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Postreinforcement changes of steady potentials in premotor cortex of monkeys
Physiology and Behavior, Vol. 9, pp. 769-772. Brain Research Publications Inc., 1972. Printed in U.S.A.
Postreinforcement Changes of Steady Potentials in Premotor Cortex of Monkeys GERALD T. STEINMETZ AND CHARLES S. REBERT 2
Stanford Research Institute, Menlo Park, California 94025
(Received 14 June 1972)
STEINMETZ, G. T. AND C. S. REBERT. Postreinforcement changes o f steady potentials in premotor cortex o f monkeys. PHYSIOL. BEHAV. 9(5) 769-772, 1972.-S1ow potential changes were recorded from premotor cortex and several subcortical regions during a reaction time foreperiod experiment. When reinforced trials were alternated in blocks of 5 trials with unreinforced trials, the cortical DC potential increased in negativity to about -300 tzV over the course of reinforced trials and declined to baseline during nonreinforced trials. Change in the cortical potential occurred after ingestion of liquid reinforcement was completed. Since positive potentials have been reported to appear in posterior cortex during reinforcement, the frontal potential was thought to be a frontally unique phenomenon and was referred to as postingestion frontal negativity (PIFN). No similar changes occurred in subcortical sites. Slow potential change
Frontal cortex
Positive reinforcement
Postingestion frontal negativity
the observations of others [2, 3, 11, 19] that cortical SP polarity shifts negatively as animals are increasingly awake or aroused, and shifts positively during sleep. There are two observations common to studies of PRS; synchronization is never obtained in frontal areas of the cortex, nor are concomitant changes noted in brain stem or diencephalic areas when monitored. The present paper describes a negative SP change in the frontal cortex (premotor area) of the monkey's brain which occurs following ingestion of liquid reinforcement (in contrast to RCPV and PRS which occur during the act of ingestion); it appears to be a true postreinforcement phenomenon and is referred to as Postingestion Frontal Negativity (PIFN).
SEVERAL investigators have reported EEG changes associated with the reception of reinforcing stimuli. Following appetitive reinforcement the slow wave ECoG in certain brain areas typically shifts from desynchronized to highly synchronized patterns of activity in the 6 - 1 0 Hz range. Clemente et al. [4] termed this phenomenon postreinforcement synchronization (PRS) which they suggested was a conditioned response to the sight, smell or taste of a food reward. Grandstaff [5], after surgically controlling visual inputs, noted PRS in the striate cortex of cats which seemed to be associated only with the motor activity of highly repetitive reflex lapping. However, Buchwald et al. [1] reported a "flavor" or palatability effect, in that synchronization was absent when cats lapped water or ate canned pet food, but appeared when lapping milk or eating highly preferred solid food (liver). Sterman and Wyrwicka [17] and Marczynski et al. [9, 10] also noted that the occurrence of PRS is closely related to desirability of a food reinforcement and that PRS is essentially similar to sleep ECoG synchronization. Marczynski et al. [8] further observed that auditory and somatosensory stimuli presented during PRS evoke potentials of greater amplitude is a function of the state of " t o n u s " of the reticular activating system (RAS), and that PRS represents a depression or relaxation of the RAS. Later, Marczynski et al. [10] described a positive steady potential (SP) shift (reward contingent positive variation-RCPV) that accompanied both PRS and sleep onset synchronization. That result was in agreement with
METHOD
Animals The animals were three mature female stumptailed macaque monkeys. Each had been tested in a reaction time (RT) foreperiod experiment [12] for approximately ten months at the time of these observations and were well trained and adapted to the apparatus. The monkeys had been implanted in 7 brain regions with nonpolarizing Ag-AgC1 electrodes modified from those described by Rowland [13]. Six of the electrodes were located subcortically in a variety of structures, including an inactive (see [12]) reference electrode in the cingulate gyrus or white matter. The 7th electrode was placed on the dura over the premotor cortex.
i Supported by a grant (NS08248) to C. Rebert from the National Institute of Neurological Diseases and Stroke, USPHS. Send reprint requests to: Charles S. Rebert, Department of Psychobiology and Physiology, Bldg. 18, Stanford Research Institute, Menlo Park, California 94025. 2
769
770
Apparatus and Procedures During training and testing in the RT study, animals were placed in a restraining chair equipped with bar-press lever and drinking tube and the chair was housed in a shielded chamber. The animals were first trained to bar-press to obtain liquid reinforcement during the presence of a light (imperative stimulus-IS). The reinforcer, hereafter called "juice", was Tang a commercially available dehydrated orange juice substitute. During the 10-sec period of IS presentation, each bar-press led to delivery of 1 cc of juice. From 1 0 - 2 0 presses were emitted during each 10-sec period. Given 15 reinforcement trials per day, about 225 cc of juice was consumed. Throughout the entire regimen the animals were maintained on a 23-hr liquid deprivation schedule for 6 days with ad lib water on the 7th. High and low frequency tones of 2-sec duration were eventually introduced. One of the tones was designated as a positive warning stimulus (WS) and was followed by the IS, which signaled the availability of liquid reinforcement. The other tone (DS--discriminative stimulus) was presented alone. The paired and unpaired tones were usually presented pseudorandomly, 15 of each per testing session with a 30-60-sec intertrial interval. Potentials from each electrode location relative to the reference were recorded on polygraph and magnetic tape for later analysis. The sequence of testing conditions included an habituation period during which neither tone was paired with reinforcement; a training period during which one tone was paired; and finally a reversal period during which the previously unpaired tone was paired with reinforcement. In the reversal phase of the RT study an attempt was made to affect the foreperiod potentials by manipulating the animal's expectancy of the paired or unpaired trials. The previously randomly presented paired and unpaired trials were presented in blocks of 5 reinforced trials followed by five nonreinforced trials throughout the 30-trial session. Under these conditions, the experimenter noted a cyclic variation of the DC potential of the premotor cortex of each animal and attempted to assess its nature and origin by a systematic manipulation of experimental parameters. The amplitude and latency of the potential shift was measured for a single bar-press response, a series of bar-presses in a single reinforcement period, and for a series of reinforcement periods. The effect of reward quality on the shift was studied by varying juice concentration (100% normal = about 25% Tang; 50% and 10% of normal). Measurements of pH for the 3 concentrations were 3.4, 3.3, and 3.12 respectively. Motivational effects were studied under two levels of liquid deprivation; Low, 3 - 4 hr deprivation and High, 2 4 - 2 6 hr deprivation. Also, under the low deprivation condition the effects of the normal juice reinforcer vs H 2 0 reinforcement were compared. Finally, two control conditions were tested. In one, animals were given juice by the experimenter without warning tones, light stimuli or bar-pressing. In the other, the WS was presented without the opportunity for bar-pressing or for juice. In each of the above conditions, the number of bar-presses and the latency of the first press were recorded.
STEINMETZ AND REBERT RESULTS AND DISCUSSION Cyclic variation of the EEG baseline associated with periods of reinforcement (paired trials) and nonreinforcement (unpaired trials) is shown in Fig. 1. Such long lasting baseline deviations were restricted to the cerebral cortex. A single reinforced trial consisting of about 15 discrete bar-presses during the 10 sec reinforcement period was followed by a negative steady potential shift (PIFN) in the premotor cortex. The shift began at the end of bar-pressing and drinking, reached a peak average amplitude of 50 t~V in about 20 sec, and subsided to baseline in another 30 sec (Fig. 2). If three or more paired trials were presented at appropriate intervals (before individual shifts subsided), the shifts would sum to an average peak of about - 3 0 0 #V, requiring 6 0 - 9 0 sec to return to baseline after the last bar-press for juice (Figs. 1 and 2). A single bar-press for juice (approximately 1 cc) did not noticeably affect the steady potential. At the highest (normal) concentration of reinforcing juice, the cumulated PIFN averaged - 3 2 0 ~V. At the medium concentration there was a reduction of average amplitude to - 2 7 2 #V. At the low concentration there was another decrease to - 2 0 4 ~V. Analysis of variance indicated that there was significant variation among the means (F = 14.32, dr= 2, 47, p < 0.01). A Newman-Keuls test also indicated that each mean differed from all others at p < 0.05. Latency and bar-press measures were not systematically affected by the three conditions of concentration. Motivational effects on the shift could not be demonstrated. There was no difference in the potential changes in the two levels of deprivation. However, it is important to note that there was also no difference in the rate of bar-pressing or the amount of juice consumed in the two conditions. However, when the animals were provided only H20 reinforcement in the low deprivation condition, the shift amplitude was sharply reduced to about - 6 5 ~V, and the rate of animal's bar-pressing decreased to nearly zero. When the animals were provided juice by the experimenter without tones or bar-pressing, the PIFN was produced with full amplitude. This finding precludes an explanation of the shift in terms of general motor activity, and indicates that the response was related to ingestion of the juice rather than to other aspects of the experimental situation. However, when the WS was presented alone without the opportunity for reinforcement (no IS), a small shift of low amplitude and short duration also occurred, representing a conditioned response which habituated rapidly. The PIFN was consistent in size and latency for all three animals and was not accompanied by similar shifts in other brain regions sampled. The present results differ from those usually obtained in relation to reinforcing stimuli, in that the shift, while maintained during drinking, did not seem to increase until ingestion ceased. This was true regardless of the duration of the reinforcement period, or the rate of bar-pressing or swallowing. The absence of postingestion SPs in the other brain regions sampled in this study indicates that the cortical response does not reflect changes in whole brain metabolism [20], but it does suggest that the response might reflect a noneuronal event related specifically to extradural recording. That epidural SP shifts can be associated with more than purely neural events is well
POST INGESTION FRONTAL NEGATIVITY
771
PREMOTOR
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POSTERIOR HYPOTHALAMUS
FIG. 1. Examples from one animal of DC baseline oscillations in the premotor cortex produced by alternating reinforcement (paired=P) and nonreinforcement (unpaired=U) trials. Reinforcement trials included a 10-sec period when bar-pressing was continuouslyrewarded and approximately 15 presses were emitted. Also shown are two subcortical areas indicating cortical localization of postingestion shifts. All recordings were DC.
>
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1 Reinforcement Trial
O O 5 Reinforcement Trials ~-~-~, Juice Only, S Trials (~'---O
Tone Only. S Trials
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.-* .-- ~ _
. . . .
m :E o
120
uJ 0 10
30
50
70
90
110
130
150
TIME IN SECONDS FROM BEGINNING OF FIRST TRIAL
FIG. 2. Postingestion frontal negativity at 30-sec intervals after initiation of the first trial under experimental and control conditions. Each plotted point is based on 6 scores from each of the 3 animals. established. The cortical dipole is made up of voltages across a layer of neural elements containing vascular substrate and glia, and is affected by pH, oxygen/carbon dioxide balances and perhaps glial potentials [3, 11 ]. An example of presumably nonneural SP effects following eating and drinking was reported by Kawamura e t al. [6] who described long term shifts occurring in rabbits 1 0 - 2 0 min after ingestion and lasting approximately one hr. They interpreted those shifts as blood-brain barrier potential alterations due to changes in the osmotic pressure of the blood plasma. However, a nonneural source of the PIFN is suggested by several considerations: ( 1 ) t h e latency of the shift was closely related to cessation of reward consumption; (2) the shift was of relatively short duration
compared to those observed by Kawamura e t aL [6] ; and (3) the amplitude of PIFN was influenced by gustatory quality that could not be attributed to the amount, or pH, of the juice ingested. However, intracortical recording is definitely needed to clarify the source of PIFN. The present results seem to most nearly correspond to those reported by Rowland and associates [14, 15, 16] who found large cumulative SP shifts in frontal cortex and other areas following ingestion of a milk-fishmeal homogenate. Those authors found cortical SP shifts related to food ingestion to be sensitive to characteristics of oral inputs (concentration and desirability), and to be blocked by loss of oral sensation (cocainization of the mouth). They also observed a sensitivity to drive state (deprivation) and an amplitude covariance of many cortical sites, suggesting a diffuse activating effect varying directly with arousing conditions. Barring any nonneural causes of the present results, likely explanations of the shift might include direct effects of oral sensory input or secondary effects mediated by a general activating mechanism. It is significant that SP changes of different duration and amplitude were observed simultaneously in this study, i.e., potentials occurring in the RT foreperiod (contingent negative variation--CNV [ 18 ] ) were superimposed on longer lasting, larger amplitude baseline variations (PIFN). Such conditions could provide a means of testing the hypothesis suggested by Knott and Irwin [7] that different CNV amplitudes of high and low anxious human subjects performing under stress, result from DC base line variations in the former group being near saturation. However, no differences were found between CNV averages based on the second paired trial of each block of five, and those based upon the fifth trials when the baseline shift was greater. The failure to find an interaction between CNVs and the baseline level was probably due to the fact that the magnitude of the baseline shift was much less than the saturation level. There were instances in two animals, however, of 2+ mV negative baseline shifts, during which
772
STEINMETZ AND REBERT
no f u r t h e r negativity was p r o d u c e d b y t h e a d m i n i s t r a t i o n o f r e i n f o r c e m e n t . CNVs were n o t , u n f o r t u n a t e l y , r e c o r d e d d u r i n g t h o s e runs. T h e s e p r e l i m i n a r y results suggest t h a t
cortical n e g a t i v i t y can n o r m a l l y r e a c h a m a x i m u m o f 2 3 m V , a n d t h e y lend some c r e d e n c e to t h e K n o t t - I r w i n hypothesis.
REFERENCES
1. Buchwald, q. A., F. E. Horvath, E. J. Wyers and C. Wakefield. E l e c t r o e n c e p h a l o g r a m rhythms correlated with milk reinforcement in cats. Nature 201 : 8 3 0 - 8 3 1 , 1964. 2. Caspers, H. Changes of cortical D. C. potentials in the sleep-wakefulness cycle. In: The Nature of Sleep edited by G. E. W. Wolstenholme and M. O'Connor. London: Churchill, 1961, pp. 237-259. 3. Caspers, H. Relations of steady potential shifts in the cortex to the wakefulness-sleep spectrum. In: Brain Function, edited by M. A. B. Brazier. Berkeley and Los Angeles: University of California Press, 1963, pp. 177-213. 4. Clemente, C. D., M. B. Sterman and W. Wyrwicka. Post-reinforcement EEG synchronization during alimentary behavior. Electroenceph. clin. Neurophysiol. 16: 355-365, 1964. 5. Grandstaff, N. W. Frequency analysis of EEG during milk drinking. Electroenceph. clin. Neurophysiol. 27: 5 7 - 6 5 , 1969. 6. Kawamura, H., D. I. Whitmoyer and C. H. Sawyer. DC potential changes recorded between brain and skull in the rabbit after eating and drinking. Electroenceph. clin_ Neurophysiol. 22: 337-347, 1967. 7. Knott, J. R. and D. A. Irwin. Anxiety, stress and the c o n t i n g e n t n e g a t i v e v a r i a t i o n . Electroenceph. clin. Neurophysiol. 24: 2 8 1 - 2 9 4 , 1968. 8. Marczynski, T. J. and J. T. Hackett. Post-reinforcement electrocorticat synchronization and facilitation of cortical somatosensory evoked potentials during instrumentally conditioned appetitive behavior in the cat. Electroenceph. clin. Neurophysiol. 26: 4 1 - 4 9 , 1969. 9. Marczynski, T. J., A. J. Rosen and J. T. Hackett. Postreinforcement electrocortical synchronization and facilitation of cortical auditory evoked potentials in appetitive instrumental conditioning. Electroenceph. din. Neurophysiol. 24: 2 2 7 - 2 4 1 , 1968. 10. Marczynski, T. J., J. L. York and J. T. Hackett. Steady potential correlates of positive reinforcement: reward contingent positive variation. Science 1 6 3 : 3 0 1 - 3 0 4 , 1969.
11. O'Leary, J. L. and S. Goldring. D-C potentials of the brain. Physiol. Rev. 44: 9 1 - 1 2 5 , 1964. 12. Rebert, C. S. Cortical and subcortical slow potentials in the monkey's brain during a preparatory interval. Electroenceph. din. Neurophysiol. 33: 389-402, 1972. 13. Rowland, V. Simple non-polarizable electrode for chronic implantation. Electroenceph. clin. Neurophysiol 13: 2 9 0 - 291, 1961. 14. Rowland, V. Cortical steady potential (direct current potential) in reinforcement and learning. In: Progress in Physiological Psychology, Vol. 2, edited by E. Stellar and J. M. Sprague. New York: Academic Press, 1968, pp. 1-277. 15. Rowland, V., H. Bradley, P. School, and D. Deutschman. Cortical steady potential shifts in conditioning. Conditional Reflex 2: 3 - 2 2 , 1967. 16. Rowland, V. and M. Goldstone. Appetitively conditioned and drive related bioelectric baseline shift in cat cortex. Electroenceph. clin. Neurophysiol. 15: 4 7 4 - 4 8 5 , 1963. 17. Sterman, M. B. and W. Wyrwicka. EEG correlates of sleep: evidence for separate forebrain substrates. Brain Res. 6: 143-163, 1967. 18. Walter, W. G., R. Cooper, V. J. Aldridge, W. C. McCallum and A. L. Winter. Contingent Negative Variation: an electric sign of sensorimotor association and expectancy in the human brain. Nature 203: 380-384, 1964. 19. Wurtz, R. H. Steady potential shifts in the rat during desynchronized sleep. Electroenceph. clin. Neurophysiol. 19: 521-523, 1965. 20. Wurtz, R. H. Steady potential fields during sleep and wakefulness in the cat. ExpINeurol. 15: 274-292, 1966.
Postreinforcement Changes of Steady Potentials in Premotor Cortex of Monkeys GERALD T. STEINMETZ AND CHARLES S. REBERT 2
Stanford Research Institute, Menlo Park, California 94025
(Received 14 June 1972)
STEINMETZ, G. T. AND C. S. REBERT. Postreinforcement changes o f steady potentials in premotor cortex o f monkeys. PHYSIOL. BEHAV. 9(5) 769-772, 1972.-S1ow potential changes were recorded from premotor cortex and several subcortical regions during a reaction time foreperiod experiment. When reinforced trials were alternated in blocks of 5 trials with unreinforced trials, the cortical DC potential increased in negativity to about -300 tzV over the course of reinforced trials and declined to baseline during nonreinforced trials. Change in the cortical potential occurred after ingestion of liquid reinforcement was completed. Since positive potentials have been reported to appear in posterior cortex during reinforcement, the frontal potential was thought to be a frontally unique phenomenon and was referred to as postingestion frontal negativity (PIFN). No similar changes occurred in subcortical sites. Slow potential change
Frontal cortex
Positive reinforcement
Postingestion frontal negativity
the observations of others [2, 3, 11, 19] that cortical SP polarity shifts negatively as animals are increasingly awake or aroused, and shifts positively during sleep. There are two observations common to studies of PRS; synchronization is never obtained in frontal areas of the cortex, nor are concomitant changes noted in brain stem or diencephalic areas when monitored. The present paper describes a negative SP change in the frontal cortex (premotor area) of the monkey's brain which occurs following ingestion of liquid reinforcement (in contrast to RCPV and PRS which occur during the act of ingestion); it appears to be a true postreinforcement phenomenon and is referred to as Postingestion Frontal Negativity (PIFN).
SEVERAL investigators have reported EEG changes associated with the reception of reinforcing stimuli. Following appetitive reinforcement the slow wave ECoG in certain brain areas typically shifts from desynchronized to highly synchronized patterns of activity in the 6 - 1 0 Hz range. Clemente et al. [4] termed this phenomenon postreinforcement synchronization (PRS) which they suggested was a conditioned response to the sight, smell or taste of a food reward. Grandstaff [5], after surgically controlling visual inputs, noted PRS in the striate cortex of cats which seemed to be associated only with the motor activity of highly repetitive reflex lapping. However, Buchwald et al. [1] reported a "flavor" or palatability effect, in that synchronization was absent when cats lapped water or ate canned pet food, but appeared when lapping milk or eating highly preferred solid food (liver). Sterman and Wyrwicka [17] and Marczynski et al. [9, 10] also noted that the occurrence of PRS is closely related to desirability of a food reinforcement and that PRS is essentially similar to sleep ECoG synchronization. Marczynski et al. [8] further observed that auditory and somatosensory stimuli presented during PRS evoke potentials of greater amplitude is a function of the state of " t o n u s " of the reticular activating system (RAS), and that PRS represents a depression or relaxation of the RAS. Later, Marczynski et al. [10] described a positive steady potential (SP) shift (reward contingent positive variation-RCPV) that accompanied both PRS and sleep onset synchronization. That result was in agreement with
METHOD
Animals The animals were three mature female stumptailed macaque monkeys. Each had been tested in a reaction time (RT) foreperiod experiment [12] for approximately ten months at the time of these observations and were well trained and adapted to the apparatus. The monkeys had been implanted in 7 brain regions with nonpolarizing Ag-AgC1 electrodes modified from those described by Rowland [13]. Six of the electrodes were located subcortically in a variety of structures, including an inactive (see [12]) reference electrode in the cingulate gyrus or white matter. The 7th electrode was placed on the dura over the premotor cortex.
i Supported by a grant (NS08248) to C. Rebert from the National Institute of Neurological Diseases and Stroke, USPHS. Send reprint requests to: Charles S. Rebert, Department of Psychobiology and Physiology, Bldg. 18, Stanford Research Institute, Menlo Park, California 94025. 2
769
770
Apparatus and Procedures During training and testing in the RT study, animals were placed in a restraining chair equipped with bar-press lever and drinking tube and the chair was housed in a shielded chamber. The animals were first trained to bar-press to obtain liquid reinforcement during the presence of a light (imperative stimulus-IS). The reinforcer, hereafter called "juice", was Tang a commercially available dehydrated orange juice substitute. During the 10-sec period of IS presentation, each bar-press led to delivery of 1 cc of juice. From 1 0 - 2 0 presses were emitted during each 10-sec period. Given 15 reinforcement trials per day, about 225 cc of juice was consumed. Throughout the entire regimen the animals were maintained on a 23-hr liquid deprivation schedule for 6 days with ad lib water on the 7th. High and low frequency tones of 2-sec duration were eventually introduced. One of the tones was designated as a positive warning stimulus (WS) and was followed by the IS, which signaled the availability of liquid reinforcement. The other tone (DS--discriminative stimulus) was presented alone. The paired and unpaired tones were usually presented pseudorandomly, 15 of each per testing session with a 30-60-sec intertrial interval. Potentials from each electrode location relative to the reference were recorded on polygraph and magnetic tape for later analysis. The sequence of testing conditions included an habituation period during which neither tone was paired with reinforcement; a training period during which one tone was paired; and finally a reversal period during which the previously unpaired tone was paired with reinforcement. In the reversal phase of the RT study an attempt was made to affect the foreperiod potentials by manipulating the animal's expectancy of the paired or unpaired trials. The previously randomly presented paired and unpaired trials were presented in blocks of 5 reinforced trials followed by five nonreinforced trials throughout the 30-trial session. Under these conditions, the experimenter noted a cyclic variation of the DC potential of the premotor cortex of each animal and attempted to assess its nature and origin by a systematic manipulation of experimental parameters. The amplitude and latency of the potential shift was measured for a single bar-press response, a series of bar-presses in a single reinforcement period, and for a series of reinforcement periods. The effect of reward quality on the shift was studied by varying juice concentration (100% normal = about 25% Tang; 50% and 10% of normal). Measurements of pH for the 3 concentrations were 3.4, 3.3, and 3.12 respectively. Motivational effects were studied under two levels of liquid deprivation; Low, 3 - 4 hr deprivation and High, 2 4 - 2 6 hr deprivation. Also, under the low deprivation condition the effects of the normal juice reinforcer vs H 2 0 reinforcement were compared. Finally, two control conditions were tested. In one, animals were given juice by the experimenter without warning tones, light stimuli or bar-pressing. In the other, the WS was presented without the opportunity for bar-pressing or for juice. In each of the above conditions, the number of bar-presses and the latency of the first press were recorded.
STEINMETZ AND REBERT RESULTS AND DISCUSSION Cyclic variation of the EEG baseline associated with periods of reinforcement (paired trials) and nonreinforcement (unpaired trials) is shown in Fig. 1. Such long lasting baseline deviations were restricted to the cerebral cortex. A single reinforced trial consisting of about 15 discrete bar-presses during the 10 sec reinforcement period was followed by a negative steady potential shift (PIFN) in the premotor cortex. The shift began at the end of bar-pressing and drinking, reached a peak average amplitude of 50 t~V in about 20 sec, and subsided to baseline in another 30 sec (Fig. 2). If three or more paired trials were presented at appropriate intervals (before individual shifts subsided), the shifts would sum to an average peak of about - 3 0 0 #V, requiring 6 0 - 9 0 sec to return to baseline after the last bar-press for juice (Figs. 1 and 2). A single bar-press for juice (approximately 1 cc) did not noticeably affect the steady potential. At the highest (normal) concentration of reinforcing juice, the cumulated PIFN averaged - 3 2 0 ~V. At the medium concentration there was a reduction of average amplitude to - 2 7 2 #V. At the low concentration there was another decrease to - 2 0 4 ~V. Analysis of variance indicated that there was significant variation among the means (F = 14.32, dr= 2, 47, p < 0.01). A Newman-Keuls test also indicated that each mean differed from all others at p < 0.05. Latency and bar-press measures were not systematically affected by the three conditions of concentration. Motivational effects on the shift could not be demonstrated. There was no difference in the potential changes in the two levels of deprivation. However, it is important to note that there was also no difference in the rate of bar-pressing or the amount of juice consumed in the two conditions. However, when the animals were provided only H20 reinforcement in the low deprivation condition, the shift amplitude was sharply reduced to about - 6 5 ~V, and the rate of animal's bar-pressing decreased to nearly zero. When the animals were provided juice by the experimenter without tones or bar-pressing, the PIFN was produced with full amplitude. This finding precludes an explanation of the shift in terms of general motor activity, and indicates that the response was related to ingestion of the juice rather than to other aspects of the experimental situation. However, when the WS was presented alone without the opportunity for reinforcement (no IS), a small shift of low amplitude and short duration also occurred, representing a conditioned response which habituated rapidly. The PIFN was consistent in size and latency for all three animals and was not accompanied by similar shifts in other brain regions sampled. The present results differ from those usually obtained in relation to reinforcing stimuli, in that the shift, while maintained during drinking, did not seem to increase until ingestion ceased. This was true regardless of the duration of the reinforcement period, or the rate of bar-pressing or swallowing. The absence of postingestion SPs in the other brain regions sampled in this study indicates that the cortical response does not reflect changes in whole brain metabolism [20], but it does suggest that the response might reflect a noneuronal event related specifically to extradural recording. That epidural SP shifts can be associated with more than purely neural events is well
POST INGESTION FRONTAL NEGATIVITY
771
PREMOTOR
T -
I
.~,L.aa,.,J
1
I
I
I I ~ P
~"~'
I
|
I
" '
.
I
CORTEX I
,.
, . L , ~
t
-
"
I I t O
I
I
I MIDLINE
200 pV
I
I
I I P
I
I
I
I
I I t U
I
I
I
I
THALAMUS
1 30
sec ,~-IT"
~ T~I -
-r
.... 4
"
~
POSTERIOR HYPOTHALAMUS
FIG. 1. Examples from one animal of DC baseline oscillations in the premotor cortex produced by alternating reinforcement (paired=P) and nonreinforcement (unpaired=U) trials. Reinforcement trials included a 10-sec period when bar-pressing was continuouslyrewarded and approximately 15 presses were emitted. Also shown are two subcortical areas indicating cortical localization of postingestion shifts. All recordings were DC.
>
360
I
H
1 Reinforcement Trial
O O 5 Reinforcement Trials ~-~-~, Juice Only, S Trials (~'---O
Tone Only. S Trials
~-.~[~"---.._.~~_ /U"-.~
.-* .-- ~ _
. . . .
m :E o
120
uJ 0 10
30
50
70
90
110
130
150
TIME IN SECONDS FROM BEGINNING OF FIRST TRIAL
FIG. 2. Postingestion frontal negativity at 30-sec intervals after initiation of the first trial under experimental and control conditions. Each plotted point is based on 6 scores from each of the 3 animals. established. The cortical dipole is made up of voltages across a layer of neural elements containing vascular substrate and glia, and is affected by pH, oxygen/carbon dioxide balances and perhaps glial potentials [3, 11 ]. An example of presumably nonneural SP effects following eating and drinking was reported by Kawamura e t al. [6] who described long term shifts occurring in rabbits 1 0 - 2 0 min after ingestion and lasting approximately one hr. They interpreted those shifts as blood-brain barrier potential alterations due to changes in the osmotic pressure of the blood plasma. However, a nonneural source of the PIFN is suggested by several considerations: ( 1 ) t h e latency of the shift was closely related to cessation of reward consumption; (2) the shift was of relatively short duration
compared to those observed by Kawamura e t aL [6] ; and (3) the amplitude of PIFN was influenced by gustatory quality that could not be attributed to the amount, or pH, of the juice ingested. However, intracortical recording is definitely needed to clarify the source of PIFN. The present results seem to most nearly correspond to those reported by Rowland and associates [14, 15, 16] who found large cumulative SP shifts in frontal cortex and other areas following ingestion of a milk-fishmeal homogenate. Those authors found cortical SP shifts related to food ingestion to be sensitive to characteristics of oral inputs (concentration and desirability), and to be blocked by loss of oral sensation (cocainization of the mouth). They also observed a sensitivity to drive state (deprivation) and an amplitude covariance of many cortical sites, suggesting a diffuse activating effect varying directly with arousing conditions. Barring any nonneural causes of the present results, likely explanations of the shift might include direct effects of oral sensory input or secondary effects mediated by a general activating mechanism. It is significant that SP changes of different duration and amplitude were observed simultaneously in this study, i.e., potentials occurring in the RT foreperiod (contingent negative variation--CNV [ 18 ] ) were superimposed on longer lasting, larger amplitude baseline variations (PIFN). Such conditions could provide a means of testing the hypothesis suggested by Knott and Irwin [7] that different CNV amplitudes of high and low anxious human subjects performing under stress, result from DC base line variations in the former group being near saturation. However, no differences were found between CNV averages based on the second paired trial of each block of five, and those based upon the fifth trials when the baseline shift was greater. The failure to find an interaction between CNVs and the baseline level was probably due to the fact that the magnitude of the baseline shift was much less than the saturation level. There were instances in two animals, however, of 2+ mV negative baseline shifts, during which
772
STEINMETZ AND REBERT
no f u r t h e r negativity was p r o d u c e d b y t h e a d m i n i s t r a t i o n o f r e i n f o r c e m e n t . CNVs were n o t , u n f o r t u n a t e l y , r e c o r d e d d u r i n g t h o s e runs. T h e s e p r e l i m i n a r y results suggest t h a t
cortical n e g a t i v i t y can n o r m a l l y r e a c h a m a x i m u m o f 2 3 m V , a n d t h e y lend some c r e d e n c e to t h e K n o t t - I r w i n hypothesis.
REFERENCES
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