Int. J. Biometeor. 1977, vol. 21, number 4, pp. 357-365.
Behavioral Effects in Monkeys Exposed to Extremely Low Frequency Electromagnetic Fields
by
J. O. de Lorge and J. D. Grissett
ABSTRACT. - - Several experiments with rhesus and squirrel monkeys on the influence of extremely 10w frequency (ELF) electromagnetic fields found no effects on behavior. Magnetic fields of 0.3 and 1.0 mT with electric fields of below 1 to 29 V / m at frequencies of 7, 10, 15, 45, 60 and 75 Hz were used. Small differences in ambulatory activity and response rate were occasionally observed, but no consistent effects between or within animals on any measures were obtained. No effects on reaction time, interresponse time, match-to-sample performance, and blood constituents were observed. Such previously reported effects may not be a consequence of ELF values alone, but are probably related to other environmental variables. INTRODUCTION In the last two decades there has been a surge of interest in the biological effects of extremely 10w frequency (ELF) electromagnetic fields. A number of reviews (Llaurado, Sances and Battocletti, 1974; K6nig, 1975; Persinger, 1975; Persinger, Ludwig and Ossenkopp, 1974) have shown this interest to be based on the accelerated use of electricity by communities throughout the world. A majority of ELF experiments generally simulated the electric and magnetic fields with plates and Helmholtz coils. However, the ELF stimuli among those studies varied to such an extent that almost no experiments have been replicated by different investigators using identical stimulus values. Variations occurred in frequency, intensity and duration, and electric and magnetic components were utilized separately or together. In most cases, when the magnetic component was manipulated, the electric component was seldom regarded or measured. Frequencies ranged from 0.1 Hz (Friedman, Becker and Bachman, 1967) to 100 Hz (Kolin, Brill and Broberg, 1959). Intensities varied from less than ambient level to very high levels, with magnetic fields from 13 #T to 0.874 T (1 tesla, T = 10,000 gauss) and electric fields from 0.007 to 30 kV/m. In the present study, frequencies from 7 to 75 Hz were used; the electric fields induced by Helmholtz coils ranged from less than 1 V/m to 29 V/m (rms)depending upon the particular experiment; and magnetic fields ranged from 0.3 to 1 mT. Two traditional approaches to the study of the interactions between electromagnetic fields and behavior exist. The first assumes that some animals have evolved with a sensitivity to electromagnetism that has enables them to reproduce more successfully than * Naval Aerospace Medical Research Laboratory, Naval Air Station, Pensacola, Florida 32508, USA. Presented at the Seventh International Biometeorological Congress, 17-23 August 1975, College Park, Maryland, USA.
358 less sensitive animals. This approach is illustrated in studies of migration and homing in pigeons (Keeton, 1972), electric location and capture of prey in fish (Werber, Sparks and Goetz, 1972), and regulation of biological rhythms in men (Wever, 1969). The second approach, taken in our research, assumes that because the basic physiology of an organism is an electrochemical process, its physiological processes might be disturbed by electromagnetic stimuli and result in observable behavioral changes. The purpose of the present series of experiments was to discover with monkeys if various behaviors, analogous to human behaviors, would be influenced by ELF magnetic and associated electric fields. Other studies have tended to be more concerned with species differences than behavior differences. Invariably, rats have been used to study ELF effects on general motor activity, man was the subject in studies of reaction time, and pigeons were subjects in migration studies. In our work we have selected behaviors previously reported to be susceptible to ELF fields, e.g., reaction time (K6nig and Krampl-Lambrecht, 1959), lever pressing (Gavalas et al., 1970), and general motor activity (Persinger et al., 1972). Other behaviors we investigated included a memory task and the monkey's ability to detect the presence of the ELF field. In addition, blood samples were analysed in some of the experiments. In toto, no indication of electromagnetic effects appeared. Occasionally trends occurred but could not be replicated either with the same or different subjects. Studies that obtain only negative results are thought to be of marginal value, particularly in behavior research. However, the demonstration that certain independent variables were of little or no consequence is of extreme practical importance, especially if maximal opportunities were present for the effects to be observed. Such was the case in the present experiments. METHOD SUBJECTS Six adult squirrel monkeys (Saimiri sciureus) were used in one series of experiments. One female, and two males were trained on a reaction time task. The other three male squirrel monkeys were trained on a variable-interval (VI) schedule of reinforcement to see if responding would be suppressed when the ELF field was present. Four adult rhesus monkeys (Macaca mulatta) were subjects in the second series of experiments. Two of these monkeys were males, and two were females. All of the animals were housed in a vivarium with normal geomagnetic fields (northerly direction, 50 #T inclined at approximately 55 ° below the horizon) and electric fields of less than 0.1 V/m. APPARATUS In each of 14 experiments Helmholtz coils surrounding animal enclosures were used to generate magnetic fields. Specific details of the arrangements and the fields are available in technical reports from this laboratory (de Lorge, 1972; 1973a; 1973b; 1974; Grissett, 1971; Grissett and de Lorge, 1971). During experimental sessions the animals were located in chambers large enough for unrestricted movement in all directions. E~ich chamber was outfitted with a work panel containing stimuli and response manipulanda in addition to apertures for food and water delivery. Panels were situated in the west end of the chamber. The enclosures were nonmetallic, noise attenuated, and isolated from floor vibrations. Noise to the chambers was masked with a 75 dB white noise. The chambers were ventilated, and during the experiments temperature, humidity, and atmospheric pressure were recorded. PROCEDURE Table l summarizes the various experiments for the squirrel monkeys and rhesus monkeys, respectively. The experiments are numbered in chronological order in each table;
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360 the squirrel monkey series was conducted first. A complete description of the tasks can be found in de Lorge and Marr (1974) whereas brief descriptions as listed in the Behavior column of the table follow: EXPERIMENTS 1-4, SQUIRREL MONKEYS. - - Reaction time was a task where the monkey was required to release a lever when a lamp was illuminated. Response suppression was a task wherein the monkeys pressing a lighted disc for food were presented with a 10-s presentation of a magnetic field to see if disc-pressing was suppressed. EXPERIMENTS 5-14, RHESUS MONKEYS. - - Reaction time in the rhesus studies required a monkey to lift a lever in the presence of a red light and release the lever when a tone was presented. Fixed-interval behavior occurred when the monkey repeatedly lifted a lever and after 20 s elapsed (FI 20-s) food pellets were delivered at the next lever lift. The match-to-sample task trained monkeys to press a center disc trans-illuminated with one of I0 different stimuli. Below the center disc were two comparison discs. A response on the center disc was followed by removal of its stimulus, and 1 s later the same stimulus appeared on one of the comparison discs. A different stimulus was on the opposite disc. When the disc with the matching stimulus was pressed reinforcement occurred. The fixed-ratio task merely required 10 lever lifts for food reinforcement. The interresponse-time task (IRT) required the monkey to wait 5 s when a green light appeared before lifting a lever. Lever responses before 5 s and after 6 s produced no reinforcement and required another 5-s wait. Lever lifts between 5 and 6 s produced a food pellet. The reaction time, fixed interval, and match-to-sample tasks occurred consecutively in the same experiments during the same sessions. The Fixed Ratio (FR) and Interresponse Time (IRT) tasks also occurred consecutively during their experiment (exp. 11). Later the IRT task alone was instituted (exps. 12-14). The Field Exposure column in the table shows the total hours the animals were in the fields and how long a daily exposure lasted. The Sessions column gives the hours an animal worked each session regardless of how long it was in the chamber and the number of sessions of exposure that occurred without an interruption. The animals were run 7 days a week in experiments 3, 8, 9 and 10. All animals were deprived of food for training. The squirrel monkeys were generally tested at about 85% of their free feeding body weights whereas the rhesus monkeys worked at weights anywhere from 70 to 100% of their free feeding weights.
RESULTS AND DISCUSSION NO effects of acute exposure to 0.3-mT magnetic fields were seen in the squirrel monkeys at either 45- or 7-Hz frequencies. The analyses included the mean number of correct responses required to receive a food pellet (reinforcement ratio) and the ratio of correct responses to total responses (efficiency ratio). The mean reaction time and its variance were also assessed. A gradual increase in the efficiency ratio and a slight decrease in the reinforcement ratio indicated a learning effect occurred but there was no evidence of any effect caused by the ELF exposure. In an extension of that study, the effects of chronic exposure to 1.0-mT, 45-Hz fields were explored (Experiment 3). The same 3 monkeys were in the fields for 42 consecutive days, 24 hours a day, although they worked on the reaction time task for only 1 hour each day. Again a gradual learning effect was seen in the efficiency ratio, reinforcement ratio, and also in reaction time, but nothing indicated an effect of the magnetic field even after 1008 hours of exposure. In Experiment 4, an attempt was made to investigate the arousing characteristics of ELF stimuli by brief presentations of a 1.0-mT, 45-Hz magnetic field while the squirrel monkeys were engaged in high, continuous rates of lever responding. Three different
361 monkeys that had never been exposed to magnetic fields were trained to respond on a VI 1-min schedule of reinforcement. Response suppression was calculated as the ratio of lever responding during the field to responding both during the field and when the field was absent. Ratios less than 0.5 indicate suppression and ratios greater than 0.5 indicate enhancement. When the 10-s presentation of the ELF field was used as a suppression stimulus, the mean ratios for the 3 monkeys were 0.49, 0.52 and 0.49, indicating that the animals were not aroused by or did not detect the brief presence of the field. Although the data varied a great deal, no consistent trends appeared. The data were typical of control ratios where no stimuli occurred. Suppression ratios in an experiment with visual stimuli alone were generally around 0.2 to 0.3. Rhesus monkeys were trained on highly complex tasks under the assumption that more stringent behavioral requirements would increase their susceptibility to the ELF stimuli. The rhesus monkeys were required to work these tasks for periods of from 2 to 8 hours. General motor activity was recorded during all of the rhesus monkey experiments. A number of behavioral changes were observed such as in ambulatory behavior, but typically these changes were not related to the ELF fields. Most performance changes were a consequence of continuous experimental sessions and elapsed time. No effect on reaction time or its associated behavior was seen during 3-hour exposures. As these same 2 rhesus monkeys experienced additional sessions, behavior on all three tasks became less variable, and when the 45- and 10-Hz fields were introduced during 8-h sessions, behavior was extremely stable, allowing a much more precise comparison to be made. When 10-Hz fields were first introduced, Experiment 7, both AR4 and AP6 produced significantly less general motor activity. This was the first and only time a consistent effect of the fields was observed and led to a replication of the 10-Hz study, Experiment 8. However, in the replication no activity changes were seen in the same two animals or later in Experiment 10 with female animals. Responding on an FI 30-s schedule of reinforcement was also not influenced by the 10-Hz fields in Experiment 8. The mean response rate per 3-s segment of the FI 30-s schedule was plotted for the 2 monkeys as a function of the field's presence. Most of the data, within an animal, representing field and no field, were very close or even overlapped. This was particularly true where the rates were greater than one response per minute. Perhaps tasks with high response rates are too insensitive and the probability of changing behavior is higher on a low rate task. The match-to-sample task produced low rate behavior although it did require more attention from the animal in that the monkey had to rely on its immediate memory to successfully complete the task. No definite differences in match-to-sample behavior were related to either the 60- or 10-Hz fields (Experiments 9 and 10) in the female rhesus monkeys, 3Z5 and 4Z7. Both animals were performing with about a 10% error, and their day-to-clay variations were much greater than field no-field variations. In Experiments 11, 12, 13, and 14 blood chemistry was investigated along with behavior. Blood samples were drawn biweekly and then weekly as the animals were exposed to 45- and 15-Hz magnetic fields. The following blood constituents were analyzed: triglycerides, creatine, hemoglobin, cholesterol, creatine phosphokinase, lactic dehydrogenase, potassium, serum glutamic oxaloacetic transaminase, calcium, red cell count, hematocrit, white blood cell count, monocytes, eosinophiles, polycytes, lymphocytes, bands, sodium, total protein, glucose, creatinine, blood urea nitrogen and serum glutamic pyruvic transaminase. Some of these indices had been implicated or suggested in other ELF studies. The values obtained fell within the range of other monkeys in our vivarium, and not one parameter consistently vaired in relation to the ELF fields. During the IRT task (Exp. 14) the animals did not detect the 45-Hz field when presented between 5 and 6 s, a circumstance which should have produced more correct responses.
362 CONCLUSIONS AND RECOMMENDATIONS Apparently the ELF electromagnetic fields explored in the present study do not have large or consistent biological effects on nonhuman primates. Although others (GavalasMedici and Magdaleno, 1975; Gavalas et al., 1970) have shown that the behavior of some monkeys, Macaca nemestrina, was influenced by electric fields, the observed effects were limited to particular voltages and frequencies. For example, one study (Gavalas et al., 1970) using 7 V/m fields found changes in the mean IRT at 7-Hz but not at 10-Hz, whereas a replicated study (Gavalas-Medici and Magdaleno, 1975) found no changes in mean IRT at 1 V/m and 10 V / m regardless of frequency. With increases in voltage level, e.g., 56 V/m, the 7-Hz and 75-Hz fields had an effect but 60-Hz fields did not. At 100 V/m these two investigators found no differences between experimental and control sessions and concluded, after gathering additional control data, that fields of that intensity produced effects that persisted from exposure sessions to control sessions. Magnetic fields were not used in those studies; hence, the reported effects are probably specific to electric fields alone. No other studies on ELF magnetic fields and monkeys have been published, although Friedman and Carey (1972) reported that static fields of 20.0 mT did have an effect on squirrel monkeys during initial exposures. Even here, however~ the effect was transient and the animals seemed to have adapted to the fields. If adaptation does occur, particularly during the first or second exposures, and if there are longlived effects, the probability of detecting ELF influences on any animal decreases tremendously. Certainly, under such circumstances, monkeys are not the optimal animal to use. It is our opinion that man is the definitive subject for ELF studies as much of the earlier indications on an ELF influence were obtained with man. Although man may be the preferred subject, the behavior most often investigated, reaction time, is not the preferred measurement. No differences in reaction time in either man (Beischer, Grissett and Mitchel, 1973) or monkey were produced by the ELF fields studied in our laboratory. Other laboratories report a variety of findings. For example, K6nig and Krampl-Lambrecht (1959) found reaction time changes to depend upon the form of the electric wave. Later, Hamer (1968) reported reaction time increased at 3 Hz and decreased at 6, 8, II, and 12 Hz. Friedman, Becker and Bachman (1967) found no changes at 0.1 Hz but did at 0.2 Hz when magnetic fields were used. K6nig ( 197 l) when replicating Hamer's earlier experiment obtained similar results. Some very recent work confused the issue even more. R. Hauf (1974) and G. Hauf (1974) found that with 50-Hz fields of l, 15, and 20 kV/m, there was a tendency toward a rise in reaction time but the ELF presence had no further effect when the fields were turned off. No intensity relationships were observed. Replications of their study in their own laboratory, however, reported decreases in reaction time (Eisemann, 1975), and when a magnetic field was used, no significant changes were observed (Mantell, 1975). In these studies the the initiating effect of the field could be interpreted as an artifact caused by the use of sophisticated subjects. The designs invariably had field off, on, and off again with session lengths of 3 hours. No counterbalancing was attempted. Most human subjects today realize that experimental conditions are changed somewhere in the middle of the sessions, and this could account for the minor changes seen. The selection of the appropriate species and the appropriate behavior continues to be a problem in ELF research. Because it is postulated that the calcium ion may be responsible for mediating ELF effects (Adey, 1974; Ludwig, 1971), studies of invertebrates whose striatal muscle fibers produce calcium spikes might be profitable, It may also be helpful to investigate animals whose environment includes food sources, home sites, and enemies associated with electromagnetic phenomena. For example, electric fish spend much of their life in mud or dark murky waters. Is it likely that animals with similar environments share electromagnetic properties? Chronic investigations, although very expensive, are needed. When possible such studies should include circadian periodicity as a measure. Wever's (1968) research in
363 this area is some of the more impressive and should be replicated. In addition to longterm experiments the effect of other climatic phenomena, especially humidity and barometric pressure, should be observed. Many studies document the effects of barometric pressure on the heart (Teng and Heyer, 1955), on urine mucopolysaccharides (Milolajczyk, Allalouf and Ber, 1969), and on animal activity (Sprott, 1967). One recent dissertation reported that pigeons could not detect a continuous or alternating magnetic field (0.91 to 1.25 Hz, 8 to 15.3/~T) yet, they were extremely sensitive to changes in atmospheric pressure (Kreithen, 1974). It is possible that for effects to be consistently observed, the ELF field should change in conjunction with pressure, humidity, a n d / o r temperature. Perhaps there is a synergistic effect. In no ELF study should it be assumed that calculated fields alone are sufficient. Actual measurements should be taken. These include not only field measurements but those of noises, odors, vibrations, humidity, temperature, time of day, barometric pressure, and all other environmental changes which should be accurately recorded and whenever possible, controlled. Other investigators (Moos et al., 1970; Reiter, 1970) have continually emphasized the importance of such details because behaviors previously reported to be influenced by ELF fields are in most cases susceptible to other environmental changes also. It has been suggested that the more uncontrolled the behavior, the more susceptible it will be to electromagnetic stimul (Gavalas-Medici and Magdaleno, 1975). This means of course that such behavior will be susceptible to all environmental changes. Operant behavior is very stable and contains many inherently controlling stimuli. In a decision to use the operant approach with any organism the reinforcement contingencies should be dependent upon the animal's ability to detect the ELF fields, such as with a conditioned emotional response or a shock avoidance response. Even in these cases, however, ELF effects have not been observed (Marr, Rivers and Burns, 1973). ACKNOWLEDGMENT The assistance of C. S. Ezell and R. J. Franklin in conducting these studies, and M. Kelly and K. Duncan for typing assistance is greatly appreciated. REFERENCES ADEY, W. R. (1974): The influence of impressed electrical fields at EEG frequencies on brain and behavior. In: Behavior and Brain Electrical Activity. H. Altshuler and N. Burch (ed.), Plenum Press, New York. BEISCHER, D. E., GRISSETT, J. D., and MITCHEL, R. E. (1973): Exposure of man to magnetic fields alternating at extremely low frequency. NAMRL-!180, Naval Aerospace Medical Research Laboratory, Pensacola, Florida. (AD 770 140). DE LORGE, J. (1972): Operant behavior of rhesus monkeys in the presence of extremely low frequency-low intensity magnetic and electric fields, Experiment 1. NAMRL-II55, Naval Aerospace Medical Research Laboratory, Pensacola, Florida. (AD 754 058). DE LORGE, J. (1973a): Operant behavior of rhesus monkeys in the presence of extremely low frequency-low intensity magnetic and electric fields, Experiment 2. NAMRL-1179, Naval Aerospace Medical Research Laboratory, Pensacola, Florida. (AD 764 532). DE LORGE, J. (1973b): Operant behavior of rhesus monkeys in the presence of extremely low frequency-low intensity magnetic and electric fields, Experiment 3. NAMRL-lI96, Naval Aerospace Medical Research Laboratory, Pensacola, Florida. (AD 774 106).
364 DE LORGE, J. (1974): A psychobiological study of rhesus monkeys exposed to extremely low frequency-low intensity magnetic fields. NAMRL-1203, Naval Aerospace Medical Research Laboratory, Pensacola, Florida. (AD A000 078). DE LORGE, J. and MARR, M. J. (1974): Operant methods assessing the effects of ELF electromagnetic fields. In: ELF and VLF Electromagnetic Field Effects. M. A. Persinger, (ed.), Plenum Publishing Corporation, New York, 145-175. EISEMANN, B. (1975): Untersuchungen ~iber Langzeiteinwirkung kleiner Wechselstr6me 50 Hz auf den Menschen. Inauguraldissertation, Medizinische Fakultat, Universit~it Freiburg im Breisgau, Germany. FRIEDMAN, H., BECKER, R. O. and BACHMAN, C. H. (1967): Effect of magnetic fields on reaction time performance. Nature (Lond.), 213: 949-956. FRIEDMAN, H. and CAREY, R. J. (1972): Biomagnetic stressor effects in primates. Physiol. Behav., 9: 171-173. GAVALAS, R. J., WALTER, D. O., HAMER, J. and ADEY, W. R. (1970): Effect of low-level, low-frequency electric fields on EEG and behavior in Macaca nemestrina. Brain Res., 18: 491-501. GAVALAS-MEDICI, R. and MAGDALENO, S. R. (19"]5): An evaluation of possible effects of 45 Hz, 60 Hz and 75 Hz electric fields on neurophysiology and behavior in monkeys. ONR Technical Report Contract =N00014-69-A-02004037. GRISSETT, J. D. (1971): Exposure of squirrel monkeys for long periods to extremely low-frequency magnetic fields: Central-nervous-system effects as measured by reaction time. NAMRL-1146, Naval Aerospace Medical Research Laboratory, Pensacola, Florida. (AD 735 456). GRISSETT, J. D., and DE LORGE, J. (1971): Central-nervous-system effects as measured by reaction time in squirrel monkeys exposed for short periods to extremely low-frequency magnetic fields. NAMRL-1137, Naval Aerospace Medical Research Laboratory, Pensacola, Florida. (AD 731 994). HAMER, J. R. (1968): Effects of low level, low frequency electric fields on human reaction time. Commun. Behav. Biol., Part A, 2: 217-222. HAU F, G. ( 1974): Untersuchungen ~iber die Wirkung energietechnischer Felder auf den Menschen. Inauguraldissertation, Medizinische Fakulgit, Universit~it M~inchen, Germany. HAUF, R. (1976)! Influence of 50 Hz alternating electric and magnetic fields on human beings. Rev. Gen. Eleetricit6 (Numero Special), 85:31-49. KEETON, W. T. (1973): Effects of magnets on pigeon homing. In: Animal Orientation and Navigation, A Symposium. S. Galler, K, Schmidt-Koening, G. Jacobs and R. Belleville (ed.), NASA SP-262, U.S. Government Printing Office, Washington, D.C., 579-594. KONIG, H. (1971): Biological effects of extremely low frequency electrical phenomena in the atmosphere. J. interdiscipl. Cycle Res., 2: 317-323. KONIG, H. L. (1975): Unsichtbare Umwelt. Heinz Moos Verlag, M~nchen. KONIG, H. L. and KREMPL-LAMBRECHT, L. (1959): l~ber die Einwirkung niederfrequenter elektrischer Felder auf das Wachstum pflanzlicher Organisrnen. Arch. Mikrobiol., 34: 204-210. KOLIN, A., BRILL, N. W. and BROBERG, P. J. (1959): Stimulation of irritable tissues by means of an alternating magnetic field. Proc. Soc, exp. Biol. (N.Y.), 102: 251-253. KREITHEN, M. L. (1974): Effects of magnetism, barometric pressure, and polarized light on the homing pigeon. Ph.D. dissertation, Cornell University, Ithaca, N.Y. Dissertation abstracts International, 1975, 35, 3168-B. (University Microfilms No. 74-29,923). LLAURADO, J. G., SANCES, A. and BATTOCLETTI, J. H. (1974): Biologic and Clinical Effects of Low-Frequency Magnetic and Electric Fields. Charles C. Thomas, Springfield, Illinois.
365 LUDWIG, H. W. (1971): Der Einfluss von elektromagnetischen TiefstfrequenzWechselfeldern auf h6here Organismen. Biomed. Technik, 16: 67-72. MANTELL, B. (1975): Untersuchungen ~iber die Wirkung eines magnetischen Wechselfeldes 50 Hz auf den Menschen. Inauguraldissertation, Medizinische Fakult~it, Universiffit Freiburg im Breisgau, Germany. MARR, J. J., RIVERS, W. K. and BURNS, C. P. (1973): The effect of low energy, extremely low frequency (ELF) electromagnetic radiation on operant behavior in the pigeon and the rat. Georgia Institute of Technology, Contract No. N00014-67-0159-0009, Office of Naval Research. MIKOLAJCZYK, H., ALLALOUF, D. and BER, A. (1968): The effect of simulated altitude (500 mm Hg) on urine acid mucopolysaccharides excretion in normal rats. Int. J. Biometeor., 12: 282-287. MOOS, W. D., CLARK, R. K., LEVAN, H. and MASON, H. C. (1970): Behavior and physiology of mice in a closely controlled environment. Int. J. Biometeor., 14: 133-154. PERSINGER, M. A. (1975): ELF and VLF Electromagnetic Field Effects. Plenum Publishing Corporation, New York. PERSINGER, M. A., LUDWIG, H. W. and OSSENKOPP, K. P. (1973): Psychophysiological effects of extremely low frequency electromagnetic fields, a review. Percept. mot. Skills, 36:1131-1159. PERSINGER, M. A., PERSINGER, M. A., OSSENKOPP, K. P. and GLAVIN, G. B. (1972): Behavioral changes in adult rats exposed to ELF magnetic fields. Int. J. Biometeor., 16: 155-162. REITER, R. (1970): Sind luftelektrische Gr6ssen als Komponenten des Bioklimas in Betracht zu ziehen? Heiz., LOft., Klima., Haustech., 21: 258-262, 279-285. SPROTT, R. L. (1967): Barometric pressure fluctuations. Effects on the activity of laboratory mice. Science, 157: 1206-1207. TENG, H. C. and HEYER, H. E. (1955): The relationship between sudden changes in weather and the occurrence of acute myocardial infarction. Amer. Heart J., 49: 9-20. WERBER, M., SPARKS, R. M. and GOETZ, A. C. (1972): The behavior of weakly electric fish (Sternarchus alb(frons) in magnetic fields. J. gen. Psychol. 86: 3-13. WEVER, R. (1968): Einfluss schwacher electro-magnetischer Felder auf die circadiane Periodik des Menschen. Naturwissenschaften, 55: 29-32.
Behavioral Effects in Monkeys Exposed to Extremely Low Frequency Electromagnetic Fields
by
J. O. de Lorge and J. D. Grissett
ABSTRACT. - - Several experiments with rhesus and squirrel monkeys on the influence of extremely 10w frequency (ELF) electromagnetic fields found no effects on behavior. Magnetic fields of 0.3 and 1.0 mT with electric fields of below 1 to 29 V / m at frequencies of 7, 10, 15, 45, 60 and 75 Hz were used. Small differences in ambulatory activity and response rate were occasionally observed, but no consistent effects between or within animals on any measures were obtained. No effects on reaction time, interresponse time, match-to-sample performance, and blood constituents were observed. Such previously reported effects may not be a consequence of ELF values alone, but are probably related to other environmental variables. INTRODUCTION In the last two decades there has been a surge of interest in the biological effects of extremely 10w frequency (ELF) electromagnetic fields. A number of reviews (Llaurado, Sances and Battocletti, 1974; K6nig, 1975; Persinger, 1975; Persinger, Ludwig and Ossenkopp, 1974) have shown this interest to be based on the accelerated use of electricity by communities throughout the world. A majority of ELF experiments generally simulated the electric and magnetic fields with plates and Helmholtz coils. However, the ELF stimuli among those studies varied to such an extent that almost no experiments have been replicated by different investigators using identical stimulus values. Variations occurred in frequency, intensity and duration, and electric and magnetic components were utilized separately or together. In most cases, when the magnetic component was manipulated, the electric component was seldom regarded or measured. Frequencies ranged from 0.1 Hz (Friedman, Becker and Bachman, 1967) to 100 Hz (Kolin, Brill and Broberg, 1959). Intensities varied from less than ambient level to very high levels, with magnetic fields from 13 #T to 0.874 T (1 tesla, T = 10,000 gauss) and electric fields from 0.007 to 30 kV/m. In the present study, frequencies from 7 to 75 Hz were used; the electric fields induced by Helmholtz coils ranged from less than 1 V/m to 29 V/m (rms)depending upon the particular experiment; and magnetic fields ranged from 0.3 to 1 mT. Two traditional approaches to the study of the interactions between electromagnetic fields and behavior exist. The first assumes that some animals have evolved with a sensitivity to electromagnetism that has enables them to reproduce more successfully than * Naval Aerospace Medical Research Laboratory, Naval Air Station, Pensacola, Florida 32508, USA. Presented at the Seventh International Biometeorological Congress, 17-23 August 1975, College Park, Maryland, USA.
358 less sensitive animals. This approach is illustrated in studies of migration and homing in pigeons (Keeton, 1972), electric location and capture of prey in fish (Werber, Sparks and Goetz, 1972), and regulation of biological rhythms in men (Wever, 1969). The second approach, taken in our research, assumes that because the basic physiology of an organism is an electrochemical process, its physiological processes might be disturbed by electromagnetic stimuli and result in observable behavioral changes. The purpose of the present series of experiments was to discover with monkeys if various behaviors, analogous to human behaviors, would be influenced by ELF magnetic and associated electric fields. Other studies have tended to be more concerned with species differences than behavior differences. Invariably, rats have been used to study ELF effects on general motor activity, man was the subject in studies of reaction time, and pigeons were subjects in migration studies. In our work we have selected behaviors previously reported to be susceptible to ELF fields, e.g., reaction time (K6nig and Krampl-Lambrecht, 1959), lever pressing (Gavalas et al., 1970), and general motor activity (Persinger et al., 1972). Other behaviors we investigated included a memory task and the monkey's ability to detect the presence of the ELF field. In addition, blood samples were analysed in some of the experiments. In toto, no indication of electromagnetic effects appeared. Occasionally trends occurred but could not be replicated either with the same or different subjects. Studies that obtain only negative results are thought to be of marginal value, particularly in behavior research. However, the demonstration that certain independent variables were of little or no consequence is of extreme practical importance, especially if maximal opportunities were present for the effects to be observed. Such was the case in the present experiments. METHOD SUBJECTS Six adult squirrel monkeys (Saimiri sciureus) were used in one series of experiments. One female, and two males were trained on a reaction time task. The other three male squirrel monkeys were trained on a variable-interval (VI) schedule of reinforcement to see if responding would be suppressed when the ELF field was present. Four adult rhesus monkeys (Macaca mulatta) were subjects in the second series of experiments. Two of these monkeys were males, and two were females. All of the animals were housed in a vivarium with normal geomagnetic fields (northerly direction, 50 #T inclined at approximately 55 ° below the horizon) and electric fields of less than 0.1 V/m. APPARATUS In each of 14 experiments Helmholtz coils surrounding animal enclosures were used to generate magnetic fields. Specific details of the arrangements and the fields are available in technical reports from this laboratory (de Lorge, 1972; 1973a; 1973b; 1974; Grissett, 1971; Grissett and de Lorge, 1971). During experimental sessions the animals were located in chambers large enough for unrestricted movement in all directions. E~ich chamber was outfitted with a work panel containing stimuli and response manipulanda in addition to apertures for food and water delivery. Panels were situated in the west end of the chamber. The enclosures were nonmetallic, noise attenuated, and isolated from floor vibrations. Noise to the chambers was masked with a 75 dB white noise. The chambers were ventilated, and during the experiments temperature, humidity, and atmospheric pressure were recorded. PROCEDURE Table l summarizes the various experiments for the squirrel monkeys and rhesus monkeys, respectively. The experiments are numbered in chronological order in each table;
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360 the squirrel monkey series was conducted first. A complete description of the tasks can be found in de Lorge and Marr (1974) whereas brief descriptions as listed in the Behavior column of the table follow: EXPERIMENTS 1-4, SQUIRREL MONKEYS. - - Reaction time was a task where the monkey was required to release a lever when a lamp was illuminated. Response suppression was a task wherein the monkeys pressing a lighted disc for food were presented with a 10-s presentation of a magnetic field to see if disc-pressing was suppressed. EXPERIMENTS 5-14, RHESUS MONKEYS. - - Reaction time in the rhesus studies required a monkey to lift a lever in the presence of a red light and release the lever when a tone was presented. Fixed-interval behavior occurred when the monkey repeatedly lifted a lever and after 20 s elapsed (FI 20-s) food pellets were delivered at the next lever lift. The match-to-sample task trained monkeys to press a center disc trans-illuminated with one of I0 different stimuli. Below the center disc were two comparison discs. A response on the center disc was followed by removal of its stimulus, and 1 s later the same stimulus appeared on one of the comparison discs. A different stimulus was on the opposite disc. When the disc with the matching stimulus was pressed reinforcement occurred. The fixed-ratio task merely required 10 lever lifts for food reinforcement. The interresponse-time task (IRT) required the monkey to wait 5 s when a green light appeared before lifting a lever. Lever responses before 5 s and after 6 s produced no reinforcement and required another 5-s wait. Lever lifts between 5 and 6 s produced a food pellet. The reaction time, fixed interval, and match-to-sample tasks occurred consecutively in the same experiments during the same sessions. The Fixed Ratio (FR) and Interresponse Time (IRT) tasks also occurred consecutively during their experiment (exp. 11). Later the IRT task alone was instituted (exps. 12-14). The Field Exposure column in the table shows the total hours the animals were in the fields and how long a daily exposure lasted. The Sessions column gives the hours an animal worked each session regardless of how long it was in the chamber and the number of sessions of exposure that occurred without an interruption. The animals were run 7 days a week in experiments 3, 8, 9 and 10. All animals were deprived of food for training. The squirrel monkeys were generally tested at about 85% of their free feeding body weights whereas the rhesus monkeys worked at weights anywhere from 70 to 100% of their free feeding weights.
RESULTS AND DISCUSSION NO effects of acute exposure to 0.3-mT magnetic fields were seen in the squirrel monkeys at either 45- or 7-Hz frequencies. The analyses included the mean number of correct responses required to receive a food pellet (reinforcement ratio) and the ratio of correct responses to total responses (efficiency ratio). The mean reaction time and its variance were also assessed. A gradual increase in the efficiency ratio and a slight decrease in the reinforcement ratio indicated a learning effect occurred but there was no evidence of any effect caused by the ELF exposure. In an extension of that study, the effects of chronic exposure to 1.0-mT, 45-Hz fields were explored (Experiment 3). The same 3 monkeys were in the fields for 42 consecutive days, 24 hours a day, although they worked on the reaction time task for only 1 hour each day. Again a gradual learning effect was seen in the efficiency ratio, reinforcement ratio, and also in reaction time, but nothing indicated an effect of the magnetic field even after 1008 hours of exposure. In Experiment 4, an attempt was made to investigate the arousing characteristics of ELF stimuli by brief presentations of a 1.0-mT, 45-Hz magnetic field while the squirrel monkeys were engaged in high, continuous rates of lever responding. Three different
361 monkeys that had never been exposed to magnetic fields were trained to respond on a VI 1-min schedule of reinforcement. Response suppression was calculated as the ratio of lever responding during the field to responding both during the field and when the field was absent. Ratios less than 0.5 indicate suppression and ratios greater than 0.5 indicate enhancement. When the 10-s presentation of the ELF field was used as a suppression stimulus, the mean ratios for the 3 monkeys were 0.49, 0.52 and 0.49, indicating that the animals were not aroused by or did not detect the brief presence of the field. Although the data varied a great deal, no consistent trends appeared. The data were typical of control ratios where no stimuli occurred. Suppression ratios in an experiment with visual stimuli alone were generally around 0.2 to 0.3. Rhesus monkeys were trained on highly complex tasks under the assumption that more stringent behavioral requirements would increase their susceptibility to the ELF stimuli. The rhesus monkeys were required to work these tasks for periods of from 2 to 8 hours. General motor activity was recorded during all of the rhesus monkey experiments. A number of behavioral changes were observed such as in ambulatory behavior, but typically these changes were not related to the ELF fields. Most performance changes were a consequence of continuous experimental sessions and elapsed time. No effect on reaction time or its associated behavior was seen during 3-hour exposures. As these same 2 rhesus monkeys experienced additional sessions, behavior on all three tasks became less variable, and when the 45- and 10-Hz fields were introduced during 8-h sessions, behavior was extremely stable, allowing a much more precise comparison to be made. When 10-Hz fields were first introduced, Experiment 7, both AR4 and AP6 produced significantly less general motor activity. This was the first and only time a consistent effect of the fields was observed and led to a replication of the 10-Hz study, Experiment 8. However, in the replication no activity changes were seen in the same two animals or later in Experiment 10 with female animals. Responding on an FI 30-s schedule of reinforcement was also not influenced by the 10-Hz fields in Experiment 8. The mean response rate per 3-s segment of the FI 30-s schedule was plotted for the 2 monkeys as a function of the field's presence. Most of the data, within an animal, representing field and no field, were very close or even overlapped. This was particularly true where the rates were greater than one response per minute. Perhaps tasks with high response rates are too insensitive and the probability of changing behavior is higher on a low rate task. The match-to-sample task produced low rate behavior although it did require more attention from the animal in that the monkey had to rely on its immediate memory to successfully complete the task. No definite differences in match-to-sample behavior were related to either the 60- or 10-Hz fields (Experiments 9 and 10) in the female rhesus monkeys, 3Z5 and 4Z7. Both animals were performing with about a 10% error, and their day-to-clay variations were much greater than field no-field variations. In Experiments 11, 12, 13, and 14 blood chemistry was investigated along with behavior. Blood samples were drawn biweekly and then weekly as the animals were exposed to 45- and 15-Hz magnetic fields. The following blood constituents were analyzed: triglycerides, creatine, hemoglobin, cholesterol, creatine phosphokinase, lactic dehydrogenase, potassium, serum glutamic oxaloacetic transaminase, calcium, red cell count, hematocrit, white blood cell count, monocytes, eosinophiles, polycytes, lymphocytes, bands, sodium, total protein, glucose, creatinine, blood urea nitrogen and serum glutamic pyruvic transaminase. Some of these indices had been implicated or suggested in other ELF studies. The values obtained fell within the range of other monkeys in our vivarium, and not one parameter consistently vaired in relation to the ELF fields. During the IRT task (Exp. 14) the animals did not detect the 45-Hz field when presented between 5 and 6 s, a circumstance which should have produced more correct responses.
362 CONCLUSIONS AND RECOMMENDATIONS Apparently the ELF electromagnetic fields explored in the present study do not have large or consistent biological effects on nonhuman primates. Although others (GavalasMedici and Magdaleno, 1975; Gavalas et al., 1970) have shown that the behavior of some monkeys, Macaca nemestrina, was influenced by electric fields, the observed effects were limited to particular voltages and frequencies. For example, one study (Gavalas et al., 1970) using 7 V/m fields found changes in the mean IRT at 7-Hz but not at 10-Hz, whereas a replicated study (Gavalas-Medici and Magdaleno, 1975) found no changes in mean IRT at 1 V/m and 10 V / m regardless of frequency. With increases in voltage level, e.g., 56 V/m, the 7-Hz and 75-Hz fields had an effect but 60-Hz fields did not. At 100 V/m these two investigators found no differences between experimental and control sessions and concluded, after gathering additional control data, that fields of that intensity produced effects that persisted from exposure sessions to control sessions. Magnetic fields were not used in those studies; hence, the reported effects are probably specific to electric fields alone. No other studies on ELF magnetic fields and monkeys have been published, although Friedman and Carey (1972) reported that static fields of 20.0 mT did have an effect on squirrel monkeys during initial exposures. Even here, however~ the effect was transient and the animals seemed to have adapted to the fields. If adaptation does occur, particularly during the first or second exposures, and if there are longlived effects, the probability of detecting ELF influences on any animal decreases tremendously. Certainly, under such circumstances, monkeys are not the optimal animal to use. It is our opinion that man is the definitive subject for ELF studies as much of the earlier indications on an ELF influence were obtained with man. Although man may be the preferred subject, the behavior most often investigated, reaction time, is not the preferred measurement. No differences in reaction time in either man (Beischer, Grissett and Mitchel, 1973) or monkey were produced by the ELF fields studied in our laboratory. Other laboratories report a variety of findings. For example, K6nig and Krampl-Lambrecht (1959) found reaction time changes to depend upon the form of the electric wave. Later, Hamer (1968) reported reaction time increased at 3 Hz and decreased at 6, 8, II, and 12 Hz. Friedman, Becker and Bachman (1967) found no changes at 0.1 Hz but did at 0.2 Hz when magnetic fields were used. K6nig ( 197 l) when replicating Hamer's earlier experiment obtained similar results. Some very recent work confused the issue even more. R. Hauf (1974) and G. Hauf (1974) found that with 50-Hz fields of l, 15, and 20 kV/m, there was a tendency toward a rise in reaction time but the ELF presence had no further effect when the fields were turned off. No intensity relationships were observed. Replications of their study in their own laboratory, however, reported decreases in reaction time (Eisemann, 1975), and when a magnetic field was used, no significant changes were observed (Mantell, 1975). In these studies the the initiating effect of the field could be interpreted as an artifact caused by the use of sophisticated subjects. The designs invariably had field off, on, and off again with session lengths of 3 hours. No counterbalancing was attempted. Most human subjects today realize that experimental conditions are changed somewhere in the middle of the sessions, and this could account for the minor changes seen. The selection of the appropriate species and the appropriate behavior continues to be a problem in ELF research. Because it is postulated that the calcium ion may be responsible for mediating ELF effects (Adey, 1974; Ludwig, 1971), studies of invertebrates whose striatal muscle fibers produce calcium spikes might be profitable, It may also be helpful to investigate animals whose environment includes food sources, home sites, and enemies associated with electromagnetic phenomena. For example, electric fish spend much of their life in mud or dark murky waters. Is it likely that animals with similar environments share electromagnetic properties? Chronic investigations, although very expensive, are needed. When possible such studies should include circadian periodicity as a measure. Wever's (1968) research in
363 this area is some of the more impressive and should be replicated. In addition to longterm experiments the effect of other climatic phenomena, especially humidity and barometric pressure, should be observed. Many studies document the effects of barometric pressure on the heart (Teng and Heyer, 1955), on urine mucopolysaccharides (Milolajczyk, Allalouf and Ber, 1969), and on animal activity (Sprott, 1967). One recent dissertation reported that pigeons could not detect a continuous or alternating magnetic field (0.91 to 1.25 Hz, 8 to 15.3/~T) yet, they were extremely sensitive to changes in atmospheric pressure (Kreithen, 1974). It is possible that for effects to be consistently observed, the ELF field should change in conjunction with pressure, humidity, a n d / o r temperature. Perhaps there is a synergistic effect. In no ELF study should it be assumed that calculated fields alone are sufficient. Actual measurements should be taken. These include not only field measurements but those of noises, odors, vibrations, humidity, temperature, time of day, barometric pressure, and all other environmental changes which should be accurately recorded and whenever possible, controlled. Other investigators (Moos et al., 1970; Reiter, 1970) have continually emphasized the importance of such details because behaviors previously reported to be influenced by ELF fields are in most cases susceptible to other environmental changes also. It has been suggested that the more uncontrolled the behavior, the more susceptible it will be to electromagnetic stimul (Gavalas-Medici and Magdaleno, 1975). This means of course that such behavior will be susceptible to all environmental changes. Operant behavior is very stable and contains many inherently controlling stimuli. In a decision to use the operant approach with any organism the reinforcement contingencies should be dependent upon the animal's ability to detect the ELF fields, such as with a conditioned emotional response or a shock avoidance response. Even in these cases, however, ELF effects have not been observed (Marr, Rivers and Burns, 1973). ACKNOWLEDGMENT The assistance of C. S. Ezell and R. J. Franklin in conducting these studies, and M. Kelly and K. Duncan for typing assistance is greatly appreciated. REFERENCES ADEY, W. R. (1974): The influence of impressed electrical fields at EEG frequencies on brain and behavior. In: Behavior and Brain Electrical Activity. H. Altshuler and N. Burch (ed.), Plenum Press, New York. BEISCHER, D. E., GRISSETT, J. D., and MITCHEL, R. E. (1973): Exposure of man to magnetic fields alternating at extremely low frequency. NAMRL-!180, Naval Aerospace Medical Research Laboratory, Pensacola, Florida. (AD 770 140). DE LORGE, J. (1972): Operant behavior of rhesus monkeys in the presence of extremely low frequency-low intensity magnetic and electric fields, Experiment 1. NAMRL-II55, Naval Aerospace Medical Research Laboratory, Pensacola, Florida. (AD 754 058). DE LORGE, J. (1973a): Operant behavior of rhesus monkeys in the presence of extremely low frequency-low intensity magnetic and electric fields, Experiment 2. NAMRL-1179, Naval Aerospace Medical Research Laboratory, Pensacola, Florida. (AD 764 532). DE LORGE, J. (1973b): Operant behavior of rhesus monkeys in the presence of extremely low frequency-low intensity magnetic and electric fields, Experiment 3. NAMRL-lI96, Naval Aerospace Medical Research Laboratory, Pensacola, Florida. (AD 774 106).
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