Neural Basis of a Pollinator’s Buffet: Olfactory Specialization and Learning in Manduca sexta

Abstract

Pollinators exhibit a range of innate and learned behaviors that mediate interactions with flowers, but the olfactory bases of these responses in a naturalistic context remain poorly understood. The hawkmoth Manduca sexta is an important pollinator for many night-blooming flowers but can learn--through olfactory conditioning--to visit other nectar resources. Analysis of the flowers that are innately attractive to moths shows that the scents all have converged on a similar chemical profile that, in turn, is uniquely represented in the moth's antennal (olfactory) lobe. Flexibility in visitation to nonattractive flowers, however, is mediated by octopamine-associated modulation of antennal-lobe neurons during learning. Furthermore, this flexibility does not extinguish the innate preferences. Such processing of stimuli through two olfactory channels, one involving an innate bias and the other a learned association, allows the moths to exist within a dynamic floral environment while maintaining specialized associations.

Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus)

“…In Petunia axillaris, genetic manipulation of the production of methyl benzoate influenced both floral attraction and visit order by pollinating hawkmoths (Klahre et al, 2011), despite the presence of multiple other compounds in the floral bouquet, including an equal emission amount of benzaldehyde (Hoballah et al, 2005). Methyl benzoate and other oxygenated aromatic volatiles, like phenylacetaldehyde and benzyl alcohol, strongly activate moth antennal receptor neurons and AL projection neurons (Shields and Hildebrand, 2001;Riffell et al, 2013), thus providing a direct link between the composition of the floral bouquet and sensory processing and behavior. As a mediator of pollinator attraction, floral scent can play a key role in the origin and maintenance of reproductive isolation between sister taxa of flowering plants, which are often separated primarily (or solely) by pollinator-based prezygotic reproductive isolation (Grant, 1949;Coyne and Orr, 2004).…”

“…For each volatile compound and mixture tested, we placed each unit into one of three different categories depending on mixture responses: equal to (Z-score within ±2.0 of the response), lower ('suppression'; Z-score ≤2.0 of the response) or higher ('synergy'; Z-score ≥2.0 of the response) than the individual volatile that produces the greatest response. Finally, representation of the single volatile and mixtures was examined at the level of the neural population through multivariate analysis and calculation of the Euclidian distances between olfactory stimuli (Riffell et al, 2009b;Riffell et al, 2013).…”

“…Extracellular activity was acquired with a RZ2 base station (Tucker-Davis Technologies) and a RP2.1 real-time processor (Tucker-Davis Technologies), and extracellular activity in the form of action potentials, or spikes, was extracted from the recorded signals and digitized at 25 kHz using Tucker-Davis Technologies data-acquisition software (Byers et al, 2013;Riffell et al, 2013). Threshold and gain settings were adjusted independently for each channel, and spikes were captured in the 4-channel, or 'tetrode', recording configuration: any spike that passed threshold on one channel triggered the capture of spikes recorded on the other three channels on the same shank.…”

Learning about natural variation of odor mixtures enhances categorization in early olfactory processing

“…The blends contain the same components, thus the varieties cannot be easily differentiated simply by the presence or absence of components. The first step was to evaluate whether the AL responds to each of the components, or whether the response to a mixture of all six might be dominated by a subset of components (Riffell et al, 2013). We used calcium imaging of projection neurons to evaluate the activation patterns of the AL by each pure component and a sixcomponent mixture.…”

Simultaneous Long-term Recordings at Two Neuronal Processing Stages in Behaving Honeybees

“…Compared to silicon probes commonly used for extracellular recordings in much larger insects like the hawk moth, locust and cockroach 40,[49][50][51] the described micro wire-electrodes are smaller, flexible and can cope easily with potential brain movements and, thus, can be reliably used in small social insects like bees and ants that show a much broader behavioral repertoire. Most silicone probes have sharp shank like structures cutting axons and neural tissue along their insertion channel, while the described micro wires are round, flexible and smaller and are hence less harmful to the surrounding tissue which is a clear advantage if the goal is to study long-term plasticity in an intact and behaving animal.…”