Table Of ContentReference: Biol. Bull. 200: 211-215. (April 2001)
Why Do Animals Have So Many The Role
Receptors?
of Multiple Chemosensors in Animal Perception
CHARLES D. DERBY* AND PASCAL STEULLET
Department ofBiology and Centerfor Behavioral Neitroscience,
Georgia State University. Atlanta. Georgia
Abstract. Many animals have an abundance and diverse exceeds the number ofcentral neurons that process sensory
assortment of peripheral sensors, both across and within information. This is particularly true for the chemical
sensory modalities. Multiple sensors offer many functional senses. For example, decapod crustaceans have millions of
advantages to an animal's ability to perceive and respond to chemosensory neurons in their cephalic and thoracic ap-
environmental signals. Advantages include extending the pendages (Derby and Atema. 1988; Laverack, 1988a, b;
ability to detect and determine the spatial distribution of Derby, 1989; Cate and Derby, 2000). and mammals have
stimuli, improving the range and accuracy ofdiscrimination tens of millions of olfactory receptor neurons (Hildebrand
among stimuli of different types and intensities, increasing and Shepherd. 1997; Weiler and Farbman, 1997). Conver-
behavioral sensitivity to stimuli, ensuring continued sensory gence ratios between peripheral and central olfactory neu-
capabilities when the probability ofdamage or other loss of rons canbe as high at 300:1 in invertebrates and vertebrates
function to some sensors is high, maintaining sensory func- (Meisami. 1989; Ache. 1991; Schmidt and Ache, 1996b;
tion overthe entire sensory surface during development and Hildebrand and Shepherd, 1997). Within a sensory modal-
gsreonwsotrhy, asntidmuilnactrieoans.inIgntthheisripcahpneers,s owfebeuhsaevitohrealcrouusttpaucteatno ity,Whanatanfiamctaolrsalesxopltayipnicwalhlyy haansimaaldsivhearsvietymuolftispelnesosrentsyopress.?
chemosensory system as the primary example to discuss One answer to this question is a general one; each animal
these functions ofmultiple sensors. These principles may be has a rich diversity ofbehaviors that enable the acquisition
applicable to the function ofautonomous robots and should ofresources needed to survive and reproduce, andextensive
be considered in their design. sensory information is required to perform these behaviors.
Thus, sensory systems have evolved to extract information
Introduction about the quality and quantity of important environmental
Each animal has a plethora of peripheral sensors that stimuli, such as the variety of wavelengths, intensities, and
enable the detection of different sensory stimuli, including patterns that constitute each animal's sensory world.
olifghste,nscohresmitchaatlsa,nvainbirmaatilonpso,ssaensdsesmacnanyboetheexrcse.eTdihneglnyumhibgehr. perIinphtehirsalpaspeenrs,orwse. Wofeferaregxupelatnhaattiomunlstfioprlethseenmuslotrisplfiucnicttyioonf
In many animals, the complement of receptor cells far in one or more ofthe following ways: ( 1 ) extend the range
of spatial sampling by increasing the sensory surface area;
(2) extend the range of types of stimuli that are discrimi-
*To whom correspondence should be addressed. E-mail: cderbyfs1 nated by having a diversity of sensors, each of which is
gsuT.heidsu.paper was originally presented at a workshop titled Invertebrate tuned to a subset of stimulus qualities, intensities, or tem-
Sensor,' Information Processing: Implications for Biologicallv Inspired poral dynamics; (3) increase the sensitivity and accuracy of
AutonomousSystems. Theworkshop,whichwasheldattheJ.ErikJonsson resolution through response summation; (4) maintain the
CenterfortheNationalAcademyofSciences,WoodsHole,Massachusetts, function ofthe system in the face ofdamage to sensors: (5)
from 15-17April 2000,wassponsoredbytheCenterforAdvancedStudies compensate for non-functioning developmental stages of
intheSpaceLifeSciencesattheMarineBiologicalLaboratory,andfunded
by the National Aeronautics and Space Administration underCooperative sensors; (6) enable formation ofspecializedcentral process-
Agreement NCC 2-896. ing centers with different behavioral functions.
211
C. D. DERBY AND P. STEULLET
In developing the ideas in this paper, we draw heavily quences. For example, the location of aesthetascs at the
from the chemical senses of crustaceans, although some anterior end of the animal places them where odor-laden
examples from other animals and sensory systems are in- currents often first reach an animal and also where fan
cluded. Nonetheless, the principles are general. Addition- organs can direct odors toward or away from their own
ally, we argue that these principles of multiple sensors may sensors (Breithaupt, 2001). In the same way, chemorecep-
be applicable to autonomous robots and should be consid- tors on the tips of legs are more likely to encounter chem-
ered in their development. icals associated with the objects in the substrate, and che-
moreceptors around the mouth will receive maximal
Multiple Sensors Enhance the Probability of Detecting stimulation when food is held in the mouthparts.
Stimuli by Enlarging the Sensory Surface Area The fact that some sensilla are innervated by both che-
moreceptor neurons and mechanoreceptor neurons makes
Having sensors distributed across an animal'sentire body
these bimodal sensilla ideal for identifying the spatial loca-
surface increases the chances that the animal will encounter
tion ofchemotactile stimuli, especially ifthe axons ofthese
environmental chemical signals. In fact, chemoreceptors are neurons project topotopically into the central nervous sys-
distributed across the body surface ofmany animals, includ-
tem. There is evidence that mechanoreceptor neurons and
ing vertebrates (fish: Caprio, 1988) and invertebrates (in- chemoreceptor neurons from bimodal sensilla on the anten-
sects: Dethier, 1976). In crustaceans, receptor neurons are nules project to the same central neuropils (Schmidt et al.,
packaged into cuticular extensions of the exoskeleton. 1992; Schmidt and Ache, 1996a), but it is notknown iftheir
called sensilla. Chemosensilla ofcrustaceans are present on maps are overlapping as in some insects (Newland et al.,
most or all surfaces (Laverack, 1988a; Derby, 1989; Gate 2000), or what is the spatial relationship between projec-
and Derby, 2000), enhancing the probability that chemical tions from mechanoreceptor neurons and chemoreceptor
signals will be encountered. neurons from the same sensillum.
A Diversity of Sensor Types Enhances the Ability to A sensory appendage can have a variety ofchemorecep-
tor neurons that differ in their sensitivities. Antennular
Discriminate Stimulus Attributes
chemoreceptorneurons oflobsters have diverse sensitivities
Although chemosensors are found all over the body and to different types or qualities of odorants, thus broadening
appendages of crustaceans, there exists a diversity of che- the range of chemical signals to which the entire organ is
mosensors with a variety ofproperties. Having an extensive sensitive (Derby and Atema, 1988; Voigt and Atema, 1992;
variety of sensors that extract different stimulus features Derby. 2000). Antennular chemoreceptor neurons also dif-
should allow an animal to have a more accurate represen- fer from each other in their sensitivities to odor concentra-
tation of its environment and aid in the discrimination of tions (Derby and Atema. 1988; Merrill et al., 1994; Daniel
these stimuli. The sensors covering the body surface of an ft ill., 1996) and in their ability to follow high-frequency
animal differ in structure, innervation, and distribution, re- odor pulses (e.g.. flicker-fusion properties) (Gomez et al.,
flecting different functions. In the case ofinsect chemosen- 1999). Thus, different neurons extract different stimulus
silla. the diversity is immense: gustatory sensilla and olfac- features, together building an image of the chemical and
tory sensilla differ in some fundamental features, but much mechanical features of the external world.
of the diversity is within either the olfactory or gustatory
modality (Dethier, 1976; Altner et ai, 1981; Shanbhag et
nl.. 1999). The diverse types of crustacean chemosensilla Multiple Sensors Increase Response Sensitivity
include unimodal sensilla e.g.. aesthetasc sensilla Through Response Summation
(Griinert and Ache, 1988: Hallberg et at.. 1997), and bi-
modal (chemo-mechano) sensilla e.g., hair pegs, hedge- Having multiple sensors allows animals to detect lower
hog and fringed sensilla, hooded sensilla, simple sensilla amplitude signals. This is because central neurons can sum
(Altner et ai. 1983; Schmidt and Gnatzy, 1984; Derby, responses from many sensory neurons, increasing signal
1989; Schmidt, 1989; Gate and Derby, 2000). The sensilla capturing and the signal-to-noise ratio and thus allowing
can be short (e.g., hair pegs and hooded sensilla are ca. 50 finer resolution between related signals (Van Drongelen et
ju,m) or long (aesthetascs can be >600 /j,m and guard setae ill.. 1978; Meisami, 1989). For example, olfactory systems
can be >1200 /xm) (Gate and Derby, 2000). These different typically have at least tens to hundreds of thousands of
sensillartypes often have restricted distributions. Forexam- receptor cells (Chase, 1986; Ache, 1991; Farbman, 1992;
ple, aesthetascs are only on the distal half of antennular Hildebrand and Shepherd, 1997). Ifeach neuron responded
lateral flagella, and hedgehog and fringed sensilla are only to one chemical with one spike above spontaneous activity
on the distal two segments of some legs. and to another chemical with two spikes, a summation
The specific distributions, structure, and innervation of involving all neurons would dramatically amplify the dif-
different sensilla undoubtedly have functional conse- ference in the magnitude ofthe responses tothe two stimuli.
ROLE OF MULTIPLE CHEMOSENSORS
thus providing the multineuronal system with a resolving In addition, turnover of neurons in olfactory systems
capacity far beyond that of one or a few neurons. causes some neurons to be nonfunctional because they are
eitherimmature orsenescing (Chase, 1986; Farbman, 1992;
Multiple Sensors Ensure Functional Integrity of a Steullet et al.. 2000a). Since the percentage of nonfunc-
Sense Organ Following Localized Damage tional cells is high in the vertebrates and invertebrates, there
Multiple sensors may serve to compensate for local dam- could be compensation by maintaining large numbers of
sensors (Chase, 1986).
age to sensory organs. Given that chemosensors are used to
probe an animal's external environment for chemical sig-
nals, these sensors are often highly exposed and vulnerable Multiple Sensors Enable Formation of Specialized
to physical, chemical, and biological damage. Damage can Central Processing Centers With Different
affect sensory function (Hamilton and Case, 1983; Bauer, Behavioral Functions
ba1gy9e89id)n,carnbeduatsfimununglctttiihpoelnaeplrsobe(anDbsaionlriisetlymietnthiaatmii,szoe2m0et0h0es)e.inmsAposarcstaanorefexduaanmmdpaalgmee-, nceensItsfraidlnifpbfreeohrcaeevnsitsoorsraeslnsoaounrtdpumttyospteossrhopaurrleodgbrdieafmfpseo,rsestnithbielanel.layFgorcreoaeutxpealrmerpdilceht,-o
aesthetascs are repeating functional units, each containing a it has been demonstrated that the function of a chemosen-
broad complement of receptor neurons with different sen- sory neuron in Caenorhabditiselegans isdeterminedby that
sitivities (Spencer, 1986; Mellon and Alones. 1993; Steullet neuron's central connections rather than by the receptor
er al., 2000b). This type oforganization ensures that local- molecules that it expresses (Troemel et al., 1997). Crusta-
ized damage does not have significant impact on an ani- ceans have not only a diversity of antennular chemo- and
mal's ability to respond to and discriminate different types mechanoreceptor types but also a diversity of sensory neu-
of chemicals (Steullet er al., 1999, 2000c; Horner et ai, ropils thatreceive theirprojections. These sensory neuropils
2000). In addition, many chemoreceptor systems, including include olfactory lobes (OLs), which receive input from
the aesthetasc system, have mechanisms for self-renewal. aesthetasc chemoreceptors (Mellon and Munger, 1990; San-
Continuous turnover, including addition and loss, of che- deman et al.. 1992; Schmidt and Ache, 1996b); lateral
moreceptors occurs inthe vertebrates (Weilerand Farbman, antennular neuropils (LANs), which are thought to receive
C1h99a7s:e CaanldofRieetlianlg.,, 11998968;) SaannddienmvaenrteabnrdatSesan(dCehmaasne,, 11999866;; cienpputtorfsroomnnobno-tahestlahteetraaslc acnhdemomreedcieapltoarnsteannndulmaerchfalnaogerlel-a
Steullet et al., 2000a; Harrison et al.. 2001a. b). This turn- (Schmidt et al., 1992; Schmidt and Ache, 1996a; Roye et
over enables the renewal of neurons that have a finite life al., 2000): and median antennular neuropils (MANs), which
span, which helps to maintain function of a system over receive projections from statocysts, equilibrium receptors,
time in spite of damage. Similar turnover also occurs in and receptors from the antennular proximal segments (San-
crustacean mechanoreceptor sensilla (Macmillan et al., deman etal. 1992; Schmidt etal., 1992: SchmidtandAche.
1998: Steullet et al., 2000a). 1993, 1996a; Cate and Roye. 1997). The organization of
these neuropils gives hints about their function. The OLs
Multiple Sensors Compensate for Nonfunctioning have a glomerular neuropil, similar to the olfactory neuro-
Developmental Stages of Sensors pils of insects (antennal neuropils) and vertebrates (olfac-
As animals develop and grow, they must add new sensors tory bulbs), in which the glomeruli represent different but
to maintain sensitivity over their enlarging body surfaces. overlapping chemical sensitivities (Hildebrand and Shep-
To ensure that the animals can detect chemicals that im- herd, 1997). This suggeststhatOLsencodechemicalquality
pinge anywhere on the body surface, the numberofsensors and are involved in olfactory discrimination. The LANs
must increase both during development (Schafer and have a bilobed organization, with each lobe receiving input
Sanchez. 1973; Laverack, 1988b) and throughout the lives from one of the two antennular flagella (Schmidt tt al.,
of those species with indeterminate growth (Mellon and 1992). Additionally, the lobes have a stratifiedorganization,
Alones, 1993). The antennular receptors of crustaceans are reflecting regionalized sensory input and stratified motor
added as units in two ways (Sandeman and Sandeman. output fromantennularmotorneurons (Schmidtetal.. 1992;
1996; Steullet et al.. 2000a). First, the antennule is com- Schmidt and Ache, 1996a). This organization suggests that
posed of many segments called annuli. and new annuli are LANs may function in the sensori-motor control of anten-
added at molting. Second, new sensillaare added toexisting nular behavior, including flicking (Maynard. 1966) or dis-
annuli. In some cases, such as aesthetascs and their associ- criminating the location of chemo-mechanostimulation on
ated chemo-mechanoreceptive sensilla, new sensilla are the antennule. The MANs are involved in maintaining equi-
added in highly organized spatial arrays. In this way. the librium (Sandeman et ai, 1992; Schmidt and Ache, 1993;
addition of annuli and sensilla creates a multiplicity of Cate and Roye. 1997), but their function may be broader
repeating, modular packages of sensors. than this (Fraser, 2001).
214 C. D. DERBY AND P. STEULLET
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