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Operant control of precentral neurons: comparison of pyramidal and non-pyramidal tract neurons
188
Brain Research, 174 (1979) 188-190 © Elsevier/North-Holland Biomedical Press
Operant control of precentral neurons: comparison of pyramidal and nonpyramidal tract neurons
ALLEN R. WYLER, CAROL A. ROBBINS and STEPHAN C. LANGE Department of Neurological Surgery, University of Washington, Seattle, Wash. 98195 (U.S.A.)
(Accepted May 31st, 1979)
Recent work from this laboratory has focused on generating a standardized single neuron operant conditioning paradigm capable of quantifying monkeys' control over precentral neurons 3-6. To minimize variables previous studies have dealt primarily with precentral neurons which could be physiologically identified as pyramidal tract neurons (PTNs). In an earlier report it was stated that PTNs were, as a group, more accurately controlled than non-PTNs a. However, since the previous studies selectively conditioned monkeys to control PTNs, it is ambiguous whether the differences in operant control between the groups of PTNs and non-PTNs were real or simply an artifact of differential training. Furthermore, since that report, it has been shown that several factors appear to correlate with the degree to which individual PTNs are controlled. For example, it was shown that PTNs responsive to discrete peripheral movements of the contralateral upper extremity are more accurately controlled than neurons which are not responsive to stimulation of peripheral mechanoreceptors 4. In addition, PTNs responsive to manipulation of distal arm joints were better controlled than those responsive to proximal arm joints 4. Consequently, it is the intention of the present study to compare more critically monkeys' control between PTNs and non-PTNs. Data are from 4 male Macaca mulatta monkeys who had been implanted with chronic extracellular recording chambers and pyramidal tract (at the level of the medullary pyramids) stimulating electrodes as described previously 3. The operant task is termed 'differential reinforcement of tonic patterns' (DRTP). Functionally this task reinforces the monkey (with applesauce) for the production of consecutive interspike intervals (ISis) within a requisite target range. (In all these experiments, the target range was 30-60 msec). D R T P periods and alternate time out periods are 5 min in duration and under computer (PDP8/e) control, and have been extensively described 8. Each behavioral period is divided into 15 sec epochs. At the end of each epoch, the computer determines the total APs fired and the total time (in msec) ISis were on and off target. Hence, for each epoch, the total time off target is considered error. At the end of each 5 min behavioral period (DRTP and time out) the mean and S. D. of time on target and error are computed. The first D R T P (DRTP1) period is baseline for each experiment and subsequent D R T P periods are compared to it. The best D R T P
189 TABLE I Means (and S.D.) of error scores and firing rates (APs/15 sec) for the 5 min behavioral periods listed. Data are from 49 PTNs and 35 non-PTNs from precentral cortex. Preconditioned
DRTP1
DRTPb
8876 ± 3759 9313 4- 3861
5916 4- 4473 6878 4- 4625
3542 4- 2473 5878 d: 4332
211 4- 121 204 ± 118
269 :L 111 255 i 122
Error
PTNs non-PTNs
Firing rate (APs/15 sec)
PTNs non-PTNs
163 ± 137 172 4- 128
( D R T P b ) p e r i o d is t h a t p e r i o d subsequent to D R T P 1 with the highest m e a n time on t a r g e t a n d the m e a n e r r o r for this p e r i o d represents the absolute accuracy with which the m o n k e y c o n t r o l l e d t h a t p a r t i c u l a r neuron. D a t a were included in this analysis only i f the following criteria were fulfilled: (a) the n e u r o n s ' A P s were unequivocally isolated, uninjured, a n d n e g a t i v e - p o s i t i v e ; (b) the n e u r o n r e m a i n e d isolated t h r o u g h at least 6 D R T P p e r i o d s (since for m o s t n e u r o n s a n a s y m p t o t e in c o n t r o l is reached by then); a n d (c) the n e u r o n ' s response to p e r i p h e r a l m a n i p u l a t i o n was a d e q u a t e l y characterized. These m a n i p u l a t i o n s included simple tactile (hair) stimulation, pressure to discrete muscle groups, a n d passive m o v e m e n t o f all u p p e r a n d m o s t lower extremity joints. A l t h o u g h we have studied over two h u n d r e d precentral neurons, only 35 nonP T N s a n d 49 P T N s fulfilled the a b o v e criteria. Table I lists the m e a n (and S.D.) e r r o r scores for the 5 min p r e c o n d i t i o n i n g , D R T P 1 a n d D R T P b p e r i o d s for the two g r o u p s o f neurons. There were no significant differences ( S t u d e n t ' s t-test) between g r o u p s for p r e c o n d i t i o n i n g a n d D R T P 1 p e r i o d s ; however, there was a significant difference (t 4.03, P < 0.001) between P T N s a n d n o n - P T N s for D R T P b . It is interesting t h a t n o significant differences in firing rate were a p p a r e n t between P T N s a n d n o n - P T N s for these 3 periods. These d a t a w o u l d a p p e a r to confirm the earlier r e p o r t t h a t P T N s , as a group, are m o r e accurately c o n t r o l l e d t h a n precentral n o n - P T N s . H o w e v e r , the original finding TABLE II Mean (and S.D.) for DRTPb error scores for 49 PTNs and 35 non-PTNs. Discrete refers to neurons activated by one passive peripheral movement whereas diffuse refers to activations by more than one movement although the manipulations might involve opposing movements of the same joint or responses to more than one form of stimulation (i.e. joint manipulation and tactile stimulation). PINs
Discrete Diffuse No field
2318 4- 784 (n = 18) 4764 4- 2329 (n = 28) 5183 4- 3904 (n = 3)
Non-PTNs
2739 ± 832 (n = 7) 4171 -4- 2003 (n = 21) 6276 ± 3816 (n = 7)
190 was determined by comparing the percentage of neurons from each group which were statistically controlled and the present data compares DRTPb error scores. If, on the other hand, the data from non-PTNs is subdivided into neurons with discrete, diffuse and no peripheral field (as previously defined 4) then no significant differences are found between PTNs and non-PTNs (Table II). It is apparent that the samples of PTNs and non-PTNs are not similar since 7/35 (20 ~ ) of non-PTNs and 18/49 (37 ~ ) of PTNs responded to discrete passive peripheral manipulation. Since there is evidence 6 that for this operant task, the accuracy with which precentral PTNs are controlled is related to the neuron's response to peripheral mechanoreceptors, it would appear that the decreased control of non-PTNs, as a group, is an artifact of our sample. For individual non-PTNs with discrete responses to peripheral manipulation the monkeys demonstrated operant control equal to PTNs. Lemon and Ported,2 sufficiently mapped 257 neurons in precentral ' a r m area' and found that 15.7 ~ of PTNs and 18.6 ~ of non-PTNs had no detectable peripheral field. In our sample, 6 ~ of PTNs and 20 ~ of non-PTNs had no mappable field. We cannot explain why our P T N sample differs so greatly from Lemon and Porter's. Btit because of our sample's bias the estimation of operant control of PTNs is most likely inflated. As factors which influence single unit control become identified, it appears that there is no significant difference between the operant control of PTNs and non-PTNs. This research was supported by N I H Research Grant NS 04053, NS 14590 and Teacher Investigator Award (A.R.W.) NS 00195 awarded by the National Institute of Neurological and Communicative Disorders and Stroke, P H S / D H E W . A.R.W. is an affiliate of the Child Development and Mental Retardation Center, University o f Washington.
1 Lemon, R. N. and Porter, R., Afferent input to movement-related precentral neurons in conscious monkeys, Proc. roy. Soc. B, 194 (1975) 313-339. 2 Lemon, R. N., Hanby, J. A. and Porter, R., Relationship between the activity of precentral neurones during active and passive movements in conscious monkeys, Proc. roy. Soc. B, 194 (1975) 341-373. 3 Wyler, A. R. and Finch, C. A., Operant conditioning of tonic firing patterns from precentral neurons in monkey neocortex, Brain Research, 146 (1978) 51-69. 4 Wyler, A. R. and Burchiel, K. J., Factors influencing accuracy of operant control of pyramidal tract neurons in monkey, Brain Research, 152 (1978) 418-421. 5 Wyler, A. R. and Burchiel, K. J., Operant control ofpyramidal tract neurons: the role of spinal dorsal columns, Brain Research, 157 (1978) 257-265. 6 Wyler, A. R., Burchiel, K. J. and Robbins, C. A., Operant control of precentral neurons: evidence against open loop control, Brain Research, (1979) in press.
Brain Research, 174 (1979) 188-190 © Elsevier/North-Holland Biomedical Press
Operant control of precentral neurons: comparison of pyramidal and nonpyramidal tract neurons
ALLEN R. WYLER, CAROL A. ROBBINS and STEPHAN C. LANGE Department of Neurological Surgery, University of Washington, Seattle, Wash. 98195 (U.S.A.)
(Accepted May 31st, 1979)
Recent work from this laboratory has focused on generating a standardized single neuron operant conditioning paradigm capable of quantifying monkeys' control over precentral neurons 3-6. To minimize variables previous studies have dealt primarily with precentral neurons which could be physiologically identified as pyramidal tract neurons (PTNs). In an earlier report it was stated that PTNs were, as a group, more accurately controlled than non-PTNs a. However, since the previous studies selectively conditioned monkeys to control PTNs, it is ambiguous whether the differences in operant control between the groups of PTNs and non-PTNs were real or simply an artifact of differential training. Furthermore, since that report, it has been shown that several factors appear to correlate with the degree to which individual PTNs are controlled. For example, it was shown that PTNs responsive to discrete peripheral movements of the contralateral upper extremity are more accurately controlled than neurons which are not responsive to stimulation of peripheral mechanoreceptors 4. In addition, PTNs responsive to manipulation of distal arm joints were better controlled than those responsive to proximal arm joints 4. Consequently, it is the intention of the present study to compare more critically monkeys' control between PTNs and non-PTNs. Data are from 4 male Macaca mulatta monkeys who had been implanted with chronic extracellular recording chambers and pyramidal tract (at the level of the medullary pyramids) stimulating electrodes as described previously 3. The operant task is termed 'differential reinforcement of tonic patterns' (DRTP). Functionally this task reinforces the monkey (with applesauce) for the production of consecutive interspike intervals (ISis) within a requisite target range. (In all these experiments, the target range was 30-60 msec). D R T P periods and alternate time out periods are 5 min in duration and under computer (PDP8/e) control, and have been extensively described 8. Each behavioral period is divided into 15 sec epochs. At the end of each epoch, the computer determines the total APs fired and the total time (in msec) ISis were on and off target. Hence, for each epoch, the total time off target is considered error. At the end of each 5 min behavioral period (DRTP and time out) the mean and S. D. of time on target and error are computed. The first D R T P (DRTP1) period is baseline for each experiment and subsequent D R T P periods are compared to it. The best D R T P
189 TABLE I Means (and S.D.) of error scores and firing rates (APs/15 sec) for the 5 min behavioral periods listed. Data are from 49 PTNs and 35 non-PTNs from precentral cortex. Preconditioned
DRTP1
DRTPb
8876 ± 3759 9313 4- 3861
5916 4- 4473 6878 4- 4625
3542 4- 2473 5878 d: 4332
211 4- 121 204 ± 118
269 :L 111 255 i 122
Error
PTNs non-PTNs
Firing rate (APs/15 sec)
PTNs non-PTNs
163 ± 137 172 4- 128
( D R T P b ) p e r i o d is t h a t p e r i o d subsequent to D R T P 1 with the highest m e a n time on t a r g e t a n d the m e a n e r r o r for this p e r i o d represents the absolute accuracy with which the m o n k e y c o n t r o l l e d t h a t p a r t i c u l a r neuron. D a t a were included in this analysis only i f the following criteria were fulfilled: (a) the n e u r o n s ' A P s were unequivocally isolated, uninjured, a n d n e g a t i v e - p o s i t i v e ; (b) the n e u r o n r e m a i n e d isolated t h r o u g h at least 6 D R T P p e r i o d s (since for m o s t n e u r o n s a n a s y m p t o t e in c o n t r o l is reached by then); a n d (c) the n e u r o n ' s response to p e r i p h e r a l m a n i p u l a t i o n was a d e q u a t e l y characterized. These m a n i p u l a t i o n s included simple tactile (hair) stimulation, pressure to discrete muscle groups, a n d passive m o v e m e n t o f all u p p e r a n d m o s t lower extremity joints. A l t h o u g h we have studied over two h u n d r e d precentral neurons, only 35 nonP T N s a n d 49 P T N s fulfilled the a b o v e criteria. Table I lists the m e a n (and S.D.) e r r o r scores for the 5 min p r e c o n d i t i o n i n g , D R T P 1 a n d D R T P b p e r i o d s for the two g r o u p s o f neurons. There were no significant differences ( S t u d e n t ' s t-test) between g r o u p s for p r e c o n d i t i o n i n g a n d D R T P 1 p e r i o d s ; however, there was a significant difference (t 4.03, P < 0.001) between P T N s a n d n o n - P T N s for D R T P b . It is interesting t h a t n o significant differences in firing rate were a p p a r e n t between P T N s a n d n o n - P T N s for these 3 periods. These d a t a w o u l d a p p e a r to confirm the earlier r e p o r t t h a t P T N s , as a group, are m o r e accurately c o n t r o l l e d t h a n precentral n o n - P T N s . H o w e v e r , the original finding TABLE II Mean (and S.D.) for DRTPb error scores for 49 PTNs and 35 non-PTNs. Discrete refers to neurons activated by one passive peripheral movement whereas diffuse refers to activations by more than one movement although the manipulations might involve opposing movements of the same joint or responses to more than one form of stimulation (i.e. joint manipulation and tactile stimulation). PINs
Discrete Diffuse No field
2318 4- 784 (n = 18) 4764 4- 2329 (n = 28) 5183 4- 3904 (n = 3)
Non-PTNs
2739 ± 832 (n = 7) 4171 -4- 2003 (n = 21) 6276 ± 3816 (n = 7)
190 was determined by comparing the percentage of neurons from each group which were statistically controlled and the present data compares DRTPb error scores. If, on the other hand, the data from non-PTNs is subdivided into neurons with discrete, diffuse and no peripheral field (as previously defined 4) then no significant differences are found between PTNs and non-PTNs (Table II). It is apparent that the samples of PTNs and non-PTNs are not similar since 7/35 (20 ~ ) of non-PTNs and 18/49 (37 ~ ) of PTNs responded to discrete passive peripheral manipulation. Since there is evidence 6 that for this operant task, the accuracy with which precentral PTNs are controlled is related to the neuron's response to peripheral mechanoreceptors, it would appear that the decreased control of non-PTNs, as a group, is an artifact of our sample. For individual non-PTNs with discrete responses to peripheral manipulation the monkeys demonstrated operant control equal to PTNs. Lemon and Ported,2 sufficiently mapped 257 neurons in precentral ' a r m area' and found that 15.7 ~ of PTNs and 18.6 ~ of non-PTNs had no detectable peripheral field. In our sample, 6 ~ of PTNs and 20 ~ of non-PTNs had no mappable field. We cannot explain why our P T N sample differs so greatly from Lemon and Porter's. Btit because of our sample's bias the estimation of operant control of PTNs is most likely inflated. As factors which influence single unit control become identified, it appears that there is no significant difference between the operant control of PTNs and non-PTNs. This research was supported by N I H Research Grant NS 04053, NS 14590 and Teacher Investigator Award (A.R.W.) NS 00195 awarded by the National Institute of Neurological and Communicative Disorders and Stroke, P H S / D H E W . A.R.W. is an affiliate of the Child Development and Mental Retardation Center, University o f Washington.
1 Lemon, R. N. and Porter, R., Afferent input to movement-related precentral neurons in conscious monkeys, Proc. roy. Soc. B, 194 (1975) 313-339. 2 Lemon, R. N., Hanby, J. A. and Porter, R., Relationship between the activity of precentral neurones during active and passive movements in conscious monkeys, Proc. roy. Soc. B, 194 (1975) 341-373. 3 Wyler, A. R. and Finch, C. A., Operant conditioning of tonic firing patterns from precentral neurons in monkey neocortex, Brain Research, 146 (1978) 51-69. 4 Wyler, A. R. and Burchiel, K. J., Factors influencing accuracy of operant control of pyramidal tract neurons in monkey, Brain Research, 152 (1978) 418-421. 5 Wyler, A. R. and Burchiel, K. J., Operant control ofpyramidal tract neurons: the role of spinal dorsal columns, Brain Research, 157 (1978) 257-265. 6 Wyler, A. R., Burchiel, K. J. and Robbins, C. A., Operant control of precentral neurons: evidence against open loop control, Brain Research, (1979) in press.