Chem. Senses 24: 459-464,
1999
© Oxford University Press 1999
Olfactory Event-related Potentials in Young and Elderly Adults: Evaluation of Tracking Task versus Eyes Open/Closed Recording
1 San Diego State University, USA, 2 Umeå University, Sweden, 3 SDSU/UCSD Joint Doctoral Program in Clinical Psychology, 4 University of California, School of Medicine, San Diego and 5 The Scripps Research Institute, USA
Correspondence to be sent to: Dr Claire Murphy, SDSU/UCSD Joint Doctoral Program, 6363 Alvarado Ct, Suite 101, San Diego, CA 92120-4913, USA. e-mail:cmurphy{at}sunstroke.sdsu.edu
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The purpose of the present study was to evaluate olfactory event-related potentials (OERPs) elicited by amyl acetate from subjects performing a visuomotor tracking task compared with the no-task conditions of eyes open and eyes closed. Task condition did not produce any reliable effects for any amplitude measure. Task type weakly influenced only P2 latency. Elder adults evinced smaller P2 and N1/P2 amplitudes and longer N1 and P2 latencies than young adults. The results suggest that tracking task performance is not necessary to obtain robust OERPs from normal subjects of a wide age range.
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Introduction |
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Several sources of subject-induced influence on event-related potentials (ERPs) have been reported (Hall, 1992
; Polich and Kok, 1995), but
a possibly important factor that is not considered is how variation in background
electroencephalogram (EEG) activity can influence the ERP components. In particular, alpha
activity (8–13 Hz) has been associated with ERP variability, since this rhythm can reach
amplitudes of >100 µV (Markand, 1990; Intriligator
and Polich, 1995; Spencer and Polich, 1999). These results
may be important for recording olfactory event-related potentials (OERPs), because the rapid
sensory adaptation and habituation of the olfactory system necessitates that relatively long
interstimulus interval (ISIs) are needed for obtaining accurate OERPs (Morgan et
al., 1997). However, the long ISI gives rise to relatively long recording times,
which will typically induce increased alpha rhythm activity, but have been found to increase ERP
amplitudes (Morgan et al., 1997; Polich, 1997b). Thus, possible interference of background EEG alpha activity with the OERP
recordings has been a methodological concern.
To counteract the possible influence of alpha activity on OERPs, a visuomotor tracking task
has sometimes been employed to engage attentional processing mechanisms and thereby inhibit
or
block alpha rhythm production (Kobal et al., 1992; Morgan et al., 1997). A commonly used task requires the subject to move a
handheld joystick, slowly and gently, so that a small square remains inside a larger, randomly
moving square on a computer terminal screen (Kobal et al., 1992). Because the task engages attentional focus and mild motor movements, it is easy to
ensure that
the subject is attending to the tracking task by monitoring performance directly during
electrophysiological recordings (Wickens et al., 1983). In
contrast, `mental' tasks that theoretically engage attentional operations (e.g. adding
or subtracting numbers successively) have been found to block alpha inconsistently—most
likely because of variegated cognitive performance across subjects and tasks (Volavka
et al., 1967; Marciani et al., 1992). Finally,
alpha activity can also be easily blocked or instigated by comparing EEG recording when eyes
are
open with an eyes closed condition—a method that is simple, noninvasive and easily
controlled (Hardle et al., 1984; Penaloza-Rojas, 1990; Marciani et al., 1992; Könönen and Partanen, 1993).
A related issue in this context is how normal aging may alter EEG and OERPs. Previous
reports have demonstrated that as normal subjects increase in age EEG power decreases and
background (alpha) frequency slows (Celesia, 1986; Dustman et al., 1990), although the association between increasing adult age and
EEG frequency slowing has not been observed consistently (Duffy et al.,
1984; Giaquinto and Nolfe, 1986; Polich, 1997a; Pollock and Schneider, 1990). More importantly,
age-related changes in alpha activity between eyes open and closed recording conditions are also
inconsistent (Markand, 1990; Könönen and
Partanen, 1993; Polich, 1997b). Given the increased interest
in the application of OERPs to assess normative aging and dementia, especially with respect to
the
olfactory P3 component (Pause et al., 1996; Polich,
1996; Geisler et al., 1999a; Morganet al., 1999) (C. Murphy et al., submitted for publication), it is
important to determine if the addition of a visuomotor task affects OERP components for normal
young and elderly adults (Evans et al., 1995; Morgan et al., 1997).
The present study was designed to comprehensively evaluate this issue by recording OERPs
in young and elderly adults in different conditions in which they either performed a visuomotor
tracking task or did not. Although the P3 OERP component reflects cognitive factors and is of
interest, the olfactory N1 and P2 components are likely to be more closely related to olfactory
sensitivity/concentration variables and will be assessed here (Lorig et al.,
1991, 1996; Kobal et al., 1992; Prah and Benignus, 1992; Schiffman, 1993;
Murphy et al., 1994; Lorig and
Verspoor, 1996; Pause et al., 1996; Morgan et al., 1997).
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Participants
A total of 40 volunteers participated, half of whom were young (mean = 25.0, SD = 3.6
years) and half of whom were elderly (mean = 72.1, SD = 6.0 years), with equal numbers of each
gender in each age group. The young adults were university students and the elderly were
recruited from a pool of participants in a longitudinal study on chemosensory function. All
participants were screened for nasal/sinus disease by means of endoscopic, rhinomanometric and
cytological examinations (Jalowayski et al., 1983; Davidson et al., 1987; Jalowayski and Zeiger, 1988).
The elderly participants were also screened for dementia with the Mini-Mental State Exam (Folstein et al., 1975) (cutoff of 26), the Fuld (1978) adaptation of the
Information–Memory–Concentration test (Blessed et al., 1968) (cutoff of 3 errors) and the Dementia
Rating Scale (Mattis, 1976) (cutoff of 124). All were right handed with
the exception of one elderly male.
Stimuli
Amyl acetate was chosen for both threshold determination and OERP recordings because it
has been used successfully to elicit OERPs in the target populations (Kobal 1985; Evans and Starr, 1993; Murphy et al.,
1994; Morgan et al., 1997). The purpose of
threshold assessment in this study was to screen out anosmics. For threshold determination, the
amyl acetate was prepared in mineral oil in 18 dilution steps, each step one-third the
concentration
of the preceding stimulus, starting with a 1% v/v solution. A two-alternative, forced-choice,
ascending method of limits was applied to determine the detection threshold (Murphy et al., 1994). The mean threshold in dilution steps was for the young was
13.4 (SD = 3.3) and for the elderly adults was 12.4 (SD = 3.8), with no reliable differences found
between the subject groups [F(1,17) < 1, P > 0.1]. These thresholds are
very similar to those previously reported for normal young and elderly adults (Morgan et al., 1997). Thus, the participants in these studies were not
anosmic.
Stimulus presentation
Olfactory stimulation for OERP recording was accomplished with a dynamic olfactometer (Murphy et al., 1994; Morgan et al., 1997) which incorporates well-established
techniques for stimulus presentation (Kobal and Hummel, 1988; Evans et al., 1993). A digital timer initiates the onset of the
OERP recording and simultaneously
generates the stimulus from the olfactometer. A tank of breathing air is used to establish a flow
rate of 7.4 l/min, with a 80% relative humidity achieved by passing the airstream through
deionized water of a constant temperature. A plastic duct delivered the air to the nostril and was
heated to raise the air to nasal temperature (36.5°C) before it passes into the nostril through
a Teflon tube (1.6 mm inner diameter) placed just inside (2–4 mm) the nostril.
Each stimulus presentation is effected by means of an electromagnetic valve which opens for
200 ms, during which time a portion of the main air flow is replaced by an equal portion of odor
flow (2.1 l/min). The switching valves were acoustically isolated and a constant flow rate into the
nostril was maintained at all times during OERP data collection. The concentration of amyl
acetate delivered by the olfactometer (909 p.p.m.) was safely below the threshold for nasal
pungency of 1648 p.p.m. (Cometto-Muñiz and Cain, 1991).
Concentration was assessed with an infrared gas spectrometer (Miran) with a ±1.8%
error variability, from samples taken in vapor state at the nose-piece. Stimulus rise time was
below 20 ms (Murphy et al., 1994). The stimuli were presented
with an ISI of 60 s to avoid adaptation/habituation (Morgan et al., 1997).
OERP recordings
EEG was recorded with gold-plated electrodes that were affixed with electrode cream and
tape from the Fz, Cz and Pz sites, referenced monopolarly to linked earlobes and grounded at the
forehead. Contamination of ERPs from eye movements was monitored with electro-ocular
activity (EOG) from electrodes placed at the outer canthus and supraocularly at the left eye.
Impedance did not exceed 10 k
and was typically below 5 k. EEG epochs were
2000 ms in duration and consisted of a 500 ms pre-stimulus and a 1500 ms post-stimulus period
sampled at 1000 Hz, with a bandpass of 0.1–30 Hz (6 dB/octave), amplified
20 000 times and stored on magnetic medium. Trials with eye blinks or artifactual
activity exceeding ±50 µV were rejected on-line and were repeated to obtain 20
artifact-free trials. There was little difference among conditions in the number of repeated trials,
typically on the order of 5–10 per condition, per subject. Velopharyngeal closure was
employed to restrict breathing to the mouth, thereby keeping nasal flow rate constant (Kobal and Hummel, 1989). The side of the nose reported by the
participant to be
most patent was used for OERP recordings (equal number for both left and right for both young
and elderly).
Procedure
On the first day, the threshold and neuropsychological assessment data were obtained. On the
second day, OERPs were recorded from each participant in three different conditions: (i) while
performing a tracking task in which a small circle and large square appeared on a video screen,
located 1 m in front of the participant's eyes, and the participant was instructed to use a
joystick to keep the small circle inside the large square that moved across the screen randomly
(Kobal et al., 1992); (ii) with eyes open and viewing a 2 cm
circular dot at a distance of 1 m; and (iii) with eyes closed. In all conditions, the participant was
instructed to raise a finger when an odor was perceived to ensure stimulus perception in the
absence of adaptation/habituation. The condition order was counterbalanced across participants
and age group. These conditions were designed to empirically assess possible effects of
task-related EEG changes and OERP measures in two clinically important populations. Although
direct measures of background EEG were not obtained because of equipment limitations, the task
conditions were modeled directly after those employed in many previous studies so that a
comprehensive evaluation of their putative effects on the OERP could be assayed empirically (Kobal et al., 1992; Morgan et al., 1997; Polich, 1997a, 1997b).
Analysis
The OERPs from each participant, task condition and electrode site were adjusted so that the
average voltage from the 500 ms pre-stimulus baseline equaled zero. Amplitudes of N1, P2 and
N1/P2 (peak-to-peak), as well as peak latencies relative to stimulus onset, were assessed visually.
A three-factor ANOVA (3 task conditions x 2 age groups x 3 electrode sites) was
conducted on each dependent variable, with Geisser–Greenhouse corrections applied to
the degrees of freedom for repeated measure factors. Post-hoc analyses were conducted with the
Newman–Keuls means comparison procedure. Table 1
summarizes
the ANOVA results. Figure 1 presents the grand averaged OERPs from
each task condition, age group, and electrode site. Figure 2 illustrates the
mean (+ 1 SE) N1, P2 and N1/P2 amplitudes. Figure 3 illustrates the
mean (+ 1 SE) N1 and P2 peak latencies.
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Results and discussion |
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Task condition did not produce any reliable effects for any amplitude measure, P > 0.10 in all cases). P2 latency was shorter for the tracking task condition overall [F(2,76) = 3.8, P < 0.05], although this outcome appeared to originate primarily from the elderly subjects, since age and electrode produced a significant interaction for P2 latency [F(2,76) = 4.2, P < 0.05]. Young subjects produced larger P2 [F(1,38) = 18.2, P < 0.001] and N1/P2 [F(1,38) = 17.9, P < 0.001] amplitudes than elderly subjects. Young subjects demonstrated shorter N1 [F(1,38) = 39.3, P < 0.001] and P2 [F(1,38) = 24.1, P < 0.001] latencies than elderly subjects. As indicated by the scalp topography patterns in Figure 2
, N1 amplitude [F(2,76) = 12.4, P < 0.001], N1/P2 amplitude [F(2,76) = 11.8, P < 0.001] and P2 latency
[F(2,76) = 14.6, P < 0.001] varied in the usual fashion with electrode
position. No other reliable effects or
interactions were observed. In sum, task type weakly influenced P2 latency, with the usual effects
of subject age and electrode observed.
Much of the work on olfactory event-related potentials has utilized amyl acetate as the
stimulus (Kobal 1985; Evans and Starr, 1993; Murphy et al., 1994; Morgan et al.,
1997); thus, the current study sought to investigate the effects of the tracking task
versus
eyes open/closed condition using this prototypical stimulus. Psychophysical work with amyl
acetate, presented for 2 s duration in squeeze bottles in anosmic individuals, indicates thresholds
for nasal pungency of 1648 p.p.m. (Cometto-Muñiz and Cain, 1991). The shorter duration of stimulation from the olfactometer in the current study (200
ms) would be expected to generate even higher thresholds for pungency. Thus, the potentials
evoked from 909 p.p.m. amyl acetate would be expected to be olfactory rather than trigeminal in
nature. Furthermore, in persons anosmic following traumatic brain injury we have observed no
OERP response to amyl acetate at a concentration slightly higher than was used in the current
study, in spite of robust ERP responses to trigeminal stimulation (Geisler et al., 1999b), thus the event-related brain potentials observed in the present study
were olfactory.
In order to afford the participant every advantage in performance, the side of the nose that he or she reported as most patent, or open, at the beginning of testing was used for stimulus presentation. Nasal patency was not measured at the beginning, during or at the end of OERP testing, and we are aware of no studies in the literature that have made such measurements during OERP experiments. This might be an interesting variable to pursue. Such measurements were outside the scope of the present study.
The current study employed thresholds for amyl acetate in order to screen for anosmia.
Effects of aging on olfactory thresholds have been observed in the general aged population (Murphy, 1986, 1993a, 1993b; Schiffman, 1986, 1993). These
studies did not screen for dementia or nasal sinus health. In studies such as the present, where the
elderly have been screened to eliminate the confounding of dementia effects from pre-clinical
and
early Alzheimer's disease, other dementias of old age and the confounding of nasal sinus
disease, observed age effects on psychophysical thresholds are substantially smaller, though
occasionally not statistically significant, than in studies of the general aging population (Morgan et al., 1997; Covington et al., 1999). It is of interest that age effects on the
OERP are robust in studies of pre-screened
elderly persons.
The elderly generated smaller P2 and N1/P2 amplitudes and longer N1 and P2 latencies than
did the young adults, as has been observed previously (Murphy et al., 1994; Evans et al., 1995; Morgan et al., 1997,
1999; Covington et al., 1999) (C.
Murphy et al., submitted for publication). In addition, the present results
are also in accord with respect to the influence of recording site and latency (Kobalet al., 1992). More important for the present purposes, it is noteworthy that the
tracking task versus eyes open/closed condition did not produce any reliable interactions with
subject age. Thus, either of these recording conditions can be used with normal young or elderly
adults.
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Acknowledgments |
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This research was supported by NIH grant DC02064 (C.M.) and training grant DC00032. We gratefully acknowledge Dr Terrence M. Davidson for endoscopic examinations, Dr Alfredo A. Jalowayski for rhinomanometric and cytological examinations, and Dr Gerd Kobal for advice and assistance with the olfactometer and OERP recordings.
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Accepted May 6, 1999
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