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Operant conditioning of the pretrigeminal cat
222
SHORT COMMUNICATIONS
Operant conditioning of the pretrigeminal cat The pretngemmal decerebrate cat has the interesting property that the forebram, although completely disconnected from somatic stlmuh, appears to be chronically awake 1-5,7-a,1~-16 Such an ~solated forebram has two sensory inputs, olfactory and v~sual, and motor outputs consisting of eye movements (predominantly m the vertical direction), accommodation, and pupdlary dllahon Orienting, tracking, habituation, classical con&tiomng, and s~mple con&tloned discriminations have been observed in the topography of these responses If the pretngemmal cat's forebram is m fact awake, it should be possible to modify its behavior by operant conditioning techniques Below we report the results of such an attempt Cats were anesthetized with halothane, placed m a stereotaxlc instrument, and a cramotomy performed on the m~dhne just posterior to the tentormm The anterior portion of the cerebellum was aspirated, exposing the floor of the fourth ventricle Decerebration was accomphshed by three passes of a specmlly shaped spatula t3 along a plane tilted 35 ° from vertical and entering the brain stem at the posterior border of the inferior colhculus Examination at autopsy in&cared that these transections were complete except for small portions of the motor tracts next to the base of the skull Because all ascendmg systems were interrupted, the forebraln was functionally Isolated On recovery from anesthesm the ammals showed all of the characteristics of the classical pretrigemmal preparation, including vertical movements of the eyes m response to moving visual stlmuh Needle electrodes were inserted m the skin above and below one of the eyes, attached to the input of a Tektronix 122 preamplifier with a bandpass of 0 2-50 c/sec, and the eye movement record thus obtained &splayed on one channel of a polygraph To provide reinforcement, a bipolar concentric electrode (tip separation 1 mm) was lowered into the region of the lateral hypothalamus (LHT) (approximate coordinates A 10 5, L 3 5, V - - 3 5), a placement which rehably produces rewarding effects m cats when stimulated electrically0,11Az The conditioning apparatus consisted of a Schmltt trigger which fired when the electro-oculogram (EOG) exceeded its threshold, thereby arbitrarily defining a response m the same manner as pressing a bar to close an electrical contact When reinforcement was available, each response ~mmedmtely triggered a tram of isolated pulses (0 5 sec tram duration, 0 2 msec pulse width, 200 pulses/see) to the lateral hypothalamus Stimulus intensities sufficient to reinforce behavior (about 1 m A peak current with L H T placements) cause m o t o r effects m Intact ammals 0,11,12, and m the decerebrate a m m a l produce a short latency eye movement In order to prevent the system from being self-exciting, a lockout circuit provided a 5 sec delay after each response before another response would be recorded or reinforcement presented Durmg all experiments the preparation was m a hghted room with its eyes uncovered, but was carefully screened from any moving object whtch might induce eye movements Three cats were used for th~s demonstration S~mllar behavior patterns were obtained from all of the preparations, although only records from cat No 3 are presented here Beginning several hours after recovery, the E O G was observed for an Bram Research, 38 (1972) 222-225
223
SHORT COMMUNICATIONS
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F~g 1 Sample iecords of operant condmonlng in a pretrlgermnal cat In each record the upper line is the electro-oculogram representing vertical eye movements, the middle hne is the cumulative response, and the bottom hne, when present, indicates the availability of reinforcement a, Spontaneous actwlty several hours after recovery from anesthesia but before condmoning b, Imtlal condmonmg c, Extraction d, Recondmonmg and extinction e, Test for sensitization Stimulation ptesented once every 10 sec See text for details With the exception of d and e, these records are not continuous with each other, although they are all from the same cat
extended period and the polarity and threshold of the Schmltt trigger adjusted to provide a low rate of 'free operant' behavior A sample of the basehne actlwty ~s shown m F~g 1, record a The upper hne m each record is the EOG, the middle hne the integral of responses or 'cumulative response' record, and the bottom hne, when present, m&cates the avallablhty of reinforcement The response is here defined as a large upward deflection in the EOG Record b shows the initial con&tlonmg of this cat with a peak stimulus current of 1 1 mA A high rate of responding appeared almost lmmedmtely after the first reinforcement, and was maintained m bursts Record c shows the termination of reinforcement, which was followed by rapid extraction Record d, approximately 1 h later, is a short session of reconditioning again followed by extinction With the exception of one early response, the recon&tlonang initially exhibits a more sustained and higher rate of response than does the beginning of the first condmonmg period (record b) The possibility remains that the data presented here result from sensltmatlon or other nonspec~fic effects, where, for example, the electrical stimulation might produce Brain Research, 38 (1972) 222-225
224
SHORT COMMUNICATION ~,
excitement and a consequent high rate of eye movements To exclude such a possibIlity, the reinforcing stimulus was delivered at a fixed rate of once every 10 sec, about the same as the average rate of reward during the previous conditioning The response recorder was locked out for the first 5 sec following each stimulation It can be seen (Fig 1, record e) that the reinforcing stimulation produced a downward deflection of the EOG, in this case the opposite direction to that defined as a response These deflections are present in the conditioning records (Fig 1, records b, c, d) immediately following each reinforcement, but are difficult to see because they are necessarily superimposed upon a large upward deflection During the sensitization test no responses were emitted, nor was there an eye movement pattern following the termination of stimulation which might be confused with extraction Some large upward swings at the onset of the test period would have triggered the response recorder if they had not fallen within the 5 sec lockout period It may therefore be concluded that the responses shown in records b, c, and d are specific to the reinforcement contingency The foregoing demonstration is consistent with the notion that the pretrigemlnal cat's forebrain is awake By using the technique of operant conditioning such animals could probably be trained to perform complex tasks, such as pattern discrimination, since their capacity for simple discriminations has already been demonstrated using classical conditiomng le The pretrigeminal cat should be an ideal subject for the study of cellular mechanisms of learning, and is much easier to prepare than the deafferented head described by Mountcastle 10 This research was supported by grants from the Alfred P Sloan Foundation and the Society of Sigma Xi Robert Shlaer held a post-doctoral fellowship provided from U S Pubhc Health Service Traming Grant No 5T01GM2037 Department of Theoretical Btology, Umverstty of Chicago, Chtcago, Ill 60637, Northwestern Umverstty Medwal School, Chicago, Ill 60611 ( U S A )
ROBERT SHLAER*
MELINDA L MYERS
1 AFFANNI, J , MARCHIAFAVA)P L, AND ZERN1CKI) B ) Oltentation reactions m the mJdpontme pretrigemmal cat, Arch ital BIol, 100 (1962) 297-304 2 AFFANNI,J , MARCHIAFAVA,P L, AND ZERNICKI) B, Conditioning in the midpontme pretngemlnal cat, Arch ltal Btol, 100 (1962) 305-3t0 3 AFFANNI,J , MARCHIAFAVA,P L, ANt~ZERNICKI,B, Higher nervous activity in cats with midpontme pretrlgemmal transectlons, Science, 137 (1962) 126-127 4 BATINI, C , MAGNI, F , PALESTINI, M ) ROSSI) G F , AND ZANCHETII, A , Neural mechanisms underlying the enduring EEG and b©havloral activation m the midpontme pretrtgemmal cat, Arch ttal Blol , 97 (1959) 13-25 5 BATINI,C , MORUZZI,M, PALESTINI,M, ROSSI,G F , ANDZANCHETT1,A, Effects oflcomplete pontme transectlons on the sleep-wakefulness rhythm" the mtdpontme pretrtgermnal preparation, Arch ztal Btol , 97 (1959) 1-12 * Present address Neurosurgtcal Research Laboratory, CMcago Wesley Memorial Hospital, Chicago, Ill 60611, U S A Brain Research, 38 (1972) 222-225
SHORT COMMUNICATIONS
225
6 DorY, R W., Condmoned rvflexes formed and evoked by brain stimulation In D E SHEER(Ed), Eleetrwal S.mulatwn of the Brain, Umv of Texas Press, Houston, 1961, pp 397-412 7 DREHER, B , MARCHIAFAVA,P L , AND ZERNICKI,B . Studies on the visual fixation reflex II The neural mechanism of the fixaUon reflex m normal and pretngvmmal cats, Acta Biol enp ( Warszawa), 25 (1965) 207-217 8 ELUL,R . AND MARCHIAFAVA,P L , Accommodation of the eye as related to behawour m the cat, Arch ztal Bzol , 102 (1964) 616-644 9 KING, F A . ANDMARCHIAFAVA.P L , Ocular movements in the mtdpontlne pretngemmal preparation, Arch ital Bwl, 101 (1963) 149-160 10 MOUNTCASTLE,V E , Some functional properties of the somatic afferent system In W A ROSENaLIT8(Ed), Sensory Commumeatwn, M I T Press. Cambridge. Mass, 1961, pp 403-436 11 NIELSON,H C , DOTY, R W . AND RUTLEDGE,L T , Motlvatmnal and perceptual aspects of subcortmal stimulation m cats, Amer J Phystol. 194 (1958) 427-432 12 WILKINSON,H A . AND PEELE, T L , Int~actamal self-sUmulat~on m cats, 1 comp Neurol, 121 (1963) 425-440 13 ZERNICKI, B , Pretngemmal cat. Brain Research, 9 (1968) 1-14 14 ZERNICKI, B , AND DREHER, B , Studies on the wsual fixation reflex I General properties of the onentaUon fixation reflex m pretngermnal and intact cats, Acta Bwl exp (Warszawa), 25 (1965) 18%205 15 ZERNICKI, B , DREHER, B , KRZYWOSINSKI, L , AND SYCHOWA, B , Some properties of the acute mldpontlne pretngemmal eat. Acta Bwl exp (Warszawa). 27 (1967) 123-139 16 ZERNICKI, B , AND OSETOWSKA, E , Conditioning and d~fferentmt~on m the chrome m~dpontme pretngemmal cat, Acta Bwl e:~p (Warszawa), 23 (1963) 25-32 (Accepted December 17th, 1971)
Brain Research, 38 (1972) 222-225
SHORT COMMUNICATIONS
Operant conditioning of the pretrigeminal cat The pretngemmal decerebrate cat has the interesting property that the forebram, although completely disconnected from somatic stlmuh, appears to be chronically awake 1-5,7-a,1~-16 Such an ~solated forebram has two sensory inputs, olfactory and v~sual, and motor outputs consisting of eye movements (predominantly m the vertical direction), accommodation, and pupdlary dllahon Orienting, tracking, habituation, classical con&tiomng, and s~mple con&tloned discriminations have been observed in the topography of these responses If the pretngemmal cat's forebram is m fact awake, it should be possible to modify its behavior by operant conditioning techniques Below we report the results of such an attempt Cats were anesthetized with halothane, placed m a stereotaxlc instrument, and a cramotomy performed on the m~dhne just posterior to the tentormm The anterior portion of the cerebellum was aspirated, exposing the floor of the fourth ventricle Decerebration was accomphshed by three passes of a specmlly shaped spatula t3 along a plane tilted 35 ° from vertical and entering the brain stem at the posterior border of the inferior colhculus Examination at autopsy in&cared that these transections were complete except for small portions of the motor tracts next to the base of the skull Because all ascendmg systems were interrupted, the forebraln was functionally Isolated On recovery from anesthesm the ammals showed all of the characteristics of the classical pretrigemmal preparation, including vertical movements of the eyes m response to moving visual stlmuh Needle electrodes were inserted m the skin above and below one of the eyes, attached to the input of a Tektronix 122 preamplifier with a bandpass of 0 2-50 c/sec, and the eye movement record thus obtained &splayed on one channel of a polygraph To provide reinforcement, a bipolar concentric electrode (tip separation 1 mm) was lowered into the region of the lateral hypothalamus (LHT) (approximate coordinates A 10 5, L 3 5, V - - 3 5), a placement which rehably produces rewarding effects m cats when stimulated electrically0,11Az The conditioning apparatus consisted of a Schmltt trigger which fired when the electro-oculogram (EOG) exceeded its threshold, thereby arbitrarily defining a response m the same manner as pressing a bar to close an electrical contact When reinforcement was available, each response ~mmedmtely triggered a tram of isolated pulses (0 5 sec tram duration, 0 2 msec pulse width, 200 pulses/see) to the lateral hypothalamus Stimulus intensities sufficient to reinforce behavior (about 1 m A peak current with L H T placements) cause m o t o r effects m Intact ammals 0,11,12, and m the decerebrate a m m a l produce a short latency eye movement In order to prevent the system from being self-exciting, a lockout circuit provided a 5 sec delay after each response before another response would be recorded or reinforcement presented Durmg all experiments the preparation was m a hghted room with its eyes uncovered, but was carefully screened from any moving object whtch might induce eye movements Three cats were used for th~s demonstration S~mllar behavior patterns were obtained from all of the preparations, although only records from cat No 3 are presented here Beginning several hours after recovery, the E O G was observed for an Bram Research, 38 (1972) 222-225
223
SHORT COMMUNICATIONS
&
l
~.J, ,d.j
..,,.a.L..~t
,,.A , .' au'~i~tl'~'i'i~'i
~v~ ,,,i.lu~. ~,M~,ht,{L.l a 'lllli'i I ....
:
5MIN.
I,[dlJl~l
:
F~g 1 Sample iecords of operant condmonlng in a pretrlgermnal cat In each record the upper line is the electro-oculogram representing vertical eye movements, the middle hne is the cumulative response, and the bottom hne, when present, indicates the availability of reinforcement a, Spontaneous actwlty several hours after recovery from anesthesia but before condmoning b, Imtlal condmonmg c, Extraction d, Recondmonmg and extinction e, Test for sensitization Stimulation ptesented once every 10 sec See text for details With the exception of d and e, these records are not continuous with each other, although they are all from the same cat
extended period and the polarity and threshold of the Schmltt trigger adjusted to provide a low rate of 'free operant' behavior A sample of the basehne actlwty ~s shown m F~g 1, record a The upper hne m each record is the EOG, the middle hne the integral of responses or 'cumulative response' record, and the bottom hne, when present, m&cates the avallablhty of reinforcement The response is here defined as a large upward deflection in the EOG Record b shows the initial con&tlonmg of this cat with a peak stimulus current of 1 1 mA A high rate of responding appeared almost lmmedmtely after the first reinforcement, and was maintained m bursts Record c shows the termination of reinforcement, which was followed by rapid extraction Record d, approximately 1 h later, is a short session of reconditioning again followed by extinction With the exception of one early response, the recon&tlonang initially exhibits a more sustained and higher rate of response than does the beginning of the first condmonmg period (record b) The possibility remains that the data presented here result from sensltmatlon or other nonspec~fic effects, where, for example, the electrical stimulation might produce Brain Research, 38 (1972) 222-225
224
SHORT COMMUNICATION ~,
excitement and a consequent high rate of eye movements To exclude such a possibIlity, the reinforcing stimulus was delivered at a fixed rate of once every 10 sec, about the same as the average rate of reward during the previous conditioning The response recorder was locked out for the first 5 sec following each stimulation It can be seen (Fig 1, record e) that the reinforcing stimulation produced a downward deflection of the EOG, in this case the opposite direction to that defined as a response These deflections are present in the conditioning records (Fig 1, records b, c, d) immediately following each reinforcement, but are difficult to see because they are necessarily superimposed upon a large upward deflection During the sensitization test no responses were emitted, nor was there an eye movement pattern following the termination of stimulation which might be confused with extraction Some large upward swings at the onset of the test period would have triggered the response recorder if they had not fallen within the 5 sec lockout period It may therefore be concluded that the responses shown in records b, c, and d are specific to the reinforcement contingency The foregoing demonstration is consistent with the notion that the pretrigemlnal cat's forebrain is awake By using the technique of operant conditioning such animals could probably be trained to perform complex tasks, such as pattern discrimination, since their capacity for simple discriminations has already been demonstrated using classical conditiomng le The pretrigeminal cat should be an ideal subject for the study of cellular mechanisms of learning, and is much easier to prepare than the deafferented head described by Mountcastle 10 This research was supported by grants from the Alfred P Sloan Foundation and the Society of Sigma Xi Robert Shlaer held a post-doctoral fellowship provided from U S Pubhc Health Service Traming Grant No 5T01GM2037 Department of Theoretical Btology, Umverstty of Chicago, Chtcago, Ill 60637, Northwestern Umverstty Medwal School, Chicago, Ill 60611 ( U S A )
ROBERT SHLAER*
MELINDA L MYERS
1 AFFANNI, J , MARCHIAFAVA)P L, AND ZERN1CKI) B ) Oltentation reactions m the mJdpontme pretrigemmal cat, Arch ital BIol, 100 (1962) 297-304 2 AFFANNI,J , MARCHIAFAVA,P L, AND ZERNICKI) B, Conditioning in the midpontme pretngemlnal cat, Arch ltal Btol, 100 (1962) 305-3t0 3 AFFANNI,J , MARCHIAFAVA,P L, ANt~ZERNICKI,B, Higher nervous activity in cats with midpontme pretrlgemmal transectlons, Science, 137 (1962) 126-127 4 BATINI, C , MAGNI, F , PALESTINI, M ) ROSSI) G F , AND ZANCHETII, A , Neural mechanisms underlying the enduring EEG and b©havloral activation m the midpontme pretrtgemmal cat, Arch ttal Blol , 97 (1959) 13-25 5 BATINI,C , MORUZZI,M, PALESTINI,M, ROSSI,G F , ANDZANCHETT1,A, Effects oflcomplete pontme transectlons on the sleep-wakefulness rhythm" the mtdpontme pretrtgermnal preparation, Arch ztal Btol , 97 (1959) 1-12 * Present address Neurosurgtcal Research Laboratory, CMcago Wesley Memorial Hospital, Chicago, Ill 60611, U S A Brain Research, 38 (1972) 222-225
SHORT COMMUNICATIONS
225
6 DorY, R W., Condmoned rvflexes formed and evoked by brain stimulation In D E SHEER(Ed), Eleetrwal S.mulatwn of the Brain, Umv of Texas Press, Houston, 1961, pp 397-412 7 DREHER, B , MARCHIAFAVA,P L , AND ZERNICKI,B . Studies on the visual fixation reflex II The neural mechanism of the fixaUon reflex m normal and pretngvmmal cats, Acta Biol enp ( Warszawa), 25 (1965) 207-217 8 ELUL,R . AND MARCHIAFAVA,P L , Accommodation of the eye as related to behawour m the cat, Arch ztal Bzol , 102 (1964) 616-644 9 KING, F A . ANDMARCHIAFAVA.P L , Ocular movements in the mtdpontlne pretngemmal preparation, Arch ital Bwl, 101 (1963) 149-160 10 MOUNTCASTLE,V E , Some functional properties of the somatic afferent system In W A ROSENaLIT8(Ed), Sensory Commumeatwn, M I T Press. Cambridge. Mass, 1961, pp 403-436 11 NIELSON,H C , DOTY, R W . AND RUTLEDGE,L T , Motlvatmnal and perceptual aspects of subcortmal stimulation m cats, Amer J Phystol. 194 (1958) 427-432 12 WILKINSON,H A . AND PEELE, T L , Int~actamal self-sUmulat~on m cats, 1 comp Neurol, 121 (1963) 425-440 13 ZERNICKI, B , Pretngemmal cat. Brain Research, 9 (1968) 1-14 14 ZERNICKI, B , AND DREHER, B , Studies on the wsual fixation reflex I General properties of the onentaUon fixation reflex m pretngermnal and intact cats, Acta Bwl exp (Warszawa), 25 (1965) 18%205 15 ZERNICKI, B , DREHER, B , KRZYWOSINSKI, L , AND SYCHOWA, B , Some properties of the acute mldpontlne pretngemmal eat. Acta Bwl exp (Warszawa). 27 (1967) 123-139 16 ZERNICKI, B , AND OSETOWSKA, E , Conditioning and d~fferentmt~on m the chrome m~dpontme pretngemmal cat, Acta Bwl e:~p (Warszawa), 23 (1963) 25-32 (Accepted December 17th, 1971)
Brain Research, 38 (1972) 222-225