@Pergamon

Neuropsychdogia, V 3 N 1 p 1 1C ~ 1 E S L A r r

P S 0 0l P i G B0 $

Lateralization of memorythe intracarotidsodium

P M P LJ I B J

for music:Evidencefromamobarbitalprocedure

W W ~ T D R [A C P A PB B RA T V C

a L J W

F t D e po T N e$ P$ NT C oE P U o TM eS cH oT U S A a l lH R eH T U

(Received 28 July 1995;accepted 20 October 1995)

Abstract-The presentstudywasconductedto determinewhethermaterial-specificmemoryforunfamiliartonalpatternscouldbedemonstratedfortherighttemporallobeduringtheintracarotidsodiumamytalprocedure( T p w ic op as ea sw e l t el e ( o r t l e ( ua s so m ef t p ad a b ap a r a l c h a d t IP aw p ru nt p aw w l s f a s o d p F i tt w n d ib et L a R p ad i o t r c h s n si n vo l m t es tH oa s ie w n d l i w t L gp e rs i gb t t R g T l f s a s r o r m t ls t ri m em f m C oo 1 E S L

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Introduction

Considerable research has been conducted regarding thecorrelation of specificbrain structures to memory func-tioning [8, 12]. Findings of this research indicate thatdifferent brain structures may mediate qualitativelydifferent aspects of memory. Dissociations have beenfound betweenprocedural and declarativememory,withprocedural memory related to subcortical functioningand declarative memory related to functioning of thehippocampal complex [3]. The specific type of infor-mation “to-be-remembered” has also been found to beimportant. “Material specific” memory has been sup-ported for learning and recallof verbalmaterial, with theleft hippocampus demonstrating relative superiority [4,8]. Memory for nonverbal, visual material has alsoreceivedsupport for beingIateralizedto rightmesialtem-poral areas [8].

Recently, research has been conducted on the specificbrain structures involvedin perception and memory for

*Addressforcorrespondence:DepartmentofNeurosurgery,UniversityofTexasMedicalSchool,6431Fannin,Suite7.148,Houston,Texas77030,U.S.A.Fax (713)794-5084.

music[10,11,13,14].Samsonand Zatorre [11]found thatwords and melodieswere recognizeddifferentlybetweenright and left temporal lobectomypatients. Left temporallobectomypatients tended to forgetmore words,whereasright temporal lobectomy patients tended to forget themelody. Samson and Zatorre [10]found that left tem-poral lobectomypatients exhibitedimpaired delayedrec-ognition for words when spoken or sung to a melody.Both leftand right temporal lobectomypatientsexhibiteddeficientmelody recognitionwhen the melody was sungwith words, whereas only the right temporal lobectomygroup demonstrated deficiencyfor recognizingmelodieswithout words. Zatorre [13]conducted a series of posi-tron emission tomography (PET) studies in 12 normalsubjects and found a relationship between right fron-totemporal activity and music retention. Specifically,theseinvestigatorsfound that right frontotemporal areasappeared to be involvedin the abilityto comparedifferenttonal qualities, thus suggestingthat these areas are inte-grally involvedin mediatingmemory for music.

The above series of studies appears to support righttemporal lobemediation of memory for music.However,it is unclear to what degreespecificmesial temporal lobestructures (i.e. the hippocampus) are involved as the

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1016 P. M. Plengeret al./Music memoryand the sodium amobarbital procedure

above studies relied on results of temporal lobectomypatients and results of PET studies assessing more lateralcerebral functioning. In the former, although patientsundergoing temporal lobectomy also undergo hip-pocampectomy, it is unclear to what degree lateral cort-ices are excised. In the PET studies, it appears that theseauthors were specifically addressing lateral cortical func-tioning.

The prese~t study employed the intracarotid sodiumamobarbital procedure (IAP) in an attempt to determinewhether right mesial temporal structures (i.e. the hippo-campus) are specifically involved in mediating memoryfor music. In addition to determining Iateralization oflanguage [1,’5, 7], the IAP is used for ascertaining lat-eralization of memory functions [6].The purpose of deter-mining lateralization of memory through the IAP istwofold: (a) assessment of the mesial temporal area con-tralateral to the side of surgery in order to prevent post-operative anterograde amnesia [5] and (b) to assist inIateralizing the side of seizure foci [6].

Through the IAP, independent assessment of each hip-pocampus is possible, thus revealing potential differencesin processing material-specific aspects of “to-be-remem-bered” information. For example, employing the IAP,Kaplan et d. [2] found a left temporal advantage formemory for verbal characteristics of objects and a righttemporal advantage for memory of the physical charac-teristics of objects. Perrine et al. [9]also found memoryfor the physical characteristics of objects to be superiorfollowingleft cerebral injection.

The IAP was expected to allow for specific com-parisons in memory performance between an isolatedintact hippocampus and an isolated “damaged” hippo-campus in a series of individualswith intractable com-plex epilepsyassociated with left temporal lobe epilepsy(LTLE) or right temporal lobe epilepsy (RTLE). Thepresent study utilized the IAP in order to determinewhether specificright temporal lobe involvementcouldbe demonstrated for memory for unfamiliar tonalpatterns. It was hypothesized that individuals sufferingfrom RTLE would perform significantlyworse duringleft cerebral injection, than would individuals sufferingfrom LTLE. However, it was predicted that no differencebetweenthe groupswould benoted during right injection.These result$ taken together would provide support fora specificrightmesialadvantage for music/tonalmemory.

Methods

Subjects

Nineteen RTLE and 12LTLE patients whowereundergoingpreoperative epilepsyevaluation at the Texas ComprehensiveEpilepsyProgram at Hermann Hospital wereevaluated duringIAP. Sideof s.$izurewasdeterminedby convergenceof multiplemeasures, includingmagnetic resonanceimaging(MRI), videoEEG monitoring, PET, SPECT and neuropsychologicalevalu-ation. The majority of the patients showedevidenceof mesial

temporal sclerosis by MRI, thus suggesting specific hippo-campal involvement.All patients were right-handed and wereleft hemisphere-dominantfor language(determinedfrom IAP)(seeTable 1 for patient demographics).With the exception ofa higher incidenceof females in the RTLE group, the patientgroups were comparable in age, full scale IQ and amount ofamytal receivedduring the IAP.

Procedure

All patients receivedbaseline assessmentapproximately 2 hbeforethe IAP. Evaluation ofmemoryfor musicwasconductedby presenting the patient with three unfamiliar four quarter-note tonal patterns via stereophonicheadphones to both ears.Each tonal pattern wasrepeatedthree timesbeforepresentationof the next pattern. Recognitionmemorywas assessedafter an8-reindelayby presentingthe patient with nine four-note tonalpatterns, three of which had been presented earlier.

IAP involvedadministration of sodium amytal to the intra-carotid artery via a femoralcatheter. Both right and left admin-istration were conducted on the same day with an average of30 min between injections. The tonal patterns were presentedas outlined above, approximately2 min followinginjection ofsodium amytal (average dose of 103.8mg; 104.6on the leftand 103.0on the right). Recognition memory was assessedaminimum of 8 min followingpresentation, or when speechandmotor functionsreturned to baseline.

Results

No significantdifferenceswere noted as a function offull scaleIQ, age of patient or dosage of amytal betweenthe RTLE and the LTLE groups.

The number of correct identificationsand false alarmerrors were recorded during each of the three phases oftesting.In order to correct for responsebias, a correctionscorewas derivedby subtracting half the number of falsepositiveerrors from correct identifications.Multivariateanalysis employing side of injection as the dependentvariable and side of lesion as the independent variableyielded a significant effect [F= 4.86; P = 0.035]. Sub-sequent comparisons indicated that there was no differ-ence between the two groups during right cerebralinjection, whereas left injection resulted in a significanteffect [t = 2.84; P < 0.01], with the RTLE group per-forming lesswell.

Results were then compared between the RTLE andLTLE groups through a seriesof pair-wisecomparisons.Table 2 indicates that significantdifferenceswere notedbetween baseline performance and both left and rightinjection for the RTLE group, with performance duringboth injections significantlyinferior. Within the LTLEgroup, the only comparison reaching significance“r-obetween right injection and baseline performance,right injectionresultingin poorer performance.

wari

with

Discussion

The results obtained indicate that during injection ofthe right cerebral hemisphere, performance was equi-

P. M. Plengeret al./Music memoryand the sodium amobarbital procedure

Table 1.Patient demographics

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Hemisphere Age Sex FSIQ Amytal level

LTLE 29.3(11) 8 M, 4 F 89.1(13) 104.6(16)RTLE 31.7(11) 8 M, 11F 88(12.3) 103(14)

FSIQ, Full scale IQ; LTLE, left temporal epilepsy;RTLE, right temporalepilepsy.

Table 2. Pairwiseanalysescomparingmemoryfor tonal patterns during right and leftinjectionswith baselineperformance

Mean (S.D.)Sideof lesion/side of injection Baseline Injection t P

LTLERight injection 1.9(1.3) 0.6(0.7) 3.18 <0.01Left injection 1.9(1.3) 1.2(1.1) 1.56 n.s.

RTLERight injection 1.8(0.9) 0.9(1.2) 2.59 <0.02Left injection 1.8(0.9) 0.15(1.0) 5.77 <0.01

LTLE, Left temporal lobe epilepsy;RTLE, right temporal lobe epilepsy.

valent regardless of the side of temporal lobe dysfunction.That is, when left temporal lobe functions were isolated,individuals performed at the same level, irrespective orwhether they had an intact or compromised left mesialtemporal structure. However, during left cerebralanesthesia, RTLE patients performed less well than didLTLE patients. This latter analysis indicates that whenthe right temporal lobe is isolated, patients with intactright mesial temporal functioning perform significantlybetter than those with right mesial temporal damage.These results taken together suggest a specific relation-ship of memory for music to right mesial temporal struc-tures. Alternatively, the lack of a significant differencebetween groups during right injection suggests that mem-ory for unfamiliar tonal patterns does not depend on leftmesial temporal integrity.

Within-group analyses also support a specific righttemporal advantage for memory for tonal patterns asonly right injection of the LTLE group resulted in asignificant decline in memory from baseline, whereasthere was no significant difference between left injectionand baseline for the LTLE group. Performance wasdecreased relative to baseline during injection of both theleft and right hemispheres for the RTLE group. There-fore, neither the impaired right hippocampus nor theintact, isolated left hippocampus was able to mediatememory for tonal patterns adequately.

One limitation in the interpretation of the above resultsis that equivalent performance noted between groupsduring right cerebral injection could be due to compro-mised perception of tonal patterns secondary to rightcerebral anesthesia. Given that the literature supports arelative right hemisphere superiority in processingunfamiliar tonal patterns [2], it could be argued that thetonal patterns could not be adequately processed due to

disruption of right lateral cerebral areas. This is a short-coming of the intracarotid sodium amytal procedure asthe effect of injection is both lateral and medial. However,patients appeared to be adequately processing the tonalpatterns during right anesthesia by verbally describingvarious parameters of the pattern, including pitch andtimbre.

The above data is consistent with previous studies [2,5] implicating a specific right temporal lobe advantagefor memory for music. Results based on PET analysishave suggested both right inferior frontal and rightsuperior temporal involvement. Specifically the superiorright temporal 1obe is thought to allow for processing ofpatch information, whereas the frontal lobe holds infor-mation in “working memory”. However due to metho-dological differences between the present study andprevious studies, different aspects of “memory” are beingaddressed. The Zatorre paradigm [13] involves fairlyshort-term memory required for pitch discrimination orfirst versus last pattern discrimination. This paradigmpresumably requires minimal time and appears to rely onimmediate memory or “working memory”. Moreover,lateral versus mesial temporal lobe functioning is impli-cated.

The present study, however, addresses recall of tonalpatterns following an interpolated delay, and thusaddresses consolidation of memory, presumably fromshort-term storage or working memory to longer-termstorage. The present results, therefore, support a specificrole for the right hippocampus in consolidating memoryfor tonal patterns.

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