In Vivo Positron Emission Tomographic
Evidence for Compensatory Changes in
Presynaptic Dopaminergic Nerve Terminals
in Parkinson’s Disease
Chong S. Lee, MD, FRCPC,* Ali Samii, MD, FRCPC,* Vesna Sossi, PhD,† Thomas J. Ruth, PhD,†
Michael Schulzer, MD, PhD,* James E. Holden, PhD,‡ Jess Wudel, LPN,* Pramod K. Pal, MD,*
Raul de la Fuente-Fernandez, MD,* Donald B. Calne, DM, FRCPC,* and A. Jon Stoessl MD, FRCPC*
Clinical symptoms of Parkinson’s disease (PD) do not manifest until dopamine (DA) neuronal loss reaches a symptom-
atic threshold. To explore the mechanisms of functional compensation that occur in presynaptic DA nerve terminals in
PD, we compared striatal positron emission tomographic (PET) measurements by using [
11
C]dihydrotetrabenazine
([
11
C]DTBZ; labeling the vesicular monoamine transporter type 2), [
11
C]methylphenidate (labeling the plasma mem-
brane DA transporter), and [
18
F]dopa (reflecting synthesis and storage of DA). Three consecutive PET scans were per-
formed in three-dimensional mode by using each tracer on 35 patients and 16 age-matched, normal controls. PET
measurements by the three tracers were compared between subgroups of earlier and later stages of PD, between drug-
naive and drug-treated subgroups of PD, and between subregions of the parkinsonian striatum. The quantitative rela-
tionships of [
18
F]dopa and [
11
C]DTBZ, and of [
11
C]methylphenidate and [
11
C]DTBZ, were compared between the PD
and the normal control subjects. We found that [
18
F]dopa K
i
was reduced less than the binding potential (B
max
/K
d
) for
[
11
C]DTBZ in the parkinsonian striatum, whereas the [
11
C]methylphenidate binding potential was reduced more than
[
11
C]DTBZ binding potential. These observations suggest that the activity of aromatic L-amino acid decarboxylase is
up-regulated, whereas the plasma membrane DA transporter is down-regulated in the striatum of patients with PD.
Lee CS, Samii A, Sossi V, Ruth TJ, Schulzer M, Holden JE, Wudel J, Pal PK, de la Fuente-Fernandez R,
Calne DB, Stoessl AJ. In vivo positron emission tomographic evidence for compensatory changes in presynaptic
dopaminergic nerve terminals in Parkinson’s disease. Ann Neurol 2000;47:493–503
Parkinson’s disease (PD) is one of the most common
neurodegenerative disorders, the main pathology of
which is the loss of dopamine (DA) neurons in the
substantia nigra and of DA nerve terminals in the stri-
atum. It has been widely accepted that there is a pre-
clinical stage in which patients with PD are asymptom-
atic despite a substantial loss of nigrostriatal DA
neurons.
1,2
The mechanisms of functional compensa-
tion during this preclinical stage are not fully under-
stood. Nevertheless, evidence from experimental studies
suggests that the loss of DA neurons is functionally
compensated by an increase in synthesis and release of
DA from surviving DA nerve terminals, as well as a
reduced rate of DA inactivation in presynaptic DA
nerve terminals.
3
Dopaminergic transmission, like other monoaminer-
gic transmission, is dependent on six processes: (1) DA
is synthesized, and then (2) packaged into synaptic ves-
icles by type 2 vesicular monoamine transporters
(VMAT2). (3) Depolarization releases DA from pre-
synaptic vesicles into the synaptic cleft. (4) DA inter-
acts with presynaptic and postsynaptic DA receptors.
(5) Extracellular DA is taken back into presynaptic DA
nerve terminals via the plasma membrane DA trans-
porter. (6) Any persisting extracellular DA is degraded
by catechol O-methyltransferase. Biochemical studies
have shown that tissue DA content and the activity of
enzymes involved in the synthesis of DA are reduced in
the DA denervated striatum.
4
The synthesis and release
of DA per residual DA nerve terminal (fractional DA
synthesis and DA release) are increased in the striatum
of patients with PD and in an animal model of
From the *Neurodegenerative Disorders Centre, Vancouver Hospi-
tal and Health Sciences Centre, and †TRIUMF, University of Brit-
ish Columbia, Vancouver, British Columbia, Canada; and ‡Depart-
ment of Medical Physics, University of Wisconsin, Madison, WI.
Received Jul 12, 1999, and in revised form Nov 19. Accepted for
publication Dec 9, 1999.
Address correspondence to Dr Lee, Neurodegenerative Disorders
Centre, Purdy Pavilion, Vancouver Hospital and Health Sciences
Centre, 2221 Wesbrook Mall, Vancouver, British Columbia, Can-
ada V6T 2B5.
Copyright © 2000 by the American Neurological Association 493