Frequency specific mechanisms in learning

ELECTROENCEPHALOGRAPHY AND CLINICAL NEUROPHYSIOLOGY

45

FREQUENCY SPECIFIC MECHANISMS IN LEARNING. I. O C C I P I T A L A C T I V I T Y D U R I N G SENSORY P R E C O N D I T I O N I N G 1 H . SCHUCKMAN 2, P H . D . AND W . S. BATTERSBY, P H . D .

Psychophysiology Laboratory, Illinois State Psychiatric Institute, Chicago, Ill. (U.S.A.) (Accepted for publication : May 15, 1964)

If the eye is exposed to a train of light flashes at low frequency, the response of the occipital cortex is characteristically a series of voltage oscillations of the same periodicity as the photic stimulus (Adrian and Matthews 1934). Although long of interest to sensory physiologists, such frequency specific responses have more recently been extensively utilized in the study of the cerebral processes subserving learning (Morrell 1961). If, for example, flickering lights or trains of clicks are paired with shock to elicit a behavioral avoidance response, then frequency specific activity develops early in the conditioning procedure (John and Killam 1959), and diminishes again when motor performance becomes proficient (Livanov and Polyakov 1945). Frequency specific activity from the cerebrum has also been linked with discriminatory behavior in cat (John and Killam 1959), but not in monkey (Chow 196l). Periodic repetitive discharges resembling frequency specific activity have also been noted in non-sensory structures (hippocampus, amygdala) during conditioning, even in the absence of intermittent stimuli (Grasty~n et al. 1959; Lesse 1959). The foregoing findings suggest that frequency specific responses are in general related to the processes underlying conditioning, but their true significance still remains unclear. Perhaps the most ingenious attempt to test the behavioral significance of frequency specific activity from the cerebrum was made in an early study by Chow et al. (1957). Cats were first trained to make an avoidance response to shock, 1 This work was supported, in part, by USPH Service G r a n t B-3691, and, in part, by Mental Health Funds, State of Illinois. 2 USPHS Post-doctoral Fellow.

using a 6/sec intermittent light as CS, and next the occipital response evoked by this same flickering light was conditioned to a preceding tone. When test trials of either tone or intermittent light were then presented without reinforcement, avoidance responses occurred to light but not to tone. The authors concluded that the conditioning of an electrographic response is not a sufficient situation for behavioral learning to occur. It should be noted, however, that unreinforced tone-light paired trials folio wed, rather thanprecededthe avoidance conditioning stage in their testing sequence. Under such a condition, an extinction of behavioral responses is to be expected, and it is quite likely to be more rapid for the previously unreinforced stimulus (tone) than for the reinforced one (light) (Seidel 1959). The present study attempted to test for a correlation between the incidence of photically evoked and behavioral avoidance responses, using a sensory preconditioning paradigm. It was hypothesized that behavioral transfer would occur under these conditions, and hence it would be possible to determine whether frequency specific brain activity was either a necessary or a sufficient condition for elicitation of behavioral responses. METHOD AND MATERIALS

Preparations Under Nembutal anesthesia, 12 pairs of electrodes were aseptically implanted in each of 7 monkeys (Macaea mulatta). Depth and pial electrode locations varied somewhat from animal to animal, but the lateral and medial aspects of the occipital lobe were always sampled on both hemispheres. All electrodes were made from Formvar insulated 5 rail tungsten wire, the tips Electroenceph. clin. Neurophysiol., 1965, 18:45-55

46

H. SCHUCKMAN AND W. S. BATTERSBY

of the pial electrodes being 0.5 mm balls about 1 cm apart, while the depth electrodes were flush cut, polished, and had a tip separation of 1-2 ram. Four stainless steel screws tapped into the anterior and posterior portions of the cranium and joined with 18 gauge wire served as the reference electrode for monopolar recording. All lead-in wires were soldered to a subminiature plug, the wires and plug cemented to the cranium with dental acrylic, and the skin then approximated over the cement base and sutured. At the conclusion of the study, the animals were used in another experiment (in preparation), following which they were sacrificed and all electrode locations verified histologically.

Apparatus During testing, the animals were restrained in monkey chairs and placed in a sound-insulated and shielded chamber (Lehigh Valley 1317C) with an attached blower which provided both air exchange and a masking noise (86 db., SPL re 0.002 dynes/cm2). Tracings were taken on a Grass model IV EEG, modified so as to provide 12 AC and 2 DC recording channels, plus one signal marker pen. (In some experiments, a Tektronix 502 oscilloscope and Grass P4 preamplifiers were used in tandem.) The signal marker pen on the EEG was used to mark the occurrence of behavioral avoidance responses. One of the DC channels was always employed to indicate stimulus presentations, the other for E M G recording from the responding hind limb, or for the integration of electrical signals from any particular lead (Grass UI-1 Unit Integrator). Three different types of stimuli were presented to the animal in the testing cubicle. The auditory stimulus (tone) consisted of a 2 sec train of square waves at 100/sec, 50% duty cycle, which drove a 6 in. loudspeaker at 98 db. SPL (re 0.002 dynes/cm2). This speaker was mounted on the inside wall of the testing cubicle. The light stimulus (flicker) was a 2 see train of square waves at 10/sec, 50% duty cycle, generated by a glow modulator tube (Sylvania R 1131 C) mounted in the door of the cubicle as a Maxwellian view optical system. Reinforcement consisted of shock (of variable strength) to the left hind leg with a 500 msec train of 5 msec square waves at 100/sec. In all cases, flexion of the left hind limb

had to be made in the immediately preceding 2 sec of time in order to successfully avoid shock. Control o f the temporal parameters of all stimuli was achieved with electronic pulse generators (Tektronix 160 series), square wave stimulators (Grass Model IV) and a specially designed automatic programmer (Lehigh Valley 1510) which determined the presence or absence of shock reinforcement depending upon the animal's response. Throughout the experiment, trials were presented at an average aperiodic repetition rate of 1 in 40 sec.

Procedure After 5 days habituation in the testing cubicle, the animals were tested in three separate stages, as follows: Stage 1. Sensorypreconditioning. Four monkeys, which formed the experimental group, always received paired presentations of tone and flicker. Each was given 50 trials per day, with each trial consisting of 2 sec of tone followed immediately by 2 sec of flicker. Three of the experimental animals received this procedure for 10 days, one for 7 days 1. Three other monkeys, the control group, never received tone and flicker in combination. One was given a randomized series of I00 trials per day of either tone or flicker (50 trials each) for 10 days. Another received 50 trials per day of tone only for 10 days. The third was given 50 tone trials (1 day), followed by 50 flicker trials per day for 8 days and, finally, one final day o f 50 tone trials. No reinforcement was used with any of the animals during this stage of the experiment. Stage 2. Avoidance conditioning. Reinforcement was now introduced, and all animals were trained to lift their left hind legs during the 2 sec of flicker presentation in order to avoid subsequent shock. Fifty flicker-shock trials per day were given until each animal reached a criterion of 90% avoidance responses for 5 consecutive days. No tones were presented to any of the animals during this stage of the experiment. Stage 3. Extinction. Shock reinforcement was now withheld, and all animals received 50 trials 1 After receiving 350 sensory preconditioning trials, Monkey No. 3 was used as a pilot subject for future procedures, and hence was eliminated from the study at this point.

Electroenceph. clin. Neurophysiol., 1965, 18:45-55

CONDITIONED OCCIPITAL RESPONSES EXP. F ----lOclsec

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Fig. 1 Sample tracings (monopolar) during preconditioning trials showing 10 c/sec activity during flicker (F), tone (T), and in the pre-tone baseline; illustrative 10 c/sec activity underscored by a grid. Notation as follows: CC, corpus callosum; PUL, pulvinar; AF, anterior frontal; PF, posterior frontal; AT, anterior temporal; PT, posterior temporal; PO, posterior occipital; AO, anterior occipital; L, left; R, right; EMG, electromyograph from responding limb; RESP, leg-lift response; STIM, stimulus (T or F). Amplitude and time calibrations as indicated.

per day of either flicker or tone, in randomized fashion (25 tone and 25 flicker trials per day), for a total of 10 days. The incidence of leg lifts to each of these stimuli was the major behavioral datum of the study. E E G analysis For each animal, the occipital lead which initially showed the greatest amplitude of frequency specific responses to flicker (at 10 c/sec) was selected, and changes from this one lead subsequently followed throughout the remainder of the experiment. Responses elsewhere will not be considered in detail in the present report. For each trial, the occurrence of 10 c/sec occipital activity was determined visually with the aid of a template, during the 2 sec presentation of the stimulus (tone or flicker) and

the immediately preceding 2 sec interval of baseline. The criterion used for the presence or absence of frequency specific activity was 5 consecutive voltage oscillations at 10 c/sec ( ~ 1 0 % ) , with a peak to peak amplitude of 25 #V or greater. The relative incidence of such activity from the sampled leads was then expressed in terms of its per cent occurrence on trials on which the record was readable; i.e., did not show movement artifacts, transient pick-up, or large DC drifts which blocked the amplifier 1. 1 More sensitive measurements might have been attained using other techniques (Morrell et al. 1960) but the equipment necessary for this type of analysis was not available. An on-line Muirhead D-788 A analyzer was used in portions of the study, but was found unsuitable since its reliability was greatly affected by electrical transients associated with the programming equipment. Electroenceph. clin. Neurophysiol., 19&~, 18:45-55

48

H. SCHUCKMAN AND W. S. BATTERSBY a n i m a l , the a m p l i t u d e o f 10 c/sec activity varied considerably, but in no simple relation to electrode locus or stage o f training. T h e r e s p o n s e to flicker c o u l d be well localized to the occipital and

RESULTS

1. General characteristics of frequency specific activity At all stages o f the e x p e r i m e n t , a n d in every

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Fig. 2 Graph at upper left portrays the relative incidence of 10 c/see occipital activity during tone presentation (dotted line), and in pre-tone baseline (solid line) as a function of tone-flicker pairings during sensory preconditioning. EEG samples below the graph illustrate 10 c/see activity during flicker and tone presentations. Top center graph gives incidence of avoidance responses as a function of flickershock trials during avoidance conditioning. EEG samples below graph illustrate 10 c/see occipital activity occurring without (trial 91) and with (trial 339) a concomitant avoidance response elicited by limb shock (S). Graph at upper right indicates incidence of avoidance responses to tone (dotted line) and to flicker (solid line) as a function of their serial presentation during extinction. EEG samples below the graph show 10 c/see occipital activity occurring without (trial 35) and with (trial 22) concomitant avoidance responses. PRE-R, pre-rolandic; POST-R, post-rolandic; R, avoidance response; other symbols as in Fig. 1.

Electroenceph. clin. Neurophysiol., 1965, 18:45-55

CONDITIONED OCCIPITAL RESPONSES

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Fig. 3 The relative incidence of tone-elicited 10 c/sec occipital activity is shown in graph at upper left, and is illustrated in the tracings on the left. The other tracings show that flicker-elicited 10 c/sec occipital activity could occur concomitantly with behavioral responses during avoidance conditioning (center tracings), and during extinction trials (tracings on the right), and could be readily detected on both monopolar and bipolar derivations. Activity from the anterior occipital lead (right hemisphere) was electronically integrated, and is indicated by INT; T, temporal cortex; PA, parietal cortex; other symbols as in Fig. I. temporal cortex, and in depth structures, in the pulvinar and lateral geniculate b o d y (Fig. 1, left). Generally, however, more widespread responses were seen in cortical as well as subcortical regions in the same animal, and even on the same day o f testing. A l t h o u g h not examined in detail, hippocampal and amygdala derivations f r o m all animals never m&nifested high voltage activity at 7 c/sec or 50 c/sec.

The middle tracings o f Fig. 1 show one o f the best examples o f conditioned tone-elicited 10 c/sec activity which was obtained in the study. It occurred at the right anterior occipital lead and at the left occipital pole. The tracings to the right o f Fig. 1 illustrate the occurrence o f 10 c/sec activity in the baseline, during tone and during flicker stimulation. These data, typical o f m a n y others, indicated that an adequate appraisal o f Electroenceph. clin. Neurophysiol., 1965, 18:45-55

50

H. SCHUCKMAN AND W. S. BATTERSBY

stage (top-center graph) show that this monkey completed the criterion run after 600 trials. Sample tracings from this stage of the experiment are shown below the graph. The curves at the upper right of Fig. 2 present the incidence of avoidance responses as a function of test trials during the randomized presentations of tone or flicker in extinction (no shock reinforcement). Avoidance responses to flicker extinguished very gradually, while those to tone fell more precipitously. It is clear, however, that the behavioral avoidance response had transferred, at least for a brief time, to the tonal stimulus. Below the graph, are two sample records from this stage of the experiment. One of these (upper tracings) illustrates that "spontaneous" avoidance responses also occurred (responses not time-correlated with the conditioning stimuli); these were rare (less than 5% of total responses), and were not tabulated in the results. The lower tracings

the problem must compare the relative incidence of 10 c/sec activity during flicker and tone presentations and in the resting baseline as well.

2. Individual data, experimental animals Fig. 2 presents the results of the entire study for one experimental monkey (No. 16). For the sensory preconditioning stage (graph at upper left), there was a gradual increase over trials in the relative incidence of tone-elicited 10 c/sec occipital activity. (This was the minimal increase noted in any experimental animal.) There was little over-all change in the immediately preceding baseline. Below the graph, are two sample records obtained during this stage of the experiment, illustrating a minimal photic response (top tracing) and very similar 10 c/sec activity occurring both to tone and to light (bottom tracing). The results of the avoidance conditioning

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Fig. 4 Curves at left compare the experimental (E) and control (C) groups with respect td~he mean incidence of conditioned avoidance responses as a function of training trials during flicker-shock avoidance conditioning. Lines of open circles represent the median performance per group (average of the number of trials at which various percentile levels of performance were attained), the lines of closed circles on either side the total range of variability; i.e., the slowest and fastest animal in each group. The adjacent bar graphs give the mean number of total trials required to complete the criterion of avoidance conditioning. Curves at right compare the experimental (E, closed circles) and control (C, open circles) with respect to the incidence of avoidance responses made to flicker (above) and to tone (below) as a function of extinction trials. Adjacent bar graphs give the total number of avoidance responses made to flicker (top) and to tone (bottom) during extinction by the experimental (E) and control (C) groups. N is number of animals, P values based on Chi square tests.

Eleetroeneeph. elin. Neurophysiol., 1965, 18:45-55

CONDITIONED OCCIPITAL RESPONSES

illustrate the more frequently obtained timecorrelated response upon which later statistical analyses were made.

3. Individual data, control animals The results obtained from control animals were quite different. One monkey, for example, received only tone trials during the entire sensory preconditioning stage (Fig. 3). The curves in the upper left indicate that no real change in the incidence of l0 c/sec occipital activity occurred either to tone or during the pre-tone baseline at this stage of the experiment. Although it did not increase in incidence as a function of trials, 10 c/sec activity occurred initially in control animals (trial 175) about as frequently as it did in experimental monkeys. The other sample record (trial 159) merely illustrates an expected and often seen phenomenon, desynchronization to tone, best detected as a slope change in an integrated record. The graph at top-center indicates that this animal easily completed the criterion run of avoidance conditioning within 450 trials. Records at this stage of the experiment (trial 320) demonstrate that the photic response could be quite localized with either monopolar or bipolar derivations. The extinction curves (graph at upper right) indicate that a large number of avoidance responses to flicker occurred, but practically none to tone. Avoidance responses to flicker were often, but not always, accompanied by 10 c/sec activity from occipital leads (sample records at the bottom). 4. Group data, sensory preconditioning stage Statistical analyses of the foregoing results were accomplished by calculating the per cent change in incidence of 10 c/sec occipital activity, to tone and in the pre-tone baseline as well, with the initial level (the first 50 trials) being set equal to zero for each animal. During tone presentation, a mean gain of 17% was obtained for the experimental group (N -- 4), --3% for the controls (N = 3). The difference in the mean change between the two groups (20%) was statistically significant as evaluated by a t test (P <0.05). No significant differences were demonstrable between groups or within groups for the changes in incidence of 10 c/sec activity which might have occurred during the pre-tone interval.

51

5. Group data, avoidance conditioning stage The results of the flicker-shock avoidance training are expressed in separate graphs per group in Fig. 4, in terms of per cent conditioned responses as a function of training trials. The mean performance of the two groups was highly similar in that both took about 500 trials to reach criterion level of avoidance conditioning (bar graphs at left). 6. Group data, transfer o.["response during extmction The right portion of Fig. 4 presents the behavioral results obtained during this phase of the experiment, interms of mean per cent conditioned responses as a function of extinction trials (no shock reinforcement). Of the two sets of curves in each group, one is for the relative frequency of avoidance responses elicited by tone, the other for those produced by flicker. Upon tone presentation (bottom curves), the experimental group responded far more often than did the controls, the difference between the two groups being highly significant as evaluated by Chi-square (P <0.001). When flickering light was presented during extinction trials (top curves), however, no statistically significant differences could be demonstrated between the two groups. These findings indicate that avoidance responses established to flicker were transferred to tone, if that tone had previously been presented to the animal in conjunction with flicker (during the sensory preconditioning stage). 7. Correlation of I0 c/sec occipital activity with avoidance responses Further analysis of the data revealed a systematic relationship between incidence of 10 c/sec occipital activity and number of responses made during extinction. In Fig. 5, the mean per cent change in incidence of 10 c/sec activity elicited by tone, is shown as a function of trial blocks during both the sensory preconditioning and extinction stages of the experiment. In the experimental group this incidence rises significantly during sensory preconditioning (as noted earlier), and then decreases during extinction. The control group, in contrast, never exhibited a change in the incidence of 10 c/sec occipital activity greater than one might expect on the basis of chance Electroenceph. clin. Neurophysiol., 1965, 18:45-55

52

H. SCHUCKMAN AND W. S. BATTERSBY IOc/sec OCCIPITAL 20-

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alone. Differences in the slopes of these functions were evaluated between groups by mean of t tests and found to be statistically significant (I" <0.05). To explore further the relationship between incidence of 10 c/sec activity and avoidance response to tone, scatter diagrams were plotted for the extinction phase of the experiment (Fig. 6). On the basis of 25 trial blocks, and combining the data for all animals in each group, per cent avoidance responses to tone were plotted on the ordinates, and incidence of 10 c/sec activity to tone (per cent of trials it was detected) on the abscissae. The best fit lines through these points, computed by the least squares method, have slopes of 0.74 and 0.18 for the experimental and control groups respectively. The linear correlation coefficients (r) were found to be statistically significant for the experimental but not for the control group. If individual trials are considered, a Chi-square analysis of the extinction data showed that, for the experimental group only, the incidence of tone-elicited 10 c/sec activity from occipital leads was proportionately greater when avoidance responses were made than when they were not made (P <0.01). On the other hand, only 40% of the total number of avoidance responses made to tone were accompanied by 10 c/sec activity; i.e., the greater number of

avoidance responses occurred without concomitant 10 c/sec activity being detected in occipital leads. DISCUSSION

The results of the present study show that the incidence of 10 c/sec occipital activity elicited by a tonal stimulus increases with the number of paired presentations of this tone with 10/sec flickering light. This finding appears to have behavioral significance inasmuch as avoidance responses subsequently established to the light are transferred to the tone (a sensory preconditioning effect). Under the latter circumstances, there is a significant correlation between frequency of avoidance responses and incidence of tone-elicited 10 c/sec activity. Only 40°/'0 of the total avoidance responses, however, occurred concomitantly with 10 c/sec activity from the occipital lobe. The hippocampal 7/sec activity or the amygdala 40/sec activity reported for cats during conditioning procedures (Grastyin et al. 1959; Lesse 1959) were never observed. This discrepancy might be due to the fact that these structures are relatively large in the monkey, and only limited samples were obtained in this study, or alternatively, that there are species differences with regard to limbic activity during learning. The present study might have succeeded in Electroenceph. clin. Neurophysiol., 1965, 18:45-55

CONDITIONED OCCIPITAL RESPONSES

53

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to tone

record

Fig. 6 Scatter diagrams for the experimental and control groups showing the relationship between incidence of avoidance responses and incidence of 10 c/sec occipital activity which occurred during the 25-trial blocks of tone stimuli presented during extinction. Pearson correlation coefficient indicated by r, significance (P) based on its standard error. obtaining behavioral transfer f r o m flicker to tone in monkeys, where the earlier study o f C h o w et al. (1957) in cats did not, because o f differences in species studied, or task complexity (shuttle-box vs. hind-limb flexion), but it seems more likely that the major variable was procedural in nature. In this study, unreinforced tone and flicker trials were not interpolated between avoidance conditioning and the test (extinction) stages o f the experiment. Hence, there was no opportunity for extinction o f the rather fragile sensory preconditioning effect to occur. A l t h o u g h t h e behavioral findings differ in the two studies, the overall conclusion to be drawn f r o m our electrographic data is not materially different from thatexpressed earlier by C h o w et al. (1957). We also noted that frequency specific occipital activity at 10 c/sec occurred without concomitant behavioral avoidance responses during the extinction trials. W h e n avoidance responses did occur (the novel finding in this study), the p r o p o r t i o n a t e incidence o f frequency specific activity was higher, but the majority o f avoidance responses (60%) were still not accompanied by any detectable 10 c/sec activity. We would agree, therefore, with the conclusion drawn by C h o w et al. (1957), namely, that conditioned frequency specific activity is not

a sufficient condition for obtaining behavioral learning. We would also add that such activity is not a necessary condition, even t h o u g h the two variables are positively correlatedk One way o f explaining the present findings is to postulate that frequency specific activity is only one o f m a n y cerebral processes subserving learning. W h a t the other processes may be is, at present, largely a matter o f conjecture. N u m e r o u s physiological theories have been advanced to account for the facts o f learning. Thus, Pavlov (1928) spoke of "irradiation" between sensory receiving areas o f the brain during conditioning. Others (Hebb 1949) have speculated about the formation o f intracerebral connections between 1 This conclusion must be limited by the conditions of the experiment; such as, the finite number of neural sites sampled, the state of light adaptation of the eye, the method of frequency analysis used, etc. The basic issue raised is what interpretation to place upon the negative evidence in view of obvious limitations of instrumentation. Such factors alone may or may not be sufficient to explain why a perfect correlation between frequency specific responses and behavioral avoidance responses was not obtained. On the other hand, it is equally plausible that more than one factor is involved in the physiological mechanism for learning, and that not all of the data can be subsumed under any one process (such as frequency specific responses). Electroenceph. clin. Neurophysiol., 1965, 18:45 55

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H. SCHUCKMAN AND W. S. BATTERSBY

stimulus and response. Still others (Klfiver 1962) have questioned this interpretation since the most characteristic feature of a learned response is the ease with which it can transfer to other stimuli; i.e., there is almost always a wide range of stimuli which are equivalent in that they evoke the same response. Birch and Bitterman (1951) have attempted to account for transfer and equivalence in terms of a hypothetical process of sensory integration ("When two different centers are contiguously activated, a functional relation is established between them such that the subsequent innervation of one will arouse the other." p. 358). The studies of Morrell and Jasper (1956), Chow et al. (1957), Yoshii and Hockaday (1958) and Yoshii et al. (1957, 1960), have all demonstrated that after sufficient pairings, auditory stimuli will elicit occipital responses similar to those initially elicited only by intermittert light. The present study has, in addition, shown that such responses may have behavioral significance. These findings give strong support to the concept of sensory integration as at least one of the cerebral processes subserving learning. The sensory integration concept of learning is also supported by one recent study where a behavioral response conditioned to an environmental stimulus was readily transferred to electrical stimulation of the brain, if both stimuli possessed the same frequency characteristics (John 1963). According to some (Nieder and Neff 1961), behavioral transfer of this kind is quite specific for cerebral locations, but others (Doty and Rutledge 1959) have reported more diffuse effects. These latter studies have the distinct advantage of being able to reveal possible cause and effect relationships, a finding which cannot be obtained by merely correlating electrographic activity with behavior. Future studies, in which the investigator directly manipulates the electrical activity of the brain, appear to offer the best hope of shedding more light on the role of frequency specific responses in learning, and more generally, on the significance of sensory integration. SUMMARY

Four monkeys with implanted electrodes were given paired presentations of tone and flicker (10/'sec) without reinforcement. Three control

animals received the same number of total trials, but never tone and flicker in paired combination. The incidence of 10 c.'sec activity in occipital regions during tone presentations increased markedly for the experimental group, but not for the controls. All animals were next trained to lift their hind legs during flicker presentations in order to avoid subsequent shock. Flicker-shock trials were given until each animal reached a criterion of 90°//o avoidance responses for five consecutive days. The experimental and control groups did not differ significantly in the learning of this avoidance response. All animals were then given tone or flicker trials in a randomized fashion without shock reinforcement (extinction trials). Although experimental and control monkeys did not differ in their responsiveness to flicker, the experimental group made significantly more avoidance responses to tone than did controls. In addition, there was a low, but statistically significant, correlation between occurrence of avoidance responses and incidence of 10 c/sec occipital activity evoked by tone in the experimental group. These findings indicate that the probability of obtaining an avoidance response is related to frequency specific activity in the cerebrum, but that the latter is neither a necessary nor a sufficient condition for obtaining the behavioral effect. REFERENCES ADRIAN, E. D. and MATTHEWS, B. H. C. Berger rhythm: potential changes from occipital lobes in man. Brain, 1934, 57: 355-385. BIRCH, H. G. and BITTERMAN, M. E. Sensory integration and cognitive theory. Psychol. Rev., 1951, 58: 355-361. CHow, K. L. Changes of brain electropotentials during visual discrimination learning in monkey. J. Neurophysiol., 1961, 24: 377--390. CHow, K. L., DEMENT, W. C. and JOHN, E. R. Conditioned electrocorticographic potentials and behavioral avoidance response in cat. J. Neurophysiol., 1957, 20: 482-493. DOTV, R. W. and RUTLEDGE, L. T. "Generalization" between cortically and peripherally applied stimuli eliciting conditioned reflexes. J. Neurophysiol., 1959, 22: 428-435. GRASTY~.N, E., LISS./~K, K., MADARASZ, 1. and DONOHOFFER, H. Hippocampal electrical activity during the development of conditioned reflexes. Electroenceph. clin. Neurophysiol., 1959, 11: 409-430. HEBB, D. O. The organization of behavior. Wiley, New York, 1949, 335 p. JOHN, E. R. Neural mechanisms of decision making. In

Electroenceph. clin. Neurophysiol., 1965, 18:45 55

CONDITIONED OCCIPITAL RESPONSES W. S. FIELDS and W. ABBOTT (Eds.), Information storage and neural control. C. C. Thomas, Springfield, 111., 1963: 243-277. JOHN, E. R. and KILLAM, K. F. Electrophysiological correlates of avoidance conditioning in the cat. J. Pharmacol. exp. Ther., 1959, 125: 252-274. KLf3VER, H. Psychological specificity - - does it exist'? In F. O. SCHMITT (Ed.), Macromolecular specificity and biological memory. M.I.T. Press, Boston, 1962: 94-98. LESSE, H. Amygdaloid electrical activity during a conditioned response. In L. VAN BOGAERT and J. RADERMEUKER(Eds.), First htternational congress of neurological sciences. Pergamon, New York, 1959, 3: 177-180. LIVANOV, M. N. and POLYAkOV, K. L. Electrical processes in the cerebral cortex of rabbits during the formation of the defensive conditioned reflex to rhythmic stimulation. Bull. Acad. Sci. USSR, 1945, 3: 286-307, as reported in V. S. Rusiyov and M. Y. RABINOVICH, Electroencephalographic researches in the laboratories and clinics of the Soviet Union. Electroenceph. clin. Neurophysiol., 1958, Suppl. 8:16. MORRELL, F. Electrophysiological contributions to the neural basis of learning. Physiol. Rev., 1961, 41: 443-494. MORRELL, F., BARLOW, J. and BRAZIER, M. A. B. Analysis of conditioned repetitive response by means of the

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average response computer. In J. WORTIS (Ed.), Recent advances in biological psychiatry. Grune and Stratton, New York, 1960: 123-137. MORRELL, F. and JASPER, H. H. Electrographic studies of the formation of temporary connections in the brain. Electroenceph. clin. Neurophysiol., 1956, 8: 201-215. NIEDER, P. C. and NEFF, W. D. Auditory information from subcortical electrical stimulation in cats. Science, 1961, 133: 1010-1011. PAVLOV, I. P. Lectures on conditioned reflexes. Liveright, New York, 1928, 414 p. SEIDEL, R. J. A review of sensory preconditioning. Psychol. Bull., 1959, 56 : 58-73. Yosnll, N. and HOCKADAV, W. J. Conditioning of frequency-characteristic repetitive electroencephalographic response with intermittent photic stimulation. Electroenceph. olin. Neurophysiol., 1958, 10: 487-502. YOSHII, N., MATSUMOTO,J., OGURA, H., SI-IIMOKt~CHI,M., YAMAGUCHI, Y. and YAMASAKI, H. Conditioned reflex and electroencephalography. Electroeneeph. clin. Neurophysiol., 1960, Suppl. 13: 199-208. YOSHH, N., PRUVOT, P. and GASTAUT, H. Electrographic activity of the mesencephalic reticular formation during conditioning in the cat. Electroenceph. clin. Neurophysiol., 1957, 9: 595-608.

Reference: SCHUCKMAN,H. and BATTERSBY,W. S. Frequency specific mechanisms in learning. I. Occipital activity during sensory preconditioning. Electroenceph. elin. Neurophysiol., 1965, 18: 45-55.