A subset of olfactory projection neurons in the brain of male Manduca sexta is described, and their role in sex pheromone information processing is examined. These neurons have extensive arborizations in the macroglomerular complex (MGC), a distinctive and sexually dimorphic area of neuropil in the antennal lobe (AL), to which the axons of two known classes of antennal pheromone receptors project. Each projection neuron sends an axon from the AL into the protocerebrum. Forty-one projection neurons were characterized according to their responses to electrical stimulation of the antennal nerve as well as olfactory stimulation of antennal receptors. All neurons exhibited strong selectivity for female sex pheromones. Other behaviorally relevant odors, such as plant volatiles, had no obvious effect on the activity of these neurons. Two broad physiological categories were found: cells that were excited by stimulation of the ipsilateral antenna with pheromones (29 out of 41), and cells that received a mixed input (inhibition and excitation) from pheromone pathways (12 out of 41). Of the cells in the first category, 13 out of 29 were equally excited in response to stimulation of the antenna with either the principal natural pheromone (bombykal) or a mimic of a second unidentified pheromone ('C-15') and were similarly excited by the natural pheromone blend. The remaining 16 out of 29 cells responded selectively, and in some cases, in a dose-dependent manner, to stimulation of the antenna with bombykal or C-15, but not both. Some of these neurons had dendritic arborizations restricted to only a portion of the MGC neuropil, whereas most had arborizations throughout the MGC. Of the cells in the second category, 9 out of 12 were excited by bombykal, inhibited by C-15, and showed a mixed response to the natural pheromone blend. For the other 3 out of 12 cells, the response polarity was reversed for the two chemically-identified odors. Two additional neurons, which were not tested with olfactory stimuli, were tonically inhibited in response to electrical stimulation of the ipsilateral antennal nerve. These observations suggest that some of the male-specific projection neurons may signal general pheromone-triggered arousal, whereas a smaller number can actively integrate inputs from the two know receptor classes (Bal- and C-15-selective) and may operate as 'mixture detectors' at this level of the olfactory subsystem that processes information about sex pheromones.
Intracellular recordings were made from the major neurites of local interneurons in the moth antennal lobe. Antennal nerve stimulation evoked 3 patterns of postsynaptic activity: (i) a short-latency compound excitatory postsynaptic potential that, based on electrical stimulation of the antennal nerve and stimulation of the antenna with odors, represents a monosynaptic input from olfactory afferent axons (71 out of 86 neurons), (ii) a delayed activation of firing in response to both electrical- and odor-driven input (11 neurons), and (iii) a delayed membrane hyperpolarization in response to antennal nerve input (4 neurons). Simultaneous intracellular recordings from a local interneuron with short-latency responses and a projection (output) neuron revealed unidirectional synaptic interactions between these two cell types. In 20% of the 30 pairs studied, spontaneous and current-induced spiking activity in a local interneuron correlated with hyperpolarization and suppression of firing in a projection neuron. No evidence for recurrent or feedback inhibition of projection neurons was found. Furthermore, suppression of firing in an inhibitory local interneuron led to an increase in firing in the normally quiescent projection neuron, suggesting that a disinhibitory pathway may mediate excitation in projection neurons. This is the first direct evidence of an inhibitory role for local interneurons in olfactory information processing in insects. Through different types of multisynaptic interactions with projection neurons, local interneurons help to generate and shape the output from olfactory glomeruli in the antennal lobe.
The neural computations used to represent olfactory information in the brain have long been investigated. Recent studies in the insect antennal lobe suggest that precise temporal and/or spatial patterns of activity underlie the recognition and discrimination of different odours, and that these patterns may be strengthened by associative learning. It remains unknown, however, whether these activity patterns persist when odour intensity varies rapidly and unpredictably, as often occurs in nature. Here we show that with naturally intermittent odour stimulation, spike patterns recorded from moth antennal-lobe output neurons varied predictably with the fine-scale temporal dynamics and intensity of the odour. These data support the hypothesis that olfactory circuits compensate for contextual variations in the stimulus pattern with high temporal precision. The timing of output neuron activity is constantly modulated to reflect ongoing changes in stimulus intensity and dynamics that occur on a millisecond timescale.
The deutocerebrum is usually regarded as a preoral neuromere subserving an antennal head segment (81). Most authors agree that it consists of two distinct neuropils (Figure 1): the antennal lobe (AL) and the antennal mechanosensory and motor center (AMMC), also called the dorsal lobe (l0, 17, 35, 39). We adhere to this classical definition, but it should be noted that a different, extended definition of the deutocerebrum has recently been suggested by Strausfeld and coworkers (105, 106). Both areas of the deutocerebrum receive primary sensory fibers from receptor cells in the antenna. Most and possibly all axons of olfactory receptor I Abbreviations: AC, anterior cell group of antennal lobe; AL, antennallobe; aL, a•lobe of the mushroom body; AMMC, antennal mechanosensory and motor center; bL, 13-lobe of the mushroom body; Ca, calyces of the mushroom body; CF, centrifugal neuron; OACT, dorsal antenno-cerebral tract; OMACT, dorso-medial antenno-cerebral tract; IACT, inner antenno cerebral tract; ILP, inferior lateral protocerebrum; IMP, inferior medial protocerebrum; LC, lateral cell group of antennal lobe; LCI, large dorsal cell cluster of the lateral cell group; LCn, postero-ventral cell cluster of the lateral cell group; LH, lateral horn; LN, local neuron; LPO, labial-palp pit organ; MACT, middle antenno-cerebral tract; MC, medial cell group of antennal lobe; MGC, macroglomerular complex; OACT, outer antenno-cerebral tract; P, pe dunculus; PO, projection neuron in dorsal antenno-cerebral tract; POM, projection neuron in dorso-medial antenno-cerebral tract; PIa,b,c, projection neuron in inner antenno-cerebral tract, types a,b,c; PM, projection neuron in middle antenno-cerebral tract; POa,b,c,d, projection neuron in outer antenno-cerebral tract, types a,b,c,d; SOG, suboesophageal ganglion; SB, sen silla basiconica; ST, sensilla trichodea. 477 0066-4170/8910101-0477$02.00 'Dendritic tree often has small side branches toward secondary glomeruli. hUniglomerular if dendritic tree is in MGC. 'Neurons innervate one glomerulus in both antennal lobes.
Summary For animals to execute odor-driven behaviors, the olfactory system must process complex odor signals and maintain stimulus identity in the face of constantly changing odor intensities [1–5]. Surprisingly, how the olfactory system maintains identity of complex odors is unclear [6–10]. We took advantage of the plant-pollinator relationship between the Sacred Datura (Datura wrightii) and the moth Manduca sexta [11, 12] to determine how olfactory networks in this insect’s brain represent odor mixtures. We combined gas chromatography and neural-ensemble recording in the moth’s antennal lobe to examine population codes for the floral mixture and its fractionated components. Although the floral scent of D. wrightii comprises at least 60 compounds, only nine of those elicited robust neural responses. Behavioral experiments confirmed that these nine odorants mediate flower-foraging behaviors, but only as a mixture. Moreover, the mixture evoked equivalent foraging behaviors over a 1000-fold range in dilution, suggesting a singular percept across this concentration range. Furthermore, neural-ensemble recordings in the moth’s antennal lobe revealed that reliable encoding of the floral mixture is organized through synchronized activity distributed across a population of glomerular coding units, and this timing mechanism may bind the features of a complex stimulus into a coherent odor percept.
We have prepared and characterized specific rabbit antisera against gamma-aminobutyric acid (GABA) coupled covalently to bovine serum albumin and keyhole-limpet hemocyanin. Using these antisera in immunocytochemical staining procedures, we have probed the antennal lobes and their afferent and efferent fiber tracts in the sphinx moth Manduca sexta for GABA-like immunoreactivity in order to map putatively GABAergic central neurons in the central antennal-sensory pathway. About 30% of the neuronal somata in the large lateral group of cell bodies in the antennal lobe are GABA-immunoreactive; cells in the medial and anterior groups of antennal-lobe cells did not exhibit GABA-like immunoreactivity. GABA-immunoreactive neurites had arborizations in all of the glomeruli in the antennal lobe. Double-labeling experiments involving tandem intracellular staining with Lucifer Yellow and immunocytochemical staining for GABA-like immunoreactivity demonstrated that at least some of the GABA-immunoreactive cells in the antennal lobe are amacrine local interneurons. Several fiber tracts that carry axons of antennal-lobe projection neurons exhibited GABA-immunoreactive fibers. Among the possibly GABA-containing projection neurons are several cells, with somata in the lateral group of the antennal lobe, that send their axons directly to the lateral protocerebrum.
Each antennal lobe in the brain of a male moth has a distinctive neuropil structure, the macroglomerular complex (MGC), which is specialized for primary processing of information about the conspecific female sex-pheromone blend. Olfactory interneurons with dendritic arborizations in the MGC were examined by means of tandem intracellular recording and staining with Lucifer Yellow. Neurons that responded selectively to stimulation of the antenna with the major pheromone component, (E,Z)-10,12-hexadecadienal, had arborizations that were restricted to a toroidal subdivision (the "toroid") of the MGC. Similarly, neurons that responded selectively to antennal stimulation with (E,Z)-11,13-pentadecadienal, a more stable mimic of a second essential but chemically unstable pheromone component, (E,E,Z)-10,12,14-hexadecatrienal, had arborizations confined to a globular subdivision (the "cumulus") of the MGC situated more proximally to the antennal nerve input. One neuron that responded to both of these stimuli clearly had arborizations in both subdivisions of the MGC. These anatomically distinct subdivisions of the MGC thus appear also to be functionally separate regions of pheromone-processing neuropil.
Serotonin (5-hydroxytryptamine; 5HT) functions in insects as a neurotransmitter, neuromodulator, and neurohormone. In the sphinx moth Manduca sexta, each of the paired antennal lobes (ALs; the primary olfactory centers in the insect brain) has one 5HT-immunoreactive (5HT-ir) neuron that projects into the protocerebrum, crosses the posterior midline, and innervates the contralateral AL; this is referred to as the contralaterally projecting, serotonin-immunoreactive deutocerebral (CSD) neuron. These neurons are thought to function as centrifugal modulators of olfactory sensitivity. To examine the phylogenetic distribution of 5HT-ir neurons apparently homologous to the CSD neuron, we imaged 5HT-like immunoreactivity in the brains of 40 species of insects belonging to 38 families in nine orders. CSD neurons were found in other Lepidoptera, Trichoptera, Diptera, Coleoptera, and Neuroptera but not in the Hymenoptera. In the paraneopteran and polyneopteran species (insects that undergo incomplete metamorphosis) examined, AL 5HT neurons innervate the ispsilateral AL and project to the protocerebrum. Our findings suggest that the characteristic morphology of the CSD neurons originated in the holometabolous insects (those that undergo complete metamorphosis) and were lost in the Hymenoptera. In a subset of the Diptera, the CSD neurons branch within the contralateral AL and project back to the ipsilateral AL via the antennal commissure. The evolution of AL 5HT neurons is discussed in the context of the physiological actions of 5HT observed in the lepidopteran AL.
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