JPhysiology (1993) 87, 141 -151 141
© Elsevier, Paris
Physiology and biochemistry of peptidergic cotransmission in Aplysia
KR Weiss a, V Brezina a, EC Cropper a, J Heierhorst a, SL Hooper a,
WC Probst a, SC Rosen b, FS Vilim a, I Kupfermann b
aDepartment of Physiology and Biophysics, Mt Sinai School of Medicine, 1 Gustave Levy Place, New York, NY 10029;
hCenter for Neurobiology and Behavior, College of Physicians and Surgeons, Columbia University, 722 West 168rh Street,
New York, NY 10032, USA
Summary - The marine mollusc Aplysia. whose simple nervous system facilitates study of the neural basis of behavior,
was used to investigate the role of peptidergic cotransmission in feeding behavior. Several novel modulatory neuropeptides
were purified and localized to identified cholinergic motorneurons. Physiological and biochemical studies demonstrated that
these peptides are released when the motorneurons fire at frequencies that occur during normal behavior, and that the
peptides modify the relationship between muscle contraction amplitude and relaxation rate so as to maintain optimal motor
output when the intensity and frequency of feeding behavior change.
Aplysia / peptidergic cotransmission / feeding behavior
Introduction
Prior to the 1970s it was generally accepted that
each neuron contains a single neurotransmitter.
Also, it was felt that the number of transmitter
substances was very limited. More recent dis-
coveries have led to the revision of these tradi-
tional views of synaptic transmission. For
example, in the last two decades it has become
apparent that numerous small bioactive peptides
are present in the nervous system (H6kfelt et al,
1984). Hundreds of these peptides are likely to
act as neurotransmitters (Snyder, 1980). Often
neuropeptides are present in neurons that contain
either additional neuropeptides or classical trans-
mitters. Thus, it now appears that individual neu-
rons typically contain various combinations of
cotransmitters, at least some of them neuropep-
tides (for reviews see Bartfai et al, 1986; H6kfelt
et al, 1984; Kupfermann, 1991). This very prob-
ably contributes to the complexity of signaling in
the brain.
Although it is now widely accepted that neu-
rons contain cotransmitters, technical difficulties
have limited attempts to characterize the role that
cotransmitters play in the nervous system under
physiological conditions (Campbell, 1987;
Kupfermann, 1991). For instance, cotransmitters
are usually released in smaller quantities than
classical transmitters. Consequently, in most sys-
tems direct evidence for cotransmitter release has
been impossible to obtain. Moreover, in order to
establish that a substance functions as a
cotransmitter it is necessary to demonstrate not
only that it is released, but that it is released in
quantities that are sufficient to activate receptors
and have physiological consequences. Since the
biological actions of putative cotransmitters are
often subtle, it has been even more difficult to
demonstrate physiological consequences of
cotransmitter release than release itself. Indeed,
in a recently published exhaustive review of
cotransmission, Kupfermann (1991) concluded
that while the cumulative evidence suggested that
cotransmission may occur under some circum-
stances, at the time of writing there was as yet
"no conclusive evidence that indicates that
cotransmission occurs under normal operation of
the nervous system".
Many of the technical difficulties encountered
in studying cotransmission can be avoided by
using relatively simple invertebrate preparations.
Many invertebrate neurons are large and reiden-
tifiable. Consequently, they can be individually
stimulated in physiological studies and then bio-
chemically characterized. There is no need for