Journal of Clinical and Experimental Neuropsychology

ISSN: 0168-8634 (Print) (Online) Journal homepage: http://www.tandfonline.com/loi/ncen19

Impairment of central auditory function in Alzheimer's disease Erich Mohr , Christiana Cox , Jill Williams , Thomas N. Chase & Paul Fedio To cite this article: Erich Mohr , Christiana Cox , Jill Williams , Thomas N. Chase & Paul Fedio (1990) Impairment of central auditory function in Alzheimer's disease, Journal of Clinical and Experimental Neuropsychology, 12:2, 235-246, DOI: 10.1080/01688639008400970 To link to this article: http://dx.doi.org/10.1080/01688639008400970

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Journal of Clinical and Experimental Neuropsychology 1990, Vol. 12, No. 2, pp. 235-246.

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Impairment of Central Auditory Function in Alzheimer’s Disease*

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Erich Mohr*, Christiane Cox*, Jill Williams+, Thomas N. Chase+ and Paul Fedio* *Medical Neurology Branch +Experimental Therapeutics Branch National Institute of Neurological and Communicative Disorders and Stroke Bethesda, M D

ABSTRACT Accuracy and laterality of ear preference on dichotic listening (DL) tasks were compared in patients with Alzheimer’s disease (AD) and a group of normal subjects, matched for age and education, using parameters (list length, stimulus matching, and order of recall), previously shown to significantly alter DL performance in normals. Alzheimer patients tended to show qualitatively similar, but significantly worse performance compared to controls as a function of increasing dichotic list length as well as stimulus set content (semantically, v. phonemically and unmatched dichotic items). Furthermore, these patients were unable to attend selectively to either the right- or left-ear and thus could not increase right- or left-ear advantages over the free recall procedure, an order of recall task easily mastered by the normal subjects. These results suggest that Alzheimer’s disease is associated with a breakdown of cortical mechanisms involved in the selective allocation of attention.

Dichotic listening (Broadbent, 1954, 1956), the simultaneous presentation of conflicting stimuli to the right and left ear, has been widely applied to the investigation of central nervous system (CNS) dysfunction, at both cortical (e.g., Niccum, Rubens, & Selms, 1983) and subcortical (e.g., Ogden, 1985) levels. While lateralization patterns differed as a function of specific CNS injury, all patients, regardless of lesion type, evidenced overall performance decrements. Although lesion sites in these studies were variable in size and location, all tended to be relatively circumscribed. Comparable research efforts in patients with m o r e diffuse CNS damage, such as Alzheimer’s disease (AD), a disorder characterized by increasing cerebral atrophy and progressive

* Portions of this paper were presented at the 14th Annual Meeting of the International Neuropsychological Society Denver, Colorado, U.S.A. 1986 Please address correspondence to: Dr. Erich Mohr, Royal Ottawa Hospital, Neuropsychology Service, 1145 Carling Ave., Ottawa, Ontorio, Canada, K17 7K4. Accepted for publication: March 2, 1989

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ERICH MOHR ET AL.

deterioration of intellectual and memory function (Katzman, 1986), have been relatively rare. One dichotic paradigm, the staggered spondaic word test, revealed significantly impaired performance in Alzheimer’s patients (Grimes, Grady, Foster, Sunderland, & Patronas 1985). Although this study extended the list of observed cognitive deficits in Alzheimer’s disease to central auditory processing, there was no attempt to investigate the pattern of dichotic performance. Studies in other realms such as verbal memory, indicating compromised, but qualitatively similar recall patterns between A D patients and matched controls (Martin, Brouwers, Cox, & Fedio, 1985), suggest that detailed examination of performance patterns beyond the simple establishment of deficits may add to the understanding of the structural and functional correlates of this disorder. The precise effect of Alzheimer’s disease on defined aspects of attention and memory remains unclear. In an attempt to explore this matter further, dichotic performance of AD patients was studied using experimental parameters previously investigated with healthy individuals as subjects: (1) order of recall (more material is correctly recalled from the channel reported first, Cooper, Achenbach, Satz, & Levy, 1967; Mohr, 1987);(2) increasing word pairs (greater list lengths yield decreasing accuracy and greater right ear preference, Mohr & Costa, 1985); (3) linguistic matching (right-ear advantages increase as a function of qualitative difficulty, Curry & Rutherford, 1967). METHOD Subjects:

+

Twenty-two right-handed patients (12 males, 10females, mean age SD and range 62.45 7.39, 53-80, education 16.00 f 3.27, 7-20 years), who satisfied DSM I11 (American Psychiatric Association, 1980) and National Institute of Neurological and Communicative Disorders and Stroke - Alzheimer’s Disease and Related Disorders Association (McKhann et al., 1984) criteria for AD, consented to participate in this study after full disclosure of its potential risks and benefits. Dementia symptoms were reported to be present for 4.00 2.88 (1-11) years in these patients and the degree of cognitive impairment (Mattis Dementia Rating Scale; Mattis, 1976) ranged from mild (137) to severe (86), with a mean of 115.77 f 12.70. Routine physical screening revealed no other significant illness in these patients. Twenty-two right-handed healthy subjects, matched for age and education (1 1 males, 11 females; age 59.82 6.67,48-72, education 15.59 2.44, 12-20 years) served as controls. All control subjects underwent a brief, routine physical examination to insure that no significant illness was present. At the time of entry into this study, all subjects received an assessment of intellectual and memory function (WAIS-R, Wechsler, 1981; WMS, Wechsler & Stone, 1945). A summary description of the demographic and psychometric data is presented in Table 1.

*

*

*

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C‘tNTRAI. AUDITORY DYSFUNCTION IN A D

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Table 1 Subject Characteristics

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Agea Educationa Symptom Duration” WECHSLER TESTS Verbal IQ Performance IQ Full Scale IQ Memory Quotient MATTTS Dementia Rating Scale

Normal Controls ( N = 22)

Alzheimer’s Patients ( N = 22)

59.82f 6.67( 48- 72) 15.59+ 2.44( 12- 20)

62.45 k 7.39 (53- 80) 16.00-t 3.27( 7- 20) 4.00+ 2.88( 1- 11)

124.00 t 12.83 (105-146) 118.45 f 13.14 ( 94-147) 123.77 12.77 (103-148) 130.59+ 11.91 (112-143)

92.73 t 13.90 (71-123)* 78.86 5 11.85 (53- 97)* 86.09 f 11.82 (64-109)* 74.18 k 11.06(56- 96)*

142.27f 1.72(139-144)

115.77 -t 12.70(86-137)*

+

Values represented are the means 3z SD and range. a-Years * Alzheimer’s patients different from normal controls at p < .001.

Procedure: A brief informal exam by a neurologist and neuropsychologist screened all subjects’ hearing (DeJong, 1979). For those suspected to have any deficits, a standard, comprehensive audiological exam was performed by a n audiologist (Grimes et al., 1985). Subjects with hearing impairments (25 d b HL below control levels a t any 1 of 8 frequencies tested) or interaural differences exceeding 5 d b (across all test frequencies, pure tone audiometry) were excluded from this study (Chocolle, 1962). Dichotic stimuli were presented via a Telephonics MX-41/AR stereo head set on a TEAC-A 108 stereo cassette deck. Calibration of intensity levels (70 d b SPL, averaged across peak amplitude of speech) was performed with a Bruel and Kjaer 2232 precision sound level meter (A scale). Stimulus materials were delivered a t the rate of 2 pairs/s (Mohr & Costa, 1985) with an intertrial interval of 15 s. The subjects initially participated in a Free Recall procedure (FR) using standard instructions, followed by an alternately varied Left-Ear (LER) or Right-Ear (RER) first order of recall condition (Order of Recall factor; “report first all the words you heard with the right/left ear, then all the words with the leftlright ear”; Mohr, 1987). Each recall condition was preceded by two, 1-word-pair practice trials, during which the respective target words were provided to the subject prior to trial presentation. Assignment of one of three tapes for each recall condition was randomly varied. All three test tapes (33 trials each) were balanced for list length (trial 1-18, 1 word pair; 19-27,2 word pairs and 28-33,3 word pairs; List Length factor; Table 2). Each trial series (1, 2, and 3 word pairs) contained a total of 36 words (18 right and 18 left) and was equally subdivided into three trial sets. Set 1 contained semantically matched stimuli (e.g., cat and deer), set 2 unmatched stimuli (e.g., hand and mouse) and the 3rd set consisted of stimuli, matched for initial phoneme (e.g., nest and nut; Linguistic Matching factor; Tablc 2). All test words were concrete, high frequency, 1-2 syllables English nouns.

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Table 2 Example of dichotic stimulus set (Tape 1)

Examples A

girl Page

B

gate pain

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1 Word Pair

Semantically Matched

jet cloud bowl fly mouse eye

truck sun spoon worm cow 1%

12.

plate cat hail arm truck sleet

door nose foot gnat hat bee

13. 14. 15. 16. 17. 18.

cold land hi11 knife clerk flame

car lake head nurse card flood

1. 2. 3. 4. 5. 6.

Unmatched

7.

8. 9. 10. 11. Phonemically Matched

2 Wordpairs

20. 21.

boat ant fork

jeep moth plate

car flea Pot

cart gnat stove

Unmatched

22. 23. 24.

bear hair storm

hat wall 1%

rain roach tick

cart bowl truck

Phonemically Matched

25. 26. 27.

wheat wit fault

note beast birth

wolf wealth fate

neck breath bush

Semantically Matched

19.

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CENTRAL AUDITORY DYSFUNCTION I N AD

3 WordPairs

Semantically Matched

28. 29.

mouse room

rat wood

Unmatched

30. 31.

sleet toe

sock

tie knife

bee cow

jet

cloud steps

32.

pine

33.

fur

fleet steel

sword grain

plate fence

flag string

gun

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Phonemically Matched

sheep hall

cow brick

pig stair

bear door

mouse

boat

stair

To avoid confounding instructional set with memory deficits of the patients, both AD and control groups were alerted by gentle tapping on the appropriate side of their headset which ear to recall first under ordered recall. This procedure was repeated after every block of 12 words, corresponding each time to the beginning of a new trial set (Table 2). Performance accuracy was assessed with the formula Right Ear correct (RC) f Left Ear correct (LC) / number of words possible. As an index of laterality the formula RCLC/RC+LC was used (for discussion see Mohr and Costa, 1985). Data analysis was performed with the use of standard ANOVA procedures, including repeated measures (Dixon et al., 1983; BMDP 2V), and where appropriate, with correlational measures (Joyner, 1985).

RESULTS Performance accuracy on dichotic listening tasks was substantially lower in the A D patients compared to control subjects (F(1,42)=58.83, p .1). Performance accuracy as a function of List Length indicated significant differences (F(2,84)=97.09, p < .0001; Fig. 1) with n o significant interaction, reflective of qualitatively similar performance of the AD patients a n d the normal subjects. Both groups tended to perform most accurately with 1 word pair a n d the least accurately with 3 word pair stimuli. Performance accuracy as a function of Linguistic Matching, on the other hand, suggested differences between sets of stimuli (semantically, v. phonemically a n d unmatched dichotic items; F(2,84)=18.86,p < .0001), as well as o n the interaction by group (F(2,84)=7.60, p < .01; Fig.2). Normal control subjects reported semantically matched stimuli more accurately than phonemically and unmatched items across recall conditions (p < .OOOl), while AD patients showed this pattern only under LEK (p < .OOOl). No other consistent differences emerged o n any of the post-hoc tests on this factor. There were n o significant group differences in laterality indices (Table 3). However, both Order of Recall as well as the interaction of Order of Recall by

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ERICH MOHR ET AL.

“s, Normal Controls

A Alzheimer

Patients

10

01

I

Word Pairs 1

‘ ’

2

3

Free Recall

I

l

l

I

l

l

1

2

3

1

2

3

Letl Ear Recall

Right Ear Recall

Figure 1 : Mean & SEM accuracy coefficientsfor AD patients and normal Controls under Free and ordered Recall for 1,2 and 3 word pairs (WP).

group yielded marked differences(F(2,78)=16.89,p