals; x is the mean discharge frequency; 8 is the standard deviation of the inter-impulse intervals).
5 Activity of Neurons of Cat on Exposure to Magnetic Fields 981 Consequently, the behavioural effects of the influence of weak magnetic fields of infralow frequency may be based on changes in the activity both of the cortical neurons and the nerve cells of individual stem structures modulating cortical functions. REFERENCES 1. V. G. Sidyakin, N. A. Temur'yants, V. B. Makeyev and B. M. Vladimirskii, Cosmic Ecology, 176 pp., Nauk dumka, Kiev (1985). 2. V. G. Sidyakin, Biofizika, 37, 647 (1992). 3. V. Mountcastle, J. Lynch, A. Georgopoulos et al, J. Neurophysiol, 38, 841 (1975). 4. T. V. Il'icheva, T. V. Orlova, 1.1. Korenyuk and V. B. Pavlenko, Fiziol zh. SSSR, 27, 29 (1991). 5. A. I. Gorbacheskaya, Arkh. anatom. gistol i embriol, 88, 5 (1985). 6. S. Foote and J. Morrison, Annu. Rev. Neurosci., Palo Alto, Calif. 10, 67 (1987). 7. A. A. Pirogov and A. A. Orlov, Fiziol zh. SSSR, 64, 1685 (1978). 8. G. Steinfels, J. Heym and B. Jacobs, Life ScL, 29, 1435 (1981). 9. K. Okano and J. Tanji, Exp. Brain Res., 66, 155 (1987). 10. J. Penit-Soria, E. Audinat and F. Crepel, Brain Res., 425, 263 (1987). 11. R. Mansbach, M. Geyer and L. Braff, Psychopharmacology, 94, 507 (1988). 12. D. Servan-Schreiber, H. Printz and J. Cohen, Science, 249, 892 (1990).
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