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Perception of aversive stimuli of different gustatory modalities in an haematophagous insect, Rhodnius prolixus

23 Apr 2019-bioRxiv (Cold Spring Harbor Laboratory)-pp 616615
TL;DR: Kissing-bugs use contact chemo-perception to avoid aversive substrates and can sensory distinguish between salty and bitter tastes, but not between different salts (sodium and potassium chloride).
Abstract: Sensory aversion is an essential link for avoiding potential dangers. Here, we studied the chemical perception of aversive compounds of different gustatory modalities (salty and bitter) in the haematophagous kissing bug, Rhodnius prolixus. Over a walking arena, insects preferred a substrate embedded with 0.3 M NaCl or KCl rather than with distilled water. Same salts were avoided when prepared at 1 M. When NaCl and KCl were confronted, no preferences were evinced by insects. A pre-exposure to amiloride interfered with the repellency of NaCl and KCl equally, suggesting that amiloride-sensitive receptors are involved in the detection of both salts. Discriminative experiments were then performed to determine if R. prolixus can distinguish between these salts. An aversive operant conditioning involving either NaCl or KCl modulated the repellency of the conditioned salt, but also of the novel salt. A chemical pre-exposure to the salts did not to modify their repellency levels. When we crossed gustatory modalities by confronting NaCl to caffeine (i.e. a bitter stimulus) no innate preferences were evinced. Aversive operant conditionings with either NaCl or Caf rendered unspecific changes in the repellency of both compounds. A chemical pre-exposure to Caf modulated the response to Caf but not to NaCl, suggesting the existence of two independent neural pathways for the detection of salts and bitter compounds. Overall results suggest that R. prolixus cannot distinguish between NaCl and KCl but can distinguish between NaCl and Caf and generalizes the response between these two aversive stimuli of different gustatory modality. Summary statement Kissing-bugs use contact chemo-perception to avoid aversive substrates. They can sensory distinguish between salty (sodium chloride) and bitter (caffeine) tastes, but not between different salts (sodium and potassium chloride).

Summary (2 min read)

1. Introduction

  • Different experimental approaches were applied to analyse the discriminatory capacities of R. prolixus.
  • Along this work the authors assume that if a particular treatment modulates the response to one stimulus but not to the other, insects are capable of discriminating among them.

2.1. Insects

  • Being nocturnal insects, all experiments were carried out during the first hours of the insects' scotophase (i.e. 1 -6 h. after lights were turned-off) in a dark experimental room.
  • This spatio-temporal arrangement allowed us to exclude external visual cues during experiments and at the same time match the maximal activity period described for triatomines (Lazzari, 1992) .

2.3. Taste preference assay: two-choice walking arena

  • Thirty replicates were performed for each experimental series.
  • Insects were used once and then discarded.
  • In each experimental series, the stimulus was assigned to the "left" or "right" side of the arena in a pseudorandom manner.
  • Discriminative experiments were performed to discern if insects can distinguish between different aversive stimuli.
  • Different pre-treatments were applied before the taste preference assays.

2.4.1. Pre-exposure to amiloride

  • One insect was gently placed over the paper inside the vial and left to freely walk during 1 minute.
  • During this time, legs, antennae, proboscis and/or other parts of the body could contact the H2O or the amiloride.
  • The insect was then removed, maintained in a different clean flask for 2 minutes and then transferred to the two-choice arena where its chemical preference was tested as explain in section 2.3.

2.4.3. Compound-specific chemical pre-exposure

  • The copyright holder for this preprint (which was not this version posted April 23, 2019.
  • Once the pre-exposure ended, the insect was removed, put in an individual flask for 2 minutes, and then its chemical preference was tested as explained in section 2.3.

2.5. Data and analyses

  • Thirty insects were tested in each experimental series.
  • The mean PI of each series was statistically compared against the expected value if there were no chemical preferences, i.e. "0" by applying One-Sample T-Tests (α = 0.05).
  • Normality and homoscedasticity were verified in all data series.
  • All figures represent the mean Preference Index (x-axis) and the chemical compounds presented at each side of the arena (y-axis).
  • Asterisks denote statistical differences between the PI and the value 0 (p < 0.05).

3.1. Salt perception: concentration-dependent behaviour

  • The copyright holder for this preprint (which was not this version posted April 23, 2019.
  • These results show that R. prolixus can detect the presence of both salts over the walking substrate, and that the concentration perceived determines the type of response evinced by these bugs.
  • In fact, concentrations close to those found over the skin of a potential host (i.e. around 0.1 M) were preferred, while higher ones, which could probably alter negatively the internal homeostasis of the insect, were repellent.
  • Experiments presented here onwards were carried out using the aversive concentration of NaCl and KCl, i.e. 1 M.

3.2.3. Aversive conditioning with salts

  • These results clearly show that R. prolixus can modify their chemical preferences after an aversive operant conditioning, i.e. they can learn to avoid punished stimuli.
  • Results evince that the observed experience-dependent plasticity is not compound specific, for what the authors still cannot discern if R. prolixus is not capable of distinguishing between these two salts, or if they can distinguish, they can learn, but they generalize between salts (i.e. distinguishing peripherally between them but transferring what they have learnt for one stimulus to the other).

3.3.1. Innate responses to Caffeine

  • These results evince that R. prolixus can sense the presence of caffeine on the walking substrate, and that this perception generates an avoidance, which is similar in intensity to that exerted by NaCl.
  • The question arises again about the capacity of R. prolixus to distinguish between these two aversive certified by peer review) is the author/funder.
  • Compounds of radically different chemical identity, i.e. a salt and an alkaloid.
  • Next experimental series involving associative and non-associative discriminatory learning protocols were designed to answer this question.

3.3.3. Chemical pre-exposure to salts and alkaloids

  • These results, in which the effect of a pre-exposure to Caf is compoundspecific, demonstrate that R. prolixus can distinguish between the salt NaCl and the alkaloid Caf, and suggest the existence of two different sensory pathways involved in the detection of aversive compounds of different gustatory modality.
  • Additionally, the authors can validate their method to analyse the taste discrimination in R. prolixus, enforcing the evidences presented before in which they suggest that NaCl and KCl are not distinguished by these insects.

4. Discussion

  • The copyright holder for this preprint (which was not this version posted April 23, 2019.
  • Additionally, it was shown that triatomines' cognitive abilities follow a circadian rhythm, performing well during the night, but not during the day (Vinauger and Lazzari, 2015) .
  • As well, studying the repellent effect of new non-toxic molecules for R. prolixus, Asparch and collaborators (2016) found that bugs are innately repelled by different bitter molecules, and that this repellence can be modulated by associative and non-associative forms of learning.
  • Indeed, after an aversive operant conditioning, the behaviour of R. prolixus changed from avoidance to indifference or even to preference, according with the protocol applied (Asparch et al., 2016) .
  • Moreover, taking in consideration that R. prolixus is an insect-vector of a human disease and that its genome has been recently sequenced (Mezquita et al., 2015) , it can become a promising model in the learning and memory field.

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Abstract: BACKGROUND It is widely believed that the human sense of smell is inferior to that of other mammals, especially rodents and dogs. This Review traces the scientific history of this idea to 19th-century neuroanatomist Paul Broca. He classified humans as “nonsmellers” not owing to any sensory testing but because he believed that the evolutionary enlargement of the human frontal lobe gave human beings free will at the expense of the olfactory system. He especially emphasized the small size of the human brain’s olfactory bulb relative to the size of the brain overall, and noted that other mammals have olfactory bulbs that are proportionately much larger. Broca’s claim that humans have an impoverished olfactory system (later labeled “microsmaty,” or tiny smell) influenced Sigmund Freud, who argued that olfactory atrophy rendered humans susceptible to mental illness. Humans’ supposed microsmaty led to the scientific neglect of the human olfactory system for much of the 20th century, and even today many biologists, anthropologists, and psychologists persist in the erroneous belief that humans have a poor sense of smell. Genetic and neurobiological data that reveal features unique to the human olfactory system are regularly misinterpreted to underlie the putative microsmaty, and the impact of human olfactory dysfunction is underappreciated in medical practice. ADVANCES Although the human olfactory system has turned out to have some biological differences from that of other mammalian species, it is generally similar in its neurobiology and sensory capabilities. The human olfactory system has fewer functional olfactory receptor genes than rodents, for instance, but the human brain has more complex olfactory bulbs and orbitofrontal cortices with which to interpret information from the roughly 400 receptor types that are expressed. The olfactory bulb is proportionately smaller in humans than in rodents, but is comparable in the number of neurons it contains and is actually much larger in absolute terms. Thus, although the rest of the brain became larger as humans evolved, the olfactory bulb did not become smaller. When olfactory performance is compared experimentally between humans and other animals, a key insight has been that the results are strongly influenced by the selection of odors tested, presumably because different odor receptors are expressed in each species. When an appropriate range of odors is tested, humans outperform laboratory rodents and dogs in detecting some odors while being less sensitive to other odors. Like other mammals, humans can distinguish among an incredible number of odors and can even follow outdoor scent trails. Human behaviors and affective states are also strongly influenced by the olfactory environment, which can evoke strong emotional and behavioral reactions as well as prompting distinct memories. Odor-mediated communication between individuals, once thought to be limited to “lower animals,” is now understood to carry information about familial relationships, stress and anxiety levels, and reproductive status in humans as well, although this information is not always consciously accessible. OUTLOOK The human olfactory system is increasingly understood to be highly dynamic. Olfactory sensitivity and discrimination abilities can be changed by experiences like environmental odor exposure or even just learning to associate odors with other stimuli in the laboratory. The neurobiological underpinnings of this plasticity, including “bottom-up” factors like regulation of peripheral odor receptors and “top-down” factors like the sensory consequences of emotional and cognitive states, are just beginning to be understood. The role of olfactory communication in shaping social interactions is also actively being explored, including the social spread of emotion through olfactory cues. Finally, impaired olfaction can be a leading indicator of certain neurodegenerative diseases, notably Parkinson’s disease and Alzheimer’s disease. New experimentation will be required to understand how olfactory sequelae might also reflect problems elsewhere in the nervous system, including mental disorders with sensory symptomatology. The idea that human smell is impoverished compared to other mammals is a 19th-century myth.

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Journal ArticleDOI
Rafael D. Mesquita1, Raquel J. Vionette-Amaral1, Carl Lowenberger2, Rolando Rivera-Pomar3, Fernando A. Monteiro1, Fernando A. Monteiro4, Patrick Minx5, John Spieth5, A. Bernardo Carvalho1, Francisco Panzera6, Daniel Lawson7, André Q. Torres1, André Q. Torres4, José M. C. Ribeiro8, Marcos Henrique Ferreira Sorgine1, Robert M. Waterhouse, Michael J. Montague5, Fernando Abad-Franch4, Michele Alves-Bezerra1, Laurence Rodrigues do Amaral9, Helena Araujo1, Ricardo Nascimento Araújo1, Ricardo Nascimento Araújo10, L. Aravind8, Georgia C. Atella1, Patrícia Azambuja4, Patrícia Azambuja1, Mateus Berni1, Paula R. Bittencourt-Cunha1, Glória R.C. Braz1, Gustavo M. Calderón-Fernández3, Claudia M. A. Carareto11, Mikkel B. Christensen7, Igor Rodrigues da Costa1, Samara G. da Costa4, Marilvia Dansa12, Carlos R. O. Daumas-Filho1, Iron F. De-Paula1, Felipe A. Dias1, George Dimopoulos13, Scott J. Emrich14, Natalia Esponda-Behrens3, Patrícia Fampa15, Rita D. Fernandez-Medina4, Rodrigo Nunes da Fonseca1, Marcio Fontenele1, Catrina Fronick5, Lucinda Fulton5, Ana Caroline P. Gandara1, Eloi S. Garcia4, Eloi S. Garcia1, Fernando A. Genta1, Fernando A. Genta4, Gloria I. Giraldo-Calderón14, Bruno Gomes4, Bruno Gomes1, Katia C. Gondim1, Adriana Granzotto11, Alessandra A. Guarneri4, Alessandra A. Guarneri1, Roderic Guigó16, Myriam Harry17, Daniel S.T. Hughes7, Willy Jablonka1, Emmanuelle Jacquin-Joly, M. Patricia Juárez3, Leonardo Koerich1, Angela B. Lange18, Jose Manuel Latorre-Estivalis4, Jose Manuel Latorre-Estivalis1, Andrés Lavore3, Gena G. Lawrence18, Gena G. Lawrence19, Cristiano Lazoski1, Claudio R. Lazzari17, Raphael R.S. Lopes1, Marcelo G. Lorenzo4, Marcelo G. Lorenzo1, Magda D. Lugon12, David Majerowicz1, Paula L. Marcet19, Marco Mariotti16, Hatisaburo Masuda1, Karyn Megy7, Ana C.A. Melo1, Fanis Missirlis20, Theo Mota10, Fernando G. Noriega21, Marcela Nouzova21, Rodrigo Dutra Nunes1, Raquel L.L. Oliveira1, Gilbert Oliveira-Silveira1, Sheila Ons3, Ian Orchard18, Lucia Pagola3, Gabriela O. Paiva-Silva1, Agustina Pascual3, Márcio G. Pavan4, Nicolás Pedrini3, Alexandre A. Peixoto4, Alexandre A. Peixoto1, Marcos H. Pereira1, Marcos H. Pereira10, Andrew Pike13, Carla Polycarpo1, Francisco Prosdocimi1, Rodrigo Ribeiro-Rodrigues22, Hugh M. Robertson23, Ana Paula Salerno, Didier Salmon1, Didac Santesmasses16, Renata Schama4, Renata Schama1, Eloy S. Seabra-Junior, Lívia Silva-Cardoso1, Mário A.C. Silva-Neto1, Matheus Souza-Gomes9, Marcos Sterkel1, Mabel L. Taracena1, Marta Tojo24, Zhijian Jake Tu25, Jose M. C. Tubio26, Raul Ursic-Bedoya2, Thiago M. Venancio12, Thiago M. Venancio1, Ana Beatriz Walter-Nuno1, Derek Wilson7, Wesley C. Warren5, Richard K. Wilson5, Erwin Huebner27, Ellen M. Dotson19, Pedro L. Oliveira1 
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Frequently Asked Questions (1)
Q1. What are the contributions in "Perception of aversive stimuli of different gustatory modalities in an haematophagous insect, rhodnius prolixus" ?

Minoli et al. this paper investigated Gustatory aversiveness perception in kissing-bugs and found that kissing bugs are more likely to experience Gustatory anversiveness than other bugs.