Editorial: Coding properties in invertebrate sensory system

Anton, Sylvia

Garm, Anders

Hedwig, Berthold G

Frontiers in Physiology

PubMed

Anders Garm

Berthold G. Hedwig

Sylvia Anton

Frontiers - Publisher Connector

EDITORIAL
published: 10 January 2017
doi: 10.3389/fphys.2016.00688
Frontiers in Physiology | www.frontiersin.org 1 January 2017 | Volume 7 | Article 688
Edited by:
Xanthe Vafopoulou,
York University, Canada
Reviewed by:
Wolfgang Rössler,
University of Würzburg, Germany
Andrew Dacks,
West Virginia University, USA
*Correspondence:
Sylvia Anton
sylvia.anton@inra.fr
Specialty section:
This article was submitted to
Invertebrate Physiology,
a section of the journal
Frontiers in Physiology
Received: 01 December 2016
Accepted: 23 December 2016
Published: 10 January 2017
Citation:
Garm A, Hedwig BG and Anton S
(2017) Editorial: Coding Properties in
Invertebrate Sensory Systems.
Front. Physiol. 7:688.
doi: 10.3389/fphys.2016.00688
Editorial: Coding Properties in
Invertebrate Sensory Systems
Anders Garm 1, Berthold G. Hedwig 2 and Sylvia Anton 3*
1Marine Biological Section, Department of Biology, University of Copenhagen, Copenhagen, Denmark, 2Department of
Zoology, University of Cambridge, Cambridge, UK, 3Neuroéthologie-RCIM, Institut National de la Recherche
Agronomique-Université d’Angers, Beaucouzé, France
Keywords: sensory signal extraction, temporal coding, neuro-ethology, olfaction, vision, mechanoreception, heat
detection
Editorial on the Research Topic
Coding Properties in Invertebrate Sensory Systems
Animals adapt their behavior according to the environment and their specific needs in a given
situation. In order to do so in an appropriate way, they need to detect, analyze, and code the relevant
sensory cues. This task is handled by sensory systems and their associated parts in the central
nervous system. With few exceptions, the amount of information present in the environment and
thus in principle available to sensory systems, is close to infinite. It is impossible and not desirable
to encode and process all the information. Therefore, the first and most important task of any
sensory system is to filter and select only the essential information—information, which potentially
will improve the fitness of the bearer. Differences in sensory information processing occur between
animals of different organization levels. Sensory coding in invertebrates and vertebrates relies on
multiple stages of processing to extract information relevant to the survival of the individual. The
wide range of organizational complexity, in combination with their relatively simple and accessible
nervous systems, makes invertebrates excellent models to study general sensory coding principles.
In addition, many invertebrate species are of socio-economic importance as pollinators, crop
pests, or as disease vectors or elicitors. Therefore, understanding their communication systems
and sensory biology is important for the development of insect management or plant protection
strategies.
In the present Research Topic in Frontiers in Invertebrate Physiology we present a series
of original papers and reviews illustrating the current directions of this field. The different
contributions indicate not only common features of sensory coding across invertebrate phyla,
but also similar processing features of complex stimuli between different sensory modalities. This
is interesting, because the characteristics of the different types of sensory stimuli are inherently
different, and require different types of detectors and potentially different ways of integration in
nervous systems. The majority of the papers treat the coding of olfactory information with its
multidimensionality, which was supposed to function under different operational constraints than
other sensory modalities, and has been a field of high research activity over the past years. However,
the articles of this Research Topic show that the extraction of behaviourally relevant signals from
all incoming environmental stimuli, as well as the detection of low intensity signals and the analysis
of temporal features can be similar across different sensory modalities, including olfaction, vision,
mechanosensation, and heat perception.
The papers treating the coding of olfactory information include work on temporal processing
and signal extraction in complex environments, and its behavioral outcomes as a function of
physiological state, as well as potential applications of the findings to control harmful insects.
Garm et al. Sensory Coding in Invertebrates
One of the major challenges for olfactory systems is to extract
behaviourally relevant information from highly complex and
dynamic signals. Hellwig and Tichy propose in a perspective
article that olfactory receptor neurons in cockroaches, which
signal sudden changes in the concentration of olfactory stimuli
as compared to a constant background stimulation, might be
used for tracking behaviourally relevant odor plumes. The
fact that OFF neurons code better for falling concentration
changes than ON neurons suggests, that they play a role in
alerting a loss of an odor plume. The paper by Brill et al.
shows that parallel processing of olfactory information via two
antennal lobe output tracts in the honey bee comprises coincident
activation patterns of projection neurons within and across
parallel tracts. The results from simultaneous recordings of
olfactory projection neurons in both tracts support the role of
spike timing in coding olfactory information (temporal code).
Another physiological property of the insect antennal lobe,
which is potentially important in temporal coding of insect
olfaction, is the afterhyperpolarization-phase of the projection
neurons. Lei et al. show in their paper, through pharmacological
experiments and modeling, some of the control mechanisms of
the afterhyperpolarization phase, and confirm the involvement
in temporally resetting the system for further odor-specific
responses.
Another challenge for olfactory systems is the extraction
of a highly relevant signal from an odor background, such
as detection of moth sex pheromones in a rich background
of plant volatiles. Whereas the common belief was that sex
pheromone and plant odors are processed and encoded by
two distinct pathways in the insect brain, Rouyar et al.
show for the first time that a structurally dissimilar plant-
derived odorant is able to activate the pheromone specific
pathway and thus might influence pheromone processing.
Badeke et al. demonstrate, however, that even though high
concentrations of single plant odors can influence female
tracking in the male noctuid moth Heliothis virescens, sex
pheromone-guided behavior is not influenced by plant odors at
natural concentrations.
Sensory processing and integration of different stimuli in
higher brain centers ultimately leads to adequate motor output.
The review by Namiki and Kanzaki addresses the function of the
lateral accessory lobe in the insect brain, which is at the interface
between multimodal sensory input and locomotor output. This
brain area is believed to be an important output region of the
brain for the control of locomotion. In a comparative approach,
structure and function of lateral accessory lobe neurons in
different insect species are discussed.
Because olfaction is widely used by many insect species, it
has become also an important model for sensory ecology and
is exploited to develop alternative methods to control harmful
insects. Reisenman and Riffell review the neurobiology of host
plant selection in the moth Manduca sexta in an ecological
context. Reisenman et al. evaluate how results from the field of
neuroethology can be used to elucidate how harmful insects, be
it crop pests or insects transmitting diseases, trace the odors of
their host plants or animal hosts. They summarize the current
knowledge on the use of semiochemicals, and how results
from applied studies improve our knowledge on detection and
processing of olfactory signals.
The tracking of host plants sometimes changes between
different life stages, and Wu et al. show that one of the odorant
binding proteins (OBPs), binding to attractant semiochemicals, is
upregulated in mated females of a pest fruit fly. This upregulation
possibly accounts for an increased attraction to their host plant.
The role of OBPs in chemosensory detection and coding is
also addressed by Sun et al. Although OBPs are often found
to be necessary for odor discrimination, the authors show that
the function of homologous OBPs in bugs can change between
species to binding of non-volatiles in the gustatory system.
The visual system basically counts the number of photons
from a certain direction during a defined time period,
and potentially also measures their energy (color) and their
polarity. The challenges here are to extract behaviourally
relevant information under limiting environmental conditions.
Two papers of this Research Topic deal with coding in the
visual system under low light conditions. Two strategies to
enhance vision in darkness are through temporal and/or spatial
summation of the photons, which will increase sensitivity on the
cost of temporal and spatial resolution, respectively. Nocturnal
bees enhance sensitivity through optical specializations but not
through temporal summation, which would probably hamper
their flight control at night (Baird et al.). Garm et al. examine
vision in a nocturnal box jellyfish, which enhances sensitivity by
having both a low temporal and spatial resolution. This visual
system seems to be optimized to code only one highly specific
information, the direction of bioluminescent flashes indicating
high prey densities.
Two papers in this Research Topic deal with different forms
of heat perception. The molecular actors of heat perception have
been very little investigated so far. Junca and Sandoz tested the
association of a heat shock with aversive olfactory conditioning
of the sting extension response, and show that the TRP channel
HsTRPA may be involved in heat detection in honeybees.
Infrared (IR) sensing has been considered as either a specialized
type of vision or thermoreception. In Jewel beetles, Schneider et
al. propose a theory, which would allow bimodal photomechanic
sensilla housed in IR organs to increase sensitivity to weak IR
signals during flight, by making use of muscular energy coupled
out of the flight motor. This mechanism could explain the
capacity of these beetles to detect wood fires over distances of
more than 100 km, allowing to find the resources for larvae
developing in fire-killed trees.
Two contributions deal with different aspects of processing
and coding of mechanosensory information. Hedwig reviews
how a series of filters at different levels of the auditory pathway
is used to process and code the male song by the female
cricket. Carrier frequency, pulse duration and the pulse pattern
are serially processed and finally tune the female phonotactic
behavior to the characteristic properties of the male calling song.
The other paper examines touch sensing in leeches. Kretzberg
et al. show that touch- and pressure-sensitive cells in the skin,
converging on common interneurons, both use quantitative and
temporal elements to encode the precise location of tactile stimuli
in order to elicit minimal, but precise avoiding behavior.
Frontiers in Physiology | www.frontiersin.org 2 January 2017 | Volume 7 | Article 688
Garm et al. Sensory Coding in Invertebrates
Altogether the work presented in this Research Topic shows
the advantage of studying coding of behaviourally active sensory
stimuli in invertebrates of different phyla as it reveals common
features in the processing of complex sensory signals and
different modalities.
AUTHOR CONTRIBUTIONS
All authors listed, have made substantial, direct and intellectual
contribution to the work, and approved it for publication.
Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2017 Garm, Hedwig and Anton. This is an open-access article
distributed under the terms of the Creative Commons Attribution License (CC
BY). The use, distribution or reproduction in other forums is permitted, provided
the original author(s) or licensor are credited and that the original publication
in this journal is cited, in accordance with accepted academic practice. No
use, distribution or reproduction is permitted which does not comply with these
terms.
Frontiers in Physiology | www.frontiersin.org 3 January 2017 | Volume 7 | Article 688


Editorial: Coding Properties in Invertebrate Sensory Systems

Animals rely on sensory input from their environment for survival and reproduction. Depending on the importance of a signal for a given species, accuracy of sensory coding might vary from pure detection up to precise coding of intensity, quality and temporal features of the signal. Highly sophisticated sense organs and related central nervous sensory pathways can be of utmost importance for animals in a complex environment and when using advanced communication systems. In sensory systems different anatomical and physiological features have evolved to optimally encode behaviourally relevant signals at the level of sense organs and central processing. The wide range of organizational complexity, in combination with their relatively simple and accessible nervous systems, makes invertebrates excellent models to study general sensory coding principles. The contributions to this e-book illustrate on one hand particular features of specific sensory systems, and on the other hand indicate not only common features of sensory coding across invertebrate phyla, but also similar processing principles of complex stimuli between different sensory modalities. The chapters show that the extraction of behaviourally relevant signals from all environmental stimuli, as well as the detection of low intensity signals and the analysis of temporal features can be similar across sensory modalities, including olfaction, vision, mechanoreception, and heat perception

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Coding Properties in Invertebrate Sensory Systems

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Hedwig, Berthold G.

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Editorial: Coding properties in invertebrate sensory systems

Garm, Anders Lydik

Copenhagen University Research Information System

u n i ve r s i t y  o f  co pe n h ag e n  Københavns UniversitetCoding properties in invertebrate sensory systemsGarm, Anders Lydik; Hedwig, Berthold G.; Anton, SylviaPublished in:Frontiers in PhysiologyDOI:10.3389/fphys.2016.00688Publication date:2017Document versionPublisher's PDF, also known as Version of recordDocument license:CC BYCitation for published version (APA):Garm, A. L., Hedwig, B. G., & Anton, S. (2017). Coding properties in invertebrate sensory systems. Frontiers inPhysiology, 7, [688]. https://doi.org/10.3389/fphys.2016.00688Download date: 03. Feb. 2020EDITORIALpublished: 10 January 2017doi: 10.3389/fphys.2016.00688Frontiers in Physiology | www.frontiersin.org 1 January 2017 | Volume 7 | Article 688Edited by:Xanthe Vafopoulou,York University, CanadaReviewed by:Wolfgang Rössler,University of Würzburg, GermanyAndrew Dacks,West Virginia University, USA*Correspondence:Sylvia Antonsylvia.anton@inra.frSpecialty section:This article was submitted toInvertebrate Physiology,a section of the journalFrontiers in PhysiologyReceived: 01 December 2016Accepted: 23 December 2016Published: 10 January 2017Citation:Garm A, Hedwig BG and Anton S(2017) Editorial: Coding Properties inInvertebrate Sensory Systems.Front. Physiol. 7:688.doi: 10.3389/fphys.2016.00688Editorial: Coding Properties inInvertebrate Sensory SystemsAnders Garm 1, Berthold G. Hedwig 2 and Sylvia Anton 3*1Marine Biological Section, Department of Biology, University of Copenhagen, Copenhagen, Denmark, 2Department ofZoology, University of Cambridge, Cambridge, UK, 3Neuroéthologie-RCIM, Institut National de la RechercheAgronomique-Université d’Angers, Beaucouzé, FranceKeywords: sensory signal extraction, temporal coding, neuro-ethology, olfaction, vision, mechanoreception, heatdetectionEditorial on the Research TopicCoding Properties in Invertebrate Sensory SystemsAnimals adapt their behavior according to the environment and their specific needs in a givensituation. In order to do so in an appropriate way, they need to detect, analyze, and code the relevantsensory cues. This task is handled by sensory systems and their associated parts in the centralnervous system. With few exceptions, the amount of information present in the environment andthus in principle available to sensory systems, is close to infinite. It is impossible and not desirableto encode and process all the information. Therefore, the first and most important task of anysensory system is to filter and select only the essential information—information, which potentiallywill improve the fitness of the bearer. Differences in sensory information processing occur betweenanimals of different organization levels. Sensory coding in invertebrates and vertebrates relies onmultiple stages of processing to extract information relevant to the survival of the individual. Thewide range of organizational complexity, in combination with their relatively simple and accessiblenervous systems, makes invertebrates excellent models to study general sensory coding principles.In addition, many invertebrate species are of socio-economic importance as pollinators, croppests, or as disease vectors or elicitors. Therefore, understanding their communication systemsand sensory biology is important for the development of insect management or plant protectionstrategies.In the present Research Topic in Frontiers in Invertebrate Physiology we present a seriesof original papers and reviews illustrating the current directions of this field. The differentcontributions indicate not only common features of sensory coding across invertebrate phyla,but also similar processing features of complex stimuli between different sensory modalities. Thisis interesting, because the characteristics of the different types of sensory stimuli are inherentlydifferent, and require different types of detectors and potentially different ways of integration innervous systems. The majority of the papers treat the coding of olfactory information with itsmultidimensionality, which was supposed to function under different operational constraints thanother sensory modalities, and has been a field of high research activity over the past years. However,the articles of this Research Topic show that the extraction of behaviourally relevant signals fromall incoming environmental stimuli, as well as the detection of low intensity signals and the analysisof temporal features can be similar across different sensory modalities, including olfaction, vision,mechanosensation, and heat perception.The papers treating the coding of olfactory information include work on temporal processingand signal extraction in complex environments, and its behavioral outcomes as a function ofphysiological state, as well as potential applications of the findings to control harmful insects.Garm et al. Sensory Coding in InvertebratesOne of the major challenges for olfactory systems is to extractbehaviourally relevant information from highly complex anddynamic signals. Hellwig and Tichy propose in a perspectivearticle that olfactory receptor neurons in cockroaches, whichsignal sudden changes in the concentration of olfactory stimulias compared to a constant background stimulation, might beused for tracking behaviourally relevant odor plumes. Thefact that OFF neurons code better for falling concentrationchanges than ON neurons suggests, that they play a role inalerting a loss of an odor plume. The paper by Brill et al.shows that parallel processing of olfactory information via twoantennal lobe output tracts in the honey bee comprises coincidentactivation patterns of projection neurons within and acrossparallel tracts. The results from simultaneous recordings ofolfactory projection neurons in both tracts support the role ofspike timing in coding olfactory information (temporal code).Another physiological property of the insect antennal lobe,which is potentially important in temporal coding of insectolfaction, is the afterhyperpolarization-phase of the projectionneurons. Lei et al. show in their paper, through pharmacologicalexperiments and modeling, some of the control mechanisms ofthe afterhyperpolarization phase, and confirm the involvementin temporally resetting the system for further odor-specificresponses.Another challenge for olfactory systems is the extractionof a highly relevant signal from an odor background, suchas detection of moth sex pheromones in a rich backgroundof plant volatiles. Whereas the common belief was that sexpheromone and plant odors are processed and encoded bytwo distinct pathways in the insect brain, Rouyar et al.show for the first time that a structurally dissimilar plant-derived odorant is able to activate the pheromone specificpathway and thus might influence pheromone processing.Badeke et al. demonstrate, however, that even though highconcentrations of single plant odors can influence femaletracking in the male noctuid moth Heliothis virescens, sexpheromone-guided behavior is not influenced by plant odors atnatural concentrations.Sensory processing and integration of different stimuli inhigher brain centers ultimately leads to adequate motor output.The review by Namiki and Kanzaki addresses the function of thelateral accessory lobe in the insect brain, which is at the interfacebetween multimodal sensory input and locomotor output. Thisbrain area is believed to be an important output region of thebrain for the control of locomotion. In a comparative approach,structure and function of lateral accessory lobe neurons indifferent insect species are discussed.Because olfaction is widely used by many insect species, ithas become also an important model for sensory ecology andis exploited to develop alternative methods to control harmfulinsects. Reisenman and Riffell review the neurobiology of hostplant selection in the moth Manduca sexta in an ecologicalcontext. Reisenman et al. evaluate how results from the field ofneuroethology can be used to elucidate how harmful insects, beit crop pests or insects transmitting diseases, trace the odors oftheir host plants or animal hosts. They summarize the currentknowledge on the use of semiochemicals, and how resultsfrom applied studies improve our knowledge on detection andprocessing of olfactory signals.The tracking of host plants sometimes changes betweendifferent life stages, and Wu et al. show that one of the odorantbinding proteins (OBPs), binding to attractant semiochemicals, isupregulated in mated females of a pest fruit fly. This upregulationpossibly accounts for an increased attraction to their host plant.The role of OBPs in chemosensory detection and coding isalso addressed by Sun et al. Although OBPs are often foundto be necessary for odor discrimination, the authors show thatthe function of homologous OBPs in bugs can change betweenspecies to binding of non-volatiles in the gustatory system.The visual system basically counts the number of photonsfrom a certain direction during a defined time period,and potentially also measures their energy (color) and theirpolarity. The challenges here are to extract behaviourallyrelevant information under limiting environmental conditions.Two papers of this Research Topic deal with coding in thevisual system under low light conditions. Two strategies toenhance vision in darkness are through temporal and/or spatialsummation of the photons, which will increase sensitivity on thecost of temporal and spatial resolution, respectively. Nocturnalbees enhance sensitivity through optical specializations but notthrough temporal summation, which would probably hampertheir flight control at night (Baird et al.). Garm et al. examinevision in a nocturnal box jellyfish, which enhances sensitivity byhaving both a low temporal and spatial resolution. This visualsystem seems to be optimized to code only one highly specificinformation, the direction of bioluminescent flashes indicatinghigh prey densities.Two papers in this Research Topic deal with different formsof heat perception. The molecular actors of heat perception havebeen very little investigated so far. Junca and Sandoz tested theassociation of a heat shock with aversive olfactory conditioningof the sting extension response, and show that the TRP channelHsTRPA may be involved in heat detection in honeybees.Infrared (IR) sensing has been considered as either a specializedtype of vision or thermoreception. In Jewel beetles, Schneider etal. propose a theory, which would allow bimodal photomechanicsensilla housed in IR organs to increase sensitivity to weak IRsignals during flight, by making use of muscular energy coupledout of the flight motor. This mechanism could explain thecapacity of these beetles to detect wood fires over distances ofmore than 100 km, allowing to find the resources for larvaedeveloping in fire-killed trees.Two contributions deal with different aspects of processingand coding of mechanosensory information. Hedwig reviewshow a series of filters at different levels of the auditory pathwayis used to process and code the male song by the femalecricket. Carrier frequency, pulse duration and the pulse patternare serially processed and finally tune the female phonotacticbehavior to the characteristic properties of the male calling song.The other paper examines touch sensing in leeches. Kretzberget al. show that touch- and pressure-sensitive cells in the skin,converging on common interneurons, both use quantitative andtemporal elements to encode the precise location of tactile stimuliin order to elicit minimal, but precise avoiding behavior.Frontiers in Physiology | www.frontiersin.org 2 January 2017 | Volume 7 | Article 688Garm et al. Sensory Coding in InvertebratesAltogether the work presented in this Research Topic showsthe advantage of studying coding of behaviourally active sensorystimuli in invertebrates of different phyla as it reveals commonfeatures in the processing of complex sensory signals anddifferent modalities.AUTHOR CONTRIBUTIONSAll authors listed, have made substantial, direct and intellectualcontribution to the work, and approved it for publication.Conflict of Interest Statement: The authors declare that the research wasconducted in the absence of any commercial or financial relationships that couldbe construed as a potential conflict of interest.Copyright © 2017 Garm, Hedwig and Anton. This is an open-access articledistributed under the terms of the Creative Commons Attribution License (CCBY). The use, distribution or reproduction in other forums is permitted, providedthe original author(s) or licensor are credited and that the original publicationin this journal is cited, in accordance with accepted academic practice. Nouse, distribution or reproduction is permitted which does not comply with theseterms.Frontiers in Physiology | www.frontiersin.org 3 January 2017 | Volume 7 | Article 688

English

Coding properties in invertebrate sensory systems

HAL-Rennes 1

A. Garm

B.G. Hedwig

S. Anton

Okina

Editorial: Coding Properties in Invertebrate Sensory SystemsSubmitted by Delphine Goven on Tue, 09/05/2017 - 12:34Titre Editorial: Coding Properties in Invertebrate Sensory SystemsType depublication Article de revueAuteur Garm, Anders [1], Hedwig, Berthold G [2], Anton, Sylvia [3]Editeur Frontiers MediaType Article scientifique dans une revue à comité de lectureAnnée 2016Langue AnglaisDate 2016Pagination 688Volume 7Titre de la revue Frontiers in physiologyISSN 1664-042XMots-clés heat detection [4], mechanoreception [5], neuro-ethology [6], olfaction [7],sensory signal extraction [8], temporal coding [9], vision [10]URL de la notice http://okina.univ-angers.fr/publications/ua16170 [11]DOI 10.3389/fphys.2016.00688 [12]Lien vers ledocument http://journal.frontiersin.org/article/10.3389/fphys.2016.00688/full [13]Titre abrégé Front PhysiolIdentifiant (ID)PubMed 28119631 [14]Liens[1] http://okina.univ-angers.fr/publications?f%5Bauthor%5D=27110[2] http://okina.univ-angers.fr/publications?f%5Bauthor%5D=27111[3] http://okina.univ-angers.fr/sylvia.anton/publications[4] http://okina.univ-angers.fr/publications?f%5Bkeyword%5D=23383[5] http://okina.univ-angers.fr/publications?f%5Bkeyword%5D=23382[6] http://okina.univ-angers.fr/publications?f%5Bkeyword%5D=23381[7] http://okina.univ-angers.fr/publications?f%5Bkeyword%5D=18685[8] http://okina.univ-angers.fr/publications?f%5Bkeyword%5D=23379[9] http://okina.univ-angers.fr/publications?f%5Bkeyword%5D=23380[10] http://okina.univ-angers.fr/publications?f%5Bkeyword%5D=4307[11] http://okina.univ-angers.fr/publications/ua16170[12] http://dx.doi.org/10.3389/fphys.2016.00688[13] http://journal.frontiersin.org/article/10.3389/fphys.2016.00688/full[14] http://www.ncbi.nlm.nih.gov/pubmed/28119631?dopt=AbstractPublié sur Okina (http://okina.univ-angers.fr)

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Editorial: Coding Properties in Invertebrate Sensory Systems.

Editorial: Coding Properties in Invertebrate Sensory Systems.

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