Olfactory and gustatory capacities of alcoholic Korsakoff patients

Neuropsychologia, Vol. 16,pp. 323to 337. 0 PergamonPressLtd. 1978.Printedin GreatBritain.

0028-3932/78/0601-0323%02.00/O

OLFACTORY AND GUSTATORY CAPACITIES OF ALCOHOLIC KORSAKOFF PATIENTS BARBARAPENDLETONJONES* Department of Psychology, Boston University and Aphasia Research Center, Boston University School of Medicine, Boston, Massachusetts, U.S.A.

NELSON BUTTERS Psychology Service, Boston VA Hospital and Aphasia Research Center, Boston University School of Medicine, Boston, Massachusetts, U.S.A.

HOWARD R. MOSKOWITZ MPi Sensory Testing, Inc. New York, New York, U.S.A. and KATHLEEN MONTGOMERY Psychology Service, Boston VA Hospital, Boston, Massachusetts, U.S.A. (Received 1I November 1977)

Abstract-The psychophysical method of magnitude estimation was used to assess the olfactory, gustatory, visual and auditory capacities of alcoholic Korsakoff patients. The Korsakoffs were most impaired in their scaling of olfactory and gustatory stimuli but did evidence some mild impairments on two of the three visual tasks. In contrast, right-hemisphere lesion patients were impaired on all three visual tasks and on an auditory task, but they scaled olfactory and gustatory stimuli in a normal manner. This dissociation indicates that the Korsakoffs difficulties with the chemical senses cannot be attributed to the complexity of the tests.

IN A RECENT study JONES, MOSKOWITZ, BUTTERS and GLOSSER [I] used the psychophysical methods of line matching and category scaling to assess olfactory and other sensory capacities in alcoholic Wernicke-Korsakoff patients. The results of this investigation indicated that such patients have a marked impairment of olfactory sensitivity, with raised thresholds for the detection of odors. It was hypothesized that the olfactory deficit of WernickeKorsakoff patients is due to thalamic and/or hypothalamic damage characteristic of the syndrome [2]. The dorsal medial nucleus of the thalamus, damaged in 100% of WernickeKorsakoff patients with a clinically confirmed memory deficit in VICTOR, ADAMS and COLLINS’ series [2], and the ventral medial nucleus of the thalamus, damaged in 58% of patients with Wernicke’s encephalopathy, Korsakoff syndrome, or both [2], are thought to be the two thalamic relays for the olfactory system in mammals [3]. In addition, the mammillary bodies, damaged in 100% of Wernicke-Korsakoff patients, may also be capable of receiving olfactory inputs via the pyriform cortex, the lateral entorhinal area, and the hippocampus (see Refs cited in [l]). *Reprint requests should be addressed to Dr. Barbara Pendleton Jones at her present address: Department of Neurology, McLean Hospital, Belmont, Massachusetts 02178, U.S.A. 323

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B. P. JONES,N.BUTTERS, H. R. MOSKOWUZand K. MONTGOMERY

In the present study, psychophysical methods were employed to assess the sensory alcoholic Wernicke-Korsakoff patients, rightcapacities of four groups of subjects: hemisphere lesion patients, nonamnesic long-term alcoholics, and normal controls. The primary objective of the study was to determine whether alcoholic Wernicke-Korsakoff patients suffer an impairment of the other chemical sense, that of taste. The ventral medial nucleus of the thalamus, damaged in 58% of VICTOR, ADAMS and COLLINS’ series of Korsakoff patients [2], is thought to be the thalamic relay for the gustatory system [4]. Although judgments of the stimulus quality of tastes would obviously be impaired in a population already shown to have reduced olfactory sensitivity, judgments of the stimulus intensity of the four basic tastes are made independently of odor, and indeed, the strongest tasting substances, such as sugars, salts, and many mineral acids, are odorless [5]. It was hypothesized that Wernicke-Korsakoff patients would show deficits in the intensity scaling of taste, but that their gustatory abnormality would be less striking than their olfactory impairment, since a smaller percentage of these patients has the lesion postulated to result in a taste deficit. Right-hemisphere lesion patients were included in the design as a brain-damaged control group. The previous finding that Korsakoff patients were impaired in the intensity scaling of odor but not of brightness or loudness [I] was open to interpretation as a complexity effect. That is, it was arguable that odor intensity scaling is simply more difficult than brightness or loudness estimation, and that the single brain-damaged group in the study, Korsakoffs, showed deficits on olfactory scaling largely as a result of task complexity. In order to resolve this issue, a second brain-damaged group, right-hemisphere lesion patients, was chosen. As is well known, patients with cortical lesions in the posterior regions of the right hemisphere are impaired on a variety of visual and visuospatial measures (e.g. [6-111). In the present study it was expected that right-hemisphere lesion patients would exhibit deficits in one or more visual magnitude estimation tasks but not on olfactory or gustatory scaling. Thus it would be possible to demonstrate the modality-specific nature of the brain-damaged groups’ deficits. Nonamnesic alcoholic subjects served as a second comparison group for Korsakoff patients since they share the common effects of long-term alcoholism but not the severe neuropathology of the Wernicke-Korsakoff syndrome. METHODS Subjects

The following four subject groups were examined: 10 long-term alcoholics, 10 alcoholic Korsakoff patients, 10 right hemisphere lesion patients, and 15 normal controls. With the exception of one female right hemisphere patient, all of the subjects were male. The mean age of each subject group was from 54 to 57 yr (alcoholics, 55.3; Korsakoffs, 56.6; right hemisphere patients, 54.3; normal controls, 57.1); an analysis of variance indicated no significant group differences in age, F(3, 41) = 0.32, P > 0.25. No subjects were chosen who had undergone surgery within the preceding two months or who had had acute viral hepatitis, Sjogren’s syndrome, or complications of thiol consumption, since all of these conditions have been shown to be associated with disorders of olfaction and/or taste [12-151. An attempt was also made to exclude all subjects who had had a broken nose or deviated septum The long-term alcoholic group consisted of individuals who had drunk heavily and consistently for at least 20 yr (mean 30.6 yr), and were either patients at the Center for Problem Drinking of the Boston VA Outpatient Clinic, patients at the Boston VA Hospital, or respondents to an advertisement. The average daily intake of these long-term problem drinkers before detoxifcation had been approximately one pint of spirits or one quart of beer, and they had been sober for a mean of 15.7 months (range 2 months-7 yr). Any individual with a history of prolonged unconsciousness due to head trauma, seizures not limited to alcohol withdrawal, or polydrug abuse was eliminated. The alcoholic Korsakoff patients had all been diagnosed by the Neurology Services of the Boston,

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Brockton, or Bedford VA Hospitals. All manifested severe anterograde amnesia and some retrograde amnesia, but none showed signs of dementia (mean Full Scale I.Q. on the WAIS of 99.1). These patients are part of the same alcoholic Korsakoff population studied by CERMAK and BUTTERS [16]. The right-hemisphere lesion subjects were patients of the Boston VA Hospital or the Braintree Hospital. These patients were all right-handed individuals who had sustained a significant, unilateral lesion in the right hemisphere.* The localization of the lesion was classified on the basis of radiological investigation (brain scan or arteriogram) or surgical reports. Table 1 presents information concerning the etiology of the lesions, presence of motor or sensory losses or visual field defects, and lobes affected in this subject group. Virtually all of these patients had some right parietal lobe damage. Table 1. Clinical profile of right hemisphere lesion group

Patient

Age

1 2 3 4 5 6

51 55 57 64 60 54

7

52

8

46

9 10

54 50

Etiology infarct infarct aneurysm infarct infarct ?infarct ?tumor tumor resection intracerebral bleed infarct trauma ; resection

Sensory loss

Visual field defect

Lesion site

Motor loss

PFT P FPT FP PO OP

+ + + -

+ + + f

HH

TP

+

+

HH

PT

f

-

HH

FTP TFP

+ +

+

HH

HH

LQ

ExpZunation of symbols: P, parietal lobe; T, temporal lobe; 0, occipital lobe; F, frontal lobe; +, presence of deficit; -, absence of deficit; f, deficit questionably present; HH, homonymous hemianopia; LQ, lower quadrantanopia. Procedure

Each subject was tested on stimulus intensity assessment in each of six perceptual continua (three visual continua and auditory, olfactory, and gustatory continua). Both patterned and non-patterned visual stimuli were used since some have argued that a spatial component is crucial for eliciting the visual impairments of right (varietal lobe) patients [lo, 111. The nonpatterned visual continuum was shades of gray, and the two patterned visual continua were circles of varying sizes and grids of varying complexity. The order of the tasks was randomized for subjects within groups. The procedure in all six tasks was the same. The method of magnitude estimation was used in order to provide maximum information about subjects’ sensory capacities. Signal detection methods only determine thresholds, whereas with magnitude estimation one can derive approximations of thresholds but also simultaneously, and more importantly, learn how subjects’ subjective estimates change with variations along a whole range of the stimulus intensities. Subjects provided verbal responses (intensity estimates from 1 to 1000) to the stimuli. For each continuum the subject judged each stimulus four times; that is, all stimuli for the task were presented in each of four consecutive randomized blocks. Prior to each block of stimuli a stimulus near the middle of the intensity range was demonstrated to the subjects and matched with the number 200 in order to provide a standard of comparison for their subsequent judgments; they were told to assign higher numbers to more intense stimuli and lower numbers to less intense stimuli. It should be noted that despite the well-known severe short-term memory deficits of Korsakoff patients, a previous study [1] showed that such patients are able to scale stimulus intensities adequately even when the standard stimulus is presented only once per continuum. Shades ofgray. The stimuli for the assessment of grayness were eight Munsell neutral gray cards (3 x 5 in., matte finish, Munsell Color Company, Inc.), each mounted on white poster board measuring 8 x 10 in.

*After the study had been completed it was judged that one right hemisphere subject (8) probably had had normal pressure hydrocephalus at the time of testing, in which case he may have had some bilateral hemispheric impairments; in any case, his right hemisphere dysfunction was markedly greater than any left hemisphere difficulties.

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The cards ranged from values 2 to 9 (in l.OO/value intervals) on the Munsell scale, value 2 being very dark

and value 9 very light. Subjects were asked to assess how dark the stimuli were, and value 6 was used as the standard stimulus. Stimuli were viewed under neutral daylight conditions, or, when daylight was poor, with normal overhead room lighting. Sizes of circles. The stimuli for the assessment of circle size were eight circles, each drawn with a felt-tip pen and a compass on heavy white construction paper (14 x 14 in.) and mounted on a white poster board square (16 j: 16 in.). The radii of the circles (increasing by geometric steps of 1.6) were 5, 8, 12.8, 20.5, 32.8, 52.4, 83.9 and 134.2 mm. The radius of the standard circle was 32.8 mm. In testing, a circle was shown to the subject for a few seconds, and he was then asked to make his judgment. Conq~/exify nf’grirls. There were seven stimuli for the assessment of grid complexity. Each grid was composed of a symmetrical arrangement of crossed lines within a square 8 x 8 in., oriented in diamond fashion on white poster board (12 x 12 in.). The diamond orientation was used to discourage subjects from counting the crossed lines. The index of complexity was the number of divisions in the grid, and the number of divisions for each (increasing by geometric steps of 2) was as follows: 4, 16, 64, 256, 1024, 4096, 16384. The number of divisions in the standard grid was 256. Subjects were initially instructed to judge how complex each grid was, but as a number of the brain-damaged subjects had difficulty understanding this instruction, subjects were asked to judge how many lines and spaces each grid had in it, e.g. a great many, only a few, or an intermediate number, and to use the numbers (from 1 to 1000) to express this judgment. In all three visual tasks, right hemisphere patients with visual field defects or with left visual neglect were positioned during testing so that the visual stimuli would tend to fall within the patient’s right visual field. Auditory intemity. Seven levels of white noise (band width approx O-8000Hz) were presented to the subjecls: 35, 45, 55, 65, 75, 85, 95 dB (pressure re 20pN/mZ). The noise source was a Grason Stadler noise generator (model 9018). A Grason Stadler 10 R attenuator (model 1293) allowed for adjustments of the clB level, while a Simpson 715 voltmeter measured the voltage across the earphones. Subjects wore Telephonics TDH-49 IO Q earphones, used binaurally. Each stimulus was presented for approx. 2 sec. Sixty&e decibels was selected as the standard stimulus. Onor intemity. iv-butyl alcohol (1-butanol) was the odorant used in the assessment of olfactory intensity scaling. An eight-channel air-dilution olfactometer (designed by Dr. Andrew Dravnicks, Illinois Institute of Technology) allowed for the separate presentation of eight different saturation levels of butanol at a 4ow rate of approx 120 ml/min. Air was provided by a laboratory air tap and was prefiltered three times (40C Beach Sta-Dri filter, 1302-3 Hankison oil filter, 1502-2 Hankison odor filter). Preliminary pressure regulation was achieved by a Watts 216-2 pressure regulator. The eight intensity levels (increasing by geometric steps of 2) were 0.16, 0.31, 0.63, 1.25, 2.5, 5, 10 and 20”/, saturation (from I1 to 1400 ppm). The standard stimulus was 2.5% saturation. The subject was asked to smell each stimulus for a few seconds and then to make his judgment. Approximately 30 set intervened between stimuli to reduce adaptation. An adjacent laboratory hood fan system aided in the recirculation of room air. Taste intensity. Eight different concentrations of sodium chloride in distilled water were used in taste intensity scaling (increasing by geometric steps of 2): 0.008, 0.016, 0.031, 0.063, 0.125, 0.25, 0.5 and 1.0 M. The standard stimulus was the 0.125 M solution. Fresh solutions were made each week, and were maintained at room tcmpcraturc. The subject sipped about f oz of solution at a time from a small unmarked paper cup, held the solution in his mouth for a few seconds, and then expelled it before making a judgment. A rinse with distilled water followed each test stimulus. Statisticnl analyses

Several different analyses were performed on the results of each scaling task. The first analysis was a comparison of the subjects’ Pearson product-moment correlation coefficients (r), which had been derived from a regression analysis [17] of the log transformations of all intensity estimates (four estimates per stimulus intensity level per task). These coefficients were thus a measure of the correlation between the subject’s subjective intensity estimates and the objective stimulus intensities in log-log coordinates. In terms of the power law for psychophysical functions, these were the coefficients of correlation between log w and log cp in the linear function which results from graphing magnitude estimation data on a log-log scale (log QJ-y b log cp + log K). Fisher’s r to Z transformation was performed on the Y values, since this transformation tends to normalize distributions ofcorrelation coc%.icnts [It:]. A simple analysis of variance (ANOVA) was then applied to the: Z values. \Vhen a signilicrunt f‘ Y,T.%obtained from the ANOVJZ, :I Newman-Keuls test was used to find which pairs of group means dilfcred si&icantly. A second analysis compared the individuals’ mean raw stimulus ratings (i.e. the mean of the four cs:iinatt:s for each stimulus intensity lsvcl) in a two-factor ANOVA wiih repJat
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of the variance-covariance matrices. When a significant interaction effect was found, the simple main effects of diagnostic category at each stimulus intensity level were analyzed further according to accepted procedure. The required level of significance for a simple main effect was set at O.OOS,*and when this criterion was met, a Scheffe test was used to ascertain which pairs of means differed. In the case of the three sensory tasks where a detection threshold estimate was feasible (audition, olfaction. gustation), a third analysis compared thresholds. The following method, based on the fact that each stimulus level was presented four times in each scaling task, was used to estimate detection thresholds. First, the level which the subject could detect (i.e. assigned a number greater than one) only fwo out of four times ‘was found. Then the level which the subject could detect three out of four times was found, and the level ntermediate to the former and the latter (the arithmetic mean) was considered to be the threshold. Thresholds ‘were compared by means of simple one-way ANOVAs and subsequent Newman-Keuls tests. The required level of significance for both types was 0.05. Finally, where thresholds were found to be elevated, a subsequent ANOVA of the slopes of the individuals’ regression equations for suprathreshold values was performed in order to reveal possible recruitment, or steepening, phenomena. This ANOVA compared slope values obtained from the data after a threshold correction had been performed [20]. For each group the mean detection threshold (C,), estimated according to the method stated above, was subtracted from each of the suprathreshold stimuli (C), to yield the effective stimulus (C -C,). Regression analyses were then performed for each individual’s magnitude estimates plotted against the effective stimuli (in log-log coordinates), and the ANOVA compared the slopes of these corrected functions. In addition to the four types of analysis reported above, ANOVAs were also performed on the slopes of the subjects’ intensity functions in log-log coordinates. The slopes are estimates of the exponents of the psychophysical functions (h in Stevens’ power law w = Kcpb, where w is perceived intensity and cpis stimulus intensity). Slopes have traditionally figure prominently in the usual psychophysical studies employing normal subjects only, with no comparison groups. As there were no significant findings from any of the ANOVAs of slopes, these analyses will not be described further.

RESULTS Shau’es oj’ grub’ There were two significant findings in the analyses of group performances on this task, both of which showed the right hemisphere group to be deficient in their ability to scale shades of gray. First, the ANOVA for correlation coefficients showed a significant group effect, F(3, 41) = 4.82, P < 0.01, with the right hemisphere patients’ Z jralues lower than those of both normal controls and alcoholic subjects, P < 0.05. This finding indicates that right hemisphere patients were significantly less accurate in their assignment of values to these visual stimuli. Second, on the two-factor ANOVA, where the stimulus level main effect, group main effect, and stimulus level by group interaction effect were all significant,f further analysis of simple main effects revealed right hemisphere scaling abnormalities. The two darkest shades of gray were rated significantly lower by the right hemisphere group than by either normal or alcoholic groups, (P < 0.001). This result suggests a reduced perceived intensity of more intense stimulus values in this continuum or perhaps a reduced ability to discriminate among shades of gray at the darker end of the continuum. Figure 1 shows the group mean estimates for shades of gray plotted on a log-log scale for convenience. For purposes of comparison, the solid line shows the scaling judgments of the normal controls, while the dotted line represents the judgments of the group which showed scaling abnormalities (right hemisphere group). It can be seen that the intensity function for shades of gray is concave downwards, as STEVENS and STEVENS have noted [21]. Sizes

qf circles

Findings difficulties,

for this task implicated with right hemisphere

both Korsakoff and right hemisphere groups as having patients impaired on two indices, and Korsakoffs on

*This value yielded a signiticancc Icvel fo;_ the family of comparisons of 0.04 for continua with 8 stimulus intensity l~vcls, and of 3.0.35 for coniinxl with 7 stimulus intensity levels. -iTable 2 provides the results of the two-factor ANOVAs for all tasks.

328

B. P. JONES,N. BIERS,

H. R. MOSKOWITZand K. MONTGOMERY

o Normals o Alcohol,cs . Korsakoffs ORight

hemtspheres

FIG. 1. Group mean ratings of shades of gray, graphed on log-log coordinates. The solid line represents the judgments of the normal control group, while the dotted line represents the judgments of the group which showed scaling abnormalities (right hemisphere group).

Table 2. Results of two-factor ANOVAs of magnitude cstlmatci Group main effect (G) -_. --____ (if‘ F Grays 3,41 3.21* Circles 3 41 3.02* Grids 3141 3.88* Loudness 3,41 2.06 Odor 3,41 2.61 Taste 3,41 2.92” Task ____

*P < 0.05. **p < 0.01.

Konservative

test.

Stimulus level main effect (S) dfi

I,41 1,4L 1,41 I,41

F

465.28”” 481.39”” 328.46*” 327.92** I,41 78.32”* 1,41 239.52*:’

Interaction (G ’ S) c/f 3.41 3.41 3,41 3,111 3,41 3.41

F

5.93”” 2.93” 4.05” 2.52 4_.J9’”

4.71*’

OLFACTORY AND GUSTATORY CAPACITIES OF ALCOHOLIC KORSAKOFF PATlENTS 1000~

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: ._ 13

2 IO -

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FIG. 2. Group mean ratings of sizes of circles, graphed on log-log coordinates. The solid line represents the judgments of the normal control group, while the dotted line represents the judgments of the group which showed scaling abnormalities (right hemisphere group). only one. The ANOVA for correlation coefficients showed a significant group difference, F(3,41) = 15.25, P < 0.01, with the Korsakoffs’ 2 values lower than those of both alcoholic and normal groups (P < O.Ol), while the right hemisphere values were lower than those of the normal group (P < 0.01). The two-factor ANOVA yielded a significant stimulus level main effect, group main effect, and interaction effect. The subsequent analyses of simple main effects showed that right hemisphere patients judged the largest circle to be significantly smaller than did alcoholics or normals (P -c 0.001). These results suggest that both Korsakoff patients and right hemisphere patients have a reduced ability to judge sizes of circles accurately, and that right hemisphere patients further perceive the size of the largest circle as smaller than other groups do.

Complexity of grids

In the estimation of grid complexity, as in the estimation of circle size, both Korsakoff patients, and to a greater extent, right hemisphere patients, were impaired. The ANOVA for correlation coefficients showed a significant difference among group means, F(3,41) = 5.47, P < 0.01, and the subsequent Newman-Keuls test showed that both Korsakoffs and right hemisphere patients had correlation coefficients significantly lower than those of the normals (P e: 0.05, both comparisons). In the two-factor ANOVA, where again both main effects and the interaction effect were significant, analysis of simple main effects showed that once again right hemisphere patients rated stimuli at the upper end of the

330

B. P. JONES, N. BUTIZRS, H. R. MOSKOWITZand K. MONTGOMERY

o Alcoholics 4 Korsokoffs ORight

hemispheres

FIG. 3. Group mean ratings of complexity of grids, graphed on log-log coordinates. The solid line represents the judgments of the normal control group, while the dotted line represents

the judgments of the group which showed scaling abnormalities (right hemisphere group). continuum lower than did other groups. The second most complex grid was rated significantly lower by right hemisphere patients than by Korsakoffs or by alcoholics (P < 0.005, both comparisons), while right the hemisphere group’s ratings of the most complex grid were lower than those of either alcoholics or normals (P < 0.001, both comparisons). Figure 3 presents the data for grid complexity. Auditory intensity Analyses of the data for intensity scaling of loudness yielded only a single significant finding, suggestive of some deficiency in the right hemisphere patients. Although the ANOVA for correlation coefficients yielded a significant result, F(3, 41) = 3.54, P < 0.05, subsequent comparison of the means by a Newman-Keuls test showed no significant pairwise differences. The two-factor ANOVA revealed the expected stimulus level main effect, a nonsignificant group main effect, and an interaction effect which was significant at approximately the 0.07 level in the conservative F test. A subsequent test of simple main effects showed that the only significant deviation was the lower rating of the loudest noise by right hemisphere patients than by normals (P < 0.005). Figure 4 presents the data for loudness estimation. Analysis of auditory detection thresholds showed no significant group differences, F(3, 41) = 1.13. P > 0.25, with all thresholds at approx 40 dB. Odor intensity Analyses of the olfactory data yielded results which largely confirmed previous findings [I]. First, the ANOVA for correlation coefficients yielded a significant result, F(3, 41) -6.96, P < 0.01, and the subsequent multiple comparison test sho\ved that Korsakoff patients had lower correlation coefficients than all other groups (P ,:- 0.01 for all three comparisons). The two-factor ANOVA resulted in a significant stimulus level main effect

OLFACTORY

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Audition

o Normals oAlcohollcs A Korsakoffs ORlght

II

35

hemispheres

I

I

I

I

I

I

45

55

65

75

85

95

d0

SPL,

re

0.0002

dyn /cm’

FIG. 4. Group mean ratings of loudness, graphed on log-log coordinates. The solid line represents the judgments of the normal control group, while the dotted line represents the judgments of the group which showed scaling abnormalities (right hemisphere group).

and interaction effect, and the subsequent analysis of simple main effects showed that Korsakoffs rated the second strongest odor concentration lower than both right hemisphere patients (P < 0.005) and alcoholics (P < O.OOl), and that they rated the strongest concentration lower than all other groups (P < 0.001 for all three comparisons). The olfactory results are presented in Fig. 5. A comparison of detection thresholds revealed a significant group difference, F(3, 41) = 7.84, P < 0.01, which was due to the fact that Korsakoffs had higher apparent thresholds than all other groups (P < 0.01 for Korsakoffs vs each other group). The mean detection threshold for Korsakoffs* was approx 8% saturation, while for the other groups it ranged from 0.2 to 0.5% saturation. A comparison of the post-threshold-correction slopes (omitting the two Korsakoff patients who were unable to smell any of the stimuli) revealed an unexpected group difference: Korsakoffs had the lowest slope value and differed only from alcoholics, who had the steepest slope (P < 0.01). This finding indicates that, unlike the steepening effect seen for Korsakoffs’ ratings of suprathreshold stimuli in the previous study, here the Korsakoffs’ intensity functions for stronger concentrations had a flattened slope. Taste intensity No group

differences

*For the two Korsakoffs saturation.

were seen in the correlation

coefficients

of the gustatory

who were unable to smell any stimuli, the threshold

intensity

was taken IO be 20”/;;

B. P. JONES, N. BUTTERS, H. R. MOSKOWITZand K. MONTGOMERY

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FIG. 5. Group mean ratings of odor intensity, graphed on log-log coordinates. The solid line represents the judgments of the normal control group, while the dotted line represents the judgments of the group which showed scaling abnormalities (Korsakoff group).

F(3,41)= 2.64,P -:0.10.The two-factor ANOVA demonstrated significant main effects for stimulus level and diagnostic category and a significant interaction effect. An analysis of simple main effects showed that Korsakoffs rated the second strongest salt solution lower than normals (P < 0.001) and the strongest solution lower than both alcoholics and normals (P < 0.001). Figure 6 presents the scaling results for taste. The taste thresholds, although slightly higher for the alcoholics (0.046 M) than for the other groups (0.012-0.029 M), were not significantly different, 1;(3, 41) = 2.10, P > 0.10. functions,

DISCUSSION The first result of note is that previous findings concerning the scaling of butanol odor, loudness, and shades of gray by alcoholic Korsakoff patients [l] were replicated. Korsakoffs demonstrated normal intensity scaling of shades of gray and loudness of white noise. In contrast they were quite impaired in their olfactory scaling capacities. As in the previous study, the group as a whole showed elevated thresholds for the detection of butanol odor as opposed to a range of 0.2-O.Ss/;I for the other groups). Second, their (8% saturation correlation coefficients (stimulus versus response) were lower than those of all other groups, indicating that their odor intensity ratings are less accurate than those of the other groups. And third. Korsakoff patients scaled the two strongest odor stimuli significantly lower than

OLFACTORY

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FIG. 6. Group mean ratings of taste intensity, graphed on log-log coordinates. The solid line represents the judgments of the normal control group, while the dotted line represents the judgments of the group which showed scaling abnormalities (Korsakoff group).

did other groups; Fig. 5 shows a trend in this direction for other stimulus points as well, and in general Korsakoffs appeared less able to discriminate among the differing odor intensities. The present study did not demonstrate a steepening or recruitment effect for Korsakoffs’ judgments of suprathreshold odors, as had been suggested by the previous study. An explanation for this difference is not readily available. The most interesting new finding for the Korsakoff group was that of a deficit in intensity scaling of salt solutions. Korsakoff patients judged the two strongest salt solutions to be significantly weaker than other subjects did. They were not impaired in their overall ability to track the stimuli (i.e. their correlation coefficients were similar to those of normals), and they had normal saline detection thresholds as estimated from the sensory functions. However, their subnormal scaling of the strongest salt solutions cotirmed a prediction of a gustatory deficit which was made on the basis of damage to the ventral medial nucleus of the thalamus [2]. It should be noted that since only about 60% of patients with either or both components of the Wernicke-Korsakoff syndrome may have lesions in the thalamic relay for the gustatory pathway [2], one would not expect a taste deficit for the group as a whole to be as striking as their olfactory impairment. The finding of a significant, although slight, abnormality in taste intensity scaling by alcoholic Korsakoff patients makes it appear even less likely that their olfactory deficits are due to olfactory bulb or olfactory nerve damage secondary to head trauma. Even if

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R. P. JONES, N. BUTTERS, H. R. MOSKOWITZand K. MONTGOMERY

one were to accept such an explanation for Korsakoffs’ deficits in odor perception, head trauma could scarcely account for their abnormality in taste intensity scaling. Furthermore, the chronic long-term alcoholics in this study, who were just as likely as the Korsakoff syndrome patients to have sustained significant head trauma, were normal in their scaling of both olfactory and gustatory stimuli. Nor is it plausible that the Korsakoffs’ taste deticit is due to a greater incidence of cigarette smoking in this group. While the Korsakoff patients had on the average smoked more than the normal controls, and while smoking has been linked with elevated detection thresholds for at least one taste, quinine [22, 231, the alcoholic subjects and right hemisphere patients had smoking histories comparable to those of the Korsakoff patients, and yet did not differ from normals in their scaling of taste intensities. The results obtained for the right-hemisphere lesion group clearly demonstrate that the Korsakoffs’ impairments in the chemical senses are not merely due to a task complexity effect. Right-hemisphere patients had no difficulty in the intensity scaling of odor and taste but were impaired on all three visual tasks. Not only were they unable to scale all three types of visual material as accurately as other groups (as shown by their lower correlation coefficients), but they showed a reduced appreciation of stimuli at the upper end of each continuum. These findings suggest that the well known impairments following lesions of the posterior portion of the right hemisphere on higher order visual and visuospatial tasks (e.g. [l1,2?,25,261) are mirrored on a more basic perceptual level. Apparently, the visuoperceptual impairments of right hemisphere patients are not limited to stimuli with a spatial component but are evident even on a task requiring brightness judgments. It is of interest to note that the Korsakoffs were deficient on the correlation coefficient index in the scaling of circles and grids. Alcoholic Korsakoff patients have previously been found to be impaired on a number of visuoperccptual and visuospatial measures [27-311, as have nonamnesic alcoholics [32-351. There is evidence that chronic, long-term alcohol abuse is accompanied in a large number of casts by significant cerebral atrophy 136-411, probably both cortical and paraventricular. It may be that the Korsakoffs’ visual scaling deficits are a manifestation of cortical atrophy, and that Korsakoffs reprcscnt an especially severe subgroup in the continuum of long-term alcoholics. The only finding from the auditory task in this study was lower scaling of the loudest noise levels by right hemisphere patients than by other groups. An abnormality of loudness estimation in the right hemisphere group may be due to the fact that a number of these patients had right temporal lobe damage, and the right temporal lobe appears to be dominant for the processing of non-verbal auditory material [42]. It is by now apparent that all of the group intensity scaling anomalies revealed by the two-factor ANOVA of the raw mean estimates assumed the same form: lower subjective estimates of the most intense stimuli within a continuum. The real significance of this phenomenon is unknown. It could be suggestive of a modality-specific sensory dulling, so that, for example, a patient with a central gustatory perceptual defect is simply not as responsive to intense stimuli in that modality. It could be indicative of a reduced ability to discriminate among different stimulus intcnsitics. w!lic!l shows ~117at the high end of the stimulus continuum. and not at the lower end, bccausc of the notorious \,ariability of all subjects’ estimates of pcrithreshold stimuli. Whatcvir its signiftcancc. ti;c fact that this \: ith the predictions c:f group dificitc phenomenon appcarcd in a rattcrn quite consonant suggests that it is a genuine manifestation of central neur-a, 1 sensory c!&its.

OLFACTORYAND OUSTATORYCAPACITIESOF ALCHOLICKORSAKOFFPATIENTS

335

Acknowledgements-This report is based on a doctoral dissertation submitted by BARBARA PENDLETON JONESto the Graduate School of Boston University. The research was supported by a National Research Service Award to BARBARA PENDLETONJO&ESand Boston University School of Medicine (U.S. Public Health Service Fellowship Fl AA05033-Ol), by NIAAA grant AA00187 to Boston University School of Medicine, and by funds from the Medical Research Service of the Veterans Administration. The authors wish to thank Dr. JAMESLILJESTRANDand the trustees and staff of the Braintree Hospital and Dr. ALLBN ADINOLFIof the Center for Problem Drinking of the Boston VA Outpatient Clinic for the opportunity to test patients. Thanks are also due to LEON KLARMAN of the U.S. Army Natick Laboratories for assistance in data analysis, to ALICE MEDALIA for help with data collection, and especially to DRS ALLAN F. MIRSKY and DOUGLAS MACNAIR for their helpful comments on an earlier draft of this report.

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Acad. Sci., U.S.A. 62, 30-37, 1969. (3. HENKIN, R. I. and SMITH, F. R. Hyposmia in acute viral hepatitis. Lancet 1, 823-826, 1971. 14. HENKIN,R. I. Disorders of taste and smell. JI Am. Med. Assoc. 218,1946, 1971. 15. HENKIN, R. I., TALAL, N., LARSON, A. L. and MATTERN, C. F. T. Abnormalities of taste and smell in Sjogren’s syndrome. Am. intern. h&d. 76, 375-383, 1972. 16. CERMAK,L. S. and BUMXRS, N. Information processing deficits of alcoholic Korsakoff patients. Quart.Jl. Stud. Alcohol 34, 1110-1132, 1973. 17. KLARMAN,L. E. and MOSKOWITZ,H. R. PSYCMB, a computer program to analyze magnitudeestimation and cross-modality matches. Unpublished computer program, U.S. Army Natick Laboratories, Natick, Massachusetts, 1974. 18. HAYS, W. L. Statistics. Holt, Rinehart & Winston, New York, 1963. 19. WINER, B. J. Statistical Principles in Experimental Design. McGraw-Hill, New York, 1962. 20. MARKS, L. E. and STEVENS,J. C. The form of the psychophysical function near threshold. Percept.

Psychophys 4, 315-318, 1968. 31. STEVENS,S. S. and STEVENS,J. C. The dynamics of visual brightness. Report PPR 246. Harvard University, Laboratory of Psychophysics, Cambridge, Massachusetts, 1960. 22. KRUT, L. H., PERRIN, M. J. and BRONTE-STEWART,B. Taste perception in smokers and non-smokers. Br med. J. 1, 384-387, 1961. :13. KAIXA~U,A. I?.,G~:x~i\ix_r, C. V. an,.I ”c~!xill-~, R. Taste thresholds for biltcriix and cig !rcttc smoking. h’nflr/.r, Lo/r
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28. OSCAR-BERMAN,M. Hypothesis testing and focusing behavior Korsakoff patients. Neuropsychologia 11, 191-198, 1973.

during concept formation

by amnesic

29. GLOSSER,G., BUTTERS,N. and KAPLAN, E. F. Visuoperceptual processes in brain damaged patients on the Digit Symbol Substitution Test. Int. J. Neurosci. 7, 59-66, 1977. K. and ADI~XOLFI, A. Some comparisons of the memory 30. BUYERS, N., CERMAK, L. S., MONTGOMERY, and visuoperceptive deficits of chronic alcoholics and patients with Korsakoff’s disease. Ale. clik exp. Res. 1, 73-80, 1977.

31. KAPUR, N. and BUTTERS,N. An analysis of visuoperceptive deficits in alcoholic Korsakoffs and longterm alcoholics. J. Stud. Alcohol. In press. 32. FITZHUGH, L. C., FITZHUGH,K. B. and REITAN, R. Adaptive abilities and intellectual functioning of hospitalized alcoholics; further considerations. Q. JI Stud. Alcohol 26, 402411, 1965. 33. GOLDSTEIN,G. and CHOTLOS,J. Dependency and brain damage in alcoholics. Percept. mot. Skills 21, 135-150, 1965. 34. GOLDSTEIN,G. and SHELLY,C. H. Field dependence and cognitive, perceptual, and motor skills in alcoholics. Q. Jl Stud. Alcohol 32, 29-40, 1971. 35. JONES,B. M. and PARSONS,0. Specific vs generalized deficits of abstracting ability in chronic alcoholics Archs. gen. Psychiat. 26, 380-384, 1972. 36. TUMARKIN,B., WILSON, J. D. and SNYDER,G. Cerebral atrophy due to alcoholism in young adults. U.S. Armed Forces med. J. 6, 67-74, 1955. 37. COURVILLE,C. B. Effects ofAlcohol on the Nervous System of Mm. San Lucas Press, Los Angeles, 1966. 38. FERRER, S. Complicationes Neurologicas Crouicas dcl Alcoholismo. Editorial Universitaria, Santiago, Chile, 1970. 39. BREWER,C. and PERRETT,L. Brain damage due to alcohol consumption: an air-encephalographic, psychometric and electroencephalographic study. Br. J. Add&. 66, 170-182, 1971. 40. Fox, J. H., RAMSEY, R. G., HUCKMAN, M. S. and PROSKE,A. E. Cerebral ventricular enlargement: chronic alcoholics examined by computerized tomography. JI Am. Med. Assoc. 236, 365-368, 1976. 41. KIRCHER, J. P. and PIERSON, C.-A. Toxicomanies et atrophie cerebrale. Essais therapeutique bases sur la pneumoencephalographie. Rev. neurol. 94, 607-610, 1956. 42. MILNER, B. Laterality effects in audition. In Interhemispheric Relatiom and Cerebral Dominance, V. B. MOUNTCASTLE (Editor), pp. 177-195. Johns Hopkins, Baltimore, 1962.

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Deutschsprachige Zusammenfassung: Die psychophysische Dlethodeder GrBRenschZtzung wurde verwendet,

331