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Latency of uncrossed and of crossed reaction in callosal agenesis
Neuropsychologia, 1971, Vol. 9. pp. 471 to 473. PergamonPress. Printedin England
NOTE LATENCY
OF UNCROSSED AND OF CROSSED IN CALLOSAL AGENESIS
REACTION
MARCEL KINSBOURNE
Division of Pediatric Neurology, Duke University Medical Center, Durham, North Carolina 27706 and MILTON FISHER
Center for the Study of Aging and Human Development, Duke University Medical Center Durham, North Carolina 27706 (Received 19 April 1971) Abstract-A patient with callosal agenesis manifested no pathological delay in crossed reaction time to unilateral stimulation. This is most readily explicable if cerebral hemisphere control of movement were bilateral in this case. WHEN
the corpus callosum is divided in an adult monkey or man [I], input limited to one hemisphere can no longer result in any finely differentiated ipsilateral response, at least of distal musculature. In agenesis of the corpus callosum in man, no such disconnection is apparent. Even if the anterior commissure remains intact, as it does in some cases of agenesis, this structure would not be expected to bear such heavy traffic [4, 51. It follows that some alternative connecting pathway must have opened up in these cases. Latency of manual reaction is normally a few milliseconds greater to crossed than to uncrossed visual stimulation [6] but JEEVES[7, 81 has reported this difference to be of the order of several hundred milliseconds in patients with callosual agenesis. He assumed that a circuitous alternative pathway through brain stem had opened up in these patients. We report a neuroradiologically verified case of collosual agenesis studied with a reaction time paradigm different in one crucial respect from that adopted by Jeeves (Experiment 1).
CASE
HISTORY
SF., a 16 yr old right-handed black male, was admitted for the investigation of headaches and delayed growth. He was the term product of an uneventful pregnancy and uncomplicated delivery (birth weight 51b. 602.). His mental and motor development were normal. The headaches had been occurring intermittently for two years, were diffusely located, and were not of a nature suggestive of migraine or raised intracranial pressure. His height was at the lo-yr level and he showed none of the concomitants of puberty. His visual acuity was 20/40 bilaterally, corrected to 20!25 with lenses of -0.50 diopters. Investigations revealed an iron deficiency anemia, but with negative upper gastro-intestinal series and barium enema, a bone age of 10.4 yr, normal levels of thyroid functions, pituitary growth hormone, gonadotrophins and thyroid stimulating hormone and negative skull and chest radiographs, electroencephalogram, brain scan. Pneumoencephalography revealed a wide space between the lateral ventricles with elevation of the third ventricle between them, but without distortion of its floor, appearences diagnostic of complete agenesis of the corpus callosum. Bilateral carotid angiograms revealed corresponding findings. Audiometry revealed normal hearing, orthoptic examination normal motor and sensory function, fusion and retinal rivalry. Verbal IQ was 81, performance 97, full scale 88. Psychiatric evaluation revealed anxiety and feelings of insecurity secondary to sexual underdevelopment suficient to account for his headaches.
EXPERIMENT
1
Latency of manual reaction to crossed and uncrossed stimuli Apparatus. An electronic three-field tachistoscope (Scientific Prototype GB) was used to present the visual stimulus for reaction. This was a back Prestotype News Gothic 24-point letter X exposed for a duration of 100 milliseconds against a lighted backgroud field and equally lighted pre- and post-exposure 471
472
NOTE
fields at 41 degrees of visual agle right or left of a central fixation mark. The presentation of the stimulus started a clock which was stopped by a manual response key released so as to register response latency to the nearest 10 msec. Procedure. The subject placed one index finger on the key and fixated the fixation mark. He was instructed to release the key as rapidly as he could upon onset of stimulation. After a practice period, 100 trials were given. Stimuli were presented with equal frequency and in random sequence to the right and to the left of fixation, without foreknowledge on the part of the subject. On half of the trials he responded with the right index finger, on half with the left, in a counterbalanced manner. (Mean msec latency) Stimuli Hand
L L R
R
230.7 266.4
2244 crossed 235.3 uncrossed
Two-way analysis of variance yielded non-significant
EXPERIMENT
F=2.24,
245.4 233.0 3 and 96 df.
2
The experiment was repeated with the modification that the stimulus now appeared with equal frequency in any of three positions, right, left, and also centrally at fixation. Ninety trials were given, randomized for location of stimulus and counterbalanced for laterality of manual response. Results
(Mean msec latency) Stimuli Response
L R
L
C
223.5 260.5
254.0 250.0
R 246.0 crossed 256.7 uncrossed
Two-way analysis of variance yielded non-significant
253.2 240.1
F=0*69, 5 and 84 df.
DISCUSSION We find no latency difference between response to uncrossed and to crossed stimulation in excess of the minor differential to be found in normal subjects [6, 91 which was not reliable in this case. How can this be explained in view of the radiological evidence that the cerebral commissure is missing, and of the vast uncrossed-crossed latency discrepancy reported by JEEVES[7] in patients with the same radiological appearance? It could be that JEEVES’subjects had some undetected abnormalities in addition to callosal agenesis which accounted for the discrepancy. However, a simpler explanation arises from the fact that JEEVES’ subjects had both hands on response keys during his experiment. In the uncrossed condition, the instruction was to respond on the same side as the stimulus; in the crossed condition, to respond on the opposite side. The former condition is highly compatible; the latter an example of gross stimulus-response incompatability. By virtue of response competition, crossed latencies elicited by this method would be relatively prolonged [lo] and this effect might well be even greater in subjects of limited intelligence, such as those studied by Jeeves. Inferences about interhemispheric lines of communication cannot derive from reaction time data of this type. Here only one hand at a time is used, response competition is avoided and no discrepancy between crossed and uncrossed latency was apparent. Even the crossed paradigm as used by Jeeves does not necessarily result in greatly prolonged latencies after collosal section. SMITH [ll] found no disproportionate post-operative latency increments after acute callosal section. An alternate neural rearrangement for which no hypothetical pathways need be assumed, would be the assumption of functional ipsilateral cortico-spinal projections [12-141.
REFERENCES 1. SPEERY, R. W., GAZZANIGA, M. S. and BOOEN, J. E. The neocortical commissures: syndrome of hemispheric deconnection. In Handbook of Clinical Neurology, J. P. VINKENand G. W. BRUYN, (Editors) Chap. 24. North-Holland, Amsterdam, 1969. 2. JEEVES,M. A. and RAJALAKSHMI,R. Psychological studies of a case of congenital agenesis of the corpus callosum. Neuropsychologica 2,247-252, 1964.
473
NOTE
SAUL, R. and SPERRY, R. W. Absence of commissurotomy symptoms with agenesis of the corpus callosum. Neurology 18,307, 1968. 4. ROBINSON,J. S. and VONEIDA,T. J. Central cross-integration of visual inputs presented simultaneously to the separate eyes. J. camp. physiol. Psychol. 57,22-28, 1964. 5. GAZZANIGA,M. S. Interhemispheric communication of visual learning. Neuropsychologiu 4, 183-189, 1966. 6. KERR, M., MINGAY, R. and ELITHORN,A. Cerebral dominance in reaction time responses. &it. J.
3.
Psych&
54, 325-336,
JEEVM, M.
1963.
studies of three cases of congenital agenesis of the corpus callosum. In G. E~TLINGER(Editor), 11, 73-93. (Little Brown, Boston, 1965. 8. JEEVES,M. A. A comparison of hemispheric transmission time in acallosals and normals. Psychonom.
I.
A. Psychological
Functions of the Corpus Callosum.
Sci. 16, 245-246,
1969.
9. BRADSHAW,J. L. and PERRIMENT,A. D. Lateralization effects and choice reaction time in a unimanual two-finger task. Percept. Psychophys. 185-188, 1970, D. E. and GREGORY,M. On the interaction of stimulus response compatability with other 10. BROADBENT, variables affecting reaction time. Brit. J. Psychol. 56, 61-67, 1965. Il. SMITH,K. Bilateral integrative action of the cerebral cortex in man in verbal association and sensory motor coordination. J. exp. Psychol. 31, 367-376, 1947. 12. BUCY, P. C. and FULTON,J. F. Ipsilateral representation in the motor and premotor cortex in monkeys. Bruin 56,318-343, 1933. 13. KUYPERS, H. G. J. M. Central cortical projections to motor and somatosensory cell groups. Brain 83, 161-186, 1960. 14. Lru, C. N. and CHAMBERS,W. W. An experimental study of the corticospinal (Maccaca mulatta). J. romp. Neural. 123, 257-212, 1964.
system in the monkey
R&urn&-Chez un suiet avec ag&Csie calleuse on ne constatait pas de retard pathologique dans le temps de r&action croisee II la stimulation unilattrale. L’explication la plus simple serait, dans ce cas, que le contrale htmisphtrique du mouvement est bilateral. Zusammenfassung-Ein Patient mit Balkenmangel bot keine pathologische Verllngerung gekreuzter Reaktionszeit auf einseitige Reizung. Diese Tatsache l%iOtsich am besten damit erkllren, daB in diesem Falle die hemisph&rische Bewegungskontrolle bilateral angelegt war.
NOTE LATENCY
OF UNCROSSED AND OF CROSSED IN CALLOSAL AGENESIS
REACTION
MARCEL KINSBOURNE
Division of Pediatric Neurology, Duke University Medical Center, Durham, North Carolina 27706 and MILTON FISHER
Center for the Study of Aging and Human Development, Duke University Medical Center Durham, North Carolina 27706 (Received 19 April 1971) Abstract-A patient with callosal agenesis manifested no pathological delay in crossed reaction time to unilateral stimulation. This is most readily explicable if cerebral hemisphere control of movement were bilateral in this case. WHEN
the corpus callosum is divided in an adult monkey or man [I], input limited to one hemisphere can no longer result in any finely differentiated ipsilateral response, at least of distal musculature. In agenesis of the corpus callosum in man, no such disconnection is apparent. Even if the anterior commissure remains intact, as it does in some cases of agenesis, this structure would not be expected to bear such heavy traffic [4, 51. It follows that some alternative connecting pathway must have opened up in these cases. Latency of manual reaction is normally a few milliseconds greater to crossed than to uncrossed visual stimulation [6] but JEEVES[7, 81 has reported this difference to be of the order of several hundred milliseconds in patients with callosual agenesis. He assumed that a circuitous alternative pathway through brain stem had opened up in these patients. We report a neuroradiologically verified case of collosual agenesis studied with a reaction time paradigm different in one crucial respect from that adopted by Jeeves (Experiment 1).
CASE
HISTORY
SF., a 16 yr old right-handed black male, was admitted for the investigation of headaches and delayed growth. He was the term product of an uneventful pregnancy and uncomplicated delivery (birth weight 51b. 602.). His mental and motor development were normal. The headaches had been occurring intermittently for two years, were diffusely located, and were not of a nature suggestive of migraine or raised intracranial pressure. His height was at the lo-yr level and he showed none of the concomitants of puberty. His visual acuity was 20/40 bilaterally, corrected to 20!25 with lenses of -0.50 diopters. Investigations revealed an iron deficiency anemia, but with negative upper gastro-intestinal series and barium enema, a bone age of 10.4 yr, normal levels of thyroid functions, pituitary growth hormone, gonadotrophins and thyroid stimulating hormone and negative skull and chest radiographs, electroencephalogram, brain scan. Pneumoencephalography revealed a wide space between the lateral ventricles with elevation of the third ventricle between them, but without distortion of its floor, appearences diagnostic of complete agenesis of the corpus callosum. Bilateral carotid angiograms revealed corresponding findings. Audiometry revealed normal hearing, orthoptic examination normal motor and sensory function, fusion and retinal rivalry. Verbal IQ was 81, performance 97, full scale 88. Psychiatric evaluation revealed anxiety and feelings of insecurity secondary to sexual underdevelopment suficient to account for his headaches.
EXPERIMENT
1
Latency of manual reaction to crossed and uncrossed stimuli Apparatus. An electronic three-field tachistoscope (Scientific Prototype GB) was used to present the visual stimulus for reaction. This was a back Prestotype News Gothic 24-point letter X exposed for a duration of 100 milliseconds against a lighted backgroud field and equally lighted pre- and post-exposure 471
472
NOTE
fields at 41 degrees of visual agle right or left of a central fixation mark. The presentation of the stimulus started a clock which was stopped by a manual response key released so as to register response latency to the nearest 10 msec. Procedure. The subject placed one index finger on the key and fixated the fixation mark. He was instructed to release the key as rapidly as he could upon onset of stimulation. After a practice period, 100 trials were given. Stimuli were presented with equal frequency and in random sequence to the right and to the left of fixation, without foreknowledge on the part of the subject. On half of the trials he responded with the right index finger, on half with the left, in a counterbalanced manner. (Mean msec latency) Stimuli Hand
L L R
R
230.7 266.4
2244 crossed 235.3 uncrossed
Two-way analysis of variance yielded non-significant
EXPERIMENT
F=2.24,
245.4 233.0 3 and 96 df.
2
The experiment was repeated with the modification that the stimulus now appeared with equal frequency in any of three positions, right, left, and also centrally at fixation. Ninety trials were given, randomized for location of stimulus and counterbalanced for laterality of manual response. Results
(Mean msec latency) Stimuli Response
L R
L
C
223.5 260.5
254.0 250.0
R 246.0 crossed 256.7 uncrossed
Two-way analysis of variance yielded non-significant
253.2 240.1
F=0*69, 5 and 84 df.
DISCUSSION We find no latency difference between response to uncrossed and to crossed stimulation in excess of the minor differential to be found in normal subjects [6, 91 which was not reliable in this case. How can this be explained in view of the radiological evidence that the cerebral commissure is missing, and of the vast uncrossed-crossed latency discrepancy reported by JEEVES[7] in patients with the same radiological appearance? It could be that JEEVES’subjects had some undetected abnormalities in addition to callosal agenesis which accounted for the discrepancy. However, a simpler explanation arises from the fact that JEEVES’ subjects had both hands on response keys during his experiment. In the uncrossed condition, the instruction was to respond on the same side as the stimulus; in the crossed condition, to respond on the opposite side. The former condition is highly compatible; the latter an example of gross stimulus-response incompatability. By virtue of response competition, crossed latencies elicited by this method would be relatively prolonged [lo] and this effect might well be even greater in subjects of limited intelligence, such as those studied by Jeeves. Inferences about interhemispheric lines of communication cannot derive from reaction time data of this type. Here only one hand at a time is used, response competition is avoided and no discrepancy between crossed and uncrossed latency was apparent. Even the crossed paradigm as used by Jeeves does not necessarily result in greatly prolonged latencies after collosal section. SMITH [ll] found no disproportionate post-operative latency increments after acute callosal section. An alternate neural rearrangement for which no hypothetical pathways need be assumed, would be the assumption of functional ipsilateral cortico-spinal projections [12-141.
REFERENCES 1. SPEERY, R. W., GAZZANIGA, M. S. and BOOEN, J. E. The neocortical commissures: syndrome of hemispheric deconnection. In Handbook of Clinical Neurology, J. P. VINKENand G. W. BRUYN, (Editors) Chap. 24. North-Holland, Amsterdam, 1969. 2. JEEVES,M. A. and RAJALAKSHMI,R. Psychological studies of a case of congenital agenesis of the corpus callosum. Neuropsychologica 2,247-252, 1964.
473
NOTE
SAUL, R. and SPERRY, R. W. Absence of commissurotomy symptoms with agenesis of the corpus callosum. Neurology 18,307, 1968. 4. ROBINSON,J. S. and VONEIDA,T. J. Central cross-integration of visual inputs presented simultaneously to the separate eyes. J. camp. physiol. Psychol. 57,22-28, 1964. 5. GAZZANIGA,M. S. Interhemispheric communication of visual learning. Neuropsychologiu 4, 183-189, 1966. 6. KERR, M., MINGAY, R. and ELITHORN,A. Cerebral dominance in reaction time responses. &it. J.
3.
Psych&
54, 325-336,
JEEVM, M.
1963.
studies of three cases of congenital agenesis of the corpus callosum. In G. E~TLINGER(Editor), 11, 73-93. (Little Brown, Boston, 1965. 8. JEEVES,M. A. A comparison of hemispheric transmission time in acallosals and normals. Psychonom.
I.
A. Psychological
Functions of the Corpus Callosum.
Sci. 16, 245-246,
1969.
9. BRADSHAW,J. L. and PERRIMENT,A. D. Lateralization effects and choice reaction time in a unimanual two-finger task. Percept. Psychophys. 185-188, 1970, D. E. and GREGORY,M. On the interaction of stimulus response compatability with other 10. BROADBENT, variables affecting reaction time. Brit. J. Psychol. 56, 61-67, 1965. Il. SMITH,K. Bilateral integrative action of the cerebral cortex in man in verbal association and sensory motor coordination. J. exp. Psychol. 31, 367-376, 1947. 12. BUCY, P. C. and FULTON,J. F. Ipsilateral representation in the motor and premotor cortex in monkeys. Bruin 56,318-343, 1933. 13. KUYPERS, H. G. J. M. Central cortical projections to motor and somatosensory cell groups. Brain 83, 161-186, 1960. 14. Lru, C. N. and CHAMBERS,W. W. An experimental study of the corticospinal (Maccaca mulatta). J. romp. Neural. 123, 257-212, 1964.
system in the monkey
R&urn&-Chez un suiet avec ag&Csie calleuse on ne constatait pas de retard pathologique dans le temps de r&action croisee II la stimulation unilattrale. L’explication la plus simple serait, dans ce cas, que le contrale htmisphtrique du mouvement est bilateral. Zusammenfassung-Ein Patient mit Balkenmangel bot keine pathologische Verllngerung gekreuzter Reaktionszeit auf einseitige Reizung. Diese Tatsache l%iOtsich am besten damit erkllren, daB in diesem Falle die hemisph&rische Bewegungskontrolle bilateral angelegt war.