Olfactory lateralization and identification in right hemisphere lesion and control patients

Vrurup,lcholnylu. Vol 27. No Prmted ,n Great Br~tam

9. pp.

1187-l

191.

1989 d

002X-393289 S3.00+0.00 1989 Pergamon Press plc

NOTE OLFACTORY LATERALIZATION AND IDENTIFICATION IN RIGHT HEMISPHERE LESION AND CONTROL PATIENTS DAVID N. BELLAS*& ROBERTA. NoVELLYt and BRENDAESKENAZI$

*Massachusetts

General Hospital, Harvard Medical School; tWest Haven VA Medical Center, School of Medicine; and $University of California, Berkeley; U.S.A. (Received 9 December

1988; accepted

Yale University

19 May 1989)

Abstract-This study investigated olfactory lateralization and identification in right hemisphere lesion and control patients. Significant group differences were found for olfactory and trigeminal lateralization and identification on unilateral and double simultaneous stimulation. In the control group, significantly greater than chance accuracy was found for lateralization and identification, whereas in the lesion group, significantly greater than chance accuracy was found for identification but not for lateralization. Olfactory detection thresholds were found not to be significantly different between the groups.

INTRODUCTION THE RESULTS of the more exterisive studies on olfaction

in brain damaged individuals include the findings that right and left temporal lobectomy, right and left orbitofrontal lobectomy, and right frontotemporal excision cause generalized olfactory information processing deficits in discrimination, identification, and recognition memory [l&12]. Olfactory detection thresholds in the lesion groups were found to be within normal limits. In addition, a cerebrovascular accident of the right hemisphere (primarily of the right parietal lobe) has been shown to cause a unilateral neglect of the left nostril [ 1, 21. In normal individuals, VON BBK~SY [16] used separate tubes to deliver the same odorant bilaterally to the two nostrils and found a lateralization of olfactory sensation by introduction of a small time difference (0.5 msec or less) or by an intensity shift (10%). SCHNEIDERAND SCHMIDT [13] replicated the von Bkkisy findings and, in addition, investigated the role of the trigeminal component in olfactory lateralization. They contrasted a “pure” odorant coffee with a strong trigeminal stimulant ammonia and delivered them, diluted with nitrogen, both unilaterally and bilaterally through tubes in the nostrils. They found that on unilateral stimulation only ammonia could be accurately lateralized and that coffee could not be lateralized in seven subjects. More recently, EHRLICHMAN[9] reported in a pilot study that normal subjects were unable to lateralize an odorant to either nostril on unilateral stimulation, unless the odorant was a trigeminal stimulant. However, Ehrlichman’s study was a pilot study with probably few subjects, and he primarily used extracts (e.g. almond extract and orange extract) as odorants. The data in the Bellas et al. [l, 21 neglect studies offered an opportunity to investigate the ability of both brain lesion and normal subjects to lateralize and identify odorants and a trigeminal stimulant on unilateral and double simultaneous stimulation. Previously, we had analyzed the data for neglect signs only (i.e. extinctions and displacements) and did not analyze the data to study lateralization in normal control subjects or identification in either lesion or control subjects. Considering the relevance of the data to the previously cited research, the present analysis focused on these two areas.

$Correspondence 725, Massachusetts

to be addressed to: David N. Bellas, PhD, Neuropsychology General Hospital, Fruit Street, Boston, MA 02114, U.S.A. 1187

Laboratory,

Vincent

Burnham

118X

NOTE

METHODS Fifteen patients with right hemisphere lesions and an equal number of hospitalized control patients participated in the study. Neurological patients were eligible if they were diagnosed by a neurologist, using clinical neurological examination or physical diagnostic procedures (e.g. electroencephalogram or computed tomography), to have suffered a cerebrovascular accident of the right hemisphere (primarily of the right parietal lobe) at least 2 weeks previously, to have a documented left unilateral neglect on the neurological examination and the Quality Extinction Test [ 141, and to have no substantial sensory impairments suflicient to account for the neglect. The control patients had a lower extremity orthopedic injury or amputation and no history of a cerebral dysfunction. Groups were matched for age, education, gender, and right hand dominance. Details of the subjects have been reported previously [ 1, 21.

All potential subjects were administered olfactory threshold testing to ensure that the nostrils were of similar olfactory sensitivity and that they did not have a primary sensory defect (i.e. anosmia or hyposmia) using a method described by ESKENAZIet a1.[10,11] and CAIN [S, 71. All potential right hemisphere lesion subjects were screened for the presence of a left unilateral neglect using a tactile double simultaneous stimulation (DSS) test-the Quality Extinction Test 1141. Following this screening process, all subjects were administered olfactory and trigeminal DSS tests. The odorants utilized in the olfactory DSS test were coffee (ground beans), peanut butter, soap (shaved Ivory). and chewing gum (Juicy Fruit). These odorants, contained in squeezable plastic bottles. were presented to subjects through an apparatus that could deliver an equal airflow of each odorant to both nostrils by depressing a lever. Subjects were first presented with each odorant and provided with its veridical name. Second, the unilateral sensitivity of each nostril and identification accuracy for the odorants were assessed. Finally, the odorants were presented in a mixed sequence with the nostrils either being stimulated simultaneously by the same odorant (8 trials), different odorants (12 trials), or no odorant (water) and one odorant (8 trials) for a total of 28 trials. The trigeminal DSS test involved adding a single pungent stimulant, vinegar (wine), as a trigeminal stimulant. The stimulant was administered in a mixed sequence with the nostrils either being stimulated simultaneously by the same trigeminal stimulant (2 trials), the trigeminal stimulant and an odorant (8 trials), or no odorant (water) and the trigeminal stimulant (2 trials) for a total of I2 trials. Details of the procedures have been reported previously [ 1.21.

RESULTS The right hemisphere lesion and control groups were compared for right and left nostril olfactory detection thresholds by means of a two-way analysis of variance and were found not to differ significantly with respect to group, nostril, or the interaction of group and nostril [F(l, 56)=1.65, P>0.05; F(1, 56)=0.06, P>O.O5; F (1. 56)=0.18, P >0.05, respectively]. Table 1 displays the means, standard deviations, and r-tests comparing the subject groups for olfactory and trigeminal lateralization and identification on unilateral and double simultaneous stimulation. The only nonsignificant difference between the groups was for trigeminal identification on unilateral stimulation. Chi-square analyses were also conducted and are presented below. When odorants were presented unilaterally [with no odorant (water) to the other nostril]. right hemisphere lesion patients lateralized them to the correct nostril only 54.1% of the trials [not significantly diRerent from chance (50%), x2(1)=0.83, P>O.20]. whereas the control patients lateralized them to the correct nostril 75.8% of the trials [significantly different from chance (50%),x2(1)=32.03, PO.20], whereas the control patients lateralized it to the correct nostril in 86.6% of the trials [significantly different from chance (50%). x’(l)= 16.13, P0.20]. whereas the control patients lateralized them correctly in 36.6% of the trials [significantly different from chance (lo%), x*(l)= 142.22, P O.20], whereas the control patients lateralired them correctly in 47.5% of the trials [significantly different from chance (lo%), x’(l)= 187.50, P
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1189

Table 1. Means, SDS and t-tests comparing subject groups for olfactory and trigeminal iateraiization identification on unilateral stimulation (US) and double simultaneous stimulation (DSS) Variable Lateraiization Odorants Trigeminai Lateraiization Odorants Trigeminai Identification Odorants Trigeminai Identification Odorants Trigeminai

Lesion patients

Control

patients

r (28)

and

P

(US)

stimulant

M SD M SD

4.33 1.45 1.13 0.35

6.06 1.94 1.73 0.45

M SD M SD

1.20 1.69 0.66 1.34

4.40 2.17 3.80 2.36

M SD M SD

7.06 0.96 1.86 0.35

7.73 0.59 I .93 0.25

M

12.80 2.48 8.33 1.63

16.67 3.01 11.80 2.21

2.16

10.01

4.02


3.81

< 0.005

4.45


2.28

<0.05

0.59

>0.05

3.83


4.88


(DSS)

stimuiant,‘Odorants (US)

stimulant (DSS)

stimuiant/Odorants

SD M SD

accuracy [significantly different from chance (20%) x2( 1) = 100.83, P O.O5] or control patients [t (28)= 1.05, P>O.O5]. When two different odorants were presented simultaneously, lesion patients achieved 53.3% identification accuracy [significantly diRerent from chance (4%) x2( I)= 2281.66, P
DISCUSSION In comparing the right hemisphere lesion and control groups, significant differences between groups were found for olfactory and trigeminal iateraiization and identification on unilateral and double simultaneous stimulation. The only exception to this was the finding of no significant difference between groups for trigeminai identification on unilateral stimulation. In addition, the groups did not differ significantly for olfactory detection thresholds in either nostril. Right and left nostrils were also found not to differ significantly in either group for olfactory identification on unilateral stimulation. With regard to the accuracy of the subject groups on the olfaction tasks, significantly greater than chance accuracy was found for the control group for iateralization and identification on unilateral and double simultaneous stimulation. The right hemisphere lesion group exhibited significantly greater than chance accuracy for identification, although only chance accuracy for iateraiization on unilateral and double simultaneous stimulation. The poor results for the right hemisphere-primarily right parietai lobe-lesion patients with regard to iateraiization can be explained by the fact that they were neglecting their left nostril on unilateral stimulation and DSS and only iateralizing accurately to their right nostril [ 1,2]. The results for the control patients are interesting in that they accurately iateraiized the odorants on unilateral stimulation 75.8% ofthe trials, significantly above chance level (50%) and contrary to the findings by SCHNEIDER and SCHMIDT [13] and EHRLICHMAN [9] who, in much smaller groaps of normal subjects, found that they could not iateraiize on unilateral stimulation unless the odorant was a trigeminai stimulant. When the stimulus soap was excluded from the analysis, because it may have a slight trigeminai component, the control patients still accurately iateraiized the remaining odorants in 73.3% of the trials, significantly greater than chance. When coffee alone was analyzed, the control patients iateralized it in 70.0% ofthe trials, still significantly above chance level and directly contrary to Schneider and Schmidt’s finding that coffee (diluted with nitrogen) could not be iateraiized above chance level.

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It would appear that lateralizing real, everyday odorants is much easier than lateraliring diluted odorants or extracts. This is consistent with CAIN’S [3 -81 findings that utilizing odorants with ecological validity, high familiarity, and qualitativediversity greatly improves identification accuracy. The fact that the present study utilized odorants which were easily identified verbally with well-known names and had high familiarity and ecological validity may have aided considerably in their identification and lateralization. The findings are supportive of Schneider and Schmidt’s and Ehrlichman’s data in that in the control patients the trigeminal stimulant was better lateral&d than the odorants on unilateral stimulation (86.6 and 75.X%, respectively). Some authors have suggested that all odorants have a trigeminal component and that this is what subjects are lateralizing [I 31. The present study utilized odorants which were subjectively considered olfactory in nature (except for the soap which may have an irritative effect). However, no objective evidence was available to document this. Perhaps there is a continuum of some odorants having a strong trigeminal component (e.g. vinegar) and others having a weak or no trigeminal component (e.g. coffee). Further research is necessary to investigate this. The right hemisphere lesion patients with primarily right parietal lobe lesions had much more difficulty with the lateralization of the odorants and much less difficulty with the identification of the odorants. Odorant identification has been associated with right and left orbitofrontal regions [ 121, right and left temporal regions [l&12], and right frontotemporal regions 1127 (with orbitofrontal areas more important than temporal areas) and should be less affected by parietal lobe lesions. Jones-Gotman and Zatorre did not find any olfactory identification deficits in their patients with left central, parietal, or posterior excisions. The present study employed primarily right parietal lobe lesion patients and found mild deficits in odorant identification on unilateral stimulation. However, the patients’ lesions were not confined to the right parietal lobe and involved more extensive right hemisphere damage including posterior frontal-temporal areas, which may account for their mild impairment. The patients’ left neglect did not affect their identification accuracy on unilateral stimulation because they simply mislocalized or displaced the identified odorant to the right nostril. In displacement, the stimulus is accurately identified, but is mislocalized to the opposite side of the body. Details of the neglect findings have been reported previously [I, 21. Olfactory detection thresholds were found not to be significantly different between the lesion and control groups for the two nostrils, which is consistent with the finding of normal thresholds in the lesion groups in the ESKENAZI (‘I al. [lo, 1 l] and JONES-GOTMAN and ZATORRE [12] studies. It is probable that the olfactory nerve, bulb, and tract were not injured in the right hemisphere-primarily right parietal lobe-lesion patients and that these areas may be primarily responsible for olfactory detection thresholds. It is interesting to note that both the right hemisphere lesion and control groups exhibited higher detection thresholds for olfactory stimulation than that expected (mean right nostril thresholds 4.66 and 5.33 and mean left nostril thresholds 4.93 and 5.26, respectively), based on data of primarily young adults (mean thresholds between 6 and 8 on a IO-point scale). This may have occurred because the lesion and control subjects employed in this study were older adults (mean ages 61.26 and 63.46. respectively). CAIN [4] and STEVENSand CAIN [ 151 provided data indicating that there is a decrease in olfactory sensitivity in the elderly. which would appear to account for the higher detection thresholds achieved by the older subjects in the present study.

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7. 8. 9.

IO. 11. 12.

of unilateral neglect in the olfactory sensory system. NeurnpsJcMoqia 26,45%52, 1988. BELLAS, D. N., NOVELLY. R. A., ESKENAZI, B. and WASSEKSTEIN,J. Unilateral displacement in the olfactory sense: a manifestation of the unilateral neglect syndrome. Cortex 24, 267-275, 1988. CAIN, W. S. To know with the nose: keys to odor identification. Science 203, 467470. 1979. CAIX, W. S. Chemosensation and cognition. In O!fircriort and Taste, VII, H. VAN DER S~ARKE (Editor). pp. 347-357. IRL Press, London, 1980. CAIN, W. S. Sumner’s ‘On testing the sense of smell’ revisited. Yule J. ho/. Med. 55, 515- 519, 1982. CAIN, W. S. Olfaction. In Sreaens’ Hundhook of Erpcrimental Psychology, Vol. I; Perception und Motirafion (revised edn) R. C. ATKINSON. R. J. HERRNSTEIN, G. LINUZEY and R. D. LLCF (Editors), pp. 409 459. John Wiley, New York, 1988. CAIN, W. S., GENT, J. F., G~~DSPEEI~, R. B. and LEONAKD, G. Evaluation of olfactory dysfunction m the Connecticut Chemosensory Clinical Research Center. Larynyoscope 98, 83-88. 1988. CAIN, W. S. and KRAUSE, R. J. Olfactory testing: rules for odor identification. Neural. Rrs. 1, 1 9, 1979. EHKLICHMAN, H. Hemispheric Asymmetry and Positire--Neyatice .4@cr. Paper presented at the Wenner Gren Center International Symposium on The Dual Brain: Unified Functioning and Specialization of the Hemispheres, Stockholm, 1986. ESKENAZI. B., CAIN, W. S.. NOVELLY. R. A. and FRIEND. K. B. Olfactory functioning in temporal lobectomy patients. Neuropsycholoyia 21, 365-374. 1983. ESKENAZI. B., CAIN, W. S., NOVELLY. R. A. and MATTSOX. R. Olfactory perception in temporal lobe epilepsy patients with and without temporal lobectomy. ~Yruropsycholoyiu 24, 553 562, 1986. JONES-GOTMAN, M. and ZATORRE. R. J. Olfactory identification deficits in patients with focal cerebral excision Neuropsycholoqia 26, 387 400. 1988.

NOTE 13.

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SCHNEIDER, R. A. and SCHMIDT, C. E. Dependency of olfactory localization on non-olfactory cues. Physiol. Behaa. 2, 305-309, 1967. 14. SCHWARTZ, A. S., MARCHOK, P. L. and FLYNN, R. E. A sensitive test for tactile extinction: results in patients with parietal and frontal lobe disease. 1. Neural. Neurosurg. Psychiat. 40, 228-233, 1977. 15. STEVENS,J. C. and CAIN, W. S. Old-age deficits in the sense of smell as gauged by thresholds, magnitude matching, and odor identification. Psychology and Aging 2, 3&42, 1987. 16. vm B~KLsY, G. Olfactory analog to directional hearing. J. appl. Physiol. 19, 369-373, 1964.