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Memory reorganization in adult brain: observations in three patients with temporal lobe epilepsy
Epilepsy Research 48 (2002) 229– 234 www.elsevier.com/locate/epilepsyres
Short communication
Memory reorganization in adult brain: observations in three patients with temporal lobe epilepsy Ulrike Gleissner *, Christoph Helmstaedter, Christian Erich Elger Uni6ersity Hospital of Epileptology, Sigmund-Frued Str. 25, 53105, Bonn, Germany Received 10 August 2001; received in revised form 1 November 2001; accepted 5 November 2001
Abstract We present three patients with left-sided temporal lobe epilepsy who exhibited preoperatively a neuropsychological pattern characteristic for interhemispheric language transfer (marked nonverbal memory deficits, relatively preserved verbal memory and language performance). The Wada test indicated atypical language dominance in two patients, but one patient was clearly left hemispheric language dominant. All patients showed a marked recovery of nonverbal memory after left-sided surgery. Results are discussed with respect to memory transfer and plasticity for memory functions in the adult brain. © 2002 Elsevier Science B.V. All rights reserved. Keywords: Memory; Reorganization; Temporal lobe epilepsy; Plasticity
1. Introduction Patients with a left temporal epilepsy usually exhibit impairments in verbal memory functions (e.g. Hermann et al., 1994). In patients with early acute left hemispheric injury a shift of language functions to the uninjured right hemisphere may occur with a concomitant decrease in visuospatial abilities for which the right hemisphere is typically dominant (Teuber, 1974; Strauss et al., 1990). Sass et al. (1995) reported evidence that in such
* Corresponding author. Tel.: + 49-228-287-4436; fax: + 49-228-287-6294. E-mail address: [email protected] (U. Gleissner).
patients the right hemisphere is mediating verbal memory as well as speech. We present three patients, who underwent a left-sided temporal lobe surgery to control a medically intractable epilepsy. The preoperative cognitive pattern in our patients (extreme nonverbal memory deficits, relatively preserved verbal memory) suggested a language transfer, and in two of the three patients the intracarotid amytal test (IAT) indicated atypical cerebral language dominance. Postoperatively, all patients strikingly recovered in nonverbal memory and showed some decline in verbal memory. We provide detailed descriptions and discuss possible mechanisms of this extraordinary pattern. We propose, that the patterns raise questions about plasticity in the adult brain and about the possibility of a pure memory shift.
0920-1211/02/$ - see front matter © 2002 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 0 - 1 2 1 1 ( 0 1 ) 0 0 3 3 3 - 3
U. Gleissner et al. / Epilepsy Research 48 (2002) 229–234
230
2. Methods About 5% of our left temporal lobe resected patients show the described pre- to postoperative memory pattern in our clinical sample. The three patients were selected because of the completeness of their data (several postoperative follow-ups, IAT). Patient characteristics are provided in Table 1. Preoperative diagnostics included high resolution magnetic resonance imaging (MRI), electroencephalography surface recordings, and seizure semiology in all patients. Additional diagnostics included recordings with sphenoidal electrodes, magnetoencephalography, and single-photon emission computed tomography in AB, intrahippocampal depth electrodes in KR and positron emission tomography in SK. The IAT procedure is described in detail by Kurthen et al. (1994). Hand dominance was assessed according to Oldfield (1971). Preoperative global intellectual functioning was estimated by a vocabulary test (Lehrl, 1978). Verbal and nonverbal memory were assessed with serial learning tasks (VLMT, Helmstaedter et
al., 2000; DCS-R, Helmstaedter et al., 1991; parallel versions postoperatively), which have been proven to be sensitive to left, respectively, right temporal lobe dysfunctions (Helmstaedter et al., 1997; Gleissner et al., 1998). Parameters of interest were learning capacity (correctly reproduced words in trial one to five), loss in delayed free recall (trial seven to trial five), and recognition performance (adjusted for mistakes) for the VLMT, and learning capacity (correctly reconstructed figures in six consecutive trials) and the number of correct reproductions in the last trial for the DCS-R. Further tests were a letter cancellation test as a measure of psychomotor speed (Brickenkamp, 1978), a numerical and a visuospatial memory span task (Milner, 1971; Tewes, 1991), phonemic fluency (Horn, 1983), the Token Test (Orgass, 1982), and a finger oscillation test. Preoperative results were judged according to norm data provided in the manuals. The significance of individual postoperative changes was judged using reliable change indices (RCIs) according to the proposals of Hermann et al. (1996). RCI provides an index of significant and reliable
Table 1 Patient characteristics Patient characteristics
AB
KR
SK
Gender Age at onset of epilepsy Age at surgery Surgical treatment Side of surgery Pathology
Female 1
Female 14
Female 1
31 Anterior TLR
44 SAH
27 TLR+MST frontal/central
Left AHS+mild cortical atrophy Brain contusion
Left AHS
Left Porencephalic cyst
Prolonged febrile seizure
Perinatal infarction of the middle cerebral artery 150 SPS/m
Bilateral
20 SPS/m, 4 CPS/m, 1 SGS in 2 years Left
Right
Right 91
Right 107
Left (right-sided hemiparesis) 100
Etiological factors Seizure type (frequency) IAT language dominance Hand dominance IQestimated
5–15 CPS/m
SAH, selective amygdalo-hippocampectomy; TLR, temporal lobe resection; MST, multiple subpial transections; AHS, Ammon’s horn sclerosis; CPS, complex partial seizure; SPS, simple partial seizure; SGS, secondary generalized seizure; m, month; IAT, intracarotid amytal test.
U. Gleissner et al. / Epilepsy Research 48 (2002) 229–234
alteration in test performance, a change that cannot be attributed to common sources of measurement error inherent in test– retest designs (e.g. practice effects, regression to the mean). Individual changes were classified as being worse or improved if they exceeded the 90% confidence intervals for the before and after difference scores derived from 85 patients with focal epilepsy who were on the waiting list for epilepsy surgery and had been tested twice (mean retest interval 11.6 months).
231
Verbal learning and recognition performance were significantly declined. SK was seizure free until 6 months after surgery. Then valproic acid and later phenobarbital was reduced and both times SK reacted with seizures. Her verbal learning had significantly declined 3 months after surgery, but matched then again the preoperative level. A similar development was evident in phonemic fluency. Finger oscillation of her left hand was significantly improved 1 year after surgery. Three years after surgery, SK presented mild deficits in verbal learning, memory span, comprehension, and speed.
3. Results 4. Discussion Preoperative results indicated strongly reduced nonverbal memory performance (\2 S.D. below the mean) and slightly impaired verbal memory functions in all patients (Table 2). Phonemic fluency was below average in all patients. Digit span was below average in KR and SK. Finger oscillation was below average in AB and SK. Psychomotor speed was reduced in KR. All other functions were within the average range. These neuropsychological profiles were atypical for a left-sided lesion and were interpreted as an indicator for a language shift. Given KR’s left-sided language dominance, her neuropsychological results were interpreted as bitemporal dysfunctions emphasized for the right side thus entailing a high risk for postoperative memory declines. Postoperatively, all patients significantly improved in nonverbal memory. These improvements were stable or even increasing, only KR showed some fluctuations in covariance with the seizure situation. Three months after surgery she had no seizures, and verbal delayed recall was significantly deteriorated. One year after surgery, she had one aura and a secondary generalized seizure, and verbal delayed recall had slightly recovered. Nonverbal memory was now below average, but as a tendency still better than before surgery. Performance declines were evident in immediate memory span and finger oscillation of her right hand. AB had a complete seizure release (Engel Outcome Class I). Follow-ups 3 months and 1 year after surgery indicated improvements also in psychomotor speed, finger oscillation, and phonemic fluency.
The preoperative neuropsychological pattern is particularly interesting in the patient KR because it can not be explained by atypical cerebral language dominance. Some studies suggested that reorganization of memory functions can lead to an interhemispheric dissociation between verbal memory and speech functions. Jokeit et al. (1996), Jokeit and Markowitsch (1999) concluded from IAT data in patients with temporal lobe epilepsy that a pure interhemispheric reorganization of episodic memory can occur. Wood et al. (1999) presented a 19 years old woman with a pattern very similar to KR as evidence for a pure verbal memory transfer. They mentioned that 15% of their patients with left hippocampal sclerosis had a similar neurocognitive pattern. Accordingly, the preoperative pattern in KR could be the result of an interhemispheric reorganization exclusively of verbal memory functions not involving language functions. Concerning her postoperative results, we pointed out that KR had as a left cerebral language dominant patient a high risk for postoperative amnesia. However, KR was not amnesic after surgery. A case with a very similar pattern regarding the pre- and postoperative development has been presented by Henke and Wieser (1996). The combination of reduced nonverbal memory together with relatively unimpaired verbal memory in a patient with left hemispheric language dominance could hence indicate a pure memory transfer and should, therefore, not necessarily be considered a contraindication for surgery.
46 −5 8
5 1 36* −4 3
19* 8* 36* −6 −3*
38* 9* 39/42 −1/0 14/12
7/13 1/3 40 −5* 12
26* 7*
3 MP
41 −3 12
19 4
12 MP
46 −4 15
8 2
Pre
SK
36* −2 13
26* 6*
3 MP
46 −5 12
22* 5*
12 MP
47 −1 11
40* 9*
36 MP
5697.6 1.19 1.8 13.9 9 1.5
35 910 7.5 91.7
Average range
−8.2/12.7 −3.7/3.1 −6.1/4.9
−11/11 −2/2.4
C.I. for a change
Pre- and postoperative memory results are listed for each patient (AB, KR, SK). KR was preoperatively tested twice. The average range and the 90% confidence interval (C.I.) for a change are given for each parameter. *, significant pre- versus postoperative change; pre, preoperative, MP, months postoperative.
Verbal memory Learning Loss in delayed recall Recognition (-failures)
Non6erbal memory Learning Recall in last trial
Pre
12 MP
Pre
3 MP
KR
AB
Table 2 Pre- and postoperative memory results
232 U. Gleissner et al. / Epilepsy Research 48 (2002) 229–234
U. Gleissner et al. / Epilepsy Research 48 (2002) 229–234
The postoperative increase of nonverbal memory ( + 1.5–3 S.D.) in all patients exceeded a normal release of contralateral functions due to seizure control or retest effects. The postoperative neuropsychological pattern is particularly interesting in the atypically language dominant patients. Their postoperative profiles had been now in agreement with a left-sided lesion, if they had a left hemispheric language dominance. A repetition of the IAT would be desirable, but can not be performed without a clinical indication because of the risk for the patient. Valid identification of atypical language dominance patterns by fMRI was not available at that time. In any case, the observed postoperative dynamics in nonverbal memory suggest a considerable plasticity in the adult brain. The distinctness of the pre- and postoperative cognitive patterns suggests a functional reorganization of memory functions taking place within a relatively short period. All our patients were clearly beyond adolescence. Thus, our results do not support the assumption, that an age between 5 and 16 years is the critical cut-off for cerebral reorganization processes to occur (Rausch et al., 1991; Jokeit and Markowitsch, 1999). Recently, substantial reorganization of the primary somatosensory cortex subsequent to amputation or chronic pain has been demonstrated in human adults (e.g. Flor et al., 1995). Therapeutically induced reversal of this reorganization, e.g. by stump anesthesia seems to be possible even decades after the original reorganization also in adults (Birbaumer et al., 1997). Our results suggest, that similar plasticity may exist in the adult brain also for higher cognitive functions. It may be relevant for a functional system if the system is simply lesioned or if it is additionally disturbed by epileptic activity. In the field of phantom-limb pain research, Spitzer (1997) has suggested that noisy inputs, e.g. from stump neuroma, cause the reorganizational changes. Ictal and interictal epileptic activity could act in a similar manner in patients with epilepsy. At least, in patient KR the postoperative cognitive development showed fluctuations in covariance with the seizure situation. A memory transfer could be understood in this context as a transitory adoption or activation of preexisting functional capacities sustained by epileptic activity.
233
Several questions remain to be answered. Why do only some patients show this pattern? What exactly constitutes a functional transfer? Although we can not explain everything about these cases we feel that they need an explanation and hope to stimulate a discussion.
References Birbaumer, N., Lutzenberger, W., Montoya, P., Larbig, W., Unertl, K., Topfner, S., Grodd, W., Taub, E., Flor, H., 1997. Effects of regional anesthesia on phantom limb pain are mirrored in changes in cortical reorganization. J. Neurosci. 17, 5503 – 5508. Brickenkamp, R., 1978. Test d2 Aufmerksamkeits-BelastungsTest. Hogrefe, Go¨ ttingen. Flor, H., Elbert, T., Knecht, S., Wienbruch, C., Pantev, C., Birbaumer, N., Larbig, W., Taub, E., 1995. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 375, 482 – 484. Gleissner, U., Helmstaedter, C., Elger, C.E., 1998. Right hippocampal contribution to visual memory: a presurgical and postsurgical study in patients with temporal lobe epilepsy. J. Neurol. Neurosurg. Psychiatry 65, 665 – 669. Helmstaedter, C., Pohl, C., Elger, C.E., 1991. Eine modifizierte version des Diagnostikums fu¨ r Cerebralscha¨ den (DCS) zur Diagnostik ra¨ umlich-visueller Geda¨ chtnisdefizite bei Patienten mit Temporallappenepilepsie. In: Scheffner, D. (Ed.), Epilepsie 90. Einhorn-Presse, Reinbeck, pp. 272 – 279. Helmstaedter, C., Lehnertz, K., Grunwald, T., Gleißner, U., Elger, C.E., 1997. Differential involvement of left temporolateral and temporo-mesial structures in verbal declarative learning and memory: evidence from temporal lobe epilepsy. Brain Cogn. 35, 110 – 131. Helmstaedter, C., Lendt, M., Lux, S., 2000. VLMT: Verbaler Lern-und Merkfa¨ higkeitstest, Testhandbuch. Hogrefe, Go¨ ttingen. Henke, K., Wieser, H.G., 1996. Bilateral medial temporal lobe damage without amnesic syndrome: a case report. Epilepsy Res. 24, 147 – 161. Hermann, B.P., Wyler, A.R., Somes, G., Dohan, F.C. Jr, Berry, A.D. III, Clement, L., 1994. Declarative memory following anterior temporal lobectomy in humans. Behav. Neurosci. 108, 3 – 10. Hermann, B.P., Seidenberg, M., Schoenfeld, J., Peterson, J., Leveroni, C., Wyler, A.R., 1996. Empirical techniques for determining the reliability, magnitude, and pattern of neuropsychological change after epilepsy surgery. Epilepsia 36, 942 – 950. Horn, W., 1983. Leistungspru¨ fsystem L-P-S. Hogrefe, Go¨ ttingen. Jokeit, H., Ebner, A., Holthausen, H., Markowitsch, H.J., Tuxhorn, I., 1996. Reorganization of memory functions
234
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after human temporal lobe damage. Neuroreport 7, 1627 – 1630. Jokeit, H., Markowitsch, H.J., 1999. Aging limits plasticity of episodic memory functions in response to left temporal lobe damage in patients with epilepsy. Adv. Neurol. 81, 251– 258. Kurthen, M., Helmstaedter, C., Linke, D.B., Hufnagel, A., Elger, C.E., Schramm, J., 1994. Quantitative and qualitative evaluation of patterns of cerebral language dominance. An Amobarbital study. Brain Lang. 46, 536 –564. Lehrl, S., 1978. Mehrfachwahl-Wortschatz-Intelligenztest MWT-B. Verlag Dr.med.Straube, Erlangen. Milner, B., 1971. Interhemispheric differences in the localization of psychological processes in man. Br. Med. Bull. 27, 272 – 277. Oldfield, R.C., 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 79. Orgass, B., 1982. Token Test, Manual. Beltz Test, Weinheim. Rausch, R., Boone, K., Ary, C.M., 1991. Right-hemisphere language dominance in temporal lobe epilepsy: clinical and neuropsychological correlates. J. Clin. Exp. Neuropsychol. 13, 217 – 231.
Sass, K.J., Silberfein, C.M., Platis, I., Westerveld, M., Buchanan, C.P., Delaney, R.C., Kim, J.H., Spencer, D.D., 1995. Right hemisphere mediation of verbal learning and memory in acquired right hemisphere speech dominant patients. J. Int. Neuropsychol. Soc. 1, 554 – 560. Spitzer, M., 1997. Noise-driven neuroplasticity in self-organizing feature maps: a neurocomputational model of phantom limbs. MD Comput. 14, 192 – 199. Strauss, E., Satz, P., Wada, J., 1990. An examination of the crowding hypothesis in epileptic patients who have undergone the carotid amytal test. Neuropsychologia 28, 1221 – 1227. Teuber, H.L., 1974. Why two brains. In: Schmitt, F.O., Worden, F.G. (Eds.), The Neurosciences. Third Study Program. MIT, Cambridge, pp. 71 – 74. Tewes, U., 1991. HAWIE-R: Hamburg-Wechsler Intelligenztest fu¨ r Erwachsene; Handbuch und Testanweisung. Huber, Bern. Wood, A.G., Saling, M.M., O’Shea, M.F., Jackson, G.D., Berkovic, S.F., 1999. Reorganization of verbal memory and language: a case of dissociation. J. Int. Neuropsychol. Soc. 5, 69 – 74.
Short communication
Memory reorganization in adult brain: observations in three patients with temporal lobe epilepsy Ulrike Gleissner *, Christoph Helmstaedter, Christian Erich Elger Uni6ersity Hospital of Epileptology, Sigmund-Frued Str. 25, 53105, Bonn, Germany Received 10 August 2001; received in revised form 1 November 2001; accepted 5 November 2001
Abstract We present three patients with left-sided temporal lobe epilepsy who exhibited preoperatively a neuropsychological pattern characteristic for interhemispheric language transfer (marked nonverbal memory deficits, relatively preserved verbal memory and language performance). The Wada test indicated atypical language dominance in two patients, but one patient was clearly left hemispheric language dominant. All patients showed a marked recovery of nonverbal memory after left-sided surgery. Results are discussed with respect to memory transfer and plasticity for memory functions in the adult brain. © 2002 Elsevier Science B.V. All rights reserved. Keywords: Memory; Reorganization; Temporal lobe epilepsy; Plasticity
1. Introduction Patients with a left temporal epilepsy usually exhibit impairments in verbal memory functions (e.g. Hermann et al., 1994). In patients with early acute left hemispheric injury a shift of language functions to the uninjured right hemisphere may occur with a concomitant decrease in visuospatial abilities for which the right hemisphere is typically dominant (Teuber, 1974; Strauss et al., 1990). Sass et al. (1995) reported evidence that in such
* Corresponding author. Tel.: + 49-228-287-4436; fax: + 49-228-287-6294. E-mail address: [email protected] (U. Gleissner).
patients the right hemisphere is mediating verbal memory as well as speech. We present three patients, who underwent a left-sided temporal lobe surgery to control a medically intractable epilepsy. The preoperative cognitive pattern in our patients (extreme nonverbal memory deficits, relatively preserved verbal memory) suggested a language transfer, and in two of the three patients the intracarotid amytal test (IAT) indicated atypical cerebral language dominance. Postoperatively, all patients strikingly recovered in nonverbal memory and showed some decline in verbal memory. We provide detailed descriptions and discuss possible mechanisms of this extraordinary pattern. We propose, that the patterns raise questions about plasticity in the adult brain and about the possibility of a pure memory shift.
0920-1211/02/$ - see front matter © 2002 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 0 - 1 2 1 1 ( 0 1 ) 0 0 3 3 3 - 3
U. Gleissner et al. / Epilepsy Research 48 (2002) 229–234
230
2. Methods About 5% of our left temporal lobe resected patients show the described pre- to postoperative memory pattern in our clinical sample. The three patients were selected because of the completeness of their data (several postoperative follow-ups, IAT). Patient characteristics are provided in Table 1. Preoperative diagnostics included high resolution magnetic resonance imaging (MRI), electroencephalography surface recordings, and seizure semiology in all patients. Additional diagnostics included recordings with sphenoidal electrodes, magnetoencephalography, and single-photon emission computed tomography in AB, intrahippocampal depth electrodes in KR and positron emission tomography in SK. The IAT procedure is described in detail by Kurthen et al. (1994). Hand dominance was assessed according to Oldfield (1971). Preoperative global intellectual functioning was estimated by a vocabulary test (Lehrl, 1978). Verbal and nonverbal memory were assessed with serial learning tasks (VLMT, Helmstaedter et
al., 2000; DCS-R, Helmstaedter et al., 1991; parallel versions postoperatively), which have been proven to be sensitive to left, respectively, right temporal lobe dysfunctions (Helmstaedter et al., 1997; Gleissner et al., 1998). Parameters of interest were learning capacity (correctly reproduced words in trial one to five), loss in delayed free recall (trial seven to trial five), and recognition performance (adjusted for mistakes) for the VLMT, and learning capacity (correctly reconstructed figures in six consecutive trials) and the number of correct reproductions in the last trial for the DCS-R. Further tests were a letter cancellation test as a measure of psychomotor speed (Brickenkamp, 1978), a numerical and a visuospatial memory span task (Milner, 1971; Tewes, 1991), phonemic fluency (Horn, 1983), the Token Test (Orgass, 1982), and a finger oscillation test. Preoperative results were judged according to norm data provided in the manuals. The significance of individual postoperative changes was judged using reliable change indices (RCIs) according to the proposals of Hermann et al. (1996). RCI provides an index of significant and reliable
Table 1 Patient characteristics Patient characteristics
AB
KR
SK
Gender Age at onset of epilepsy Age at surgery Surgical treatment Side of surgery Pathology
Female 1
Female 14
Female 1
31 Anterior TLR
44 SAH
27 TLR+MST frontal/central
Left AHS+mild cortical atrophy Brain contusion
Left AHS
Left Porencephalic cyst
Prolonged febrile seizure
Perinatal infarction of the middle cerebral artery 150 SPS/m
Bilateral
20 SPS/m, 4 CPS/m, 1 SGS in 2 years Left
Right
Right 91
Right 107
Left (right-sided hemiparesis) 100
Etiological factors Seizure type (frequency) IAT language dominance Hand dominance IQestimated
5–15 CPS/m
SAH, selective amygdalo-hippocampectomy; TLR, temporal lobe resection; MST, multiple subpial transections; AHS, Ammon’s horn sclerosis; CPS, complex partial seizure; SPS, simple partial seizure; SGS, secondary generalized seizure; m, month; IAT, intracarotid amytal test.
U. Gleissner et al. / Epilepsy Research 48 (2002) 229–234
alteration in test performance, a change that cannot be attributed to common sources of measurement error inherent in test– retest designs (e.g. practice effects, regression to the mean). Individual changes were classified as being worse or improved if they exceeded the 90% confidence intervals for the before and after difference scores derived from 85 patients with focal epilepsy who were on the waiting list for epilepsy surgery and had been tested twice (mean retest interval 11.6 months).
231
Verbal learning and recognition performance were significantly declined. SK was seizure free until 6 months after surgery. Then valproic acid and later phenobarbital was reduced and both times SK reacted with seizures. Her verbal learning had significantly declined 3 months after surgery, but matched then again the preoperative level. A similar development was evident in phonemic fluency. Finger oscillation of her left hand was significantly improved 1 year after surgery. Three years after surgery, SK presented mild deficits in verbal learning, memory span, comprehension, and speed.
3. Results 4. Discussion Preoperative results indicated strongly reduced nonverbal memory performance (\2 S.D. below the mean) and slightly impaired verbal memory functions in all patients (Table 2). Phonemic fluency was below average in all patients. Digit span was below average in KR and SK. Finger oscillation was below average in AB and SK. Psychomotor speed was reduced in KR. All other functions were within the average range. These neuropsychological profiles were atypical for a left-sided lesion and were interpreted as an indicator for a language shift. Given KR’s left-sided language dominance, her neuropsychological results were interpreted as bitemporal dysfunctions emphasized for the right side thus entailing a high risk for postoperative memory declines. Postoperatively, all patients significantly improved in nonverbal memory. These improvements were stable or even increasing, only KR showed some fluctuations in covariance with the seizure situation. Three months after surgery she had no seizures, and verbal delayed recall was significantly deteriorated. One year after surgery, she had one aura and a secondary generalized seizure, and verbal delayed recall had slightly recovered. Nonverbal memory was now below average, but as a tendency still better than before surgery. Performance declines were evident in immediate memory span and finger oscillation of her right hand. AB had a complete seizure release (Engel Outcome Class I). Follow-ups 3 months and 1 year after surgery indicated improvements also in psychomotor speed, finger oscillation, and phonemic fluency.
The preoperative neuropsychological pattern is particularly interesting in the patient KR because it can not be explained by atypical cerebral language dominance. Some studies suggested that reorganization of memory functions can lead to an interhemispheric dissociation between verbal memory and speech functions. Jokeit et al. (1996), Jokeit and Markowitsch (1999) concluded from IAT data in patients with temporal lobe epilepsy that a pure interhemispheric reorganization of episodic memory can occur. Wood et al. (1999) presented a 19 years old woman with a pattern very similar to KR as evidence for a pure verbal memory transfer. They mentioned that 15% of their patients with left hippocampal sclerosis had a similar neurocognitive pattern. Accordingly, the preoperative pattern in KR could be the result of an interhemispheric reorganization exclusively of verbal memory functions not involving language functions. Concerning her postoperative results, we pointed out that KR had as a left cerebral language dominant patient a high risk for postoperative amnesia. However, KR was not amnesic after surgery. A case with a very similar pattern regarding the pre- and postoperative development has been presented by Henke and Wieser (1996). The combination of reduced nonverbal memory together with relatively unimpaired verbal memory in a patient with left hemispheric language dominance could hence indicate a pure memory transfer and should, therefore, not necessarily be considered a contraindication for surgery.
46 −5 8
5 1 36* −4 3
19* 8* 36* −6 −3*
38* 9* 39/42 −1/0 14/12
7/13 1/3 40 −5* 12
26* 7*
3 MP
41 −3 12
19 4
12 MP
46 −4 15
8 2
Pre
SK
36* −2 13
26* 6*
3 MP
46 −5 12
22* 5*
12 MP
47 −1 11
40* 9*
36 MP
5697.6 1.19 1.8 13.9 9 1.5
35 910 7.5 91.7
Average range
−8.2/12.7 −3.7/3.1 −6.1/4.9
−11/11 −2/2.4
C.I. for a change
Pre- and postoperative memory results are listed for each patient (AB, KR, SK). KR was preoperatively tested twice. The average range and the 90% confidence interval (C.I.) for a change are given for each parameter. *, significant pre- versus postoperative change; pre, preoperative, MP, months postoperative.
Verbal memory Learning Loss in delayed recall Recognition (-failures)
Non6erbal memory Learning Recall in last trial
Pre
12 MP
Pre
3 MP
KR
AB
Table 2 Pre- and postoperative memory results
232 U. Gleissner et al. / Epilepsy Research 48 (2002) 229–234
U. Gleissner et al. / Epilepsy Research 48 (2002) 229–234
The postoperative increase of nonverbal memory ( + 1.5–3 S.D.) in all patients exceeded a normal release of contralateral functions due to seizure control or retest effects. The postoperative neuropsychological pattern is particularly interesting in the atypically language dominant patients. Their postoperative profiles had been now in agreement with a left-sided lesion, if they had a left hemispheric language dominance. A repetition of the IAT would be desirable, but can not be performed without a clinical indication because of the risk for the patient. Valid identification of atypical language dominance patterns by fMRI was not available at that time. In any case, the observed postoperative dynamics in nonverbal memory suggest a considerable plasticity in the adult brain. The distinctness of the pre- and postoperative cognitive patterns suggests a functional reorganization of memory functions taking place within a relatively short period. All our patients were clearly beyond adolescence. Thus, our results do not support the assumption, that an age between 5 and 16 years is the critical cut-off for cerebral reorganization processes to occur (Rausch et al., 1991; Jokeit and Markowitsch, 1999). Recently, substantial reorganization of the primary somatosensory cortex subsequent to amputation or chronic pain has been demonstrated in human adults (e.g. Flor et al., 1995). Therapeutically induced reversal of this reorganization, e.g. by stump anesthesia seems to be possible even decades after the original reorganization also in adults (Birbaumer et al., 1997). Our results suggest, that similar plasticity may exist in the adult brain also for higher cognitive functions. It may be relevant for a functional system if the system is simply lesioned or if it is additionally disturbed by epileptic activity. In the field of phantom-limb pain research, Spitzer (1997) has suggested that noisy inputs, e.g. from stump neuroma, cause the reorganizational changes. Ictal and interictal epileptic activity could act in a similar manner in patients with epilepsy. At least, in patient KR the postoperative cognitive development showed fluctuations in covariance with the seizure situation. A memory transfer could be understood in this context as a transitory adoption or activation of preexisting functional capacities sustained by epileptic activity.
233
Several questions remain to be answered. Why do only some patients show this pattern? What exactly constitutes a functional transfer? Although we can not explain everything about these cases we feel that they need an explanation and hope to stimulate a discussion.
References Birbaumer, N., Lutzenberger, W., Montoya, P., Larbig, W., Unertl, K., Topfner, S., Grodd, W., Taub, E., Flor, H., 1997. Effects of regional anesthesia on phantom limb pain are mirrored in changes in cortical reorganization. J. Neurosci. 17, 5503 – 5508. Brickenkamp, R., 1978. Test d2 Aufmerksamkeits-BelastungsTest. Hogrefe, Go¨ ttingen. Flor, H., Elbert, T., Knecht, S., Wienbruch, C., Pantev, C., Birbaumer, N., Larbig, W., Taub, E., 1995. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 375, 482 – 484. Gleissner, U., Helmstaedter, C., Elger, C.E., 1998. Right hippocampal contribution to visual memory: a presurgical and postsurgical study in patients with temporal lobe epilepsy. J. Neurol. Neurosurg. Psychiatry 65, 665 – 669. Helmstaedter, C., Pohl, C., Elger, C.E., 1991. Eine modifizierte version des Diagnostikums fu¨ r Cerebralscha¨ den (DCS) zur Diagnostik ra¨ umlich-visueller Geda¨ chtnisdefizite bei Patienten mit Temporallappenepilepsie. In: Scheffner, D. (Ed.), Epilepsie 90. Einhorn-Presse, Reinbeck, pp. 272 – 279. Helmstaedter, C., Lehnertz, K., Grunwald, T., Gleißner, U., Elger, C.E., 1997. Differential involvement of left temporolateral and temporo-mesial structures in verbal declarative learning and memory: evidence from temporal lobe epilepsy. Brain Cogn. 35, 110 – 131. Helmstaedter, C., Lendt, M., Lux, S., 2000. VLMT: Verbaler Lern-und Merkfa¨ higkeitstest, Testhandbuch. Hogrefe, Go¨ ttingen. Henke, K., Wieser, H.G., 1996. Bilateral medial temporal lobe damage without amnesic syndrome: a case report. Epilepsy Res. 24, 147 – 161. Hermann, B.P., Wyler, A.R., Somes, G., Dohan, F.C. Jr, Berry, A.D. III, Clement, L., 1994. Declarative memory following anterior temporal lobectomy in humans. Behav. Neurosci. 108, 3 – 10. Hermann, B.P., Seidenberg, M., Schoenfeld, J., Peterson, J., Leveroni, C., Wyler, A.R., 1996. Empirical techniques for determining the reliability, magnitude, and pattern of neuropsychological change after epilepsy surgery. Epilepsia 36, 942 – 950. Horn, W., 1983. Leistungspru¨ fsystem L-P-S. Hogrefe, Go¨ ttingen. Jokeit, H., Ebner, A., Holthausen, H., Markowitsch, H.J., Tuxhorn, I., 1996. Reorganization of memory functions
234
U. Gleissner et al. / Epilepsy Research 48 (2002) 229–234
after human temporal lobe damage. Neuroreport 7, 1627 – 1630. Jokeit, H., Markowitsch, H.J., 1999. Aging limits plasticity of episodic memory functions in response to left temporal lobe damage in patients with epilepsy. Adv. Neurol. 81, 251– 258. Kurthen, M., Helmstaedter, C., Linke, D.B., Hufnagel, A., Elger, C.E., Schramm, J., 1994. Quantitative and qualitative evaluation of patterns of cerebral language dominance. An Amobarbital study. Brain Lang. 46, 536 –564. Lehrl, S., 1978. Mehrfachwahl-Wortschatz-Intelligenztest MWT-B. Verlag Dr.med.Straube, Erlangen. Milner, B., 1971. Interhemispheric differences in the localization of psychological processes in man. Br. Med. Bull. 27, 272 – 277. Oldfield, R.C., 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 79. Orgass, B., 1982. Token Test, Manual. Beltz Test, Weinheim. Rausch, R., Boone, K., Ary, C.M., 1991. Right-hemisphere language dominance in temporal lobe epilepsy: clinical and neuropsychological correlates. J. Clin. Exp. Neuropsychol. 13, 217 – 231.
Sass, K.J., Silberfein, C.M., Platis, I., Westerveld, M., Buchanan, C.P., Delaney, R.C., Kim, J.H., Spencer, D.D., 1995. Right hemisphere mediation of verbal learning and memory in acquired right hemisphere speech dominant patients. J. Int. Neuropsychol. Soc. 1, 554 – 560. Spitzer, M., 1997. Noise-driven neuroplasticity in self-organizing feature maps: a neurocomputational model of phantom limbs. MD Comput. 14, 192 – 199. Strauss, E., Satz, P., Wada, J., 1990. An examination of the crowding hypothesis in epileptic patients who have undergone the carotid amytal test. Neuropsychologia 28, 1221 – 1227. Teuber, H.L., 1974. Why two brains. In: Schmitt, F.O., Worden, F.G. (Eds.), The Neurosciences. Third Study Program. MIT, Cambridge, pp. 71 – 74. Tewes, U., 1991. HAWIE-R: Hamburg-Wechsler Intelligenztest fu¨ r Erwachsene; Handbuch und Testanweisung. Huber, Bern. Wood, A.G., Saling, M.M., O’Shea, M.F., Jackson, G.D., Berkovic, S.F., 1999. Reorganization of verbal memory and language: a case of dissociation. J. Int. Neuropsychol. Soc. 5, 69 – 74.