Extra- and intracellular recordings from an intact brain preparation were used to study the effects of 5-hydroxytryptamine (5-HT or serotonin) on projection neurons in the sexually dimorphic macroglomerular complex (MGC) in the antennal lobe of the male moth Manduca sexta. The MGC is a group of three identified glomeruli specialized for synaptic processing of primary afferent information about the multi-component sex pheromone of the female. We investigated the modulatory effects of 5-HT on pheromone-evoked local field potentials in the MGC. The magnitude and duration of these potentials, which are thought to be generated by a population of pheromone-sensitive projection neurons of the MGC, were increased by 5-HT. Using intracellular recordings from the neurites of individual MGC projection neurons, we found that 5-HT increased the number of action potentials in response to pheromonal stimulation. These findings correlate well with earlier experiments that used other recording techniques. Our results are further evidence that 5-HT modulates a population of pheromone-sensitive MGC projection neurons that relay information about the pheromonal stimulus from the MGC to higher-order centers in the protocerebrum and are therefore pivotal for mate-finding and odor-guided behavior.

Bell
R. A.
,
Joachim
F. A.
(
1976
).
Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms
.
Ann. Ent. Soc. Am
69
,
365
–.
Byrne
J. H.
,
Kandel
E. R.
(
1996
).
Presynaptic facilitation revisited: state and time dependence
.
J. Neurosci
16
,
425
–.
Carew
T. J.
(
1996
).
Molecular enhancement of memory function
.
Neuron
16
,
5
–.
Carew
T. J.
,
Sahley
C. J.
(
1986
).
Invertebrate learning and memory: from behavior to molecules
.
Annu. Rev. Neurosci
9
,
435
–.
Christensen
T. A.
,
Harrow
I. D.
,
Cuzzocrea
C.
,
Randolph
P. W.
,
Hildebrand
J. G.
(
1995
).
Distinct projections of two populations of olfactory receptor axons in the antennal lobe of the sphinx moth Manduca sexta
.
Chem. Senses
20
,
313
–.
Christensen
T. A.
,
Heinbockel
T.
,
Hildebrand
J. G.
(
1996
).
Olfactory information processing in the brain: encoding chemical and temporal features of odors
.
J. Neurobiol
30
,
82
–.
Christensen
T. A.
,
Hildebrand
J. G.
,
Tumlinson
J. H.
,
Doolittle
R. E.
(
1989
).
Sex pheromone blend of Manduca sexta: responses of central olfactory interneurons to antennal stimulation in male moth
.
Arch. Insect Biochem. Physiol
10
,
281
–.
Christensen
T. A.
,
Waldrop
B. R.
,
Hildebrand
J. G.
(
1998
).
Multitasking in the olfactory system: context-dependent responsesto odors reveal dual GABA-regulated coding mechanisms in single olfactory projection neurons
.
J. Neurosci
18
,
5999
–.
Fan
R.-J.
,
Anderson
P.
,
Hanson
B. S.
(
1997
).
Behavioural analysis of olfactory conditioning in the moth Spodoptera littoralis (Boidsd.) (Lepidoptera: Noctuidae)
.
J. Exp. Biol
200
,
2969
–.
Gelperin
A.
,
Kleinfeld
D.
,
Denk
W.
,
Cooke
I. R. C.
(
1996
).
Oscillations and gaseous oxides in vertebrate olfaction
.
J. Neurobiol
30
,
110
–.
Gilmore
J. U.
(
1938
).
Observations on the hornworms attacking tobacco in Tennessee and Kentucky
.
J. Econ. Ent
31
,
706
–.
Gray
C. M.
(
1994
).
Synchronous oscillations in neuronal systems: mechanisms and functions
.
J. Computat. Neurosci
1
,
11
–.
Hammer
M.
,
Menzel
R.
(
1995
).
Learning and memory in the honeybee
.
J. Neurosci
15
,
1617
–.
Hansson
B. S.
,
Christensen
T. A.
,
Hildebrand
J. G.
(
1991
).
Functionally distinct subdivisions of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta
.
J. Comp. Neurol
312
,
264
–.
Hartlieb
E.
(
1996
).
Olfactory conditioning in the moth Heliothis virescens
.
Naturwissenschaften
83
,
87
–.
Hawkins
R. D.
,
Kandel
E. R.
,
Siegelbaum
S. A.
(
1993
).
Learning to modulate transmitter release: themes and variations in synaptic plasticity
.
Annu. Rev. Neurosci
16
,
625
–.
Heinbockel
T.
,
Christensen
T. A.
,
Hildebrand
J. G.
(
1995
).
Subunit architecture of the macroglomerular complex and the integrative function of output neurons in the moth, Manduca sexta
.
Chem. Senses
20
,
707
–.
Heinbockel
T.
,
Christensen
T. A.
,
Hildebrand
J. G.
(
1999
).
Temporal tuning of odor responses in pheromone-responsive projection neurons in the brain of sphinx moth Manduca sexta
.
J. Comp. Neurol
409
,
1
–.
Hildebrand
J. G.
(
1995
).
Analysis of chemical signals by nervous systems
.
Proc. Natl. Acad. Sci. USA
92
,
67
–.
Hildebrand
J. G.
,
Shepherd
G. M.
(
1997
).
Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla
.
Annu. Rev. Neurosci
20
,
595
–.
Homberg
U.
,
Hildebrand
J. G.
(
1989
).
Serotonin-immunoreactive neurons in the median protocerebrum and suboesophageal ganglion in the sphinx moth Manduca sexta
.
Cell Tissue Res
258
,
1
–.
Homberg
U.
,
Hoskins
S. G.
,
Hildebrand
J. G.
(
1995
).
Distribution of acetylcholinesterase activity in the deutocerebrum of the sphinx moth Manduca sexta
.
Cell Tissue Res
279
,
249
–.
Kaissling
K.-E.
,
Hildebrand
J. G.
,
Tumlinson
J. H.
(
1989
).
P. KLOPPENBURGANDT. HEINBOCKEL1709 5-HT modulates pheromone-evoked potentials Pheromone receptor cells in the male moth Manduca sexta
.
Arch. Insect Biochem. Physiol
10
,
273
–.
Kandel
E. R.
,
Schwartz
J. H.
(
1982
).
Molecular biology andlearning: modulation of transmitter release
.
Science
218
,
433
–.
Kent
K. S.
,
Hoskins
S. G.
,
Hildebrand
J. G.
(
1987
).
A novel serotonin-immunoreactive neuron in the antennal lobe of the sphinx moth Manduca sexta persists throughout postembryonic life
.
J. Neurobiol
18
,
451
–.
Kloppenburg
P.
,
Ferns
D.
,
Mercer
A. R.
(
1999
).
Serotonin enhances central olfactory neuron responses to female sex pheromone in the male sphinx moth Manduca sexta
.
J. Neurosci
19
,
8172
–.
Kloppenburg
P.
,
Hildebrand
J. G.
(
1995
).
Neuromodulation by 5-hydroxytryptamine in the antennal lobe of the sphinx moth Manduca sexta
.
J. Exp. Biol
198
,
603
–.
Laurent
G.
(
1996
).
Dynamical representation of odors by oscillating and evolving neural assemblies
.
Trends Neurosci
19
,
489
–.
Laurent
G.
,
Davidowitz
H.
(
1994
).
Encoding of olfactory information with oscillating assemblies
.
Science
265
,
1872
–.
Laurent
G.
,
Naraghi
M.
(
1994
).
Odorant-induced oscillations in the mushroom bodies of the locust
.
J. Neurosci
5
,
2993
–.
Laurent
G.
,
Wehr
M.
,
Davidowitz
H.
(
1996
).
Temporal representation of odors in an olfactory network
.
J. Neurosci
16
,
3837
–.
Laurent
G.
,
Wehr
M.
,
MacLeod
K.
,
Stopfer
M.
,
Leitch
B.
,
Davidowitz
H.
(
1996
).
Dynamic encoding of odors with oscillating neuronal assemblies in the locust brain
.
Biol. Bull
191
,
70
–.
Lingren
P. D.
,
Greene
G. L.
,
Davis
D. R.
,
Baumhover
A. H.
,
Henneberry
T. J.
(
1977
).
Nocturnal behavior of four Lepitopteran pests that attack tobacco and other crops
.
Ann. Ent. Soc. Am
70
,
161
–.
Linn
C. E.
,
Roelofs
W. L.
(
1986
).
Modulatory effects of octopamine and serotonin on male sensitivity and periodicity of response to sex pheromone in the cabbage looper moth, Trichoplusia ni
.
Arch. Insect Biochem. Physiol
3
,
161
–.
MacLeod
K.
,
Baecker
A.
,
Laurent
G.
(
1998
).
Who reads temporal information contained across synchronized and oscillatory spike trains?
.
Nature
395
,
693
–.
MacLeod
K.
,
Laurent
G.
(
1996
).
Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies
.
Science
274
,
976
–.
Masson
C.
,
Mustaparta
H.
(
1990
).
Chemical informationprocessing in the olfactory system of insects
.
Physiol. Rev
70
,
199
–.
Matsumoto
S. G.
,
Hildebrand
J. G.
(
1981
).
Olfactory mechanisms in the moth Manduca sexta: response characteristics and morphology of central neurons in the antennal lobes
.
Proc. R. Soc. Lond. B
213
,
249
–.
Menzel
R.
,
Muller
U.
(
1996
).
Learning and memory in honeybees: From behavior to neural substrates
.
Annu. Rev. Neurosci
19
,
379
–.
Mercer
A. R.
,
Erber
J.
(
1983
).
The effects of amines on evoked potentials recorded in the mushroom bodies of the bee brain
.
J. Comp. Physiol
151
,
469
–.
Pichon
Y.
,
Sattelle
D. B.
,
Lane
N. J.
(
1972
).
Conduction processes in the nerve cord of the moth Manduca sexta in relation to its ultrastructure and haemolymph ionic composition
.
J. Exp. Biol
56
,
717
–.
Rospars
J. P.
,
Hildebrand
J. G.
(
1992
).
Anatomical identification of glomeruli in the antennal lobes of the male sphinx moth Manduca sexta
.
Cell Tissue Res
270
,
205
–.
Sigg
D.
,
Thompson
C. M.
,
Mercer
A. R.
(
1997
).
Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera
.
J. Neurosci
17
,
7148
–.
Stopfer
M.
,
Bhagavan
S.
,
Smith
B. H.
,
Laurent
G.
(
1997
).
Impaired odour discrimination on desynchronisation of odour-encoding neuronal assemblies
.
Nature
390
,
70
–.
Stopfer
M.
,
Laurent
G.
(
1999
).
Short-term memory in olfactory network dynamics
.
Nature
402
,
664
–.
Sun
X. J.
,
Tolbert
L. P.
,
Hildebrand
J. G.
(
1993
).
Ramification pattern and ultrastructural characteristic of the serotonin immunoreactive neuron in the antennal lobe of the moth Manduca sexta: A laser scanning confocal and electron microscopic study
.
J. Comp. Neurol
338
,
5
–.
Tumlinson
J. H.
,
Brennan
M. M.
,
Doolittle
R. E.
,
Mitchell
E. R.
,
Brabham
A.
,
Mazomenos
B. E.
,
Baumhover
A. H.
,
Jackson
D. M.
(
1989
).
Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel
.
Arch. Insect Biochem. Physiol
19
,
155
–.
Wehr
M.
,
Laurent
G.
(
1996
).
Temporal combinatorial encoding of odours with oscillations
.
Nature
384
,
162
–.
This content is only available via PDF.