11
Biologicul Psycho/o~ 23 (1986) 127-137 worth-Holiand NASAL AIRFLOW ASYMMETRIES AND HUMAN PERFORMANCE Raymond KLEIN *, David PILON and Susan PROSSER Deparrment of Psychology, Dalhousie b’niversity, Halifax, Nova Scotia, Canada David SHANNAHOFF-KHALSA ** The Sulk Institute for Biologicul Studies Accepted for publication 16 April 1986 Recent studies of the nasal cycle and forced u&nostril breathing have demonstrated that integrated EEG amplitudes are greater over the hemisphere contralateral to the dominant (less congested) or unblocked nostril. Two experiments were designed to determine if asymmetries in nasal airflow, occurring naturally as a result of the nasal cycle or artificially as a result of forced uni-nostril breathing have consequences for human performance on verbal and spatial tasks that are preferentially performed by the left and right hemispheres respectively. A significant relation- ship was obtained between the pattern of nasal airflow with normal breathing and relative spatial vs verbal performance. Forced urn-nostril breathing had no effect on performance. The purpose of this study was to determine if the quality of performance on he~sphere specific tasks (spati~/verbal) is related to lateral asymmetries in the pattern of nasal airflow. The existence of certain ultradian rhythms forms the background for this study. A variety of psychological and physiological parameters show cyclic oscillations with periods in the 80-120 min range. The best known of these is the alternation between REM and NREM phases during sleep (Aserinsky & Kleitman, 1953). Many other parameters, including gastric contractions and secretions, oral activity, daydrea~ng content, and magnitude of the spiral after-effect also exhibit rhythms with similar variations in periodicity (for reviews see Kripke, 1974; Lavie, 1982). Kleitman (1963) used the term ‘basic rest activity cycle’ (BRAC) to express the idea that these various parameters reflect a basic &radian rhythm that continues throu~out *Send correspondence to: Raymond Klein, Department of Psychology, Dalhousie University, Halifax, Nova Scotia B3H 451, Canada **Current address: The Khalsa Foundation for Medical Science, P.O. Box 2708, Del Mar, CA92014, U.S.A. 0301-0511/86/$3.50 0 1986, Elsevier Science Publishers B.V. (North-Holland) 127

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Biologicul Psycho/o~ 23 (1986) 127-137 worth-Holiand

NASAL AIRFLOW ASYMMETRIES AND HUMAN PERFORMANCE

Raymond KLEIN *, David PILON and Susan PROSSER

Deparrment of Psychology, Dalhousie b’niversity, Halifax, Nova Scotia, Canada

David SHANNAHOFF-KHALSA **

The Sulk Institute for Biologicul Studies

Accepted for publication 16 April 1986

Recent studies of the nasal cycle and forced u&nostril breathing have demonstrated that integrated EEG amplitudes are greater over the hemisphere contralateral to the dominant (less congested) or unblocked nostril. Two experiments were designed to determine if asymmetries in nasal airflow, occurring naturally as a result of the nasal cycle or artificially as a result of forced uni-nostril breathing have consequences for human performance on verbal and spatial tasks that are preferentially performed by the left and right hemispheres respectively. A significant relation- ship was obtained between the pattern of nasal airflow with normal breathing and relative spatial vs verbal performance. Forced urn-nostril breathing had no effect on performance.

The purpose of this study was to determine if the quality of performance on he~sphere specific tasks (spati~/verbal) is related to lateral asymmetries in the pattern of nasal airflow. The existence of certain ultradian rhythms forms the background for this study. A variety of psychological and physiological parameters show cyclic oscillations with periods in the 80-120 min range. The best known of these is the alternation between REM and NREM phases during sleep (Aserinsky & Kleitman, 1953). Many other parameters, including gastric contractions and secretions, oral activity, daydrea~ng content, and magnitude of the spiral after-effect also exhibit rhythms with similar variations in periodicity (for reviews see Kripke, 1974; Lavie, 1982). Kleitman (1963) used the term ‘basic rest activity cycle’ (BRAC) to express the idea that these various parameters reflect a basic &radian rhythm that continues throu~out

*Send correspondence to: Raymond Klein, Department of Psychology, Dalhousie University, Halifax, Nova Scotia B3H 451, Canada

**Current address: The Khalsa Foundation for Medical Science, P.O. Box 2708, Del Mar, CA92014, U.S.A.

0301-0511/86/$3.50 0 1986, Elsevier Science Publishers B.V. (North-Holland)

127

128 R. Klein et al. / Nostrrls and performance

the day. 1 There is also a cyclic alternation in left vs right nasal airflow efficiency, which is called the nasal cycle (Keuning, 1968). Its period varies widely from about 1 to 8 hours with a mean of about 2-3 hours during waking in humans (Hasegawa & Kern, 1977; Keuning, 1968; Soubeyrand, 1964). The nasal cycle is controlled by sympathetic/parasympathetic innervation of the nasal mucosa. When sympathetic activity to one side dominates, the result is vaso-constriction and thus decongestion on that side, while the enhanced parasympathetic activity on the other side simultaneously results in congestion (Keuning, 1968; Stoksted, 1953). The brain mechanisms underlying the nasal cycle are not well understood. It is known that stimulation of areas of the hypothalamus associated with defence reactions produces nasal vasoconstric- tion (Eccles & Lee, 1981). It seems unlikely that the hypothalamic responses so far observed can completely account for the nasal cycle however, since the response to unilateral stimulation was usually bilateral, and even when ipsi- lateral vasoconstriction was observed it was not accompanied by contralateral vasodilation.

Although the apparent differences in period suggest that the BRAC and the nasal cycle may not be related, two lines of research suggest a linkage. First, it has been proposed that the BRAC is characterized by a rhythmic alternation in hemispheric efficiency or dominance (Broughton, 1975). In a daytime study of performance, Klein and Armitage (1979) obtained evidence in support of this proposal. They found that performance on verbal and spatial tasks showed 90-100 min oscillations which were 180” out of phase (when perfor- mance on one task was improving performance on the other was declining). 2 Second, since by its very nature the nasal cycle involves lateralized activity, one might hypothesize that it is in some way linked to the changes described above. Two studies by Werntz, Bickford, Bloom and Shannahoff-Khalsa (1981, 1983) of EEG and its relation to nasal airflow support this possibility. In one study (Werntz et al., 1983) nasal airflow and EEG were monitored simultaneously for extended periods. The results showed that integrated EEG

t Although the existence of daytime rhythms in these various measures is established, their

relation to the REM/NREM alternation during sleep and their correlation in the daytime are

controversial issues (Kripke, 1974; Lavie, 1982). Therefore, our use of the term BRAC to refer

to a single daytime rhythm with a period between SO-120 min should be viewed as tentative and

hypothetical. ’ Although one group of investigators has failed to replicate this finding (Kripke, Fleck,

Mullaney, & Levy, 1983) there is reason to believe (Gopher & Lavie, 1982) that their use of

knowledge of results and monetary incentives may have masked performance oscillations with

periodicities in this range. In addition, converging evidence from studies of left vs right

hemisphere task performance upon awakenings from REM and NREM sleep (Gordon, Froo- man, & Lavie, 1982; Lavie, Matanya, & Yehuda, 1984) provides support for the association

between the BRAC and shifting hemispheric efficiency.

R. Klein et al. / Nostrils andperformance 129

amplitudes were greater over the hemisphere contralateral to the dominant nostril, and when nasal airflow shifted, so did integrated EEG amplitudes. 3,4 In an extension, Werntz et al. (1981; this presented paper has since been submitted for publication, Werntz, Bickford, & Shannahoff-Khalsa, 1986) demonstrated that the EEG pattern could be modified by forced uni-nostril breathing. In particular, when asked to breath through the non-dominant nostril, there was a shift in the distribution of EEG activity over the two hemispheres. Although most EEG researchers associate greater integrated EEG amplitudes with hemispheric inactivity (Donchin, Kutas, & McCarthy, 1977; but see Ray & Cole, 1985), Werntz et al. (1981, 1983) made the opposite assumption which is discussed in detail in Werntz et al. (1986). Thus, although the data of Werntz et al. indicates a relation between hemispheric activation and the pattern of nasal airflow, the direction of this relationship remains to be determined.

With these facts reviewed, we will now turn to some outstanding questions. Does the nasal cycle play a causal role in the cyclic changes in cognitive style observed by Klein and Armitage (1979)? Are both rhythms the consequence of some other process, such as the BRAC, or is there no relation between them? Is the asymmetric brain activity that is associated with asymmetrical nostril breathing functionally significant in mental life, or is it only a reflection of non-cognitive processes? Two experiments were designed to help answer these questions. Our strategy was circumscribed. 5 Each experiment sought to determine if relative performance on verbal vs spatial tasks: (1) is correlated with naturally occurring asymmetries in nasal airflow; and (2) can be in- fluenced by forced uni-nostril breathing. In particular, if greater ‘total EEG over one hemisphere is an indication of greater relative activation of that hemisphere, then right handed subjects (whose language skills are located primarily in the left hemisphere) should show a relative verbal performance advantage when the right nostril is dominant or unobstructed, while a relative

3 For 17 out of the 19 subjects reported to show shifts in the nasal cycle by Werntz et al. (1983)

only integrated total EEG was reported. For 1 subject integrated beta, and for another

integrated alpha, beta, theta and delta were reported in addition to total EEG. The magnitude and direction of the nasal-EEG correlation with these other frequencies was the same as for

total EEG.

4 The terms dominant and non-dominant nostril will be used to refer to the nostril with more or

less efficient flow of air, respectively.

5 A more difficult, but also more powerful strategy would be to monitor nasal airflow, EEG and performance in several subjects over an extended period are pursuing such strategies independently.

of Klein and Shannahoff-Khalsa

130 R. Klein et al. / Nostrils and performance

spatial performance advantage should be observed with left nostril breathing. 6 If, on the other hand, greater ‘total EEG’ implies hemispheric inactivation, then the opposite results should be obtained. Finally, no relationship between verbal/spatial performance and nasal airflow asymmetries might indicate that the EEG asymmetries have no consequences for human performance or that our methods are not sensitive enough to detect the changes.

Each experiment examined separately the relationship between nasal air- flow and verbal vs spatial task performance during free breathing, and either during or after a period of forced uni-nostril breathing. The experiments were similar enough that they have been described together. The major difference was that the first experiment used nose plugs in the forced uni-nostril stage of the experiment to block airflow through one nostril, whereas in the second experiment, subjects used the pad of their ipsilateral thumb. The former procedure permits performance tests during forced uni-nostril breathing, whereas the latter does not.

2. Method

2. I. Subjects

The subjects were 126 right-handed male and female volunteers who wrote with a non-inverted posture. They were paid $4-6 for their participation. Thirty four subjects (16 male, 18 female) participated in Experiment 1 and 92 subjects (40 male, 52 female) participated in Experiment 2.

2.2. Materials

Each subject was supplied with a pencil, a small mirror, and a test booklet. Subjects in Experiment 1 were also supplied with noseplugs (rubber clamp type). The test booklet contained general instructions, specific instructions on

6 Data along these lines are reported in an unpublished master’s thesis (Beubel, 1977). Beubel

reported that right nasal dominance and right forced uni-nostril breathing were associated with

relatively better verbal performance. Beubel’s finding with nasal dominance is consistent with our results; in contrast, we found no effect of forced uni-nostril breathing (see Results and

Discussion, below). Three differences between the present study and Beubel’s should be noted

when considering this discrepancy: (1) Her tasks emphasized complex memory processes while

ours emphasized simpler perceptual ones; (2) her sample (all males) was smaller (only 17

subjects contribute to conclusions about forced nostril breathing); (3) all her subjects were practitioners of Kundalini yoga (with between 0.5 and 7 years of experience), while our subjects

were randomly sampled college students. Further discussion of this study and its relation to the present one will await the appearance of an article based on this thesis (currently in preparation

by Khalsa (formerly Beubel) and Shannahoff-Khalsa).

R. Klein et al. / Nostrils and performance 131

each phase of the experiment, paper and pencil tests of verbal and spatial performance, and nasal congestion rating forms. The performance tasks were the same as those used by Klein and Armitage (1979) and involved rapidly deciding if stimulus pairs were the same or different. The stimuli for the verbal task were upper and lower case letter pairs. For the spatial task the stimuli were pairs of random 7 dot patterns. For a more complete description of the tasks see Klein and Armitage (1979).

2.3. Procedure

Subjects were tested in small groups ranging from 4-12. They sat in a group testing room, with plenty of space between subjects. After subjects were assembled, they were given a general overview of the experiment. Then they were given practice on the verbal and spatial tasks and were shown how to monitor their nasal airflow by breathing on a mirror and noting which patch of mist is smaller and or fades more quickly (the non-dominant nostril). Airflow measures, on a scale from - 1 (right dominant) to + 1 (left dominant) were taken before and after the performance tests during free breathing. Manual blockage of one nostril for a period of about 15 min was accom- plished with a nose plug (clamping the septum and side of the nose together) in Experiment 1 (34 subjects), while in Experiment 2 (92 subjects) the pad of the ipsilateral thumb was used to block airflow for 30 min. The sequence of events in each experiment is shown in fig. 1. Subjects performed the verbal and spatial tests during normal breathing (El & E2), while wearing a nose plug blocking off only one nostril (El) or after a 30 min uni-nostril breathing exercise (E2). Note that in Experiment 1, two performance tests were con- ducted while breathing through only one nostril and that each nostril was blocked in turn, with half the subjects starting with their dominant and half their non-dominant nostril (as indicated by the immediately preceding nasal airflow score). In Experiment 2, no tests were taken during uni-nostril breath- ing. Half the subjects in this experiment blocked their dominant, and half their non-dominant nostril. Note that nasal airflow was monitored before and after all performance tests, except those during manual blockage of one nostril.

2.4. Data analysis

The performance tests were scored to determine how many correct responses were made during each test phase for the verbal and spatial tasks. For each phase of each experiment the mean and standard deviation (across subjects) of the verbal and spatial scores were computed. Each subject’s spatial and verbal score for that phase was normalized (converted to 2 scores) by subtracting from it the group mean and dividing by the standard deviation. For each subject and phase a single measure of spatial vs verbal performance was

132 R. Klein et al. / Nostrils and performance

Experiment 1 Block Dominant Block NonDominant

I NPNT,N T, T,:N T, N

Block NonDominant Block Dominant

Experiment 2

Block Dominant

I NP PNT,N N T,N

I lnst~ctions P Practice Performance Test

T Performance Test N Nasal Dominance Measurement

Fig. 1. Sequence of events for each experiment. Dotted lines indicate the 30 min period during

which subjects did forced uni-nostril breathing. Subjects in each experiment were divided into 2

groups, one blocking the dominant the other the non-dominant nostril. In Experiment 1 all

subjects switched nostrils after 15 min. Performance tests (T) were 2 mm with each task (verbal,

spatial) for Experiment 1 and 3 min for Experiment 2. Note that each experiment provides two

performance tests during free breathing.

calculated by subtracting the verbal from the spatial Z score for that phase. A tr~sformed score of 0.0 indicates that the subjects relative spatial/verbal performance was the same as the group average for that phase of the experiment, whereas negative scores indicate relatively better verbal perfor- mance and positive scores indicate relatively better spatial performance.

3. Results

Three kinds of statistical analysis were used to explore the relationship between relative spatial/verbal performance and pattern of nasal airflow in this study. The first analysis examines the correlation between the pattern of airflow for a particular test phase and the spatial-verbal Z score for that test. For this correlation, airflow was the average of the airflow scores before and after the performance assessment. If these were not the same in sign (i.e. a switch in nasal dominance occurred during the performance test) for a given subject, then that subject was not included in calculating the correlation for that test phase. There were two test phases in each experiment that can be

R. Klein et al. / Nostrils and performance 133

Table 1

Correlations between performance and congestion (upper rows) and between change in perfor-

mance and change in congestion (lower rows). (a) Criterion for use of subject was a congestion

change of at least 0.5; (b) criterion for use of subject was a sign change in the congestion score

Experiment

1

2

Combined

1

2

Combined

la

2a

Combined

lb

2b

Combined

Test phase

1

1

4

2

1 “S 4

1 “S 2

1 “S 4

1 “S 2

Correlation df Level of significance

0.303 29 0.1

0.159 85 n.s.

0.197 114 0.05

0.148 28 ns.

0.202 76 0.1 0.187 104 0.05

0.467 3 ns.

0.120 19 n.s.

0.167 22 ns.

0.251 4 ns.

0.161 10 ns.

0.187 14 n.s.

subjected to this analysis (see fig. 1). The results of these analyses are shown in table 1 and fig. 2. Although none of the 4 individual correlations are signifi- cant at the 0.05 level, 2 were marginally significant at the 0.10 level, and all 4 were in the same direction. In such circumstances it is desirable to take advantage of the combined power of the two experiments by pooling the correlation coefficients across the independent samples. 7 When this was done, the correlations for both the first (ri14 = 0.197) and second (rro4 = 0.187) unobstructed periods were significant at the 0.05 level. The direction of this significant relationship is consistent with the claim that right nostril domi- nance is associated with relatively better verbal performance and left nostril dominance is associated with better spatial performance. 8

The second analysis correlated the direction of any change in the pattern of airflow with the direction of change in relative spatial/verbal performance. This test was repeated using two different selection criteria for airflow change. One criterion was to use only subjects who showed a sign change in airflow

When different samples provide correlations between the same variables it is legitimate to combine them to get a single estimate of population correlation (see, e.g. Guilford & Fruchter,

1977, 318-320).

Although the spatial/verbal subtraction score has the advantages of increasing the signal-to-noise

ratio and eliminating certain forms of between subject variance, it was felt that some readers

might be interested in the separate correlations between congestion and the verbal and spatial

performance measures. Combining the correlations across experiments as in table 1, yields the

following: Congestion vs verbal performance, (El Tl +E2 Tl) r1r4 = 0.079, n.s.; (El T4+E2

T2) r,, = 0.032, n.s.; Congestion vs spatial performance, (El Tl + E2 Tl) rr14 = 0.27, p < 0.005;

(El T4+ E2 T2) rrM = 0.21, p i 0.05.

134 R. Kkm et ul. / Nostrils and performance

a l

3 2-

;;i * * *

0

I l .T .

2- c

*

Is * l

z * * * *

zf i- as

:* ** * * *

l i L *

** :** *

0-_:’ * *v----+-y I

i * * **a*

l r

1 1

-1. ** ** l * l * a a ** l

z l * **

‘-2_ * * *

*

-3 I( ’ II -1.0

Right ’ 1%

Left

b

l I *

t

d ** * * *

’ * l *

I* * l l *r

** l **< i ;

* * ---xy-* ** * **

;:* l **; * i

h+ *

l *

** *

I I I I 1

-1.0 Right ’

1.0 Left

Nasal Dominance

Fig. 2. Scatterplots showing relative verbal vs spatial performance as a function of nasal

dominance for each subject. (a) Experiment 1, first test during free breathing; (b) Experiment 1,

second test during free breathing; (c) Experiment 2, first test; (d) Experiment 2, second test.

between the two unobstructed performance tests; the other was to use only subjects who demonstrated a change in nasal airflow above 0.5 units (i.e. l/4 of the scale) during this period. Again, any subject who showed a sign change during a performance test were excluded. The correlations between change in nasal dominance and change in performance were in the same range as those observed for relative performance, and are shown in table 1. They failed to reach significance, however, because of the reduced degrees of freedom.

The third analysis examined the effect of forced uni-nostril breathing. Here, t tests were performed that divide the subjects into 2 groups, those blocking the right and those blocking the left nostril. In El, this involved two t tests, one on the first and one on the second test during forced uni-nostril breathing;

R. Klein et al. / Nostrils andperformance 135

Table 2

Student’s t tests comparing relative verbal vs spatial performance as a function of which nostril

was (El) or had been (E2) breathing freely. Negative numbers indicate relatively better verbal

performance. Number of subjects in each group are shown in parentheses

Phase Unobstructed nostril

R L

f-value

Experiment 1 2 -0.151 (20) 0.215 (14) -0.312

3 0.055 (14) - 0.039 (20) 0.071

2 & 3 (within) - 0.066 (34) 0.066 (34) - 0.679

Experiment 2 2 0.058 (42) - 0.049 (50) 0.081

in E2, this involved one t test on performance during the first test after uni-nostril breathing (as a function of which nostril had been blocked). None of these t values approached significance (see table 2). Further sub-division according to whether the dominant or non-dominant nostril was blocked also failed to produce any significant effects. Since subjects in Experiment 1 blocked each nostril in turn, it was also possible to do a paired t test which evaluated whether blocking the right vs left nostril affected the spatial verbal performance scores. Although the pattern was in the same direction as the correlations, only 20 out of the 34 subjects were affected this way and the t was not even marginally significant (see table 2).

4. Discussion

There was a tendency for subjects exhibiting right nostril dominance to perform verbal tasks better (relative to spatial performance) than subjects exhibiting left nostril dominance. The consistent pattern in 4 separate test phases reinforces this conclusion, and the correlation between airflow and performance was significant in two separate test phases (before and after uni-nostril breathing) when the results of the two experiments were combined. One may question whether this correlation is due to within subject fhtctua- tions in the nasal cycle, or to between subject differences in nasal airflow. That is, the observed correlation might be consistent with the claim that individual differences in nasal dominance are correlated with individual differences in relative verbal vs spatial performance (Levy, Heller, Banich & Burton, 1983). Although this statistical comparison alone is ambiguous on this point, con- verging evidence for the claim that the performance/airflow correlation is due to the nasal cycle is provided by the similar magnitude of the (albeit nonsig- nificant) correlations between performance change and airflow change. A more extensive experiment in which performance and the pattern of nasal

136 R. Klein et ui. / Nostrils and performunce

airflow are both monitored over an interval of time sufficient to observe one or more shifts of nasal dominance will be needed to firmly resolve this issue.

Finally, in this study no effect of forced uni-nostril breathing on relative verbal vs spatial performance was observed. This result creates a potential problem in the context of the significant correlations between performance and airflow. On the one hand, our findings with unobstructed breathing provide support for the idea (Werntz et al., 1983) that the pattern of nasal dominance is correlated with asymmetries in hemispheric activation. In par- ticular, under the same conditions which produced greater integrated EEG amplitudes over the right hemisphere (left nostril dominance) we found greater relative spatial performance, and vice versa. On the other hand, forced uni-nostril breathing which also has dramatic effects on the distribution of EEG over the two hemispheres (Werntz et al., 1981), had no effect on performance. This apparent inconsistency may depend on procedural details. In the Werntz et al. (1981) study EEG changes were observed during forced uni-nostril breathing, but the exercise did not always produce a lasting change in nasal dominance. Thus, in Experiment 2, where performance was assessed after, but not during forced uni-nostril breathing, failure to obtain perfor- mance differences as a function of which nostil had been blocked is not a direct contradiction. In Experiment 1, performance was tested during forced uni-nostril breathing, but this was accomplished with a passive and uncomfor- table technique (noseplugs) rather than an active breathing exercise. Further study using both the EEG and performance paradigms could help to resolve this problem.

Acknowledgements

This research was made possible by a Natural Sciences and Engineering Research Council of Canada grant to Raymond Klein, and by a personal donation from D. Shannahoff-Khalsa. D. Shannahoff-Khalsa is grateful to Dr. Yogi Bhajan for his suggestions.

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