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In their natural environment animals face complex and highly dynamic olfactory input. This requires fast and reliable processing of olfactory information, in vertebrates as well as invertebrates. Parallel processing has been shown to improve processing speed and power in other sensory systems like auditory or visual. In the olfactory system less is known about olfactory coding in general and parallel processing in particular. With its elaborated olfactory system and due to their specialized neuroanatomy, honeybees are well-suited model organism to study parallel olfactory processing. The honeybee possesses a unique neuronal architecture - a dual olfactory pathway. Two mirror-imaged output projection neuron (PN) pathways connect the first olfactory processing stage, the antennal lobe (analog to the vertebrates olfactory bulb, OB), with the second, the mushroom body (MB) known to be involved in orientation and learning and memory, and the lateral horn (LH). The medial antennal lobe-protocerebral tract (m-APT) first innervates the MB and thereafter the LH, while the other, the lateral-APT (l-APT) projects in opposite direction. The neuroanatomy and evolution of these pathways has been analyzed, yet little is known about its physiology. To analyze the function of the dual olfactory pathway a new established recording method was designed and is described in the first chapter of this thesis (multi-unit-recordings). This is now the first time where odor response from several PNs of both tracts is recorded simultaneously and with high temporal precision. In the second chapter the PN odor responses are analyzed. The major findings are: both tracts responded to all tested odors but with differing characteristics. Since recent studies describe the input to the two tracts being rather similar, the results now indicate differential odor processing along the tracts, therefore this is a good indicator for parallel processing. PNs of the m-APT process odors in a sparse manner with delayed response latencies, but with high odor-specificity. PNs of the l-APT in contrast respond to several odor stimuli and respond in general faster. In some PN originating from both tracts, characteristics of odor-identity coding via response latencies were found. Analyzing the over-all dynamic range of the PNs both l- and m-APT PNs were tested over a large odor concentration range (10-6 to 10-2) (3. chapter). The PNs responded with linear and non-linear correlation of the response strength to the odor concentration. In most cases the l-APT is comparatively more sensitive to low odor concentrations. Response latency decreases with increasing odor concentration in both tracts. Alternative coding principles and elaboration on the hypothesis whether the dual olfactory pathway may contribute coincidental innervation to the next higher-order neurons, the Kenyon cells (KC), is subject of the 4. chapter. Cross-correlations and synchronous responses of both tracts show that in principle odors may be coded via temporal coding. Results suggest that odor processing is enhanced if both tracts contribute to olfactory coding together. In another project the distribution of the inhibitory neurotransmitter GABA (gamma-aminobutyric acid) was measured in the bee’s MB during adult maturation (5. chapter). GABAergic inhibition is of high importance in odor coding. An almost threefold decrease in the total amount of GABAergic innervation was found during adult maturation in the l- and m-APT target region, in particular at the change in division of labor during the transition from a young nurse bee to an older forager bee. The results fit well into the current understanding of brain development in the honeybee and other social insects during adult maturation, which was described as presynaptic pruning and KC dendritic outgrowth. Combining anatomical and functional properties of the bee’s dual olfactory pathway suggests that both rate and temporal coding are implemented along two parallel streams. Comparison with recent work on analog output pathways of the vertebrate’s OB indicates that parallel processing of olfactory information may be a common principle across distant taxa.
There is evidence that pheromones are communicative signals in animals. However, the existence and function of human pheromones are still under discussion. During the last years several substances have been labeled as putative human pheromones and especially 4,16–androstadien-3-one (androstadienone), found in male and female sweat, became subject of intense investigation. In contrast to common odors androstadienone presumably modulates human physiological and psychological reactions. Data suggest that androstadienone might influence the processing of visual cues, specifically faces or affective stimuli, via projections from the fusiform gyrus and the amygdala. Moreover, attentional processes may be modulated, which is supported by explicit and implicit behavioral data. This thesis includes three experimental studies examining effects of androstadienone exposure on behavioral and cortical reactions to visual and emotional stimuli. The main hypotheses were that androstadienone might influence human behavior to and perception of visual cues. The first study sought to clarify androstadienone effects on attention-related reactions as well as on behavioral tendencies. Motoric approach-avoidance reactions in response to happy and angry facial expressions were investigated in 30 women and 32 men. Participants either inhaled androstadienone or a control solution, without knowing the real content, while performing the following task: they had to push away or to pull towards them a joystick as fast as possible in reaction to either an angry or a happy cartoon face, which was presented on a computer screen. Results showed that androstadienone modulated the participant´s task performance by accelerating the reaction speed compared to the control compound. Faster reactions were observed particularly when reacting to angry faces but not when reacting to happy faces. This might be explained by the finding that human body odors, the source of androstadienone, were found to activate the human fear system, i.e. modulating fear-related attentional processes. Therefore, the quicker reaction towards angry faces with exposure to androstadienone could be due to an enhanced allocation of attentional resources towards fear-related cues like angry faces. Results also showed that androstadienone enhanced men´s approach tendency towards faces independent of emotional expressions. This observation might be explained by androstadienone´s former shown ability to improve attractiveness ratings of other persons. In this regard, the endogenous odor might enhance evaluations of faces in men and, thus, might improve their willingness to approach social stimuli. In contrast to men, women already showed in the control condition higher approach tendency towards faces. Therefore, androstadienone might rather maintain than enhance the approach score in women. In the second study event-related brain potentials (ERPs) triggered by social and non-social visual stimuli were investigated by means of electroencephalography. In a double-blind between-subjects design 51 women participated. Twenty-eight women inhaled androstadienone, whereas 23 women inhaled a control solution. Four different picture categories, i.e. real faces, pictures with couples, pictures with social and non-social scenes, each including three different valence categories, i.e. positive, negative and neutral, should clarify the stimulus type or context androstadienone is acting on. The androstadienone compared to the control odor did not influence brain responses significantly. Explorative analyses, however, suggested that androstadienone influences the processing of faces. While in the control group angry faces elicited larger P300 amplitudes than happy faces, the androstadienone group showed similar P300 amplitudes concerning all emotional expressions. This observation tentatively indicates that the endogenous odor might indeed affect the neuronal responses to emotional facial stimuli, especially late components reflecting evaluative processes. However, this observation has to be verified and further investigated, in particular whether androstadienone caused reduced responses to angry faces or enhanced responses to happy faces. The third study investigated androstadienone effects on face processing especially in men. ERPs elicited by happy, angry and neutral cartoon faces, which were presented on a computer screen, were measured while 16 men, not knowing the applicated odor, inhaled either androstadienone or a control solution. Exposure to androstadienone significantly increased later neuronal responses, the P300 amplitude. This belated component of the ERP reflects attention allocation and evaluative processes towards important stimuli. Therefore, androstadienone might facilitate central nervous face processing by enhancing attention towards these stimuli. In sum, the current results corroborate the notion of androstadienone as an active social chemosignal. In minute amounts and not detectable as an odor it influenced cortical and motoric reactions. Therefore, it might be concluded that androstadienone indeed affects cognitive functions like attentional processes and in turn affects our behavior. The current results further support the notion that androstadienone acts like a human modulator pheromone, namely modulating ongoing behavior or a psychological reaction to a particular context, changing stimulus sensitivity, salience and sensory-motor integration. However, these conclusions remain tentative until further replication takes place, best in ecologically valid environments. Furthermore, one has to keep in mind that the current studies could not replicate several previous findings and could not verify some hypotheses assuming communicative effects of androstadienone. Thus, the main assumption of this thesis that androstadienone is an active chemosignal is still challenged. Also, whether the term “pheromone” is indeed suitable to label androstadienone remains open.
The behavior of honeybees and bumblebees relies on a constant sensory integration of abiotic or biotic stimuli. As eusocial insects, a sophisticated intraspecific communication as well as the processing of multisensory cues during foraging is of utter importance. To tackle the arising challenges, both honeybees and bumblebees have evolved a sophisticated olfactory and visual processing system.
In both organisms, olfactory reception starts at the antennae, where olfactory sensilla cover the antennal surface in a sex-specific manner. These sensilla house olfactory receptor neurons (ORN) that express olfactory receptors. ORNs send their axons via four tracts to the antennal lobe (AL), the prime olfactory processing center in the bee brain. Here, ORNs specifically innervate spheroidal structures, so-called glomeruli, in which they form synapses with local interneurons and projection neurons (PN). PNs subsequently project the olfactory information via two distinct tracts, the medial and the lateral antennal-lobe tract, to the mushroom body (MB), the main center of sensory integration and memory formation. In the honeybee calyx, the sensory input region of the MB, PNs synapse on Kenyon cells (KC), the principal neuron type of the MB. Olfactory PNs mainly innervate the lip and basal ring layer of the calyx. In addition, the basal ring receives input from visual PNs, making it the first site of integration of visual and olfactory information. Visual PNs, carrying sensory information from the optic lobes, send their terminals not only to the to the basal ring compartment but also to the collar of the calyx. Receiving olfactory or visual input, KCs send their axons along the MB peduncle and terminate in the main output regions of the MB, the medial and the vertical lobe (VL) in a layer-specific manner. In the MB lobes, KCs synapse onto mushroom body output neurons (MBON). In so far barely understood processes, multimodal information is integrated by the MBONs and then relayed further into the protocerebral lobes, the contralateral brain hemisphere, or the central brain among others.
This dissertation comprises a dichotomous structure that (i) aims to gain more insight into the olfactory processing in bumblebees and (ii) sets out to broaden our understanding of visual processing in honeybee MBONs.
The first manuscript examines the olfactory processing of Bombus terrestris and specifically investigates sex-specific differences. We used behavioral (absolute conditioning) and electrophysiological approaches to elaborate the processing of ecologically relevant odors (components of plant odors and pheromones) at three distinct levels, in the periphery, in the AL and during olfactory conditioning. We found both sexes to form robust memories after absolute conditioning and to generalize towards the carbon chain length of the presented odors. On the contrary, electroantennographic (EAG) activity showed distinct stimulus and sex-specific activity, e.g. reduced activity towards citronellol in drones. Interestingly, extracellular multi-unit recordings in the AL confirmed stimulus and sex-specific differences in olfactory processing, but did not reflect the differences previously found in the EAG. Here, farnesol and 2,3-dihydrofarnesol, components of sex-specific pheromones, show a distinct representation, especially in workers, corroborating the results of a previous study. This explicitly different representation suggests that the peripheral stimulus representation is an imperfect indication for neuronal representation in high-order neuropils and ecological importance of a specific odor.
The second manuscript investigates MBONs in honeybees to gain more insights into visual processing in the VL. Honeybee MBONs can be categorized into visually responsive, olfactory responsive and multimodal. To clarify which visual features are represented at this high-order integration center, we used extracellular multi-unit recordings in combination with visual and olfactory stimulation. We show for the first time that information about brightness and wavelength is preserved in the VL. Furthermore, we defined three specific classes of visual MBONs that distinctly encode the intensity, identity or simply the onset of a stimulus. The identity-subgroup exhibits a specific tuning towards UV light. These results support the view of the MB as the center of multimodal integration that categorizes sensory input and subsequently channels this information into specific MBON populations.
Finally, I discuss differences between the peripheral representations of stimuli and their distinct processing in high-order neuropils. The unique activity of farnesol in manuscript 1 or the representation of UV light in manuscript 2 suggest that the peripheral representation of a stimulus is insufficient as a sole indicator for its neural activity in subsequent neuropils or its putative behavioral importance. In addition, I discuss the influence of hard-wired concepts or plasticity induced changes in the sensory pathways on the processing of such key stimuli in the peripheral reception as well as in high-order centers like the AL or the MB. The MB as the center of multisensory integration has been broadly examined for its olfactory processing capabilities and receives increasing interest about its visual coding properties. To further unravel its role of sensory integration and to include neglected modalities, future studies need to combine additional approaches and gain more insights on the multimodal aspects in both the input and output region.
The aim of this project was to investigate whether reflex-like innate facial reactions to tastes and odors are altered in patients with eating disorders. Qualitatively different tastes and odors have been found to elicit specific facial expressions in newborns. This specificity in newborns is characterized by positive facial reactions in response to pleasant stimuli and by negative facial reactions in response to unpleasant stimuli. It is, however, unclear, whether these specific facial displays remain stable during ontogeny (1). Despite the fact that several studies had shown that taste-and odor-elicited facial reactions remain quite stable across a human’s life-span, the specificity of research questions, as well as different research methods, allow only limited comparisons between studies. Moreover, the gustofacial response patterns might be altered in pathological eating behavior (2). To date, however, the question of whether dysfunctional eating behavior might alter facial activity in response to tastes and odors has not been addressed. Furthermore, changes in facial activity might be linked to deficient inhibitory facial control (3). To investigate these three research questions, facial reactions in response to tastes and odors were assessed. Facial reactions were analyzed using the Facial Action Coding System (FACS, Ekman & Friesen, 1978; Ekman, Friesen, & Hager, 2002) and electromyography.