interhemispheric functional differences in prefrontal cortex of monkeys

JOURNAL OF NEUROBIOLOGY, VOL. 6, NO. 1, PP. 39-49

INTERHEMISPHERIC FUNCTIONAL DIFFERENCES IN PREFRONTAL CORTEX OF MONKEYS

J. S. STAMM, A. GADOTTI, and S. C. ROSEN

State University of New York at Stony Brook, Stony Brook, New York 11790

SUMMARY

Monkeys had nonpolarizable electrodes implanted bilaterally in prefrontal (principal sulcus) , precentral, and occipital cortex. They were trained on a spatial delayed-response (DR) task (8-sec intratrial delay), while cortical potentials were recorded. Three groups of monkeys were trained to 90% criterion: ( A ) 4 monkeys with only the right hand (the left wrist was attached to the testing chair); ( B ) 2 monkeys with only the left hand; and (C) 2 monkeys with the left and right hands on alternate sessions. Intermanual transfer tests were then given.

Averaged steady potential (SP) shifts of several seconds duration were found in prefrontal cortex during cue presentation and the early portion of the intratrial delay and from the precentral area during the choice response. Evaluations of these SP shift magnitudes indicated: ( I ) Training with only one hand resulted in substantially larger SP shifts in the prefrontal and precentral areas contralateral to the responding hand; (2) alternate hand training resulted in somewhat larger prefrontal SP shifts in the right hemisphere; (3) intermanual transfer had marked effects on the precentral SP shifts, with larger magnitudes in the hemisphere contralateral to the responding hand, but had little effect on the magnitudes of both prefrontal SP shifts. (4) Subsequent training of Group C monkeys with only one hand resulted in greater SP shifts in the prefrontal area contralateral to the responding hand and in decreased SP shifts in the ipsilateral prefrontal area; and (5) additional intermanual transfer tests had no effects on SP shift magnitudes from both prefrontal areas. These findings indicate a dissociation in interhemispheric functions between the precentral and prefrontal cortical areas, with the former implicated in motor organization for the contralateral limb, and the latter in mediation of mnemonic processes, primarily in one hemisphere. This hemispheric specialization is affected by the hand-training procedure, but other endogenous or experiential factors may be involved.

INTRODUCTION

Our understanding of higher cortical functions in mammalian behavior has been derived predominantly from the results of ablation experiments.

39 1975 by John Wiley & Sons, Inc.

40 S T A M M , G A D O T T l , A N D ROSEN

With regard to the role of associalion cortex, bilateral ablations of cir- cumscribed cortical areas are required to severely disrupt the animal’s performance on complex tasks that involve perceptual, mnemonic, or as- sociative functions. Thus, bilateral resection of cortex in the principal sulcus of the monkey’s dorsolateral prefrontal cortex results in the animal’s inability to solve the delayed response task, whereas unilater<al ablation of this segment, or bilateral damage to other association areas, does not produce a pronounced deficit.

The apparent findings of bilateral cortical implication in behavioral processes have led to the concept of “functional equivalence” between homologous structures in the two hemispheres. However, this interpretation appears a t variance with localizations of higher order processes in the human brain, where the evidence indicates functional specialization in each hemisphere. Furthermore, reports published in recent years have provided some evidence for hemispheric specialization in the monkey. Tests for hand preference (Warren, 1953; Ettlinger and Moffett, 1964) have shown left- or right-hand dominance in some monkeys, but also an appreciable incidence of ambidexterity; and commissurotomized monkeys reportedly exhibit a preference for use of one hemisphere in the solution of discrimination problems (Gazzaniga, 1963, 1971).

We have adapted a different experimental technique for evaluating localization of ccrtical functions, namely that of recording electrocortical potentials in monkeys with intact brains during performance on complex tasks (Stamm and Rosen, 1969, 1972). Monkeys with chronically implanted nonpolarizable electrodes in the prefrontal, precentral, and occipital areas were trained on a spatial delayed-response (DR) task. The DR trial begins with illumination of a left or right display window (the cue), followed by an intratrial delay, and then illumination of both display windows. A reward is given to the monkey for pressing on the cued window. We have obtained averaged surface-negative steady potential (SP) shifts of several seconds duration during the course of the DR trial, with the time course of each SP shift dependent upon electrode location. A pronounced SP shift was recorded from prefrontal cortex during cue presentation and the early portion of the intratrial delay, and from the precentral area in relation to the monkey’s responses. The prefrontail SP shift was considered an expression of the implication of the prefrontal segment in the formation of spatial short-term memory required for task solution (Stamm and Rosen, 1972). Our findings are consonant with results obtained by the recording of prefrontal neuronal discharges (Fuster and Alexander, 1971; Fuster, 1973) and by disruptive electrocortical stimulation (Stamm, 1969; Stamm and Rosen, 1973). In our experiments one arm of the monkey was restrained and systematic recordings were generally obtained only from the hemisphere contralateral to the responding hand.

Information with regard to possible hemispheric differences in task mediation might be obtained with bilateral recordings of cortical SP shifts

P K E F R O N T A L C O R T E X OF MONKEYS 41

when monkeys are tested with different responding hands. The present experiments were designed to evaluate several hypotheses with regard to functional interrelations among the prefrontal and precentral cortical areas, namely: (a ) functional equivalence between the two prefrontal areas, which would be indicated by synchronous SP shifts from both areas, regardless of the responding hand; or ( b ) coordination between a prefrontal segment and its ipsilateral precentral area as expressed by greater SP shi€ts from both areas when the contralateral hand is used for responding; or (c) functional superiority of one prefrontal area, as seen by greater shifts in that hemisphere, regardless of the responding hand. Our findings in favor of the last interpretation raise further questions as t o the ontogeny and stability of such prefrontal superiority, i.e., whether it is endogenously determined or develops in relation to the monkey’s training experience.

METHOD AND RESULTS

DPlayed response apparatus

For daily testing the monkey was placed in a restraining chair which immobilized its head and restricted movements of one of its arms by means of a wristcuff that was clamped to a shelf on the chair. The chair was placed in front of a vertical opaque panel which contained two transparent circular display windows (3.5 cm diam, 6.5 cm apart) at the monkey’s eye level. Each window was covered by a transparent disk which could he depressed by the monkey. Below the window was a transparent food cup into which 45 mg sucrose pellets were dispensed. Each trial began with cue presentation when one of the disks was illuminated for 1 sec with white light. Both windows then remained dark for the intratrial delay (generally 8 sec), and then were illuminated with blue light. A press by the monkey on either disk extinguished the blue illumination for the intertrial interval (generally 18 sec). A correct response was followed by delivery of a sugar pellet and 1 / 2 sec illumination of the food cup.

Electrodes and recording

During aseptic surgery under nembutal anesthesia, pairs of Ag-AgC1 nonpolarizable electrodes were chronically implanted bilaterally in prefrontal, precentral, and occipital cortex. The electrodes were similar to those described by Rowland (1968) and each one consisted of a tapered glass capillary tube, filled with saline agar gel. Immersed in the gel was a 1 cm coil of chlorided silver wire, with a lead that emerged from the wide sealed end of the tube. The open end of the tube presented a circular recording surface of 1-2 mm in diameter, and the tube was cut to the desired length a t the time of surgery. At each cortical site one electrode was placed on the pial surface and the other in adjacent white matter, with a 5-10 mm separation between tips. For some monkeys the right precentral surface electrode was placed on the dura, or was not implanted. For the prefrontal placement the principal sulcus was gently opened and the surface electrode was inserted in the posterior half of the sulcus while the reference electrode was implanted in cortex lateral or medial to the sulcus. The electrode leads were soldered to points on Amphenol connectors which were cemented to the skull. Fascia and skin were sutured around the cement mound.

During recording sessions the Amphenol plug was connected by shielded low-noise cables to dc preamplifiers of a Grass Polygraph. Output from the power amplifiers led t o a 7-channel FM magnetic tape recorder, which also recorded a trigger pulse 6 sec before the DR trial.

42 S T A M M , GADOTTI , AND ROSEN

Data analysis

Each session's data that had been recorded on magnetic tape were subsequently avrrxged in forty-trial blocks for approximately 32 sec epochs with a PDP-12A computer. For additional analysis three 6-sec segments of the averaged curve w e ~ e selected, namely the segment: ( a ) immediately preceding cue presentation (base line level); ( b ) immediately following onset of the cue; and (c) following onset of the blue illumination of the response disks. Computations were then made of the areas lying between the base line level and the SP shifts of the other two segments.

EXPERIMENT I

Procedure

Four immature speciosa monkeys were used which had previously been highly over- trained on 8-sec DR. They had been trained for responding only with the right hand a t 120 trials per session for 171 to 313 sessions (mean of 24,480 trials). The monkeys were therefore calm in the apparatus and responded consistently above 90% correct. During the present expeiiment they were retrained with the right hand for 6 to 10 sessions (at 120 trials per session) and on the following day tested for transfer with the left hand.

Results

Left-hand testing continued for a t least 10 sessions.

The averaged SP shifts (Fig. 1) were substantially larger in the left than the right prefrontal areas during overtraining with the right hand and this difference in shift magnitudes persisted during transfer tests with the left hand. By contrast, the magnitudes of the precentral SP shifts were affected by intermanual transfer-the left

TABLE 1 Effect of Intermanual Transfer on Magnitudes of Steady Potential Shifts

~~ ~ ~ ~-

SP Shift Magnitude (pv x sec) from cortical area: ~~ ~- _ _ -~ ~~ ~

Left Right Left Right Left Prefrontal Prefrontal Precentral Precentral Occipital

M o n - R . L. R. L. R. L. R. L. R. L. key Hand Hand Hand Hand Hand Hand Hand Hand Hand Hand

~ . ~~ ~- ~- ~~~~~~

276'' 155 125 20 30 478 77 180 130 275h 120 103 16 0 230 128 84 170 334 278 271'1 186 174 2 -47 545 -17 267b 128 43 25 56 284 4 6 -28 153 162

279' 65 74 79 152 637 249 -29 470 ' 281" 67 10 92 108 205 153 56 93 62 - 6 280" 70 75 148 114 178 -19 16 -15 31 39

~ ~~~~ ~ _ _ _ _ ~ ~ Averages for the first 40 trials of 2-session blocks (each 120 trials) before and after

intermanual transfer. Shifts are for 6-sec epochs, time-locked to cue-onset for prefrontal and occipital, and to choice-response for precentral areas, with reference to 6-seo epochs preceding cue onset.

Intermanual transfer from right to left hand (Experiment I). Intermanual transfer from left to right hand (Experiment 11). For training on alternate days with right and left hand (Experiment 11). Averages

are for left- and right-hand sessions, respectively. <' Electrodes not implanted.

PREFRONTAL CORTEX OF MOiVKEYS

RIGHT H A N D L E F T H A N D

43

L M 1, I

/,, - c u e

...94J++ -!"?&%*+y ',L% bf@ 4 response &?2hyxb*r' u l +++dy\4vw&% LO ~~. I

f negat ive # ? b 7 - Lo r "..p -

Fig. 1. Averaged cortical steady potential shifts for monkey 1267, recorded with transcortical electrodes from prefrontal, precentral, and occipital areas during testing on 8-sec delayed response task. Electrodes were implanted in pairs~ t one on the cortical surface (except RM, on dura), the other in adjacent white matter. Each trace represents an average of 40 trials and is of 32-sec duration. The monkey was trained extensively with the right hand and then given intermanual transfer tests to the left hand. L = left; R = right; F = prefrontal (principalis); M = precentral (motor); 0 = occipital area. Calibration: vertical lines = 25 pV. Surface nega- tivity upward. Cue duration = 1 sec.

precentral shift became appreciably smaller, whereas the right shift showed a small increase in magnitude. Since the precentral cortical SP shifts were affected by the monkey's arm and hand movements, which occurred a t irregular periods during the DR trial, it was often impossible to obtain reliable averaged SP shift measures during the intratrial delay. In view of the time-locked occurrence of the choice response, the precentral SP shift magnitudes were computed for 6-sec epochs following this response. The small SP shifts from the right precentral location (Fig. 1) are probably reflections of the dural placement of the surface electrode in this monkey. Intermanual transfer also had no noticeable effects on the SP shifts from the occipital electrode placement.

The results for each of the 4 monkeys are summarized by Table 1, which presents the magnitudes of SP shifts before and after intermanual transfer. The transfer effects were evaluated by ratios of the difference in shift magnitude between p'e- arid posttransfer tests to the pretransfer test magnitude. The ratios for the left p i efrontal area indicated small decreases in SP shifts in three monkeys and an appreciable de- crease in $267 (Fig. 2). The ratios, however, indicated greater decreases in the left precentral than left prefrontal area for every monkey and the difference in magnitude of the changes was significant for the group of monkeys (Mann-Whitney U = 1, p = 0.029). Intermanual transfer did not result in consistent changes in SP shift magnitudes from the right prefrontal areas- they increased in two monkeys and decreased


L A RIGHT HAND 200

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L E F T HAND ,,, -

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.*.- - 4 -.--*-- *- - 1271

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4 2 4 6 8 1 0

TESTING SESSIONS Fig. 2. Magnitudes of averaged prefrontal SP shifts (uV-sec) recorded during

delayed response performance for four monkeys that had been trained with the right hand. The data are for two session blocks immediately before and after transfer to the left hand. Computer averages were obtained for the first 40 trials of 120 trial testing sessions. The magnitude of averaged shifts were determined for 6-sec periods following cue-onset with reference to 6-sec periods preceding the cue.

in two subjects. The occipital SP shifts were also not consistently affected by intermanual transfer. The differences hetween left and right prefrontal SP shift magnitudes were evaluated by two-tailed t-tests. For the combined data of left- and right-hand testing sessions the left prefrontal SP shifts were significantly larger a t p < 0.02 for monkey $267 and a t p < 0.01 for each of the other subjects. Intermanual transfer did not result in significant changes of left prefrontal SP shift magnitudes, withp > 0.20 for every subject. The magnitudes of right prefrontal SP shifts were l o o small for statistical evaluations.

These findings suggest an asymmetry in prefrontal functions, with the left hemisphere primarily implicated in mediation of delayed response, regardless of the responding hand. The lack of substantial right prefrontal SP shifts might indicate that this area is not implicated in task performance or, alternatively, that the electrode con- figurations were inappropriate for adequate recordings. The latter explanation seems

PREFRONTAL CORTEX OF MONKEYS 45

unlikely, however, since consistent results were obtained for every monkey and the left prefrontal, as well as both precentral and occipital electrodes, remained functional. In order to examine thi!: explanation more directly and to obtain additional information with regard t o hemispheric differences, the second experiment was conducted.

EXPERIMENT I1

Procedure

Four experimentally naive speciosa monkeys were used. They were first adapted to sitting in the chair and given hand preference tests by letting them reach for peanuts with both hands unrestrained. They then received training on DR a t 120 trials per session. The delay was initially zero seconds and then gradually increased until the monkeys responded on an 8-sec DR a t 90% correct. Two monkeys were trained to respond only with their left hand, while the others were trained during alternate sessions with their left and right hands. After they had attained stable performance the hand-training procedures were changed, as explained for each monkey in the following section. It was not possible to complete the testing program for every monkey.

Results

The recordings for all four monkeys showed SP shifts of substantial magnitudes from both the left and right prefrontal areas (Fig. 3) . The two monkeys that were trained with their left hands had differing magnitudes of prefrontal SP shifts, but in

~~

L E F T

, - - * - - . _ A _ _

IW - ~. - w \ -.4->. _ , D - - . '

B

0 I I I I I 1 I I I I I 1 I I I 1 I I I I I 1 ' P

u 2 4 6 8 0 1 2 1 4 lb 18 20 22 24 2b 28 30 32 Y 3b 24 40 42

TESTING SESSIONS

Fig. 3. Magnitudes of averaged prefrontal steady potential shifts (pV-sec) recorded during delayed response performance. Averages represent the first 40 trials of 120 trial testing sessions. Averaged SP shift magnitudes for 2-session blocks were computed for 6-sec periods following cue-onset with reference to 6-see periods preceding the cue. Monkeys were trained with hand alternation during successive sessions. (B and D) Monkeys were first trained with the left hand. Intermanual transfer tests are as indicated for responding hand.

(A and C)


both the right SP shifts were larger than Ihtrse from the left area. For $286 (Fig. 3D) the right prefrontal shift was significantly larger from the s tar t of training (t-test, p < 0.001); for $279 (Fig. 3B) the larger right prefrontal shift developed only during the course of training and the difference between prefrontal shift magnitudes was statistically significant ( p < 0.02) only for the final 10 sessions of left-handed training. Tnterrnanual transfer for $279, as indicated by Table 1, had only small effects on the prefrontal SE’ shiits, but resulted in marked changes in SP shift magnitudes from both the right and left precentral areas. During continued training with the right hand the magnitudes of the two prefrontal SP shifts again diverged (Fig. 3H), so that during the final 10 sessions the right prefrontal magnitude was significantly ( p < 0.05) larger than tha t from the left ai.ea. For this monkey combined mean left and right prefrontal SP shifts were larger with the left than the right responding hand ( p < 0.01). These results are in agreement with the findings of Experiment I, namely that training with only one responding hand results in greater SP shifts from ?,he contralateral prefrontal area and that, intermanual transfer does not appreciably affect the magnitudes of the shifts.

The monkeys who received training with both hands (1.280, 4281) showed a n unusual degree of session-to-session fluctuations in magnitudes of prefrontal SP shifts (Fig. 3A,C). This finding might be the consequence of their having to readjust to the changing testing conditions, although their performance scores remained consistently above 90% correct. The mean SP shift magnitudes during the alternate-hand training period were larger for the right than the left prefrontal areas, at p < 0.05 for $280 and p < 0.02 for h281. However the prefrontal SP shift magnitudes for left- and right-hand training did not differ significantly ( p > 0.2). The findings for precentral SP shifts (Table 1) are consistent with those obtained in Experiment I, in that the shift magnitudes for each hemisphere were generally greater when the contralateral hand was used for responding. The inconsistent data for fi280 during the alternate-hand training might be a reflection of the unstahle response patterns that were exhibited by this subject.

An impressive finding is the marked divergence in SP shift magnitudes during the course of the extensive training by monkey 7281 (Fig. 3A). This occurred most rapidly during the 10-session period of left-hand training when the right prefrontal SP shift increased t o twice its former magnitude and tha t from the left prefrontal area declined toward base line level. The substantial difference in shift magnitudes continued during the subsequent 24 recorded sessions of right-handed testing. Com- parisons between the initial alternate-hand training period and the final sessions with right-hand testing showed a significant increase in the right prefrontal SP shift, magnitude ( p < 0.001), but the decline in the left prefrontal magnitudes was not significant ( p > 0.10). The interspersed test sessions with the left hand during the final testing ljhase resulted in little change of SP shift magnitudes from either prefrontal area. The difference in shift magnitudes between the prefrontal areas during the course of overtaining is consistent with the findings obtained for the four monkeys in Experiment I.

Our findings of prontrunced hemispheric differences between the prefrontal areas in all eight monkeys raises the questions of behavioral signs of left or right differences’. The tests conducted during the adaptation period when peanuts were presented to each monkey from its right or left visual field indicated reaching preferences by six monkeys. However, the direction of these preferences was not related t o the hemisphere from which greater prefrontal SP shift.s were recorded. An interesting finding was obtained for !L281, one of the monkeys t h a t did not exhihit a reaching preference. Counts of interresponse presses during DR performance showed tha t in 103 out of 130 sessions this monkey pressed more often to the left than to the right disk. Moreover, the monkey’s mean error responses for a total of 61 sessions were 1.7% t o the right, hu t only 0.7% to the left disk. These findings of preferred left orientation during testing might he related t o the initially higher magnitude SP shifts from the right than the left prefrontal area.

PREFRONTAL CORTEX OF M O N K E Y S 47

DISCUSSION

With the present method of recording cortical steady potentials during perfarmance of the delayed response task we have obtained evidence for a dissociation of hemispheric functions between the monkey’s precentral and prefrontal areas. Averaged surface negative shifts from precentral areas are time-locked to motor responses and are affected by intermanual transfer. The SP shifts from either hemisphere are consistently of greater magnitude for the contralateral than the ipsilateral responding hand. By contrast, the surface negative SP shifts from the prefrontal areas which occur during the intratrial delay interval are not appreciably affected by intermanual transfer and are of greater magnitude in one hemisphere, regardless of the responding hand. The most pronounced and stable differences between the left and right prefrontal SP shifts were found in the monkeys that had received extensive training with one hand, where high magnitude SP shifts were found from the contralateral hemisphere, whereas SP shifts from the ipsilateral side were near base line level, and did not increase during prolonged intermanual transfer testing. These findings of interhemispheric differences in prefrcntal functions are in agreement with those obtained in experiments with brief electrocortical stimulation (Stamm and Rosen, 1973). Correct delayed response performance was disrupted with stimulation during the intratrial delay period, only when it was applied to the prefrontal cortex contralateral to the (rained hand and identical effects were found during intermanual transfer testing. However, stimulation applied to the other hemisphere did not impair correct performance, regardless of the responding hand. Corresponding findings were obtained with regard to inferotemporal cortical functions in performance of delayed-matching-to-sample tasks (Kovner and Stamm, 1972).

In the present experiment we attempted to obtain further information with regard to the ontogeny of hemispheric differences for the prefrontal SP shifts. During DR training with the procedure of daily alternations between the responding hands there were relatively small differences between the left and right prefrontal SP shifts. Subsequent training of only a few sessions resulted in a marked divergence between the magnitudes of the two prefrontal SP shifts and these were unaffected by intermanual transfer tests. It appears therefore that a major determinant for hemispheric localization of the prefrontal SP shifts is a relatively brief period of training with only one hand. During these sessions mediation of mnemonic processes may become localized in the prefrontal area contralateral to the trained hand while ipsilateral mnemonic functions become suppressed. The temporal relationships between the development of the prefrontal SP shifts during the cue and early delay periods and the activa- tion of unit discharges in the principal sulcus during DR performance (Fuster and Alexander, 1971; Fuster, 1973) provide evidence that these two electrocor tical measures reflect identical neuronal processes. WOW- ever, Fuster (1973) found no interhemispheric differences in the distribu-

48 S T A M M , GADOTTI , AND KOSEN

tions of activated prefrontal units. This finding is not unexpected be- cause his experimental arrangement required the monkey to respond to the two choice objects with different hands, whereas in our experiments only one hand was available for the choice responses.

The present findings are not inconsistent with the contributions of other factors that would predispose the monkey toward hemispheric preferences. Thus, some of our monkeys have exhibited both hand and response preferences, the former mostly for the right hand. Hand preferences have also been found for rhesus monkeys and baboons that were trained 011 other tasks and reports indicate a predominance of left-handed animals (Warren, 1953; Ettlinger and Moffett, 1964; Butler and Francic;, 1973). The differing findings obtained in these and the present study might be attributed to species differences, the methods for assaying hand preference, or the general lack of pronounced handedness in primates. By using the split-brain technique, Gazzaniga (1963, 1971) obtained evidence for right hemispheric dominaiice during discrimiiia tion performance, but he was able to shift the hemispheric preference by differ- ential rewarding of responses that were mediated by each hemisphere. In our experiments we were unable to affect the hemispheric localization by means of extensive training with the ipsilateral hand. However, it might be possible to affect interhemispheric differences in SP shifts by appropriate behavioral techniques. In this way, Rosen, Sandrew and Stamm (1974) have been able to markedly enhance or reduce unilateral prefrontal SP shifts with methods of operant conditioning. It seems therefore, that hemispheric preferences in the monkey are not entirely endogenous, but can be affected by the appropriate experimental methods.

The evidence from the present and other studies indicates that the monkey’s two hemispheres are not equivalent in the mediation of “higher order functions,” such as short-term memory, but that the mediating system becomes functional in only one hemisphere. The experimental evidence, however, does not support the concept that the monkey is en- dowed with a “dominant hemisphere.”

This investigation was supported by National Science Foundation Grant BO 35735- The authors wish to express their appreciation for the technical assistance of XO1.

Mr. Richard Reeder and Mr. Barry Sandrew.

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Accepted for publication November 15, 1974

interhemispheric functional differences in prefrontal cortex of monkeys

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