Lateralization of Human Olfaction:
Cognitive Functions and Electrophysiology
Daniel A. Broman
Department of Psychology
Umeå University, Sweden
2006
All my genius is in my nostrils
- Nietzsche
Copyright © 2006 Daniel A. Broman
ISBN 91-7264-166-5
Printed by Solfjädern Offset AB, Umeå
II
ABSTRACT
Broman, D.A. (2006). Lateralization of human olfaction: cognitive functions and
electrophysiology. Doctorial dissertation from the Department of Psychology, Umeå
University, SE-90187, Umeå, Sweden: ISBN 91-7264-166-5
In this thesis lateralization of olfactory functions was investigated by both
behavioral and electrophysiological assessment, the latter with the
olfactory event-related potential (OERP) technique. The olfactory sense
is primarily ipsilateral in that a stimulus that is presented to one nostril is
initially processed in the same hemisphere. This makes it possible to
observe differences between stimulated nostrils as an indication of
hemispheric difference. Study I explored differences in olfactory cognitive
functions with respect to side of rhinal stimulation and demonstrated
that familiarity ratings are higher at right- compared to left-nostril
stimulation. No differences were found in episodic recognition memory
or free identification, possibly reflecting inter-hemispheric interactions in
higher cognitive functions. Effects of repetition priming were present in
odor identification and tended to be more pronounced when tested via
left nostril. Study II further investigated the effect of previous exposure in
odor identification by a different experimental set-up, and demonstrated
effects of repetition priming when tested via left- but not right-nostril
stimulation. This finding indicates the importance of reconsidering
possible sequential effects in olfactory research. Study III examined
methodological aspects of an OERP protocol with respect to stimulus
duration, which was used in Study IV. No differences in amplitudes or
latencies where found between the stimulus durations of 150, 200 and
250 ms, suggesting the commonly used duration of 200 ms in a standard
protocol. Study IV investigated laterality effects in OERPs with respect to
side of stimulation and electrode site. The results showed consistent
amplitudes and latencies regardless of rhinal side of stimulation. Larger
amplitudes were demonstrated on left hemisphere and midline compared
to right hemisphere, possibly explained by smaller N1/P2 amplitudes at
the right-hemisphere sites at left-nostril stimulation. Apart from a
proposed OERP protocol, the findings support the notions of a righthemisphere predominance in processes related to olfactory perception
and indicate, in accordance with other findings, a left-side advantage in
conceptual repetition priming.
KEY WORDS: Human olfaction, Laterality, Olfactory processes, Odor familiarity,
Odor identification, OERP
III
ACKNOWLEDGEMENTS
First and foremost I sincerely want to thank my supervisor Dr. Steven
Nordin. I am also deeply indebted to Dr. Mats J. Olsson. Further, I want
to thank my other co-authors, with a special acknowledge to Jonas
Olofsson as first author on the fourth article included in the thesis, Dr.
Lars Nyberg and Lena Öman for valuable comments on the thesis, and
Dr. Gregory Neely for valuable comments on manuscript. Moreover,
thanks to Dr. Claire Murphy and her group at the Life-Span Human
Senses Laboratory, SDSU/UCSD, San Diego, USA and Dr. Per Møller
and his group at the Sensory Science Laboratory, KVL, Copenhagen,
Denmark, for inviting me to visit their laboratories and conducting
olfactory research as a pre-doctorial fellow. Finally, I would like to thank
the Kempe Foundation, the Sweden-America Foundation and the
Wallenberg Foundation for financially supporting me and my research.
IV
LIST OF PAPERS
This doctorial thesis is based on the following studies:
I.
Broman, D.A., Olsson, M.J. & Nordin, S. (2001). Lateralization of olfactory cognitive functions: effects of rhinal side of
stimulation. Chemical Senses, 26, 1187-1192.
II.
Broman, D.A. & Wising, A. (submitted). Effects of repetition
priming and stimulated nostril on odor identification.
III.
Broman, D.A., Nordin, S., Gilbert, P.E. & Murphy, C.
(submitted). Olfactory event-related potentials from varying
stimulus duration in young and elderly adults.
IV.
Olofsson, J.K., Broman, D.A., Gilbert, P.E., Dean, P., Nordin,
S. & Murphy, C. (2006). Laterality of the olfactory eventrelated potential response. Chemical Senses, 31, 699-704.
V
VI
TABLE OF CONTENTS
INTRODUCTION AND BACKGROUND
Anatomy of the human olfactory system
Research methods in human olfaction
Behavioral testing
Methods measuring neural activity
Olfactory lateralization
Absolute sensitivity
Discrimination
Recognition memory
Identification
Neural activity
1
2
3
3
5
8
9
9
10
10
11
RESEARCH OBJECTIVES
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SUMMARY OF EMPIRICAL STUDIES
Study I: Lateralization of Olfactory Cognitive Functions:
Effects of Rhinal Side of Stimulation
Study II: Effects of Repetition Priming and Stimulated
Nostril on Odor Identification
Study III: Olfactory Event-Related Potentials from Varying
Stimulus Duration in Young and Elderly Adults
Study IV: Laterality of the Olfactory Event-Related
Potential Response
14
14
16
18
19
GENERAL DISCUSSION
Behavioral findings
ERP findings
Lateralization of olfactory function
Conclusions
21
21
22
22
27
REFERENCES
29
VII
VIII
INTRODUCTION AND BACKGROUND
Historically the chemical senses have, compared to the other senses, not
been extensively investigated. Although scientific studies have been
investigating aspects of perception and cognition in the olfactory sense
for more than a century (e.g., Fischer & Penzoldt, 1886; Toulouse &
Vaschide, 1899; Zwaardemaker, 1895), the extent of work in this field is
modest in relation to research in vision and audition. In some aspects this
may perhaps seem natural since vision and audition are more related to
several higher cognitive functions, such as speech communication and
reading. The understanding for these sensory systems and their basic
transduction is also deeper. It is only a couple of years ago that the
chemical senses received their first Noble Prize for findings concerning
the olfactory receptors (Buck & Axel, 1991, for the subsequent work see,
for example, Buck 2000; Buck 2004). However, somewhat intriguing,
the relation between molecular structure and the perceived odor is still
not clearly understood. For example, the imaginative theory that the
perception of a certain odorant is determined by molecular vibrations
coded by the receptors (Turin, 1996) had some bearing until recently
when it was experimentally tested with no support for it (Keller &
Vosshall, 2004).
In addition to the aspects mentioned above, one reason for odor
perception and cognition not having been as vividly explored as vision
and audition is probably related to difficulties associated with the
stimulus. Visual and auditory stimuli are in many aspects easier both to
produce and present with superior control. They are also less complicated
to measure in physical units, to vary in a single dimension (e.g.,
frequency or amplitude) and to categorize. Odor categorization is a good
example of possible caveats related to stimuli. Several attempts have over
the years been made to find good categorization systems (e.g., Linnaeus,
1756; Henning, 1916; Amoore, 1963). However, as noted by Doty
(1991), odor categorization is still enigmatic and classification schemes
focused on explaining olfactory function have, more or less, fallen out of
favor in the past decades. One reason for the lack of a classification
system related to odor perception that is generally agreed on is probably
that the odor information to a large extent is based on experience and
therefore also individually tuned. For issues related to this, see Hudson
(1999) and Wilson and Stevenson (2003). Recently, results from an
imaging study indicate different coding of odor quality and odorant
structure in human piriform cortex, which may explain why odor quality
1
to some extent can be independent of simple odorant structure
(Gottfried, Winston & Dolan, 2006). At first inspection, it is easy to
believe that since the olfactory sense not is involved in higher-cognitive
function in the same way as the visual or auditory sense it is also less
optimalized in humans. Trygg Engen (1991) would probably argue for
the opposite, based on its purpose this sense is extremely well suited. We
may not learn new languages or solve mathematical problems with
assistance from the olfactory sense, but we certainly make up our minds
about what to eat, and not to eat, on bases of the olfactory system and
can also detect the smell of a fire.
Anatomy of the human olfactory system
In humans there are two chemical senses with receptors present in the
nose that have been proved to contribute to our perception of odorants
(e.g., Cain, 1974; Cometto-Muñiz & Cain, 1990; Doty, Brugger, Jurs,
Orndorff, Snyder & Lowry, 1978). In addition to the transduction of
odor information by the olfactory nerve (CN I), chemo-somatosensory
information including irritation and pungency is mediated by the
trigeminal nerve (CN V). Most odorants that we are exposed to are also,
at least at higher concentrations, to some extent trigeminal (Doty, 1975).
Interestingly, when an odor without trigeminal properties is
monorhinally presented it is not possible to tell whether it is presented to
the left nostril or to the right. To be able to localize nostril of stimulation
the odor has to have trigeminal properties (Kobal, van Toller &
Hummel, 1989; Radil & Wysocki, 1998). However, for a different view
see a recent neuroimaging notion about spatial information abilities
(Porter, Anand, Johnson, Khan & Sobel, 2005).
The olfactory nerve (CN I) is formed by the axons of millions of
receptor cells in the olfactory epithelium. The cilia of the receptor cells
are distributed in the nasal mucosa in the upper part of the cavity of each
nostril and respond to chemical stimulation. Different types of receptors
code for different odorants depending on their chemical structure. The
axons of the receptor cells traverse the cribriform plate and extend into
glomeruli in the olfactory bulb. The olfactory bulbs are located on the
lower surface of the frontal lobes, and each receptor projects ipsilateral to
one glomerulus in the bulb. The glomeruli contain dendrites of mitral
and tufted cells. These second-order neurons project via the lateral
olfactory tract directly to the primary olfactory cortex of each hemisphere
(Price, 1990).
2
The primary olfactory cortex consists of the anterior olfactory nucleus
located in a dorsal segment of the olfactory bulb, piriform cortex and
entorhinal cortex. Close to these areas, and with several connections, we
also find the hippocampus and the amygdala (McLean & Shipley, 1992).
Olfactory information is later transferred to parts of neocortex, including
oritofrontal cortex, by direct projections from primary olfactory cortex as
well as by connections via thalamus (Doty, Bromley, Moberg &
Hummel, 1997). By first inspection, the earliest inter-hemispheric
connection would be by the medial olfactory tract. However, this
structure does not seem to be developed in humans (Price, 1990). Thus,
possible projections between the hemispheres with respect to odor
information are via anterior commisure, with few contralateral
connections with respect to the olfactory system (Shipley & Ennis,
1996), and later via corpus callosum. Accordingly, initial olfactory
processing in the main olfactory system is primarily ipsilateral.
Research methods in human olfaction
Behavioral testing
There are numerous ways to assess olfactory functions by means of
behavioral testing. The tests vary from measuring perceptual functions,
such as odor detection, to, for example, odor recognition memory or
odor identification that also tap on higher cognitive processes. Absolute
detection, the lowest concentration of an odorant possible to detect, is
commonly studied by the psychophysical method of constant stimuli or
method of limits (Engen, 1971). In the method of constant stimuli a set
of stimuli is presented repeatedly in a randomized order. The data
obtained can be displayed as a psychometric ogive function, and the
threshold is often defined as the stimulus concentration that can be
detected in 50% of the cases. The method of limits is less time
consuming, but can also be less precise. This method starts with a
stimulus that is clearly above or below the absolute threshold and
thereafter presents stimuli in descending or ascending series with small
intervals until the absolute threshold is reached. The staircase procedure
is a variant of this method that shifts the series order when the threshold
is reached (Gescheider, 1997). Similarly, these methods can be used for
studying odor discrimination with respect to both intensity and quality.
However, the most common way to assess discrimination abilities is by
3
making direct comparisons between stimuli. One way is by
same/different judgments after inspection of odor pairs, another is by
finding the different stimulus out of three.
There are different ways to test odor identification. The most
complex and difficult type of identification is probably by veridical
naming, i.e., correct verbal naming of an odorant without any further
information. An easier type of task is to identify an odor with provided
alternatives, a so-called multiple-choice test. The typical way to study
episodic memory in olfaction is by testing recognition memory. The test
consists of an encoding phase were the participants are presented to a set
of odorants followed by a retrieval phase, including presentation of the
encoded odors to be recognized (targets), and previously not encoded
odors (lures). Perceived properties of an odor stimulus, such as intensity,
valence and familiarity, can also be rated. One common psychophysical
method is by means of magnitude estimation, most frequently used for
intensity ratings. The relation between stimulus proportion and the
perceived magnitude can be described by the psychophysical power law
presented by S.S. Stevens (1957). Another way to measure the magnitude
of the percept is by using scales. Both numerical scales with verbal
anchors, for example the category-ratio scale (Borg, 1982; Borg, 1998;
Borg & Borg, 1998) and the label-magnitude scale (Green, Shaffer &
Gilmore, 1993; Green, Dalton, Cowart, Shaffer, Rankin & Higgins,
1996), and the visual-analog scale (Dexter & Chestnut, 1995; Neely,
Ljunggren, Sylven & Borg, 1992) are considered to provide measurement
on a ratio-scale level.
Even if the majority of olfactory research is conducted more or less by
non-standardized stimuli and assessments, there is an increase of
standardized olfactory tests available for different purposes. For example,
the University of Pennsylvania Smell Identification Test (UPSIT; Doty,
Shaman & Dann, 1984), the San Diego Odor Identification Test
(SDOIT; Andersson, Maxwell & Murphy, 1992), the Scandinavian
Odor Identification Test (SOIT; Nordin, Brämerson, Lidén & Bende,
1998), all of these identification test with forced-choice alternatives.
Other tests, measuring various functions, are the Connecticut
Chemosensory Clinical Research Center Tests (CCCRC; Cain, 1989) for
absolute detection and identification, and the Sniffin’ Sticks (Hummel,
Sekinger, Wolf, Pauli & Kobal, 1997) measuring absolute detection,
intensity, quality discrimination, and identification.
4
Methods measuring neural activity
During the last two decades the use of methods measuring neural activity
has dramatically grown in human olfactory research, especially the
technique of ERP and the imaging techniques of PET and fMRI. For
pioneering work using the techniques of ERP and neuroimaging in
olfactory research, see Kobal (1981) and Zattore and colleagues (Zatorre,
Jones-Gotman, Evans & Meyer, 1992), respectively. These research
methods are powerful tools for the study of human olfaction and can
naturally also provide useful information concerning lateralization of
olfactory functions.
Event-related potentials
Event-related potentials (ERPs) reflect electrophysiological activity
evoked by a stimulus. For a single recording this neural electrical activity
is a relatively small section of the registered electroencephalogram (EEG)
that is mainly caused by non-stimulus related activity. By computing the
mean electrical activity from repeated stimulus presentations with a timelocked stimulus onset, the noise ratio in the event-related activation will
be reduced and provide an electrophysiological waveform related to the
stimulus and task of interest (Handy, 2005). In this wave, reflecting
electrophysiological activity elicited by a specific stimulus and time frame,
components can be identified as positive or negative peaks in relation to a
pre-stimulus baseline. The peaks are commonly named by their
positive/negative deflection and position in relation to stimulus onset.
For example, P1 for the first positive peak, N1 for the first negative peak,
P2 for the second positive peak, N2 for the second negative, and P3 for
the third positive peak. See Figure 1. The peaks of interest to interpret for
a specific research question depends on stimulus modality, task given to
the participant, study design and research questions (Polich, 2003).
Latencies of different types of peaks are closely related to the stimulus
modality. For example, in audition N1 and P3 are sometimes referred to
as N100 and P300, respectively, because of their approximate presence in
ms after stimulus onset.
5
30
P3
Amplitude (µV)
20
P2
10
0
-1 0
N1
-2 0
0
200
400
600
800
1000
1200
1400
1600
L a te n c y (m s )
Figure 1. Example of an ERP registration with the N1, P2 and P3 components inserted
(noteworthy, the P3 component has typically a lower amplitude).
In olfactory event-related potentials (OERPs) the component of a
possible P1 is rarely studied due to the small and unreliable amplitude,
neither has there been extensive focus on N2 in OERPs. The main
components of interest in OERP research have instead been N1, P2 and
P3, and in the most studies amplitudes and latencies of these peaks and
their relation to each others have been investigated (e.g. N1/P2, peak-topeak difference). The early components, in olfaction studied by N1, and
in some cases also by P2, are often referred to as sensory components that
reflect more exogenous aspects in relation to the stimulus (Kobal, 2003).
Later peaks, especially P3 and to some extent P2 (which in olfaction
sometimes together with P3 constitutes a late positive complex rather
than isolated peaks), reflect more endogenous components of more
cognitive nature. OERPs can be recorded from electrodes placed on any
position on the scalp. Usually, the recording sites follow the International
10-20 system with origin points from nasion, inion and prearciulars
(Evans, Kobal, Lorig & Prah, 1993). Based on these points, electrodes are
placed along the saggital and coronal plane. Following the midline (z=0)
in the saggital plane, the site labelled Cz (central zero) is of equal distance
to nasion and inion, the site Fz (frontal zero) is located 20% of the
distance between nasion and inion anterior of Cz, and the site Pz (parital
zero) is at the same distance posterior of Cz. In the coronal plane,
following the central axis, the main points from left to right are labeled
6
T3, C3, Cz, C4, T4 (i.e., odd numbers refer to the left hemisphere and
even numbers to the right hemisphere), with similar distance distribution
as for the points in the saggital plane. On basis of these main axes, other
points are given, for example F3 (frontally on left hemisphere) placed
perpendicular to Fz and C3. See Figure 2.
Figure 2. Recording sites, according to the International 10-20 system, used in Study III
(only midline sites: FZ, CZ, PZ) and Study IV.
Haemodynamic techniques
With functional neuroimaging it is possible to investigate brain activity
with good and reliable spatial resolution. Positron emission tomography
(PET) commonly measures local changes in blood flow (Raichle, 1994).
When a specific area is more activated there is an increase of regional
cerebral blood flow (rCBF), and this increase in rCBF is measured by a
tracer, such as 15O. The temporal resolution in this technique is rather
poor and the experimental set-up is limited to block design. Neural
activity measured by local differences in blood flow can also be studied by
functional magnetic resonance imaging (fMRI). Changes in rCBF are
with this method studied through differences in blood oxygenation, and
the so-called blood oxygen level dependent (BOLD) signal is measured
by a magnetic resonance scanner (Ogawa, Lee, Kay & Tank, 1990). In
comparison to PET, one advantage of fMRI is the better temporal
resolution that also permits event-related designs, even though these
designs are, hitherto, not commonly used to study olfaction. Other
advantages include fMRI being non-invasive and less expensive. A major
disadvantage of fMRI in olfactory research is the presence of artefacts in
the signal in areas consisting of air and tissue. Although there are
methods to reduce this type of artefact located in olfactory regions in
7
ventromedial prefrontal cortex (Liu, Sobering, Duyn & Moonen, 1993;
Yang, Darzinski, Eslinger & Smith, 1997; Zald & Pardo, 2000), the
signal quality in this area is only moderate (Royet & Plailly, 2004).
Stimuli presentation is often a methodological issue in olfactory
research and the use of imaging techniques makes no exception to that.
Besides adaptation and habituation problems in the commonly used
block design, and administration problem in the scanner, effects of
sniffing behaviour and baseline contrasts contribute to somewhat
conflicting imaging findings. The most striking inconsistency concern
registered activation in the primary olfactory cortex. Although, the signal
artefacts in this region in some cases may contribute to the discrepancies
in the fMRI results, this is obviously not the whole explanation, since
PET studies also show inconsistency in finding activation in the primary
olfactory cortex. It has previously been well demonstrated that sniffing
behaviour affect olfactory processing (Laing, 1983; Teghtsoonian,
Teghtsoonian, Berglund & Berglund, 1978). However in relation to
imaging, Sobel and colleagues (Sobel at al., 1998, Sobel et al., 2000)
reported that sniffing odorless air elicited activation in primary olfactory
cortex. Consequently, the use of that type of task as baseline condition
for contrast analysis can explain the lack of activation in some imaging
results. Possible effects of adaptation and habituation have also been
suggested explanations for the different results in finding primary
olfactory cortex activation (Poellinger et al. 2001; Sobel et al., 2000). To
conclude, lack of demonstrated activation in primary olfactory cortex in
olfactory imaging results should not be interpreted as lack of involvement
of primary olfactory cortex in olfactory processing.
Olfactory lateralization
The fact that the initial processing in the olfactory system is principally
ipsilateral to the stimulated nostril, and the direct projections to olfactory
related areas in cortex, provide a unique opportunity among the senses to
investigate lateralization differences by means of behavioral testing. A
great deal of the knowledge about olfactory lateralization originates from
studies in patient groups with cerebral complications, either by
comparing left- versus right-nostril performance, or by comparing
patients with left- versus right-hemisphere lesions. More recently, new
and better techniques to study neural activity have been developed that
provide further understanding of lateralization of olfactory function, and
some of these findings will also be discussed below.
8
Absolute sensitivity
Studies that have investigated differences in absolute sensitivity between
left- and right-nostril stimulation with behavioral measurements have in
many cases shown somewhat conflicting findings. For odor-detection
thresholds, Youngentob and associates (Youngentob, Kurtz, Leopold,
Mozell & Hornung, 1982) reported differences between the nostrils,
where left-handed participants were more sensitive in the left nostril and
right-handed participants tended to be more sensitive in the right nostril.
In contrast, Cain and Gent (1991) found right-nostril superiority in
detection sensitivity, irrespective of handedness. In addition, a study of
Koelega (1979) failed to find any differences in thresholds between
nostrils. Furthermore, no side differences regardless of handedness were
found by either Zatorre and Jones-Gotman (1990) or Betchen and Doty
(1998). Interestingly, these two studies had the largest sample sizes of
those cited above, and both used phenyl ethyl alcohol (PEA), an odor
with limited trigeminal properties (Doty et al., 1978). To conclude, if
differences between the nostrils in absolute sensitivity do exist, the size of
this effect is probably rather small, and the results suggest a right-nostril
superiority, at least for right-handed individuals.
Discrimination
In discrimination, in accordance with absolute sensitivity, the findings are
somewhat conflicting, but they seem to indicate a similar right-nostril
superiority. In investigating odor quality discrimination, Zatorre and
Jones-Gotman (1990) reported a right-nostril advantage irrespective of
handedness. In line with that finding, a right-nostril advantage has also
been reported by Martinez and colleagues (Martinez, Cain, de Wijk,
Spencer, Novelly & Sass, 1993). However, Hummel, Mohammadian and
Kobal (1998) reported that left-handed participants had a left-nostril
advantage for this task. In a study by Savic and Berglund (2000), a
significant right-nostril superiority in quality discrimination was present
only for unfamiliar, but not for familiar odors. Interestingly, inspection
of the presented results in Table 2 of that study reveals that, nominally,
the right-nostril advantage is present also for familiar odors, which raises
the question whether the lack of a significant difference in this case can
be related to ceiling effects. A right-nostril advantage has also been shown
in an intensity categorization task, which also taps on memory functions,
9
although these findings were statistically significant only for women
(Pendense, 1987).
Recognition memory
Studies of odor recognition memory have reported hemispheric
differences in patient groups. Several investigations (Abraham & Mathai,
1983; Jones-Gotman & Zatorre, 1993; Rausch, Serafetinides & Crandall,
1977) have shown that patients with right-temporal lobe lesions perform
more poorly than patients with left-temporal lobe lesions in odor
recognition tests. This somewhat consistent finding may suggest a righthemisphere superiority in odor recognition. Further, investigating healthy
participants in a cross-modal recognition task (odor-word, odor-picture)
with the odor as the first stimulus presented birhinally, the response time
was faster when the second stimulus (word or picture) was presented to
the right hemisphere compared to the left hemisphere (Zucco &
Tressoldi, 1989). Using a unimodal recognition task, Olsson and Cain
(2003) found no differences in memory performance between nostrils,
although the response latency was shorter when tested on the right-nostril
compared to the left. However, in a study by Bromley and Doty (1995)
the results showed no evidence for a right-nostril advantage in
recognition memory, using either a single or a multiple target test. In
accordance, Annett, Ford and Gifford (1996) found no side differences
in odor recognition without verbal elaboration in an experiment with a
birhinal retrieval phase.
Identification
Gordon and Sperry (1969) found that patients with surgically
disconnected hemispheres are able to identify odors verbally when
presented to the left but not the right nostril, which could be explained
by a left-side lateralization for language. Noteworthy, using non-verbal
tests the patients were able to identify odors presented to the right nostril.
However, there are indications of a left-hemisphere advantage in odor
identification in patients with separated hemispheres, as performance
with both verbal and non-verbal identification is superior in left-nostril
stimulation. These results may not necessarily indicate a left-side
dominance in odor identification, per se, they could have other possible
explanations, such as hemispheric differences in cross-modal comparisons
10
or verbal experimental settings (Gordon, 1974). In addition, odor
identification studies in patient groups with focal neuropathology or
lobotomy have not shown side-related differences (Carroll, Richardson &
Thompson, 1993; Eskenazi, Cain, Novelly & Mattson, 1986). Somewhat
unexpected in relation to that, Herz and colleagues reported that
odorants presented to the left nostril are more frequently named correctly
than odorants presented to the right nostril in healthy participants (Herz,
McCall & Cahill, 1999).
Neural activity
Using the ERP technique, Kobal, Hummel and van Toller (1992) found
an interaction between stimulated nostril and odorant type on N1 and P2
latencies. The odorant vanillin elicited longer latencies at left- compared
to right-nostril stimulation, whereas the odorant hydrogen sulfide elicited
shorter latencies at left- compared to right-nostril stimulation. Since all
participants experienced the odor of vanillin as pleasant and the odor of
hydrogen sulfide as unpleasant this effect was interpreted as possibly
caused by their difference in odor hedonics. A similar result pattern in
ERP recordings between stimulated nostrils and odor hedonicity has
repeatedly been described by Kobal and colleagues. Thus, they reported
larger amplitudes and longer latencies in left- compared to right-nostril
stimulation for pleasantly perceived stimuli, and the reversed for
unpleasantly perceived stimuli (Kobal, Hummel & Pauli, 1989; Kobal &
Hummel, 1991; Hummel & Kobal 1994). Recently, by using a bimodal
odorant, that stimulates both the olfactory and trigeminal system,
alternating left- and right-nostril stimulation between participants,
Lundström and Hummel (2006) found that women generally had larger
amplitudes and longer latencies over left- compared to right-hemisphere
sites while men showed the reversed pattern. Unfortunately in this
respect, no analyses including side of stimulation were reported. In a
study that elegantly combined magnetic source imaging and ERP
recordings, the overarching result pattern indicated higher lefthemisphere activity in relation to right-hemisphere activity at leftcompared to right-nostril stimulation and higher left-hemisphere activity
in relation to right-hemisphere activity for vanilla compared to hydrogen
sulfide (Kettenmann, Hummel, Stefan & Kobal, 1997).
In neuroimaging, hemispheric differences were revealed in the
classical study by Zatorre and colleagues (1992), showing activity
corresponding to the piriform cortex in each hemisphere, in the right
11
orbitofrontal cortex and the left inferior medial frontal lobe for birhinal
stimulation. Activation in right orbitofrontal cortex, alternatively stronger
activation in right than in left orbitofrontal cortex, are one of the most
consistently reported results in imaging studies in olfaction, regardless of
imaging technique and experimental set-up (e.g., Jones-Gotman et al.,
1993; Small et al., 1997; Sobel et al., 1998; Royet et al., 1999; Yousem et
al., 1997; Dade, Jones-Gotman, Zatorre, & Evans, 1998; Plailly et al.,
2004). Furthermore, this right-side activation has been shown to be
present regardless of stimulated nostril (Savic & Gulyas, 2000).
Interestingly, monorhinal and birhinal stimulation seems to elicit
approximately the same activity pattern (Zatorre & Jones-Gotman,
2000). The notions of this right-hemisphere predominance may be
associated with olfactory tasks that tap on perceptual processing. For
example, right orbitofrontal cortex activation was found during both
pleasantness and intensity judgments (Zatorre, Jones-Gotman & Rouby,
2000). Moreover, Royet and colleagues (1999, 2001) have consistently
showed involvement of right orbitofrontal cortex in studies that
examined odor familiarity. However, highly aversive odorants do instead
show activations in left orbitofrontal cortex and amygdala (Zald & Pardo,
1997; Gottfried, O'Doherty & Dolan, R.J., 2002). Furthermore, Royet
et al. (2000) demonstrated increased left hemisphere activity, e.g., in
orbitofrontal cortex and superior frontal gyrus, to emotionally valenced
odorants, as well as to emotionally valenced visual and auditory stimuli.
Accordingly, conducting hedonic judgments of odors has shown more
activation in left orbitofrontal cortex compared to passive smelling of the
same stimuli (Royet, Plailly, Delon-Martin, Kareken & Segebarth, 2003).
In investigating odor identification, Kareken and associates (Kareken,
Mosnik, Doty, Dzemidzic & Hutchins, 2003) showed left inferior
frontal activity, possibly reflecting semantic analysis, and Savic and
colleagues (Savic, Gulyas, Larsson & Roland, 2000) found activation in
left insula in discrimination tasks of odor intensity and odor quality.
These findings are in agreement with the results by Royet et al. (1999,
2001, 2003) which suggest that complex semantic tasks, that may be
associated with naming, show left-hemisphere activation.
RESEARCH OBJECTIVES
The four studies in this thesis are all designed to provide results that can
contribute to extend the knowledge of neuropsychological aspects of
12
human olfaction. More specifically, the main focus has been on the
lateralization of olfactory cognitive functions assessed by behavioral
testing and by OERP recordings. The lateralization of olfactory functions
assessed by behavioral testing was studied by investigating performance in
left- versus right-nostril stimulation in healthy participants. Functions
explored for lateralization differences were perceived familiarity,
recognition memory, memory experience in terms of remember responses
that reflect recollection of a specific episode, and know responses that
reflect recollection without contextual information, free identification
and effects of previous exposure in free identification (Study I).
The next paper (Study II) further investigated lateralization effects in
free identification and effects of previous exposure on free identification.
This study is motivated by findings in Study I regarding repetition
priming and lateralization on odor identification, and in relation to these
findings somewhat contradictory reports. The aim was to study whether
conflicting findings may complement each other and be explained by a
broader perspective.
The majority of research studies on olfactory functions heavily
depend on good stimulus control, stringent presentation procedures and
knowledge about possible effects caused by changes in various stimulus
dimensions. Historically, this may, in particular, have concerned research
using psychophysical methods. However, nowadays this is also of great
importance in methods measuring neural activity. The aim of Study III
was therefore to extend the knowledge about how a OERP protocol, also
to be used in Study IV, is affected by different stimulus durations. The
study investigated effects caused by variations (±50 ms) from the
commonly used stimulus duration of 200 ms. In order to also investigate
if different stimulus durations affect OERPs in populations where clear
and reliable registrations can be more crucial to practice, both a group of
healthy elderly participants and a group of young healthy subjects were
tested. In addition, age differences were studied.
The final paper (Study IV) concerns olfactory lateralization by means
of OERP registrations in young healthy participants. The protocol used is
based on Study III, and in accordance with the result regarding
appropriate stimulus duration. The research questions targeted here were
particularly OERP activation related to different sites on the coronal
plane (i.e., left hemisphere, midline, right hemisphere) and left- versus
right-nostril stimulation, and possible interaction effects of these
variables.
13
SUMMARY OF EMPIRICAL STUDIES
Study I: Lateralization of Olfactory Cognitive Functions:
Effects of Rhinal Side of Stimulation
Aim
This study investigated the olfactory functions of familiarity, recognition
memory and identification with respect to behavioral differences between
left- and right-nostril stimulation. Based on behavioral research on
lateralization of olfactory functions in healthy participants the
hypothesized results were a right-side advantage for more sensory-related
functions. Since lateralization of higher cognitive functions rarely have
been studied, the expected outcome in this respect was less clear.
Methods
Forty young, right-handed adults (20 men and 20 women) participated
who were screened for loss in odor sensitivity. In an initial encoding
phase the participant was monorhinally presented with 24 randomly
selected odorous stimuli (out of 48 stimuli, all relatively common odors
without trigeminal impact) to be rated with respect to familiarity on a
bipolar visual analog scale (VAS) ranging from not familiar to very
familiar. In a retrieval phase, 10 min later, the initial 24 odors and 24
new odors were presented. The first task was to report whether the odor
had been presented in the previous encoding phase. The response time
for this was also measured. Next, the participant rated his/her confidence
in the response on a VAS, and if the participant responded that the odor
had been present in the encoding phase he/she did also report the
recollective experience in terms of remember or know. Where remember,
reflected a recollection with specific contextual aspects encountered in the
study phase, and know, reflected a recollection without any contextual
information. Thereafter, the final task was to freely identify the odor by
veridical naming.
14
Results
The familiarity ratings were significantly higher at right- compared to
left-nostril stimulation. However, no side differences were shown in
recognition memory for performance (A´), response criterion (B´´),
confidence rating, response time, or memory experience
(remember/know). Neither were side differences found in identification,
although a repetition effect was shown such that previously presented
stimuli were significantly more frequently identified compared to new
stimuli. See Table 1.
Table 1. Mean values for various measures of olfactory cognitive functions.
_________________________________________________________________________
Left nostril
Right nostril
_________________________________________________________________________
Familiarity rating (proportion)
0.54
0.59
Recognition memory
Performance (A´)
0.75
0.76
Response criterion (B´´)
- 0.36
- 0.35
Confidence rating (proportion)
0.58
0.59
Response time (geometric means; s)
Hit
4.35
4.14
Correct rejection
5.87
5.88
False alarm
5.48
5.73
Miss
6.73
7.13
Memory experience (n)
Remember response
5.25
5.05
Know response
3.98
4.15
Identification (n)
Old stimuli (encoding & retrieval phase)
2.75
2.55
New stimuli (retrieval phase)
1.98
2.20
_________________________________________________________________________
Conclusions
The study showed a right-nostril advantage for perceived odor familiarity,
supporting previous notations about a right-side advantage for tasks
related to odor perception. No side differences were found in episodic
recognition or in identification. However, a significant effect of repetition
priming in identification was found. This effect seems to be more
pronounced for left- compared to right-nostril stimulation, which raises
the question about the nature of lateralization in olfactory priming.
15
Study II: Effects of Repetition Priming and Stimulated
Nostril on Odor Identification
Aim
The notation of a possible left-nostril/hemisphere superiority in odor
identification has previously been reported from some studies but not
from other. Additionally, Study I indicated a left-nostril advantage on
priming effects in relation to cognitive olfactory functions. The present
study further investigated these two aspects of olfactory lateralization.
The expected results were effects of previous exposure in terms of
improved performance. It was further expected that this effect of previous
exposure would be more pronounced when tested in the left-nostril, and
thus revealing a left-nostril advantage in odor identification explained by
previous exposure.
Methods
Fifteen men and 15 women who all were young adults participated. All
participants were healthy, right-handed, reported normal chemosensory
function and had normal odor detection sensitivity according to tests. In
a first session the participant was monorhinally, alternating left- and
right-nostril stimulation, presented with 16 odorants to be identified the
odor by veridical naming. In a following session, conducted the next day,
the same procedure was used with the exception that the eight odorants
presented to the left nostril in the first session were presented to the right
nostril, and contrary for the other eight odorants. To prevent serial effects
or other effects related to the presentation order, lists of 15 pairs
(consisting of List A and List B) of randomized stimuli order were used.
The participants were matched into pairs in which one participant was
presented with List A in the first session and List B in the second session,
while the other participant in the pair started with List B followed by List
A.
Results
The initial analyses showed that the identification rate was higher in the
second compared to the first session and for left- compared to right16
nostril stimulation, but no interaction effect. Additional analyses that
were conducted in order to closer investigate the effects of session and
nostril showed no differences between left- and right-nostril stimulation
in either the first or second session. Furthermore, no significant
differences were found between right-nostril stimulation in session two
compared to the other three conditions. However, identification was
found to be superior in left-nostril stimulation in session two compared
to both right- and left-nostril stimulation in session one. See Figure 3.
Analyses of logarithmic response time in correct identifications showed
an effect of session, with faster response times in session two, but no
nostril or interaction effects.
Figure 3. Differences in number of correct identifications at left- and right-nostril
stimulation in Session 1 and 2, tested by paired t-tests.
Conclusions
This study provides further support for the existence of repetition effects
on olfactory functions. Noteworthy, these effects seem to be more
pronounced when tested in the left nostril. The results do also
demonstrate that the left-nostril advantage in odor identification may be
explained by effects of repeated testing.
17
Study III: Olfactory Event-Related Potentials from Varying
Stimulus Duration in Young and Elderly Adults
Aim
Stimulus presentation is a factor that has to be carefully considered in
order to obtain valid OERP recordings. Several studies have investigated
how stimulus dimensions, such as concentration and interstimulus
interval, affect the OERPs. However, surprisingly little concern has been
shown for stimulus duration, and the issue of temporal summation has
been scarcely investigated in the olfactory sense compared to other
modalities. One aim of this study was therefore to look closer into how
this stimulus parameter affects OERPs in order to evaluate a stimulus
protocol for OERP recordings that also would be applied for the
investigation of laterality in Study IV. Another aim of the study was to
compare different age groups with regards to OERPs, both in order to
gain more information about OERP in different age groups per se, and
additionally to investigate whether OERP recordings in elderly would
benefit from a stimulus protocol with a longer duration.
Methods
Twenty-one healthy persons participated who were screened for loss in
odor sensitivity and constituted two age groups (M=23.7 and M=79.1
years). The odor stimulus consisted of a non-trigeminal concentration of
amyl acetate presented by an olfactometer with the stimulus durations of
150, 200 and 250 ms. Neuroelectric activity was recorded at the electrode
sites Fz, Cz and Pz (midline). After each stimulus recording the
participants rated the perceived odor intensity on the Labeled Magnitude
Scale. The participants were presented with the three stimulus durations
in blocks separated by a 10 min break.
Results
The results of a factorial analysis of variance showed no main effect of
stimulus duration for latencies of the OERPs, although it showed a
significant main effect of age group, such that the elderly had longer
latencies than the younger. No significant main effects for duration or age
18
group were revealed by a factorial analysis of variance for OERP
amplitudes. Furthermore, there were no significant differences in
perceived intensity ratings, neither for duration nor age group, and no
interaction between these variables.
Conclusions
The results suggest that the different stimulus durations used in this
study do not have a significant impact on the OERP latencies or
amplitudes elicited in healthy young adults. It is further suggested that
the typically used duration time of 200 ms in OERPs protocols is
appropriate for general purposes including studies of laterality. However,
the results indicate that the stimulus duration should perhaps be more
carefully considered in OERPs studies of older participants or possibly
clinical populations. The study also indicates that these differences in
duration time (±50 ms) do not seem to affect the perceived odor
intensity.
Study IV: Laterality of the Olfactory Event-Related Potential
Response
Aim
This study investigated lateralization in olfaction with the OERP
technique. The objectives of the study were twofold, first to better
understand whether rhinal side of stimulation has an impact on the
latencies and amplitudes of the recorded brain waves. Behavioral studies
have demonstrated differences between nostrils in olfactory function, but
very few studies have previously focused on differences for rhinal side of
stimulation regarding OERPs. The second objective was to study
hemispheric differences in odor information processing by means of
OERP recordings. Based on results from imaging techniques, in which
differences in hemispheric activation are commonly reported in olfactory
research, it is of interest to approach this issue also with the OERP
method that provide excellent time resolution.
19
Methods
Twenty-eight young, right-handed, adults (14 men and 14 women)
participated who were screened for loss in odor sensitivity. The
participants’ OERPs were recorded for stimulation in both nostrils in
separate blocks. The odor stimulus amyl acetate was presented by an
olfactometer while neuroelectric activity was recorded at the electrode
sites Fz, Cz, Pz (midline), F3, C3, P3 (left hemisphere) and F4, C4, P4
(right hemisphere).
Results
No significant main effect of rhinal side of stimulation was found on
amplitude. An effect of coronal site was revealed, suggesting significantly
smaller amplitudes for right-hemisphere sites compared to midline and
left-hemisphere sites. Interaction effects were found for peak x nostril and
coronal site x peak x nostril. The latter interaction was explained by
smaller N1/P2 amplitudes at the right-hemisphere sites in left-nostril
stimulation and may explain the first interaction and the effect of coronal
site. No significant main effects were shown on latencies, neither for
rhinal side of stimulation nor site.
Conclusions
The present study showed consistent amplitudes and latencies across
rhinal sides of stimulation. This finding indicates that stimulus
presentations at either the right or the left nostril are sufficient in order
for accurate assessment and interpretation of OERPs recordings.
Furthermore, some analyses revealed hemispheric differences on
amplitude. The results in this perspective are not easily interpreted and
imply that more OERPs research in this field is needed for an extended
view.
20
GENERAL DISCUSSION
The primary aim of this thesis was to investigate lateralization of olfactory
cognitive functions and electrophysiological processes. This was
conducted by behavioral testing (Study I and Study II) using monorhinal
stimulation comparing left- and right-nostril performance. By using the
OERP technique, olfactory lateralization was examined by means of
stimulated nostril and hemispheric site (Study IV). This was conducted
on bases of an evaluated OERP protocol with respect to stimulus
duration (Study III).
Behavioral findings
The olfactory functions targeted in this thesis ranged from perceptually
oriented functions in familiarity judgments (Study I) to higher cognitive
ones in recognition memory (Study I) and free identification by veridical
naming (Study I and Study II). Effects of previous exposure in odor
identification were also investigated in both studies. Familiarity ratings
were found to be higher at right- compared to left-nostril stimulation. No
differences between stimulated nostrils were revealed in episodic
recognition memory that was tested with respect to hit performance,
response criterion, response confidence and response time. Noteworthy,
the reported memory experience showed nominally more know responses
in right-nostril stimulation and more remember responses in left-nostril
stimulation. Since know responses are associated with perceptual fluency
and familiarity-based memory, while remember responses reflect a
conceptual, more distinctive, component of recognition, this is in
agreement with a right-side predominance of olfactory functions related
to perceptual processes.
Odor identification and effects of previous exposure in odor
identification were investigated in both Study I and II. In Study I no
difference was found in identification between left- and right-nostril
stimulation. However, an effect of repetition was present, showing that
odors presented in both the encoding and retrieval phase were identified
at a higher rate compared to odors presented only in the retrieval phase.
Subanalyses showed that this priming effect was significant at left-nostril,
but not at right-nostril stimulation. To complement these findings in
odor identification, this function was measured again in Study II, in two
separate sessions with one day in between. Noteworthy, an odorant was
21
in Study I presented to the same nostril in the two sessions and in Study
II to the opposite nostril in the two sessions. Study II showed, in
accordance to Study I, effects of previous exposure, and did also show
effects of rhinal-side of stimulation. Further analyses demonstrated that
both these effects are caused by better identification at left-nostril
stimulation due to previous exposure.
ERP findings
Study III examined an OERP protocol with respect to stimulus duration
and demonstrated no differences between the investigated durations.
Study IV, based on the protocol of Study III, shows consistent
amplitudes and latencies regardless of rhinal side of stimulation. Some
analyses revealed hemispheric differences in amplitude, suggesting
generally higher amplitudes in the parietal site on the left-hemisphere.
Importantly, interaction effects were found that indicate that smaller
N1/P2 amplitudes at the right-hemisphere sites at left-nostril stimulation
can explain the results of side-related differences. Among the findings,
these two studies suggest that a standard protocol for OERP recordings
using 200 ms stimulus duration can be assessed by either left- or rightnostril stimulation.
Lateralization of olfactory function
The result in Study I, showing that odors presented to the right nostril
are rated as more familiar than odors presented to the left nostril, are in
line with several other notions about lateralization differences in human
olfaction. This finding agrees well with the notion of a right nostril
dominance in other perceptually oriented functions, such as odor
discrimination (Zatorre & Jones-Gotman, 1990), pleasantness judgments
(Bensafi, Rouby, Farget, Bertrand, Vigouroux & Holley, 2003) and
primed edibility judgments (Olsson & Fridén, 2001). The results from
imaging studies clearly suggest higher right hemisphere activity related to
odor perception (e.g., Small, Jones-Gotman, Zatorre, Petrides & Evans,
1997; Sobel et al., 1998; Yousem et al., 1997; Zatorre et al., 1992). More
specifically associated to the present finding, Royet and colleagues (2001)
demonstrated higher right orbitofrontal cortex activation in familiarity
judgments compared to other olfactory tasks, and Plailly et al. (2005)
22
showed, by contrasting a familiarity task with a detection task, that the
odor familiarity judgments activated right piriform cortex.
Somewhat related to familiarity and familiarity processing, the
finding in Study I of nominally more know responses tested via the right
nostril agrees with results from other modalities indication a right
hemisphere superiority for processes related to know responses and a left
hemisphere superiority for processes related remember responses (Blaxton
& Theodore, 1997; Henson, Rugg, Shallice, Josephs & Dolan, 1999). In
olfaction, the finding that patients with right-temporal lobe lesions
perform more poorly than patients with left-temporal lobe lesions in odor
recognition, indicate a right-hemisphere superiority also in odor
recognition (Abraham & Mathai, 1983; Jones-Gotman & Zatorre, 1993;
Rausch, Serafetinides & Crandall, 1977). Imaging studies point in the
same direction; in inspecting odor recognition Savic and colleagues
(2000) reported activity in the right piriform cortex but not the left, and
Dade et al. (1998) reported unilateral right orbitofrontal activity.
However, (a) the general lack of difference between stimulated nostril in
memory performance in Study I, (b) the result by Bromley and Doty
(1995), that odor recognition memory is better under bilateral than
unilateral test conditions, and particularly, (c) the study by Dade, Zatorre
and Jones-Gotman (2002), which elegantly combined results in patients
with temporal-lobe lesion and imaging results in healthy, indicating an
active role of the piriform cortex in odor memory processing and without
any clear hemispheric superiority in this function; unitedly suggest that
odor recognition memory may normally also involve inter-hemispheric
processing.
The results of odor identification performance at left- compared to
right-nostril stimulation showed no differences between nostrils, neither
in Study I or Study II, without previous exposure. These findings are
convergent with other findings in healthy participants (Jones-Gotman et
al., 1997; Olsson & Cain, 2003), as well as in patients with cerebral
lesions (Eskenazi et al., 1986; Carroll, Richardson & Thompson, 1993;
Jones-Gotman et al., 1997), and do not support the notion of a leftnostril superiority in odor identification (Herz, McCall & Cahill, 1999;
Homewood & Stevenson, 2001).
This raises at least two questions. First, why would there be a leftnostril superiority in odor identification? At first sight this seems natural
since there is a left-hemisphere specialization in processes related to
language (e.g., Cabeza & Nyberg, 2000) and odor identification, at least
operationally defined as odor naming taps on these processes.
Accordingly, neuroimaging data show left inferior frontal activity during
23
odor identification, possibly reflecting semantic analysis (Kareken et al.,
2003) and the results by Royet and colleagues (1999, 2001, 2003)
suggest that complex semantic tasks, that may be associated with naming,
show left-hemisphere activations. On the other hand, by inspecting the
literature about odor identification, the first striking aspect is the poor
performance. A classical example is the study by Cain (1979), in which
the participants initially freely named only 36 of the 80 presented odors.
The approximately same performance, about 50%, in free odor
identification is commonly noted in other studies (e.g., Cain, de Wijk,
Lulejian, Schiet & See, 1998; Distel & Hudson, 2001, Engen 1987;
Larsson & Bäckman, 1997). The difficulty to identify odors have several
proposed explanations; one is the notion of a weak linkage between
language processes and olfaction (Richardson & Zucco, 1989; Schab,
1991). Interestingly, many studies that have explored this phenomenon
indicate difficulties at earlier perceptual stages, such as discrimination and
categorization, rather than difficulties in verbalizing or naming the
odorant, and perceptual functions in olfaction are commonly noted, if
anything, to be predominantly right sided (see Royet & Plailly, 2004).
For example, Cain and Potts (1996) showed that failure to identify an
odor most probably can depend on a higher cognitive stage involving
verbal labeling, as well as on a perceptual stage. Nevertheless, their study
suggests that identification difficulties in most cases depend rather on the
perceptual failure than on failure associated with the process of verbal
labeling. Further support for this view is provided by the paper by
Jönsson and colleagues (Jönsson, Tchekhova, Lönner & Olsson 2005)
that shows that the inability to correctly name odors is due to failure to
recognize the odor rather than to a poor association between the odor
and the proper name. Obviously, this does not imply a lack of higher
cognitive processes in odor identification, and the task is probably
interhemispheric in healthy participants.
As a second raised question, why do some studies indicate a leftnostril superiority whereas other studies do not? The conflicting findings
can probably be explained by differences in experimental set-ups, as well
as in the analyzing and hypothesis testing of the data. In the study by
Herz and colleagues (Herz, McCall & Cahill, 1999), that indicate a leftnostril advantage, the hypotheses was tested by a χ2 test, while other
studies concerning odor identification commonly use parametric tests
with the results analyzed over participants. That study did also include
two sessions that permitted effects of previous exposure, something that
will be further discussed below. In the study by Homewood and
Stevenson (2001), in which 102 participants were tested in large groups,
24
the identification responses were divided into the categories No name
provided, Incorrect, Partially correct, and Correct. No differences between
the nostrils were found except for the category Correct for which a onetailed t-test reached significance that revealed a left-nostril advantage. An
interesting notion to be made is that if the categories Correct and Partially
correct are collapsed the mean identification of left- and right-nostril
stimulation is exactly the same (see Table 2 in the article).
Both Study I and Study II demonstrate effects of repetition priming,
where previously exposed odors were identified to a larger extent.
Interestingly, this effect is predominantly present when tested by leftnostril stimulation, regardless whether the stimulus initially is presented
to the left nostril (Study I) or the right nostril (Study II), demonstrated
also by Olsson and Cain (2003). This finding also agree with the notion
that left hemisphere is associated with conceptual types of priming in
other sensory modalities (Marsolek, 1999). Moreover, based on the effect
of previous exposure, the present studies indicate that what at first sight
appears to be a left-nostril advantage in odor identification in some cases
can be explained by a sequence effect related to the study design. See
Figure 4 for illustration. These results additionally display the importance
to interpret the results with respect to effects of previous exposure in
olfactory studies in general.
The findings in study IV demonstrate no main differences for
amplitudes or latencies in OERPs with respect to rhinal side of
stimulation. This result has recently been showed also in another study
including 95 participants (Stuck, Frey, Freiburg, Hörmann, Zahnert &
Hummel, 2006). Interestingly, subanalyses in Study IV revealed
hemispheric differences on amplitude that suggest generally higher
amplitudes in the parietal site on the left-hemisphere. Further inspection
indicates that smaller N1/P2 amplitudes at the right-hemisphere sites in
left-nostril stimulation can explain these results of side-related differences.
A tentative way to explain this finding in relation to lateralization of
olfactory function is that left- compared to right-nostril stimulation elicits
less activation in the olfactory regions in the right hemisphere known to
be particularly involved in perceptual processing. In that case, this finding
compliment, and indicate an explanation of the demonstrated rightnostril advantage in tasks related to odor perception.
25
Number of correct
identifications
5
4
Left nostril
Right nostril
3
2
Broman et al. (2001)
1
0
Latency (log s) of subvocal
identifications
New odors
Old odors
0,5
0,4
0,3
0,2
Olsson & Cain (2003)
0,1
0,0
Control odors
Primed odors
Number of correct
identifications
5
4
3
2
Broman & Wising (submitted)
1
0
Number of correct
identifications
Session 1
Session 2
?
? ?
?
Herz et al. (1999)
Session 1
Session 2
Figure 4. Illustration of studies that have used a design that permits effects of previous
exposure when investigating differences in identification between rhinal side of
stimulation.
26
Lateralization of olfactory functions has been demonstrated to be
related to handedness in some studies (e.g., Hummel, Mohammadian &
Kobal, 1998; Youngentob, et al., 1982) but not in others (e.g., Betchen
& Doty, 1998; Zatorre & Jones-Gotman, 1990). In a fMRI study by
Royet and colleagues (2003), left- and right-handed showed, at least in
some areas, reversed activation pattern between hemispheres in response
to odors. In general, cognitive functions seem to be less lateralized in lefthanded compared to right-handed individuals (e.g., Laeng & Peters,
1995; Springer & Deutsch, 2003), although the results in olfactory
function still are to limited for any conclusions. However, the studies in
this thesis cannot compliment this literature, since they only included
right handed participants.
Olfactory research in general show that when a gender difference is
demonstrated women perform better than men (e.g., Cain, 1982; Doty,
Applebaum, Zusho & Settle, 1985; Engen, 1987; Larsson, Lövdén &
Nilsson, 2003). Regarding gender differences in lateralization of olfactory
functions per se, on the basis of the hitherto existing studies, there is no
general indication that men and women differ systematically. The present
studies that investigate laterality differences (I, II & IV) include an equal
number of men and women. Furthermore, all results about laterality
differences presented in this thesis have additionally been analyzed with
respect to gender without any demonstrated interactions.
Conclusions
The work in this thesis may contribute to extending the knowledge of
psychological functions in human olfaction. The finding that small
variations in stimulus duration do not seem to considerably affect OERP
waveform is important for the development of a standard OERP
protocol. In a similar vein, the included OERP study concerning
lateralization showed that a protocol using monorhinal stimulation of
either left- or right-nostril probably is sufficient for the majority of
applications. That study does also show the usefulness of this method,
with satisfying temporal resolution of neural activity, to investigate
olfactory lateralization. Although, the obtained results suggest some
clarifications, they certainly call for more research in this field with more
intricate research questions and more elaborated designs. The finding of a
right-nostril advantage in familiarity is in line with results from imaging
studies and supports the view of right-side dominance in basic perceptual
processing of odors. The idea of a general left-nostril superiority in odor
27
identification without effects of previous exposure is not supported,
neither by Study I or by Study II, since none of them initially showed
significant effects in identification between nostrils. However, both
studies demonstrate consistent effects of previous exposure in odor
identification and indicate more pronounced effects tested by the left
nostril.
28
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