I I Y Y Y OPA (O,erceil\ P u b h h e r s Associalion) I\; V

Published by license undcr

the Gordon and Brcach Science
Publishers imprint
Prinlcd In Mela\\ln

Brief Communication
Int J Neurosci Downloaded from informahealthcare.com by University of California Irvine on 11/07/14

TREATMENT WITH AC PULSED

ELECTROMAGNETIC FIELDS IMPROVES
OLFACTORY FUNCTION IN PARKINSON'S
DISEASE
REUVEN SANDYK"
Dtymrtment of' Neuroscience af the Institute ,fi)r Biorncvkal Engineering and
Rehahilitution Services of' Touro Colkge, Dix Hills, N Y , I 1746, USA
For personal use only.

Olfactory dysfunction is a common symptom of Parkinson's diseasc (PD). It may manifest in the
early stages of the disease and infrequently may even antedate the onset of motor symptoms. The
cause of olfactory dysfunction in PD remains unknown. Pathological changes characteristic o f
PD (i.c.,Lewy bodies) have been demonstrated in the olfactory bulb which contains a large
population of dopaminergic neurons involved in olfactory information processing. Since
dopaminergic drugs d o not affect olfactory threshold in P D patients, it has been suggested that
olfactory dysfunction in these patients is not dependent on dopamine deficiency. I present two
fully medicated Parkinsonian patients with long standing history of olfactory dysfunction in
whom recovery of smell occurred during therapeutic transcranial application of A C pulsed
electromagnetic fields (EMFs) in the picotesla flux density. In both patients improvement of
smell during administration of EMFs occurred in conjunction with recurrent episodes of yawn-
ing. The temporal association between recovery of smell and yawning behavior is remarkable
since yawning is mediated by activation of a subpopulation of striatal and limbic postsynaptic
dopamine 112 receptors induced by increased synaptic dopamine release. A high density of
dopamine D2 receptors is present in the olfactory bulb and tract. Degeneration of olfactory
dopaminergic neurons may lead to upregulation (f.~,., supersensitivity) of postsynaptic dopatnine
D2 receptors. Presumably, small amounts of dopamine released into the synapses ofthe olfactory
bulb during magnetic stimulation may cause activation of these supersensitive receptors resulting
in enhanced sense of smell. Interestingly. in both patients enhancement of smell perception
occurred only during administration of EMb-s of 7 H 7 fiequency implying that the release of
dopamine and activation of dopamine D2 receptors in the olfactory bulb was partly frequency
dependent. In fact. weak magnetic ficlds have been found to cause interaction with biological
systems only within narrow frequency ranges (i.e.,frequency windows) and the existence of such
frequency ranges has been explained on the basis of the cyclotron resonance model.

*Address lor correspondence: P.O. Box 453. Roslyn Heights, NY 11577-0453, USA

-..
77 j
 226 R. SANDYK

Keywords; Electromagnetic fields; Parkinson’s disease; yawning; olfactory dysfunction; post-

synaptic dopamine D2 receptors; olfactory bulb

Olfactory dysfunction is a common symptom of Parkinson’s disease (PD)

with 75% -90% of patients demonstrating impairment of smell with objec-
tive testing (Korten and Meulstee, 1980; Doty et al., 1988; 1989). Olfactory
dysfunction is often present in the early stages of the disease and infrequent-
ly may even antedate the motor disability (Korten and Meulstee, 1980; Quinn
et al., 1987; Murofushi et al., 1991; Doty et al., 1992a; Wenning et al., 1995;
Int J Neurosci Downloaded from informahealthcare.com by University of California Irvine on 11/07/14

Hawkes et al., 1997). In fact, olfactory testing has been proposed for pre-
symptomatic screening to identify individuals at risk for P D (Doty et al.,
1995). Impaired olfactory function has also been reported in patients with
atypical Parkinsonism including multisystem atrophy (MSA) and progressive
supranuclear palsy (PSP) (Wenning et al., 1995) although patients with
MPTP-induced Parkinsonism reportedly do not experience appreciable
changes in smell perception (Doty et al., 1992b). Olfactory impairment in
PD is unrelated to the duration of the disease, degree of motor or cognitive
disability, or current therapy with levodopa or anticholinergic drugs (Ward
et al., 1983; Quinn et al., 1987; Doty et al., 1988; 1989; 1992a). The cause of
For personal use only.

olfactory dysfunction in P D remains unknown. The olfactory bulb contains a

substantial population of dopaminergic neurons (Nickel1 et al., 1991;
Coronas et al., 1997) and characteristic pathological changes of Parkinsonism
( i e . , Lewy bodies) have been demonstrated in the olfactory bulb, particularly
in the anterior olfactory nucleus of P D patients (Pearce et al., 1995; Hawkes
et al., 1997). Thus, it has been proposed that degeneration of the olfactory
neural pathways, particularly the mesolimbic projection areas may be associa-
ted with decreased sense of smell in patients with PD (Korten et al., 1980;
Murofushi et al., 1991). Since olfactory dysfunction in PD is unaffected by
treatment with dopaminergic or cholinergic drugs and apomorphine, a
dopmaine agonist, failed to influence olfactory threshold in P D (Quinn et al.,
1987; Doty et al., 1992; Roth et al., 1998), it has been suggested that in PD this
symptom is not dependent on dopamine deficiency (Roth et al., 1998).
I present two fully medicated Parkinsonian patients with long standing
olfactory dysfunction in whom improvement of the sense of smell occurred
during therapeutic transcranial applications of AC pulsed electromagnetic
fields (EMFs) in the picotesla flux density. In these patients subjective
recovery of olfactory function coincided with recurrent episodes of yawning
during the administrations of EMFs of 7 Hz frequency. The manifestation of
yawning in association with recovery of olfactory function in these patients is
remarkable since yawning is a dopaminergic behavior which is mediated by
 OLFACTORY DYSFUNCTION IN PARKINSON’S DISEASE 221

the activation of a subpopulation of postsynaptic dopamine D2 receptors in

the striatum and limbic dopaminergic areas. A high density of dopaminergic
D2 receptors has been demonstrated in the olfactory bulb and tract and their
activation by the release of presynaptic dopamine during pulsed applications
of EMFs may be associated with recovery of olfactory functions in PD.

CASE REPORTS
Int J Neurosci Downloaded from informahealthcare.com by University of California Irvine on 11/07/14

Case I This 73 year old right handed man was diagnosed with PD in 1981
at the age of 56 after he developed micrographia and stiffness of the right
arm. He began treatment with levodopa in 1991 and about 3 years ago devel-
oped “on-off” fluctuations in motor performance. At the time of evaluation
in November of 1998 he had stage IV PD on the Hoehn and Yahr disability
scale (1967) and was experiencing severe motor disability due to declining
resposiveness to levodopa associated with rapid and unpredictable “on-off ”

fluctuations in motor performance with well over 25% of the day spent in
“off” periods. During ‘‘off’’ periods he was completely immobile and
required a wheelchair for ambulation. His speech was hypophonic and
For personal use only.

slurred and there was constant drooling. However, during “on” periods he
ambulated with a cane. His posture was stooped and his knees and elbows
were in a flexed position. He shuffled his feet and exhibited a resting tremor
in the right hand. At the time of presentation he was taking a total of 10
tablets of carbidopa-levodopa (Sinement; 25/100) per day, which he found
to be the only effective medication. Due to increasing motor disability he
elected to undergo transcranial treatment with electromagnetic fields
(EMFs) of 7.5 picotesla flux density. The patient received, on 4 consecutive
days, two successive treatments per day. The EMFs were applied directly
over the head through a set of 24 flat coils using the Sandyk Electromagnetic
Stinulator in a quiet room that was magnetically unshielded. A 5 H z
sinusoidal wave was administered in the first treatment and a 7 H z
sinusoidal wave was administered in the second treatment. Each treatment
was applied for 20 minutes separated by a 10 minutes interval. The patient’s
eyes were shielded during each treatment, which was initiated at mid-
morning during an “on” period about 30 -45 minutes after the patient was
medicated with levodopa. During the application of the first magnetic
treatment on the first day the patient felt relaxed and slightly sleepy but did
not yawn. However, within lominutes of administration of the second
EMFs treatment (using a 7 H z sinusoidal wave), the patient yawned 3
successive times without stretching with each yawn lasting almost
 228 R. SANDYK

10seconds. He denied sleepiness or change in his level of alertness.

Immediately after termination of these episodes of yawning the patient
announced unexpectedly that his sense of smell became acute. He appeared
sensitive to the smell of perfume and other odors in the room. Remarkably,
the patient had lost his sense of smell about 12 years ago and he reported
that prior to the onset of his Parkinsonism he had a distinctly acute sense of
smell. His deficient sense of smell was unaffected previously by treatment
with levodopa or dopamine receptor agonists such as bromocriptine or
pergolide and he denied changes in smell in relation to “on-off” fluctuations
Int J Neurosci Downloaded from informahealthcare.com by University of California Irvine on 11/07/14

in his motor performance. The dramatic recovery of this patient’s sense of

smell was temporary lasting only several hours after termination of
magnetic treatment. Interestingly, on each of the following days the patient
experienced, during the administration of the second magnetic treatment of
7 Hz frequency, recurrent episodes of yawning, without stretching, which
were followed by a temporary improvement of his sense of smell.

Case II This 49 year old right handed woman developed micrographia and
stiffness of the right arm at the age of 38. She has been treated with
carbidopa-levodopa since the age of 40 and was functioning well until about
For personal use only.

a year prior to her initial presentation when she began to experience wors-
ening of her symptoms with increasing tremor and stiffness of the right arm
and hand, increasing bradykinesia, stiffness of the neck, debilitating fatigue,
and increasing depression and anxiety. At the time of her initial presentation
in July of 1998 she was classified stage 111 on the Hoehn and Yahr disability
scale (1967) and was treated with a sustained release carbidopa-levodopa
(Sinement CR; 25/ 100, 6 tabs/d), carbidopa-levodopa (Sinement 25/100;
3 tabs/d), sertraline hydrochloride (100 mg/d), and ergoloid mesylates (3 mg/
d). Since June of 1998 she has been treated with Sinemet (25/100; 6-8 tabs/
day) combined with transcranially applied electromagnetic fields (EMFs)
which were administered about every 4 weeks each time for 5 consecutive
days. Over the following 6 months the patient demonstrated a dramatic
recovery of her Parkinsonism and during her visit in December 1998 she was
classified having stage 1 PD on the Hoehn and Yahr disability scale. The
patient received in December of 1998 daily (mid-morning), on 4 consecutive
days, two successive treatments with EMFs using the Sandyk Electro-
magnetic Stimulator in a quiet and artificially illuminated room that was
magnetically unshielded. The Electromagnetic Stimulator produced an AC
pulsed EMF of 7.5 picotesla flux density which was applied transcranially
via a set of 24 flat coils placed over the patient’s head. A 5 H z sinusoidal
wave was used in the first treatment of 20 minutes duration and following an
 O L F A C T O R Y D Y S F U N C T I O N IN PARKINSON’S DISEASE 229

interval of 15 minutes during which time the device was turned off, a second
treatment of 7 Hz sinusoidal wave was administered for 20 minutes. The
patient’s eyes were shielded during the applications of EMFs. Treatment
with EMFs was initiated each time during an “on” period about 20-
30 minutes after the patient was medicated with carbidopa-levodopa.
Characteristically, during the administration of the first treatment the
patient reported feeling relaxed and towards the end of the treatment she felt
slightly drowsy and yawned few times. During the second treatment she felt
more awake and alert and yawned and stretched more frequently.
Int J Neurosci Downloaded from informahealthcare.com by University of California Irvine on 11/07/14

Unexpectedly, during the second treatment, while receiving a 7 Hz

sinusoidal wave, the patient reported that her sense of smell became more
acute. With continued treatment she experienced a more dramatic
enhancement of smell perception and became sensitive to various odors in
the room. The improvement in the sense of smell was temporary each time
decreasing in acuity towards the evening. The patient recalled that over the
past 4- 5 years her sense of smell had diminished and was unaffected by the
severity of the disease or treatment with dopaminergic medications.
For personal use only.

DISCUSSION

The temporal association between the occurrence of yawning episodes and

the recurrence of the sense of smell in these patients is remarkable as it may
provide additional clues into the dopaminergic pathogenesis of olfactory
dysfunction in PD. Yawning is considered a brainstem regulated behavior
nhich is often associated with changes in arousal and activity levels
(Bnenninger et ul., 1996). It is frequently but not always associated with
stretching. The neuropharmacology of yawning is complex and presently
incompletely understood (Argiolas and Melis, 1998). The yawning reflex is
under the control of several neurotransmitters and neuropeptides at the
central level (Argiolas and Melis, 1998). Among the neurotransmitters in-
volved, dopamine has been shown to induce yawning responses in experi-
mental animals and humans (Serra et al., 1986; 1987; Yamada et al., 1986;
La1 et u/., 1987; Blin e t a / . , 1990; Blin et id., 1991; Argiolas and Melis, 1998).
In levodopa treated PD patients yawning has been observed during
transition to “on” periods (Goren and Friedman, 1998). Experimental
lesion studies indicate that the striatum may be an important site involved in
yawning behavior (Yamada e t al., 1986; Zarrindast et a/., 1995a, b).
Apomorphine and other dopamine receptor agonists administered in high
 230 R. SANDYK

doses to rats systemically or directly into the striatum induce yawning

(Mogilnicka and Klimek, 1977; Zarrindast et al., 1995a, b; Rollinson et al.,
1979; Szechtman, 1984; Yamada et al., 1986). Pharmacological studies
indicate that yawning is mediated by activation of a subpopulation of
postsynaptic dopamine D2 receptors which occurs in response to increased
synaptic dopamine release (Serra et al., 1986; 1987; Matsumoto et al., 1989).
These receptors are highly sensitive to dopamine agonists and differ
pharmacologically from dopamine D2 receptors which mediate motor stimu-
lation or stereotypy (Serra et al., 1986). Yawning induced by transcranial
Int J Neurosci Downloaded from informahealthcare.com by University of California Irvine on 11/07/14

administration of AC pulsed picotesla flux density EMFs of 7 Hz frequency

may be mediated by stimulation of a subpopulation of central postsynaptic
dopamine D2 receptors presumably in response to acute increased presynaptic
dopamine release. Since in these patients recovery of the sense of smell
occurred in temporal association with recurrent episodes of yawning, it is
possible that activation of postsynaptic dopamine D2 receptors in the
olfactory bulb and its central projections mediated the temporary recovery in
olfactory functions. It is noteworthy that the olfactory bulb is the only
telencephalic region containing dopamine neurons which are scattered in the
outer zone of the bulb and form part of a set of interneurons that have been
For personal use only.

collectively designated as group A 15 (Halasz et al., 1977). Olfactory nerve

activity is a potent regulator of bulb dopamine metabolism and continued
afferent input to the olfactory nerve is necessary to maintain stable dopamine
levels (Philpot et al., 1998). In P D degeneration of these neurons in the
olfactory bulb and tract may lead to an upregulation (i.e., supersensitivity) of
postsynaptic dopamine D2 receptor sites (Guthrie et al., 1991), which are
highly concentrated in the olfactory bulb (Charuchinda et al., 1987; Nickel1
et al., 1991; Guthrie et al., 1997; Coronas et al., 1997). Presumably, small
concentrations dopamine released acutely into the synapses of bulbar
dopaminergic neurons during transcranial magnetic stimulation is sufficient
to activate these supersensitive postsynaptic dopamine D2 receptors to induce
reactivation of the sense of smell in P D patients.
I t is noteworthy that enhancement of olfactory function in both patients
occurred each time only during the administration of the second magnetic
treatment employing a sinusoidal wave of 7 Hz frequency. These findings
imply that the magnetically evoked release of dopamine and activation of
postsynaptic dopamine D2 receptors in the olfactory bulb may be frequency
dependent as has been shown with respect to the release of retinal dopamine
by electrical field stimulation (Dubocovich and Hensler, 1986). Dopamine
release is regulated by calcium channels which are present in the nerve
terminals (Kato et al., 1992; Watanabe et al., 1998). Exposure to magnetic
 OLFACTORY DYSFUNCTION IN PARKINSON'S DISEASE 23 1

fields stimuli has been shown to affect the functioning of calcium channels
and distribution of calcium ions, thereby, altering the release of neuro-
transmitters (Kavaliers and Ossenkopp, 1987). The release of calcium ions
from an in vitro brain tissue preparation is frequency dependent (Blackman
et al., 1990), thus supporting the notion that interaction of weak magnetic
fields with biological systems occurs only within a narrow range of frequen-
cies (iz., frequency windows) which can be explained on the basis of the
cyclotron resonance model (Smith et al., 1987; Leitgeb, 1990).
In summary, while olfactory dysfunction in PD reportedly is unaffected
Int J Neurosci Downloaded from informahealthcare.com by University of California Irvine on 11/07/14

by treatment with dopaminergic drugs it may improve, albeit temporarily,

by transcranial administration of AC pulsed EMFs of picotesla flux density.
The recovery of smell, which occurred in these patients in association with
recurrent episodes of yawning during treatment with EMFs, suggest that in
P D olfactory dysfunction is associated with dopamine deficiency in the
olfactory bulb and its central limbic projections. These observations also
suggest that the dopamine receptors mediating yawning (i.e., postsynaptic
D2 receptors) are also involved in the pathogenesis of olfactory dysfunction
in PD. Therefore, recovery of olfactory function in P D may be an additional
clinical marker of postsynaptic dopamine D2 receptor activity.
For personal use only.

References
Argiolas, A. & Melis, M. R. (1998) The neuropharmacology of yawning. European Journal of
Pharmacology, 343, 1 16.
-

Baenninger, R., Binkley, S. & Baenninger, M. (1996) Field observations of yawning and activity
in humans. Physiologji and Behavior, 59, 421 -425.
Blackman, C. F., Benane, S. G., House, D. E. & Elliott, D. J. (1990) Importance of alignment
between local DC magnetic field and an oscillating magnetic field in responses of brain
tissue in vitro and in vivo. Bioelectromagnetics, 11, 159 - 167.
Blin, 0..Masson, G., Azulay, J . P., Fondarai, J. & Serratrice, G. (1990) Apomorphine-indued
blinking and yawning in healthy volunteers. British Journal o/ Clinical Pharmacology, 30.
769 773.
-

Blin. 0..Azulay, J. P., Masson, G. & Serratrice, G. (1991) Yawning. Physiopathology and neuro-
pharmacology. Therapie, 46, 37-43.
Charuchinda, C., Supavilai, P., Karobath, M . & Palacios, J. M . (1987) Dopamine D2 receptors
in the rat brain: autoradiographic visualization using a high-affinity selective agonist
ligand. Journal of Neuroscience, 7, 1352 1360.
-

Coronas, V., Srivastava, L. K., Liang, J. J., Jourdan, F. & Moyse, E. (1997) Identification and
localization of dopamine receptor subtypes in rat olfactory mucosa and bulb: a com-
bined in .siru hybridization and ligand binding radioautographic approach. .Journal n f
Chwnical Neuroanatomy, 12, 243-257.
Doty, R. L., Deems, D. A. & Stellar, S. (1988) Olfactory dysfunction in Parkinsonism: a general
deficit unrelated OGto neurologic signs, disease stage or disease duration. Neurology, 38,
1237- 1244.
Doty, R. L., Riklan, M . , Deems, D. A,, Reynolds, C . & Stellar, S. (1989) The olfactory and
cognitive deficits of Parkinson's disease: evidence for independence. Annals of Nrurolo'qj,.
25. 166-171.
 232 R. SANDYK

Doty, R. L., Stern, M . B., Pfeiffer, C., Gollomp, S. M. & Hurtig, H . 1. (1992a) Bilateral
olfactory dysfunction in early stage treated and untreated idiopathic Parkinson’s disease.
Journal of Neurology Neurosurgery and Psychiatry, 55, 138 142.
-

Doty, R. L., Singh, A,, Tetrud, J. & Langston, J. W. (1992b) Lack of major olfactory dys-
function in MPTP-induced Parkinsonism. Annals of Neurology, 32, 97 100. -

Doty, R. L., Bromley, S. M. & Stern, M. B. (1995) Olfactory testing as an aid in the diagnosis of
Parkinson’s disease: development of optimal discrimination criteria. Neurodegeneration,
4, 93-97.
Dubocovich, M. L. & Hensler, J. G. (1986) Modulation of 3H-dopamine released by different
frequencies of stimulation from rabbit retina. British Journal of Pharmacology, 88, 51 - 61.
Goren, J. L. & Friedman, J. H. (1998) Yawning as an aura for an L-dopa-induced ‘on’ in
Parkinson’s disease. Neurology, 50, 823.
Guthrie, K. M., Pullara, J. M., Marshall, J. F. & Leon, M . (1991) Olfactory deprivation in-
Int J Neurosci Downloaded from informahealthcare.com by University of California Irvine on 11/07/14

creases dopamine D2 receptor density in the rat olfactory bulb. Synapse, 8, 61 70.
~~

Halasz, N., Ljungdahl, A., Hokfelt, T., Johansson, O., Goldstein, M., Park, D . & Biberfeld, P.
(1 977) Transmitter histochemistry of the rat olfactory bulb: I. immunohistochemical
localization of monoamine synthesizing enzymes. Support for intrabulbar, periglomerular
dopamine neurons. Brain Research, 126, 455 -474.
Hawkes, C. H., Shephard, B. C. & Daniel, S. E. (1997) Olfactory dysfunction in Parkinson’s
disease. Journal of Neurology Neurosurgery and Psychiatry, 62, 436 -446.
Hoehn, M. M. & Yahr, M . D. (1967) Parkinsonism: onset, progression and mortality.
Neurology, 17, 427-442.
Kato, T., Otsu, Y., Furune, Y. & Yamamoto, T. (1992) Different effects of L-, N- and T-type
calcium channel blockers on striatal dopamine release measured by microdialysis in freely
moving rats. Neurochemistry International, 21, 99- 107.
Kavaliers, M . & Ossenkopp, K. P. (1987) Calcium channel involvement in magnetic field
inhibition of morphie-induced analgesia. Naunyn Schmiedehergs Archives of Pharmacolog~~.
336, 308 3 IS.
-
For personal use only.

Korten, J. J. & Meulstee, J. (1980) Olfactory disturbances in Parkinsonism. Clinical Neurologj,

rmd Neurosurgerj,, 82, 1 13 1 18.
Lal, S., Grassino, A., Thavundayil, J. X. & Dubrovsky, B. (1987) A simple method for the study
of yawning in man induced by the dopamine receptor agonist apomorphine. ProRress in
Neuropsychopharniacolog.v and Biological Psqvhiatry, 11 223 228.
~ -

Leitgeb, N. (1990) Cyclotron resonance as a cause of biological effects of weak electric and
magnetic fields’? Biomedizinische Technologie, 35, 135 138.
-

Matsumoto, S., Yamada, K., Nagashima, M., Matsuo, N., Shirakawa, K. & Furukawa, T.
( 1 989) Potentiation by serotonergic inhibition of yawning induced by dopamine receptor
agonists in rats. Pharmacology Biochemistry and Behavior, 32, 8 15 - 8 18.
Mogilnicka, E. & Kilmek, V. (1977) Drugs affecting dopamine neurones and yawning
behaviour. Pharmacolog-v Biochemistry and Behavior, 7, 303 305.
-

Murofushi, T., Mizuno, M., Osanai, R . & Hayashidd, T. (1991) Olfactory dysfunction in
Parkinson’s disease. Journal of Otolaryngology and Relates Specialities, 53, 143 146.
-

Nickell, W . T.. Norman, A . B., Wyatt, L. M . & Shipley, M. T. (1991) Olfactory bulb DA
receptors may be located on terminals of the olfactory nerve. NeuroReport, 2, 9- 12.
Pearce, R. K., Hawkes, C. H. & Daniel, S. E. (1995) The anterior olfactory nucleus in
Parkinson’s disease. Movement Disorders, 10, 283 287.
-

Philpot, B. D., Men, D., McCarty, R. & Brunjes, P. C. (1998) Activity dependent regulation of
dopamine content in the olfactory bulbs of naris-occluded rats. Neuroscience, 85,969-977.
Quinn, N. P., Rossor, M. N . & Marsden, C. D. (1987) Olfactory threshold in Parkinson’s
disease. Journal of Neurology Neurosurgery and Psychiatry, 50, 88 - 89.
Rollinson, R. D., Wiggins, W. S. & Gilligdn. B. S. (1979) Drug-induced yawning successfully
treated with pimozide. Archives of Neurologj., 36, 253.
Roth, J., Radil, T.. Ruricka, E., Jech, R. & Tichy, J. (1998) Apomorphine does not influence
olfactory threshold in Parkinson’s disease. Functional Neurologr. 13, 99- 103.
Sandyk, R. (1992) Weak magnetic fields in the treatment of Parkinson’s disease with the ‘on-
off’ phenomenon. Internutioncrl Journul of Nwrosciencr, 66, 97 106. -
 OLFACTORY DYSFUNCTION IN PARKINSON’S DISEASE 233

Smith, S. D., McLeod, B. R., Liboff, A . R. & Cooksey, K . (1987) Calcium cyclotron resonance
and diatom mobility. Bioelectromugnerie~.8 , 2 I S 227.
-

Serra, G., Collu, M . & Gessa, G. L. (1986) Dopamine receptors mediating yawning: are they
autoreceptors‘ European Journal ~/Phar~,iucology, 120, 187- 192.
Serra, G., Collu. M. & Gessa, G. L. (1987) Yawning is elicited by D2 dopamine agonists but is
blocked by the D1 antagonist, SCH 23390. fs~’chophurmuco/ogj~, 91. 330- 333.
Szechtman, H. (1984) Timing of yawns induced a small dose of apomorphine and its alteration
by naloxone. Progress in Neurops~..chophrrr~~iueology
and Biological Psjdiiutry, 8 , 743 746.
Ward, C. D., Hess. W. A. & Calne, D. B. (1983) Olfactory impairment in Parkinson’s disease.
Neurology, 33, 943 946.
Watanabe, Y.. Lawlor. G. F;. & Fujiwara, M. (1998) Role of nerve terminal L-type Ca”
channel in the brain. Lifk Sciencrs, 62, 1671 1675.
-

Wenning, G. K . , Shephard, B., Hawkes, C.. Petruckevitch, A , , Lees, A . & Quinn, N. (1995)
Int J Neurosci Downloaded from informahealthcare.com by University of California Irvine on 11/07/14

Olfactory function in atypical Parkinsonian syndromes. Actu Nrurolg+a Scandinuvica. 91.

247 250.
-

Yamada, K . , Tanaka, M., Shibata, K. & Furukawa, T. (1986) Involvement of septa1 and striatal
dopamine D-2 receptors in yawning behavior in rats. Psvehopliarniucology, 90, 9- 13.
Zarrindast, M. R., Toloui, V. & Hashemi. B. (199Sa) Effect of GABA-ergic drugs on
physostigmine-induced yawning in rats. Ps~c.hopurmucolo~J‘ (Berlin). 122, 297- 300.
Zarrindast, M . R., Fatehi, F. & Mohagheghi-Badi, M. (1995b) Effects of adenosine agents on
apomorphine-induced yawning in rats. P.s~.c,/iophurmucoloX?., 122, 292 296.
-
For personal use only.