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Comparative EEG frequencies in rhesus, stumptail, and cynomolgus monkeys
270
Eleetroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
CLINICAL
AND
LABORATORY
NOTES
COMPARATIVE EEG FREQUENCIES IN RHESUS, STUMPTAIL, A N D CYNOMOLGUS MONKEYS 1 M . F. JURKO, P H . D . AND O. J. ANDY, M . D .
Laboratory of Experimental Behavior, Department of Neurosurgery, University of Mississippi Medical Center, Jackson, Miss. (U.S.A.) (Accepted for publication: February 17, 1967) terns may exist between closely related species of monkeys.
The objective of this study is to establish a comparative baseline of spontaneous dominant EEG rhythm in three different species of Macaca monkeys: Rhesus (mulatta), Stumptail (speciosa), and Cynomolgus (irus). This report is made to provide background for investigations utilizing electroencephalographic criteria in species other than the Rhesus and to demonstrate that differences in EEG pat-
METHOD
Mortkeys Seventeen Rhesus, seventeen Stumptail, and five Cynomolgus monkeys were studied. These animals were between 2 and 3 years of age. Animals were allowed to become accustomed to the primate laboratory for 3 months before beginning EEG recordings. The technician who performed the EEGs was responsible for the handling and care of
1 Aided in part by National Institutes of Health Grant F R 00155. 20
RHESUS
STUMPTAIL
:;
15
v
°
CYNOMOLGUS
E _
.
.
.
.
;;
4_m
E
10
U [-
fi_
)i
,,
ii
"~
!;
i;,
;!
7
8
g
10
11 12 14 16+
ii
;i
?."
.. . . . . ................ ,,
7
8
9
.
.
.
.
.
.
ii )! ii ii
;;
10 11 12 14 16+
;;
;-
;;
8
9
10
. . . .
,,
,,
11 12 14 16+
c/sec Fig. 1 Spontaneous EEG frequency distribution. Frequencies of 13 c/see are included in the 12 c/see bar and those of 15 c/sec in the 14 c/see bar. Sixteen-plus includes frequencies of 16 c/see and above. The percentage amounts of the given frequencies were accumulated from records taken during the awake but quiet state of the animals. (See text.)
Electroenceph. clin. Neurophysiol., 1967, 23:270-272
271
COMPARATIVE EEG STUDY IN MACACA MONKEYS RFP
RFP RPO
23g
RH1
160
RH3
244
12.5 ,'~.,~.~
RPO
269
224
270
279
227
274
,,.,,.,~
227
235
243
RH 5
RH2
223
268
221
275
278
RH 4 225 241
237 238
271
240
242
236
t
276
Fig. 2 Spontaneous awake EEG patterns in the Rhesus. Note that individual animals (numbered between the two runs) possess a predominantly slow or fast frequency pattern. The animals are arranged in the order of slow to fast frequencies from left to right. RFP (right fronto-parietal), RPO (right parieto-occipital). Calibrations: 50 #V, 1 sec.
L__
Fig. 4 Spontaneous awake EEG patterns in the Stumptail. Note the tendency for fast frequencies to be dominant in most animals. The different animals are designated by the numbers between the runs. Leads and calibration as in Fig. 2.
these animals because, as found by Caveness (1962), if the animal is familiar with, and trusts the person doing the recording, it tends to become reasonably docile and more tractable.
RFP
RPO
222
156 ~-~v~,V
,~
EEG testing procedure 155
153
154
164
l _ _
Fig. 3 Spontaneous awake EEG patterns in Cynomolgus. Note the tendency for mixtures of slow and fast frequencies within the same animal. The different animals are designated by the numbers between the runs. Leads and calibration as in Fig. 2.
All examinations were done in the same room which was small, quiet, and semi-darkened. N o sedatives or tranquilizing drugs were employed. The monkey was placed on an elevated wooden saddle in a prone position. For the animal's comfort, the body rested on a relatively broad base. The hanging limbs were restrained with soft cloth straps. The chin was held in midline by being positioned between two small padded supports. N o rigid restraints were used because they led to struggling and thus to the development of muscle and movement artifacts. Six small Grass scalp electrodes were held to the scalp with bentonite paste. These were placed in 3 laterally equidistant and bilaterally symmetrical positions over the frontal, temporal and occipital regions as outlined by Caveness (1962). Bipolar recordings were made between the frontoparietal and parieto-occipital areas bilaterally. Unipolar recordings with indifferent electrodes at the ear, the back, and nose were not feasible because they accentuated artifacts. The recording instrument was a Grass Model III-C electroencephalograph. Each monkey was tested 3 times on successive weeks. The animals were held sufficiently long at each testing, usually 30', to establish the spontaneous waking rhythm at rest. The animals did not drift into sleep.
Electroenceph. clin. Neurophysiol., 1967, 23:270-272
272
M.F. JURKO AND O. J. ANDY
EEG evaluation
DISCUSSION
The 3 EEGs on each monkey were visually analyzed as follows: Frequency was determined according to recurrence, in time, of a given wave pattern irrespective of wave duration. The total period of time for the appearance of specific frequencies was determined only from the artifact free episodes. Thirty-minute periods of E E G recordings were made. In order to obtain an approximate evaluation of the behavioral state of the animal during recordings, the mean periods (in minutes) of episodic movement artifacts and those of artifact free episodes were determined.
Statistical analysis Analysis of variance was used to evaluate the difference in the mean time of restless versus quiet periods during recordings. The test was used to evaluate differences in frequencies between groups.
RESULTS
Behavioral state of the animals For all animals, the mean period of restlessness and movement ranged from 12.9 to 13.2 min and the mean period of quiet state from 2.5 to 3.5 min. It should be stressed that the period of movement was approximately 4--5 times greater than the mean period of the quiet state. A n analysis of variance was done between the three animal groups for the two periods analyzed, and there was no significant difference between them. The animals were not asleep during the quiet periods of recording. They were awake without manifesting agitation and movement and their tracings did not display sleep patterns.
Our finding of a 10 c/sec E E G frequency mode in the awake Rhesus is in accord with the results of Caveness (1962) who reported 9.8 c/see as the average waking frequency in fourteen Rhesus monkeys 1-2 years of age. Our results suggest that the dominant awake EEG frequency is faster in the Stumptail and Cynomolgus monkeys. In comparison to the Rhesus and Stumptail, the Cynomolgus showed a spread in frequency representations of nearly equal amounts. It is also of interest that there was a relatively large amount of frequencies of 6-9 c,/sec in the Rhesus compared to the small amount of these frequencies in the Cynomolgus and Stumptail. Differences in E E G frequency patterns have been found among animals representing similar orders but lower than primates. Shlafer (1966) recently reported that guinea pigs and white rats belonging to the same order (rodentia) show a difference in the frequency of the spontaneous background E E G activity. In guinea pigs, the most characteristic background was 5-10 c/sec; and in rats, it was 10-15 c/see.
SUMMARY The awake EEG frequency patterns were compared in three species of Macaca monkeys: Rhesus (mulatta),. Stumptail (speciosa), and Cynomolgus (irus). Relatively slower frequencies were present in the Rhesus than in Stumptail and Cynomolgus. The variability of frequency distribution between species was least in the Stumptail and greatest in the Cynomolgus.
Frequency distribution The percentage amount of EEG during quiet periods for which the frequency could be determined consisted of 66.6% in the Rhesus, 61.4% in the Cynomolgus and 56.3 % in the Stumptail. Each of the species appeared to possess a dominant mode which differed from one another (Fig. 1). In the Rhesus, the mode was at 10 c/see and in the Stumptail at 12 c/sec. These were significantly different at the 0.001 level. In contrast, the mode of 14 c/see in the Cynomolgus was not significantly different from the 12 c/see mode in the Stumptails. However, it was significantly different from the 10 c/see mode of the Rhesus (0.I0). As readily seen in the graphed frequency distribution, the spread of amounts of specific frequencies around the modes differs between each species (Fig. 1). In the Rhesus, there is a tendency for a bimodal type of pattern with a second and less prominent mode at approximately 8 c/see. It is of interest that within a given animal the frequency tends to be predominantly in the slower or faster range (Fig. 2). In contrast, the Cynomolgus shows a plateau pattern with the amounts of frequencies progressively incaeasing as one approaches the mode of 14 c/sec. A mixture of fast and slow frequencies tends to be present within the same animal (Fig. 3). In the Stumptail, there appears to be a somewhat equal distribution around a very dominant 12 c/see mode (Fig. 4).
R~SUM~ FREQUENCES COMPAREES DE L'EEG CHEZ LES SINGES" RHI~SUS, STUMPTAIL ET CYNOMOLGUS Les auteurs comparent les fr6quences de I'EEG d'6veil chez trois e s p i e s de singes Macaca: rhesus (mulatta), stumptail (speciosa) et cynomolgus (irus). Des fr6quences relativement plus lentes que chez les stumptail et cynomolgus sont pr~sentes chez le rh6sus. La variabilit~ de la distribution des fr6quences entre espba:es est la plus faible chez les stumptail et la plus 6levee chez les cynomoigus.
The authors wish to acknowledge the technical assistmace of Miss C. Dearman and Mr. R. Dearmma. REFERENCES
CAVENESS, W. F. Atlas of eleetroencephalography in the developing monkey, Macaea mulatta. Addison-Wesley, Reading, Mass., 1962, 145p. SHLAFER,T. P. Comparative characteristics of electrical activity of the cerebral cortex neurons of white rats and guinea pigs. Electroenceph. din. Neurophysiol.,
1966, 20:418
Reference: JtmKO, M. F. and ANDY, O. J. Comparative E E G frequencies in rhesus, stumptail, and cynomolgus monkeys. Electroenceph. din. Neurophysiol., 1967, 23: 270-272.
Eleetroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
CLINICAL
AND
LABORATORY
NOTES
COMPARATIVE EEG FREQUENCIES IN RHESUS, STUMPTAIL, A N D CYNOMOLGUS MONKEYS 1 M . F. JURKO, P H . D . AND O. J. ANDY, M . D .
Laboratory of Experimental Behavior, Department of Neurosurgery, University of Mississippi Medical Center, Jackson, Miss. (U.S.A.) (Accepted for publication: February 17, 1967) terns may exist between closely related species of monkeys.
The objective of this study is to establish a comparative baseline of spontaneous dominant EEG rhythm in three different species of Macaca monkeys: Rhesus (mulatta), Stumptail (speciosa), and Cynomolgus (irus). This report is made to provide background for investigations utilizing electroencephalographic criteria in species other than the Rhesus and to demonstrate that differences in EEG pat-
METHOD
Mortkeys Seventeen Rhesus, seventeen Stumptail, and five Cynomolgus monkeys were studied. These animals were between 2 and 3 years of age. Animals were allowed to become accustomed to the primate laboratory for 3 months before beginning EEG recordings. The technician who performed the EEGs was responsible for the handling and care of
1 Aided in part by National Institutes of Health Grant F R 00155. 20
RHESUS
STUMPTAIL
:;
15
v
°
CYNOMOLGUS
E _
.
.
.
.
;;
4_m
E
10
U [-
fi_
)i
,,
ii
"~
!;
i;,
;!
7
8
g
10
11 12 14 16+
ii
;i
?."
.. . . . . ................ ,,
7
8
9
.
.
.
.
.
.
ii )! ii ii
;;
10 11 12 14 16+
;;
;-
;;
8
9
10
. . . .
,,
,,
11 12 14 16+
c/sec Fig. 1 Spontaneous EEG frequency distribution. Frequencies of 13 c/see are included in the 12 c/see bar and those of 15 c/sec in the 14 c/see bar. Sixteen-plus includes frequencies of 16 c/see and above. The percentage amounts of the given frequencies were accumulated from records taken during the awake but quiet state of the animals. (See text.)
Electroenceph. clin. Neurophysiol., 1967, 23:270-272
271
COMPARATIVE EEG STUDY IN MACACA MONKEYS RFP
RFP RPO
23g
RH1
160
RH3
244
12.5 ,'~.,~.~
RPO
269
224
270
279
227
274
,,.,,.,~
227
235
243
RH 5
RH2
223
268
221
275
278
RH 4 225 241
237 238
271
240
242
236
t
276
Fig. 2 Spontaneous awake EEG patterns in the Rhesus. Note that individual animals (numbered between the two runs) possess a predominantly slow or fast frequency pattern. The animals are arranged in the order of slow to fast frequencies from left to right. RFP (right fronto-parietal), RPO (right parieto-occipital). Calibrations: 50 #V, 1 sec.
L__
Fig. 4 Spontaneous awake EEG patterns in the Stumptail. Note the tendency for fast frequencies to be dominant in most animals. The different animals are designated by the numbers between the runs. Leads and calibration as in Fig. 2.
these animals because, as found by Caveness (1962), if the animal is familiar with, and trusts the person doing the recording, it tends to become reasonably docile and more tractable.
RFP
RPO
222
156 ~-~v~,V
,~
EEG testing procedure 155
153
154
164
l _ _
Fig. 3 Spontaneous awake EEG patterns in Cynomolgus. Note the tendency for mixtures of slow and fast frequencies within the same animal. The different animals are designated by the numbers between the runs. Leads and calibration as in Fig. 2.
All examinations were done in the same room which was small, quiet, and semi-darkened. N o sedatives or tranquilizing drugs were employed. The monkey was placed on an elevated wooden saddle in a prone position. For the animal's comfort, the body rested on a relatively broad base. The hanging limbs were restrained with soft cloth straps. The chin was held in midline by being positioned between two small padded supports. N o rigid restraints were used because they led to struggling and thus to the development of muscle and movement artifacts. Six small Grass scalp electrodes were held to the scalp with bentonite paste. These were placed in 3 laterally equidistant and bilaterally symmetrical positions over the frontal, temporal and occipital regions as outlined by Caveness (1962). Bipolar recordings were made between the frontoparietal and parieto-occipital areas bilaterally. Unipolar recordings with indifferent electrodes at the ear, the back, and nose were not feasible because they accentuated artifacts. The recording instrument was a Grass Model III-C electroencephalograph. Each monkey was tested 3 times on successive weeks. The animals were held sufficiently long at each testing, usually 30', to establish the spontaneous waking rhythm at rest. The animals did not drift into sleep.
Electroenceph. clin. Neurophysiol., 1967, 23:270-272
272
M.F. JURKO AND O. J. ANDY
EEG evaluation
DISCUSSION
The 3 EEGs on each monkey were visually analyzed as follows: Frequency was determined according to recurrence, in time, of a given wave pattern irrespective of wave duration. The total period of time for the appearance of specific frequencies was determined only from the artifact free episodes. Thirty-minute periods of E E G recordings were made. In order to obtain an approximate evaluation of the behavioral state of the animal during recordings, the mean periods (in minutes) of episodic movement artifacts and those of artifact free episodes were determined.
Statistical analysis Analysis of variance was used to evaluate the difference in the mean time of restless versus quiet periods during recordings. The test was used to evaluate differences in frequencies between groups.
RESULTS
Behavioral state of the animals For all animals, the mean period of restlessness and movement ranged from 12.9 to 13.2 min and the mean period of quiet state from 2.5 to 3.5 min. It should be stressed that the period of movement was approximately 4--5 times greater than the mean period of the quiet state. A n analysis of variance was done between the three animal groups for the two periods analyzed, and there was no significant difference between them. The animals were not asleep during the quiet periods of recording. They were awake without manifesting agitation and movement and their tracings did not display sleep patterns.
Our finding of a 10 c/sec E E G frequency mode in the awake Rhesus is in accord with the results of Caveness (1962) who reported 9.8 c/see as the average waking frequency in fourteen Rhesus monkeys 1-2 years of age. Our results suggest that the dominant awake EEG frequency is faster in the Stumptail and Cynomolgus monkeys. In comparison to the Rhesus and Stumptail, the Cynomolgus showed a spread in frequency representations of nearly equal amounts. It is also of interest that there was a relatively large amount of frequencies of 6-9 c,/sec in the Rhesus compared to the small amount of these frequencies in the Cynomolgus and Stumptail. Differences in E E G frequency patterns have been found among animals representing similar orders but lower than primates. Shlafer (1966) recently reported that guinea pigs and white rats belonging to the same order (rodentia) show a difference in the frequency of the spontaneous background E E G activity. In guinea pigs, the most characteristic background was 5-10 c/sec; and in rats, it was 10-15 c/see.
SUMMARY The awake EEG frequency patterns were compared in three species of Macaca monkeys: Rhesus (mulatta),. Stumptail (speciosa), and Cynomolgus (irus). Relatively slower frequencies were present in the Rhesus than in Stumptail and Cynomolgus. The variability of frequency distribution between species was least in the Stumptail and greatest in the Cynomolgus.
Frequency distribution The percentage amount of EEG during quiet periods for which the frequency could be determined consisted of 66.6% in the Rhesus, 61.4% in the Cynomolgus and 56.3 % in the Stumptail. Each of the species appeared to possess a dominant mode which differed from one another (Fig. 1). In the Rhesus, the mode was at 10 c/see and in the Stumptail at 12 c/sec. These were significantly different at the 0.001 level. In contrast, the mode of 14 c/see in the Cynomolgus was not significantly different from the 12 c/see mode in the Stumptails. However, it was significantly different from the 10 c/see mode of the Rhesus (0.I0). As readily seen in the graphed frequency distribution, the spread of amounts of specific frequencies around the modes differs between each species (Fig. 1). In the Rhesus, there is a tendency for a bimodal type of pattern with a second and less prominent mode at approximately 8 c/see. It is of interest that within a given animal the frequency tends to be predominantly in the slower or faster range (Fig. 2). In contrast, the Cynomolgus shows a plateau pattern with the amounts of frequencies progressively incaeasing as one approaches the mode of 14 c/sec. A mixture of fast and slow frequencies tends to be present within the same animal (Fig. 3). In the Stumptail, there appears to be a somewhat equal distribution around a very dominant 12 c/see mode (Fig. 4).
R~SUM~ FREQUENCES COMPAREES DE L'EEG CHEZ LES SINGES" RHI~SUS, STUMPTAIL ET CYNOMOLGUS Les auteurs comparent les fr6quences de I'EEG d'6veil chez trois e s p i e s de singes Macaca: rhesus (mulatta), stumptail (speciosa) et cynomolgus (irus). Des fr6quences relativement plus lentes que chez les stumptail et cynomolgus sont pr~sentes chez le rh6sus. La variabilit~ de la distribution des fr6quences entre espba:es est la plus faible chez les stumptail et la plus 6levee chez les cynomoigus.
The authors wish to acknowledge the technical assistmace of Miss C. Dearman and Mr. R. Dearmma. REFERENCES
CAVENESS, W. F. Atlas of eleetroencephalography in the developing monkey, Macaea mulatta. Addison-Wesley, Reading, Mass., 1962, 145p. SHLAFER,T. P. Comparative characteristics of electrical activity of the cerebral cortex neurons of white rats and guinea pigs. Electroenceph. din. Neurophysiol.,
1966, 20:418
Reference: JtmKO, M. F. and ANDY, O. J. Comparative E E G frequencies in rhesus, stumptail, and cynomolgus monkeys. Electroenceph. din. Neurophysiol., 1967, 23: 270-272.