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Temporal ordering deficits following anterior temporal lobectomy
BRAIN
AND
LANGUAGE
Temporal
11,
Ordering
195-203 (1980)
Deficits following Lobectomyl
Anterior
Temporal
IRA SHERWIN Veterans Administration Medical Center, Bedford, Massachusetts and Harvard Medical School
AND ROBERTEFRON Veterans Administration Medical Center, Martinez, California and University of California, Davis Subjects were required to report the pitch sequence of two IO-msec tones of different frequency presented monaurally while the stimulus onset asynchrony (SOA) between the two tones was varied. The value of the SOA at which the subjects achieved an 80% correct sequence report was determined by an adaptive procedure without feedback. This measure was compared in the right and left ears, on subjects with a right or left anterior temporal lobectomy and on a normal control group. The results reveal an elevated threshold for performing temporal order judgments in the ear contralateral to the surgical lesion.
INTRODUCTION
Damage to the dominant (left) hemisphere resulting from strokes, tumors, atrophy, or trauma has been reported to produce a deficit in the Supported by the Veterans Administration, USPHS Grant NSO2808, and a grant in aide from Ciba-Giegy. This paper was read in part at the 1lth Epilepsy International Symposium, September 1978, Vancouver, British Columbia, Canada. This work was conducted at the Reed Neurological Research Center, UCLA. The authors are pleased to acknowledge their indebtedness to Dr. Richard D. Walter who generously made available the resources of The Center and to the staff members who gave unstintingly of their time and talents to make this study possible. We are also indebted to the members of the Clinical Neurophysiology Program, in particular to Dr. Paul H. Crandall, for the opportunity to examine his surgical patients and for the many rewarding discussions regarding their clinical problems. Special thanks are due: Dr. R. Rausch and her staff for performing the pure tone audiometry and Drs. M. A. B. Brazier and D. Howes for invaluable comments on many aspects of this work. Address reprint requests to Dr. Ira Sherwin, The Neurophysiology Unit, Research Service, Veterans Administration Medical Center, Bedford MA 01730. 195 0093-934)(/80/050195-O9SO2.00/0 Copyright @I W80 by Academic Press, Inc. All rights of reproduction in any form reserved.
196
SHERWIN
AND EFRON
subject’s capacity to report the correct sequence of two or more rapidly successive stimuli (Efron, 1963; Edwards & Auger, 1965; Holmes, 1965; Carmon & Nachsohn, 1971; Swisher & Hirsh, 1972; Sherwin, 1977). In all of these studies it was observed that the stimulus onset asynchrony (SOA) had to be increased markedly before such left-brain-damaged subjects could reliably report the correct temporal sequence. This was true in the visual as well as auditory modality (Efron, 1963; Swisher & Hirsh, 1972), and also occurred when audio and visual stimuli were combined (Carmon & Nachsohn, 1971). Since these individuals could make reliably correct temporal order judgments if the SOA was prolonged, the deficit could not be attributed to any generalized cognitive disturbances of understanding, attention, or memory, but was considered to represent a specific perceptive disability in the processing of rapidly presented sequential stimuli. Several of these investigators (Efron, 1963; Edwards & Auger, 1%5; Swisher & Hirsh, 1972) noted that a severe deficit in making temporal order judgments was strongly correlated with the presence of aphasia. In two of the cited studies, in which only nonaphasic patients were studied (Carmon & Nachsohn, 1971; Sherwin, 1977), it was found that abnormally high thresholds also tended to predominate in but were not restricted to patients with left-hemisphere lesions. In sum, the results of the previous experiments seem to indicate the following: (A) that the severity of the deficit is greatest in subjects with left-hemisphere lesions that are associated with aphasia, particularly a “fluent” aphasia; (B) that the severity of the deficit in patients with a left-hemisphere lesion without an aphasia may also be severe but the correlation is more variable; and (C) that severe deficits in patients with right-hemisphere lesions occur more variably still. It should be noted, however, that all of the studies cited above were conducted prior to the widespread use of computerized axial tomography. Consequently, the size and the precise location of the lesion which raised the threshold for temporal order judgments could not be specified. Although these studies implied a particular correlation with temporal lobe lesions, without these critical data, it is not possible to be certain what cerebral region(s) has to be damaged before the deficit is produced. Similarly it cannot be determined whether there is any correlation between the size of the lesion and the severity of the temporal order deficit. The present study was undertaken to provide a more refined analysis of the role of the right and left temporal lobes in the performance of an auditory temporal ordering task in patients with essentially identical resections of the anterior portion of one temporal lobe. In such a unique group of patients, any significant individual differences in performance could not be attributed to variations in the size or location of the lesion within the temporal lobe. Morever, since some data (Swisher & Hirsh 1972) suggest that the deficit may depend, in part, on the spatial location
197
TEMPORAL ORDERING POSTLOBECTOMY
of the stimuli, we specifically focused on the comparative effects of stimulating the ears monaurally. SUBJECTS Eleven patients who had undergone unilateral temporal lobectomy for the treatment of medically intractable epilepsy were studied. Nine of them were examined postoperatively only, but two were tested preoperatively as well. None had a significant hearing loss (using pure tone audiometry) in the range of frequencies employed in the present study nor did they have any manifestations of aphasia. Eight age-sex-matched normal subjects were used as controls; none had any history of hearing dysfunction. Table 1 lists the composition of the patient and normal control groups which were approximately matched for age and sex. Men predominate in this sample as they do in the population of patients from which they were drawn. The mean interval between surgery and the date of testing (P.O.@ was 9 years. Based on stereoelectroencephalography, all patients had been diagnosed as having a unilateral, temporal lobe, epileptogenic focus. In each case the focus was excised by an enbloc anterior temporal lobectomy. Measured along the sylvian fissure, the posterior limit of the excision was located 5.5 cm from the tip of the temporal lobe on the left side and 6.5 cm on the right side. The structures removed included the temporal pole, uncus, amygdala, hippocampal gyrus, the anterior 2.5 cm of the hippocampus, and all of the temporal neocortex anterior to the posterior limit of the excision. In no instance was any portion of Heschl’s gyrus removed. Of the 11 surgical specimens, 7 revealed mesial temporal sclerosis, 1 contained a hamartoma, and 2 had very slow growing gliomas. In one case no definite anatomical lesion was found. Excluding the two cases examined preoperatively and in whom it was too soon to judge, all but one patient (A.D.) had excellent relief of their seizures.
PSYCHOPHYSICAL METHODS Sinusoidal stimuli of 1000 and 3000 Hz having a duration of 10 msec with 2.5-msec rise-decay times were presented monaurally by earphone. To ensure that the stimuli presented to the test ear did not stimulate the contralateral ear via bone conduction, they were delivered at a sound pressure level of 50 db, a level sufficient for all subjects to perform the task monaurally. The instrumentation used to generate and deliver these monaural stimuli is illustrated in Fii. 1. Prior to formal testing, the subjects were exposed to each of the pure tones in isolation until it was obvious that they could identify and verbally label each (“high pitch” or “low pitch”) without error. Subjects were then exposed to pairs of tone bursts. Each pair, hereafter referred to as a “trial,” was composed of one high- and one low-pitched tone. Thus, a trial could consist of either a low-high or a high-low pitch sequence. The selection of either the high- or low-frequency tone as the leading stimulus was varied for successive presentations in a pseudorandom fashion which assured an equal probability of occurrence for both sequences. Using a forced choice paradigm without corrective feedback, and while varying the stimulus onset asynchrony (SOA) in lo-msec steps, the subject was required to TABLE 1
N Female Male Age B P.Ok
T-lobectomy
Controls
11 2 9 33 9
8 3 5 30 -
198
SHERWIN AND EFRON
I
DIGITAL LOGIC AND TIMING
SYSTEMS
TAPE RECORDER CHAN.- I CHIN.‘2
I/
~~ 1 AUDIO GATE 2
REVERSING WITCH ATTENUATOR
FIG. 1. Continuous sine wave oscillations of 3000 and 1000 Hz were prerecorded on magnetic tape. During the experiment, these signals were reproduced on the tape recorder, filtered (to increase signal to noise ratios), passed through a reversing switch to two audio gates (ICONIX 0137), and then through two attenuators to a single earphone. The opening and closing of these gates were under the control of a digital logic and timing system (ICONIX 62574010) accurate to + .Ol msec which was used to vary the stimulus onset asynchrony for each trial. Although Gates 1 and 2 were always opened and closed in the same order, the use of the reversing switch between trials enabled the experimenter to select a high-low or low-high frequency sequence. report alter each trial, which sequence he had heard. A transformed adaptive procedure (Wetherill & Levitt, 1%5) was used to determine the SOA required to achieve an 80% correct response rate. To accomplish this the SOA was reduced by one IO-msec step after three consecutive correct responses and was increased by one IO-msec step following a single incorrect response. Twenty such up-down transition values were obtained in one experimental session and the mean and standard deviation were calculated. Four such sessions were conducted, two for the right and two for the left ear. For approximately half the subjects the left ear was tested first; in the other half the right ear was tested first. TO minimize potential learning and fatigue effects, the order in which the two ears were tested was reversed in the third and fourth sessions.
RESULTS The results for each ear for each subject are shown in Table 2. For the control subjects the differences in SOA between the left and right ear were not statistically significant. All patients with a left temporal lobectomy had higher temporal order thresholds in the right ear. For subject S.D., however, this difference did not reach significance at the .Ol level. In contrast, the patients with a right temporal lobectomy had higher thresholds in their left ear except for subject D.R. who performed more
53.13
22.00
7
8
difference
27.00
6
significant
28.75 14.29 31.82 50.71 35.00
1 2 3 4 5
* Statistically
Left ear
Control subject no.
(p < .Ol).
23.00
55.00
32.78
26.88 22.50 35.50 50.00 31.67
Right ear S.J. F.J. E.R. S.D. G.G. (postop) G.G. Weep)
Left lobectomy
11.67
24.00 331.88 10.50 30.33 11.88
Left ear
*
* * *
TABLE 2 AUDITORYTHRESHOLD(MSEC)FORTEMFQRAL
7.50
39.55 373.75 18.00 33.33 23.75
Right ear
L.R. (PostoP) L.R. (preop)
D.P. A.D. T.A. O.F. D.R.
Right lobectomy
ORDERJUDGMENTS
15.00
27.78
38.13 72.22 52.19 282.50 156.82
Left ear
15.00
*
17.50
18.13 57.65 39.33 179.44 164.50
* * * *
Right ear
200
SHERWIN
AND EFRON
poorly with his right ear (the ear ipsilateral to his lesion). However, the difference in D.R.‘s performance with the right and left ear was not statistically significant. The results of the performance by these 11 postoperative patients indicate that an anterior temporal lobectomy elevates the threshold for correct temporal order judgments for stimuli presented to the contralateral ear. This conclusion is strongly reinforced by the results obtained on the two patients studied preoperatively. Prior to temporal lobectomy their right and left ear temporal order thresholds were not significantly different. An asymmetry in performance developed after surgery and this asymmetry was in the direction which was anticipated from the results of the other nine subjects who were tested only postoperatively. It should be noted that three patients-F.J., O.F., and D.R.-had exceptionally high thresholds in both ears, having valves similar to those patients reported by Efron (1963), Edwards and Auger (1%5), and Swisher and Hirsh (1972), all of whom had aphasia. Yet, none of these three patients had any sign of aphasia. Moreover, in two of them (O.F. and D.R.) the lobectomy was performed on the nondominant (right) side. From this we conclude that neither aphasia nor a dominant hemisphere lesion is a necessary or sufficient requirement for the exceptionally high thresholds found bilaterally. DISCUSSION The main results of these experiments reveal that anterior temporal lobectomy raised the threshold for temporal order judgments in the ear contralateral to the lesion. The fact that a unilateral temporal lobe lesion can result in a contralateral auditory deficit is not, in itself, new: Bocca, Calearo, Cassinari, and Migliavacca (1955) showed that speech discrimination is impaired, Gersuni, Batu, Karaseva, and Tonkonogii (1971) and Baru (1971) showed that temporal summation is impaired in the ear contralateral to a temporal lobe lesion. What was unexpected, however, was that such a contralateral effect could be produced by a lesion of the temporal lobe which is anterior to Heschl’s gyrus (primary auditory cortex) and did not involve any of the classical auditory association areas. However, recent anatomical studies on the monkey by Rockland and Pandya (1977) have revealed the presence of a neuronal loop connecting the ipsilateral primary visual cortex to the anterior temporal pole and probably, via the entorhinal cortex, to the hippocampus and amygdala. Closely juxtaposed to this pathway is a similar loop originating in and returning to the primary auditory cortex (D.N. Pandya, personal communication). If analogous pathways exist in man, they would surely have been compromised by the surgical excisions in these 11 patients. It seems possible that damage to such a neural system might modify auditory cortex function comparable to the way in which stimulation of the
TEMPORAL
ORDERING
POSTLOBECTOMY
201
centrifugal (efferent) auditory control system modulates the function of lower level afferent auditory systems (See Desmedt, 1975 for review). Whether or not damage to this presumed pathway is related to the elevated contralateral threshold for auditory temporal order judgments seen in these patients, the experimental results unequivocally indicate that the anterior temporal lobe is involved in the performance of this auditory function. Whitfield (1%8) in his studies on the auditory system has suggested that “many of the anomalies in discriminative ability uncovered by ablation studies may be explicable on this basis,” i.e., in terms of damage to such efferent pathways. It would appear that elevation of the threshold for making temporal order judgments in the ear contralatera1 to an anterior temporal lobectomy may be one of the “anomalies” predicted by Whitfield. As previously indicated, the focus of the present study was to determine the effect of a temporal lobe lesion on the ipsi- and contralateral ear performance. Although the increase in the threshold for temporal order judgments in the contralateral ear was statistically significant, it was not a large effect. It was also found by Swisher and Hirsh (1972) in their group of patients with right-hemisphere lesions (size and location unspecified) but not in their group of left-hemisphere lesions all of whom had an aphasia and essentially equal elevations of threshold in both ears. Their patients with fluent aphasia had thresholds at least fourfold higher than the nonfluent aphasics whose lesions were probably located more anteriorly. The findings of Swisher and Hirsh (1972) coupled with those of the present study suggest that there may be two types of temporal-orderthreshold elevations produced by a temporal lobe lesion. In the first type (I) the deficit is a small one, is confined to the ear contralateral to the lesion, and may be found only with lesions restricted to the anterior portion of the temporal lobe. The type II deficit is a large one, is seen in equal degree in both ears, and seems to be strongly associated with more posteriorly located lesions (perhaps on the right as well as the left). The observed prevalence of the type II deficit in association with fluent aphasias may be a coincidental finding. Similarly placed lesions in the more posterior parts of the right temporal lobe are more difficult to diagnose clinically, are less likely to result in hospitalization, and thus may be under represented in the populations of right-brain-damaged subjects tested by previous investigators. A close inspection of Table 2 indicates that three of our patients (F.J., O.F., and D.R.) had both types of deficit. Their thresholds were markedly elevated in both ears, having a magnitude characteristic of the type II deficit, but, in addition, there was in two of them a small but significant contralateral (type I) deficit as well. It is not obvious why only these three subjects also displayed the type II deficit. Although the surgical lesions were essentially identical in all 11 patients, the possibility cannot be
202
SHERWIN AND EFRON
excluded that these 3 subjects still have a residual pathological condition in the remaining part of the affected temporal lobe-or even additional pathology in the unoperated temporal lobe. Alternatively, the use of subjects, all of whom were chronic epileptics, raises the possibility that this pathological process itself might induce a functional reorganization of the temporal lobe(s). Although the type II deficit was also noted by others in their subjects with nonepileptogenic lesions it is appropriate to excercise some caution in inferring from our results the role played by the anterior temporal lobe in the normal brain. Consonant with our findings and those of others (supravide) it is possible that the small contralateral effect (type I) may be explicable in terms of the neuroanatomical and electrophysiological mechanisms already discussed. However, these essentially unilateral mechanisms do not seem to provide an adequate explanation for the large type II deficits which involve both ears. Interestingly, based on recent anatomical studies, Van Hoesen, Rosene, and Mesulam (1979) have suggested that the integrity of the anterior temporal lobe, in particular the subicular cortex, “may be essential for many complex mental processes.” Before a full explanation can be offered more information will be required. In particular, it may be useful to determine if increasing the task difficulty in some nontemporal respect (e.g., by decreasing the frequency difference of the two tones or by adding noise) changes the temporal order thresholds differently in brain-damaged, compared to normal, subjects. REFERENCES Baru, A.V. 1971. Absolute thresholds and frequency difference limens as a function of sound duration in dogs deprived of the auditory cortex. In G. V. Gersuni (Ed.), Sensory processes at the neuronal and behavioral levels. New York: Academic Press. Pp. 265-286. Bocca, E., Calearo, C., Cassinari, V., & Migliavacca, F. 1955.Testing “cortical” hearing in temporal lobe tumors. Acta Oto-Laryngologica 45, 289-304. Carmon, A., & Nachsohn, I. 1971. Effect of unilateral brain damage on perception of temporal order. Cortex, 7, 410-418. Desmedt, J. E. 1975. Physiological studies of the efferent recurrent auditory system. In W. D. Keidel and W. D. Neff (Eds.), Handbook ofsensory physiology. Berlin: SpringerVerlag. Vol. V/2, pp. 219-246. Edwards, A. E., & Auger, R. 1%5. The effect of aphasia on the perception of precedence. In Proc. 73rd Annu. Co& Amer. Psychol. Assoc. Amer. Psychol. Assoc., Washington, D.C. Pp. 207-208. Efron, R. 1%3. Temporal perception, aphasia and deja vu. Brain, 86, 403-424. Gersuni, G. V., Baru, A. V., Karaseva, T. A., & Tonkonogii, I. M. 1971.Effects of temporal lobe lesions on perception of sounds of short duration. In G. V. Gersuni (Ed.), Sensory processes at the neuronal and behavioral levels. New York: Academic Press. Pp. 287-300. Holmes, H. 1%5. Disordered perception of auditory sequences in aphasia. PhD Thesis, Harvard University. Rockland, K. 8, & Pandya, D. N. 1977. Some observations on laminar origins and terminations of occipito-temporal cortical connections in rhesus monkey. Neuroscience Abstracts, 3, 211.
TEMPORAL ORDERING POSTLOBECTOMY
203
Sherwin, I. 1977. Clinical and EEG Aspects of temporal lobe epilepsy with behavior disorder, the role of cerebral dominance. McLean Hospital Journal, Special Issue (June), 40-50. Swisher, L., and Hirsh, I. J. 1972. Brain damage and the ordering of two temporally successive stimuli. Neurophsychologia, 10, 137-152. Van Hoesen, G. W., Rosene, D. L., & Mesulam, M. M. 1979.Subicularinput from temporal cortex in the rhesus monkey. Science, 205, 608-610. Wetherill, G. B., & Levitt, H. 1965. Sequential estimation of points on a psychometric function. British Journal of Mathematical and Statistical Psychology, 18, l-10. Whitheld, I. D. 1968. Centrifugal control mechanisms of the auditory pathway. In A. V. S. Dereuck & J. Knight (Eds.), Hearing mechanisms in vertebrates: A Ciba symposium. Boston: Little, Brown. Pp. 246-254.
AND
LANGUAGE
Temporal
11,
Ordering
195-203 (1980)
Deficits following Lobectomyl
Anterior
Temporal
IRA SHERWIN Veterans Administration Medical Center, Bedford, Massachusetts and Harvard Medical School
AND ROBERTEFRON Veterans Administration Medical Center, Martinez, California and University of California, Davis Subjects were required to report the pitch sequence of two IO-msec tones of different frequency presented monaurally while the stimulus onset asynchrony (SOA) between the two tones was varied. The value of the SOA at which the subjects achieved an 80% correct sequence report was determined by an adaptive procedure without feedback. This measure was compared in the right and left ears, on subjects with a right or left anterior temporal lobectomy and on a normal control group. The results reveal an elevated threshold for performing temporal order judgments in the ear contralateral to the surgical lesion.
INTRODUCTION
Damage to the dominant (left) hemisphere resulting from strokes, tumors, atrophy, or trauma has been reported to produce a deficit in the Supported by the Veterans Administration, USPHS Grant NSO2808, and a grant in aide from Ciba-Giegy. This paper was read in part at the 1lth Epilepsy International Symposium, September 1978, Vancouver, British Columbia, Canada. This work was conducted at the Reed Neurological Research Center, UCLA. The authors are pleased to acknowledge their indebtedness to Dr. Richard D. Walter who generously made available the resources of The Center and to the staff members who gave unstintingly of their time and talents to make this study possible. We are also indebted to the members of the Clinical Neurophysiology Program, in particular to Dr. Paul H. Crandall, for the opportunity to examine his surgical patients and for the many rewarding discussions regarding their clinical problems. Special thanks are due: Dr. R. Rausch and her staff for performing the pure tone audiometry and Drs. M. A. B. Brazier and D. Howes for invaluable comments on many aspects of this work. Address reprint requests to Dr. Ira Sherwin, The Neurophysiology Unit, Research Service, Veterans Administration Medical Center, Bedford MA 01730. 195 0093-934)(/80/050195-O9SO2.00/0 Copyright @I W80 by Academic Press, Inc. All rights of reproduction in any form reserved.
196
SHERWIN
AND EFRON
subject’s capacity to report the correct sequence of two or more rapidly successive stimuli (Efron, 1963; Edwards & Auger, 1965; Holmes, 1965; Carmon & Nachsohn, 1971; Swisher & Hirsh, 1972; Sherwin, 1977). In all of these studies it was observed that the stimulus onset asynchrony (SOA) had to be increased markedly before such left-brain-damaged subjects could reliably report the correct temporal sequence. This was true in the visual as well as auditory modality (Efron, 1963; Swisher & Hirsh, 1972), and also occurred when audio and visual stimuli were combined (Carmon & Nachsohn, 1971). Since these individuals could make reliably correct temporal order judgments if the SOA was prolonged, the deficit could not be attributed to any generalized cognitive disturbances of understanding, attention, or memory, but was considered to represent a specific perceptive disability in the processing of rapidly presented sequential stimuli. Several of these investigators (Efron, 1963; Edwards & Auger, 1%5; Swisher & Hirsh, 1972) noted that a severe deficit in making temporal order judgments was strongly correlated with the presence of aphasia. In two of the cited studies, in which only nonaphasic patients were studied (Carmon & Nachsohn, 1971; Sherwin, 1977), it was found that abnormally high thresholds also tended to predominate in but were not restricted to patients with left-hemisphere lesions. In sum, the results of the previous experiments seem to indicate the following: (A) that the severity of the deficit is greatest in subjects with left-hemisphere lesions that are associated with aphasia, particularly a “fluent” aphasia; (B) that the severity of the deficit in patients with a left-hemisphere lesion without an aphasia may also be severe but the correlation is more variable; and (C) that severe deficits in patients with right-hemisphere lesions occur more variably still. It should be noted, however, that all of the studies cited above were conducted prior to the widespread use of computerized axial tomography. Consequently, the size and the precise location of the lesion which raised the threshold for temporal order judgments could not be specified. Although these studies implied a particular correlation with temporal lobe lesions, without these critical data, it is not possible to be certain what cerebral region(s) has to be damaged before the deficit is produced. Similarly it cannot be determined whether there is any correlation between the size of the lesion and the severity of the temporal order deficit. The present study was undertaken to provide a more refined analysis of the role of the right and left temporal lobes in the performance of an auditory temporal ordering task in patients with essentially identical resections of the anterior portion of one temporal lobe. In such a unique group of patients, any significant individual differences in performance could not be attributed to variations in the size or location of the lesion within the temporal lobe. Morever, since some data (Swisher & Hirsh 1972) suggest that the deficit may depend, in part, on the spatial location
197
TEMPORAL ORDERING POSTLOBECTOMY
of the stimuli, we specifically focused on the comparative effects of stimulating the ears monaurally. SUBJECTS Eleven patients who had undergone unilateral temporal lobectomy for the treatment of medically intractable epilepsy were studied. Nine of them were examined postoperatively only, but two were tested preoperatively as well. None had a significant hearing loss (using pure tone audiometry) in the range of frequencies employed in the present study nor did they have any manifestations of aphasia. Eight age-sex-matched normal subjects were used as controls; none had any history of hearing dysfunction. Table 1 lists the composition of the patient and normal control groups which were approximately matched for age and sex. Men predominate in this sample as they do in the population of patients from which they were drawn. The mean interval between surgery and the date of testing (P.O.@ was 9 years. Based on stereoelectroencephalography, all patients had been diagnosed as having a unilateral, temporal lobe, epileptogenic focus. In each case the focus was excised by an enbloc anterior temporal lobectomy. Measured along the sylvian fissure, the posterior limit of the excision was located 5.5 cm from the tip of the temporal lobe on the left side and 6.5 cm on the right side. The structures removed included the temporal pole, uncus, amygdala, hippocampal gyrus, the anterior 2.5 cm of the hippocampus, and all of the temporal neocortex anterior to the posterior limit of the excision. In no instance was any portion of Heschl’s gyrus removed. Of the 11 surgical specimens, 7 revealed mesial temporal sclerosis, 1 contained a hamartoma, and 2 had very slow growing gliomas. In one case no definite anatomical lesion was found. Excluding the two cases examined preoperatively and in whom it was too soon to judge, all but one patient (A.D.) had excellent relief of their seizures.
PSYCHOPHYSICAL METHODS Sinusoidal stimuli of 1000 and 3000 Hz having a duration of 10 msec with 2.5-msec rise-decay times were presented monaurally by earphone. To ensure that the stimuli presented to the test ear did not stimulate the contralateral ear via bone conduction, they were delivered at a sound pressure level of 50 db, a level sufficient for all subjects to perform the task monaurally. The instrumentation used to generate and deliver these monaural stimuli is illustrated in Fii. 1. Prior to formal testing, the subjects were exposed to each of the pure tones in isolation until it was obvious that they could identify and verbally label each (“high pitch” or “low pitch”) without error. Subjects were then exposed to pairs of tone bursts. Each pair, hereafter referred to as a “trial,” was composed of one high- and one low-pitched tone. Thus, a trial could consist of either a low-high or a high-low pitch sequence. The selection of either the high- or low-frequency tone as the leading stimulus was varied for successive presentations in a pseudorandom fashion which assured an equal probability of occurrence for both sequences. Using a forced choice paradigm without corrective feedback, and while varying the stimulus onset asynchrony (SOA) in lo-msec steps, the subject was required to TABLE 1
N Female Male Age B P.Ok
T-lobectomy
Controls
11 2 9 33 9
8 3 5 30 -
198
SHERWIN AND EFRON
I
DIGITAL LOGIC AND TIMING
SYSTEMS
TAPE RECORDER CHAN.- I CHIN.‘2
I/
~~ 1 AUDIO GATE 2
REVERSING WITCH ATTENUATOR
FIG. 1. Continuous sine wave oscillations of 3000 and 1000 Hz were prerecorded on magnetic tape. During the experiment, these signals were reproduced on the tape recorder, filtered (to increase signal to noise ratios), passed through a reversing switch to two audio gates (ICONIX 0137), and then through two attenuators to a single earphone. The opening and closing of these gates were under the control of a digital logic and timing system (ICONIX 62574010) accurate to + .Ol msec which was used to vary the stimulus onset asynchrony for each trial. Although Gates 1 and 2 were always opened and closed in the same order, the use of the reversing switch between trials enabled the experimenter to select a high-low or low-high frequency sequence. report alter each trial, which sequence he had heard. A transformed adaptive procedure (Wetherill & Levitt, 1%5) was used to determine the SOA required to achieve an 80% correct response rate. To accomplish this the SOA was reduced by one IO-msec step after three consecutive correct responses and was increased by one IO-msec step following a single incorrect response. Twenty such up-down transition values were obtained in one experimental session and the mean and standard deviation were calculated. Four such sessions were conducted, two for the right and two for the left ear. For approximately half the subjects the left ear was tested first; in the other half the right ear was tested first. TO minimize potential learning and fatigue effects, the order in which the two ears were tested was reversed in the third and fourth sessions.
RESULTS The results for each ear for each subject are shown in Table 2. For the control subjects the differences in SOA between the left and right ear were not statistically significant. All patients with a left temporal lobectomy had higher temporal order thresholds in the right ear. For subject S.D., however, this difference did not reach significance at the .Ol level. In contrast, the patients with a right temporal lobectomy had higher thresholds in their left ear except for subject D.R. who performed more
53.13
22.00
7
8
difference
27.00
6
significant
28.75 14.29 31.82 50.71 35.00
1 2 3 4 5
* Statistically
Left ear
Control subject no.
(p < .Ol).
23.00
55.00
32.78
26.88 22.50 35.50 50.00 31.67
Right ear S.J. F.J. E.R. S.D. G.G. (postop) G.G. Weep)
Left lobectomy
11.67
24.00 331.88 10.50 30.33 11.88
Left ear
*
* * *
TABLE 2 AUDITORYTHRESHOLD(MSEC)FORTEMFQRAL
7.50
39.55 373.75 18.00 33.33 23.75
Right ear
L.R. (PostoP) L.R. (preop)
D.P. A.D. T.A. O.F. D.R.
Right lobectomy
ORDERJUDGMENTS
15.00
27.78
38.13 72.22 52.19 282.50 156.82
Left ear
15.00
*
17.50
18.13 57.65 39.33 179.44 164.50
* * * *
Right ear
200
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AND EFRON
poorly with his right ear (the ear ipsilateral to his lesion). However, the difference in D.R.‘s performance with the right and left ear was not statistically significant. The results of the performance by these 11 postoperative patients indicate that an anterior temporal lobectomy elevates the threshold for correct temporal order judgments for stimuli presented to the contralateral ear. This conclusion is strongly reinforced by the results obtained on the two patients studied preoperatively. Prior to temporal lobectomy their right and left ear temporal order thresholds were not significantly different. An asymmetry in performance developed after surgery and this asymmetry was in the direction which was anticipated from the results of the other nine subjects who were tested only postoperatively. It should be noted that three patients-F.J., O.F., and D.R.-had exceptionally high thresholds in both ears, having valves similar to those patients reported by Efron (1963), Edwards and Auger (1%5), and Swisher and Hirsh (1972), all of whom had aphasia. Yet, none of these three patients had any sign of aphasia. Moreover, in two of them (O.F. and D.R.) the lobectomy was performed on the nondominant (right) side. From this we conclude that neither aphasia nor a dominant hemisphere lesion is a necessary or sufficient requirement for the exceptionally high thresholds found bilaterally. DISCUSSION The main results of these experiments reveal that anterior temporal lobectomy raised the threshold for temporal order judgments in the ear contralateral to the lesion. The fact that a unilateral temporal lobe lesion can result in a contralateral auditory deficit is not, in itself, new: Bocca, Calearo, Cassinari, and Migliavacca (1955) showed that speech discrimination is impaired, Gersuni, Batu, Karaseva, and Tonkonogii (1971) and Baru (1971) showed that temporal summation is impaired in the ear contralateral to a temporal lobe lesion. What was unexpected, however, was that such a contralateral effect could be produced by a lesion of the temporal lobe which is anterior to Heschl’s gyrus (primary auditory cortex) and did not involve any of the classical auditory association areas. However, recent anatomical studies on the monkey by Rockland and Pandya (1977) have revealed the presence of a neuronal loop connecting the ipsilateral primary visual cortex to the anterior temporal pole and probably, via the entorhinal cortex, to the hippocampus and amygdala. Closely juxtaposed to this pathway is a similar loop originating in and returning to the primary auditory cortex (D.N. Pandya, personal communication). If analogous pathways exist in man, they would surely have been compromised by the surgical excisions in these 11 patients. It seems possible that damage to such a neural system might modify auditory cortex function comparable to the way in which stimulation of the
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centrifugal (efferent) auditory control system modulates the function of lower level afferent auditory systems (See Desmedt, 1975 for review). Whether or not damage to this presumed pathway is related to the elevated contralateral threshold for auditory temporal order judgments seen in these patients, the experimental results unequivocally indicate that the anterior temporal lobe is involved in the performance of this auditory function. Whitfield (1%8) in his studies on the auditory system has suggested that “many of the anomalies in discriminative ability uncovered by ablation studies may be explicable on this basis,” i.e., in terms of damage to such efferent pathways. It would appear that elevation of the threshold for making temporal order judgments in the ear contralatera1 to an anterior temporal lobectomy may be one of the “anomalies” predicted by Whitfield. As previously indicated, the focus of the present study was to determine the effect of a temporal lobe lesion on the ipsi- and contralateral ear performance. Although the increase in the threshold for temporal order judgments in the contralateral ear was statistically significant, it was not a large effect. It was also found by Swisher and Hirsh (1972) in their group of patients with right-hemisphere lesions (size and location unspecified) but not in their group of left-hemisphere lesions all of whom had an aphasia and essentially equal elevations of threshold in both ears. Their patients with fluent aphasia had thresholds at least fourfold higher than the nonfluent aphasics whose lesions were probably located more anteriorly. The findings of Swisher and Hirsh (1972) coupled with those of the present study suggest that there may be two types of temporal-orderthreshold elevations produced by a temporal lobe lesion. In the first type (I) the deficit is a small one, is confined to the ear contralateral to the lesion, and may be found only with lesions restricted to the anterior portion of the temporal lobe. The type II deficit is a large one, is seen in equal degree in both ears, and seems to be strongly associated with more posteriorly located lesions (perhaps on the right as well as the left). The observed prevalence of the type II deficit in association with fluent aphasias may be a coincidental finding. Similarly placed lesions in the more posterior parts of the right temporal lobe are more difficult to diagnose clinically, are less likely to result in hospitalization, and thus may be under represented in the populations of right-brain-damaged subjects tested by previous investigators. A close inspection of Table 2 indicates that three of our patients (F.J., O.F., and D.R.) had both types of deficit. Their thresholds were markedly elevated in both ears, having a magnitude characteristic of the type II deficit, but, in addition, there was in two of them a small but significant contralateral (type I) deficit as well. It is not obvious why only these three subjects also displayed the type II deficit. Although the surgical lesions were essentially identical in all 11 patients, the possibility cannot be
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excluded that these 3 subjects still have a residual pathological condition in the remaining part of the affected temporal lobe-or even additional pathology in the unoperated temporal lobe. Alternatively, the use of subjects, all of whom were chronic epileptics, raises the possibility that this pathological process itself might induce a functional reorganization of the temporal lobe(s). Although the type II deficit was also noted by others in their subjects with nonepileptogenic lesions it is appropriate to excercise some caution in inferring from our results the role played by the anterior temporal lobe in the normal brain. Consonant with our findings and those of others (supravide) it is possible that the small contralateral effect (type I) may be explicable in terms of the neuroanatomical and electrophysiological mechanisms already discussed. However, these essentially unilateral mechanisms do not seem to provide an adequate explanation for the large type II deficits which involve both ears. Interestingly, based on recent anatomical studies, Van Hoesen, Rosene, and Mesulam (1979) have suggested that the integrity of the anterior temporal lobe, in particular the subicular cortex, “may be essential for many complex mental processes.” Before a full explanation can be offered more information will be required. In particular, it may be useful to determine if increasing the task difficulty in some nontemporal respect (e.g., by decreasing the frequency difference of the two tones or by adding noise) changes the temporal order thresholds differently in brain-damaged, compared to normal, subjects. REFERENCES Baru, A.V. 1971. Absolute thresholds and frequency difference limens as a function of sound duration in dogs deprived of the auditory cortex. In G. V. Gersuni (Ed.), Sensory processes at the neuronal and behavioral levels. New York: Academic Press. Pp. 265-286. Bocca, E., Calearo, C., Cassinari, V., & Migliavacca, F. 1955.Testing “cortical” hearing in temporal lobe tumors. Acta Oto-Laryngologica 45, 289-304. Carmon, A., & Nachsohn, I. 1971. Effect of unilateral brain damage on perception of temporal order. Cortex, 7, 410-418. Desmedt, J. E. 1975. Physiological studies of the efferent recurrent auditory system. In W. D. Keidel and W. D. Neff (Eds.), Handbook ofsensory physiology. Berlin: SpringerVerlag. Vol. V/2, pp. 219-246. Edwards, A. E., & Auger, R. 1%5. The effect of aphasia on the perception of precedence. In Proc. 73rd Annu. Co& Amer. Psychol. Assoc. Amer. Psychol. Assoc., Washington, D.C. Pp. 207-208. Efron, R. 1%3. Temporal perception, aphasia and deja vu. Brain, 86, 403-424. Gersuni, G. V., Baru, A. V., Karaseva, T. A., & Tonkonogii, I. M. 1971.Effects of temporal lobe lesions on perception of sounds of short duration. In G. V. Gersuni (Ed.), Sensory processes at the neuronal and behavioral levels. New York: Academic Press. Pp. 287-300. Holmes, H. 1%5. Disordered perception of auditory sequences in aphasia. PhD Thesis, Harvard University. Rockland, K. 8, & Pandya, D. N. 1977. Some observations on laminar origins and terminations of occipito-temporal cortical connections in rhesus monkey. Neuroscience Abstracts, 3, 211.
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Sherwin, I. 1977. Clinical and EEG Aspects of temporal lobe epilepsy with behavior disorder, the role of cerebral dominance. McLean Hospital Journal, Special Issue (June), 40-50. Swisher, L., and Hirsh, I. J. 1972. Brain damage and the ordering of two temporally successive stimuli. Neurophsychologia, 10, 137-152. Van Hoesen, G. W., Rosene, D. L., & Mesulam, M. M. 1979.Subicularinput from temporal cortex in the rhesus monkey. Science, 205, 608-610. Wetherill, G. B., & Levitt, H. 1965. Sequential estimation of points on a psychometric function. British Journal of Mathematical and Statistical Psychology, 18, l-10. Whitheld, I. D. 1968. Centrifugal control mechanisms of the auditory pathway. In A. V. S. Dereuck & J. Knight (Eds.), Hearing mechanisms in vertebrates: A Ciba symposium. Boston: Little, Brown. Pp. 246-254.