Proc. Nat!. Acad. Sci. USA Vol. 91, pp. 5853-5857, June 1994 Neurobiology Comparison of directional selectivity in identified spiking and nonspiking mechanosensory neurons in the crayfish Orconectes limosus (mechanoreception/stlmulus coding/directionaity) JURGEN TAUTZ* AND MARK R. PLUMMERt Theodor-Boveri Institut fMr Biowissenschaften, Lehrstuhl ffr Verhaltensphysiologie und Soziobiologie, Universitit Am Hubland, D-97074 Wirzburg, Federal Republic of Germany ABSTRACT We have recorded electrical activity from two identified synaptically coupled mechanosensory interneurons in the abdominal nervous system of the crayfish Orconectes limosus and have studied their responses to constant-velocity water-jet stimuli presented from different directions. The two neurons, the ascending caudal photoreceptor (CPR) and the local directionally selective neuron, responded preferentially to stimuli delivered ipsilaterally to their dendritic input regions. Both neurons featured responses consisting of a phasic excit- atory "on" response and a tonic depolarizing plateau. The different response components showed various degrees of di- rectional selectivity: The Initial "on" peak of the response was the least sensitive and the plateau was the most sensitive to stimulus direction. The CPR showed a sharp cut-off in respon- siveness to contralateral stimuli, whereas the local directionally selective neuron showed a more gradual decrease in its direc- tional responsiveness. This difference is a consequence of the feed-forward lateral inhibition that the local directionally selective neuron exerts on the CPR and of the threshold for initiation of action potentials in the CPR. A comparison of the spiking response of the CPR with its generator potential shows that the number and frequency of action potentials are a more sensitive indicator of directional preference than the generator potential response. The directional characteristic of the CPR is discussed as a filter matched to a specific spatial aspect of biologically relevant water movements. The translation of stimulus information from the amplitude of a receptor potential to the number and frequency of action potentials is a process that can occur at different stages in various sensory systems. For example, in the vertebrate mechanosensory system, the process can occur within a single cell, the Pacinian corpuscle, as the generator potential gives rise to action potentials (1). In the vertebrate visual system, however, the stimulus information can be conveyed in an analog form through several neuronal stages and not be converted to an action potential format until reaching the ganglion cell layer of the retina (e.g., ref. 2). The functional advantages and disadvantages of both dec- remental (nonspiking) and impulse conduction have been discussed in great detail (e.g., refs. 3-5): Passive conduction provides an accurate but typically nonlinear transformation of the input signal. This accuracy could be preserved in an impulse code. However, neurons producing action potentials not only code voltage as a parameter but also use voltage as a trigger mechanism to generate impulses. To avoid spiking to even subtle voltage fluctuations, neurons are protected by a threshold for impulse initiation. Threshold, on the other hand, reduces the capacity for differentiation between dif- ferent events coded by voltages below the threshold value. Passive decremental conduction can only be performed over certain distances. It has, however, the great advantage of an extremely rapid conduction velocity, which is important for rapid information processing. Projection neurons with large axons must depend on impulse conduction, which is much slower in its propagation speed compared to a non- spiking system. Several of these mechanosensory neurons in the crayfish have been shown to respond selectively to particular direc- tions and frequencies of oscillatory water currents. In par- ticular, neurons have been shown to respond preferentially to either "headward" or "tailward" water currents (6). In addition, a feed-forward lateral inhibitory pathway involving an identified nonspiking neuron generates a side-specific bias as well (7, 8). In the present study, we attempt to investigate the directional characteristic of sensitivity (DCS) of these neurons in more detail, with specific emphasis given to the question of what information is coded by the spiking and by the nonspiking components of the responses and why both kinds of neurons may be involved in the central processing of mechanical stimuli. In this study, we have examined two of the identified mechanosensory interneurons in the crayfish. These are, according to nomenclature of Reichert and coworkers (7, 9), the nonspiking local directionally selective (LDS) neuron and, postsynaptic to it, the spiking caudal photoreceptor (CPR; ref. 10), which has its output region in the brain of the crayfish (11, 12). The CPR, in addition to being a mechan- oreceptive interneuron, produces action potentials in re- sponse to direct illumination (10). METHODS Animal Care. Orconectes limosus were obtained from a local supplier and maintained in large aerated tanks and fed ad libitum. Animals ranged in size from 4 to 10 cm (rostrum to tailfan). Stimuli. The experimental chamber consisted of a 15-liter tank in which the preparation could be suspended. The isolated tailfan with the attached ventral cord was mounted dorsal-side down on the underside of a platform that was secured in the tank. The abdominal nervous system was threaded through an opening in the platform onto a piece of wax. Small pins were used to fasten the abdominal ganglia into place. The water current stimulus consisted of a constant stream of saline directed toward the center of the tailfan via a small Abbreviations: CPR, caudal photoreceptor; LDS, local directionally selective; DCS, directional characteristic of sensitivity; PST, peri- stimulus time; EPSP, excitatory postsynaptic potential; IPSP, inhib- itory postsynaptic potential. *To whom correspondence should be addressed. tPresent address: Department of Biological Sciences, Nelson Bio- logical Laboratory, Rutgers University, Piscataway, NJ 08955- 1059. 5853 The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Transcript
Proc. Nat!. Acad. Sci. USAVol. 91, pp. 5853-5857, June 1994Neurobiology
Comparison of directional selectivity in identified spiking andnonspiking mechanosensory neurons in the crayfishOrconectes limosus
(mechanoreception/stlmulus coding/directionaity)
JURGEN TAUTZ* AND MARK R. PLUMMERtTheodor-Boveri Institut fMr Biowissenschaften, Lehrstuhl ffr Verhaltensphysiologie und Soziobiologie, Universitit Am Hubland, D-97074 Wirzburg, FederalRepublic of Germany
ABSTRACT We have recorded electrical activity from twoidentified synaptically coupled mechanosensory interneuronsin the abdominal nervous system of the crayfish Orconecteslimosus and have studied their responses to constant-velocitywater-jet stimuli presented from different directions. The twoneurons, the ascending caudal photoreceptor (CPR) and thelocal directionally selective neuron, responded preferentially tostimuli delivered ipsilaterally to their dendritic input regions.Both neurons featured responses consisting of a phasic excit-atory "on" response and a tonic depolarizing plateau. Thedifferent response components showed various degrees of di-rectional selectivity: The Initial "on" peak of the response wasthe least sensitive and the plateau was the most sensitive tostimulus direction. The CPR showed a sharp cut-off in respon-siveness to contralateral stimuli, whereas the local directionallyselective neuron showed a more gradual decrease in its direc-tional responsiveness. This difference is a consequence of thefeed-forward lateral inhibition that the local directionallyselective neuron exerts on the CPR and of the threshold forinitiation of action potentials in the CPR. A comparison of thespiking response of the CPR with its generator potential showsthat the number and frequency of action potentials are a moresensitive indicator of directional preference than the generatorpotential response. The directional characteristic of the CPR isdiscussed as a filter matched to a specific spatial aspect ofbiologically relevant water movements.
The translation of stimulus information from the amplitude ofa receptor potential to the number and frequency of actionpotentials is a process that can occur at different stages invarious sensory systems. For example, in the vertebratemechanosensory system, the process can occur within asingle cell, the Pacinian corpuscle, as the generator potentialgives rise to action potentials (1). In the vertebrate visualsystem, however, the stimulus information can be conveyedin an analog form through several neuronal stages and not beconverted to an action potential format until reaching theganglion cell layer of the retina (e.g., ref. 2).The functional advantages and disadvantages of both dec-
remental (nonspiking) and impulse conduction have beendiscussed in great detail (e.g., refs. 3-5): Passive conductionprovides an accurate but typically nonlinear transformationof the input signal. This accuracy could be preserved in animpulse code. However, neurons producing action potentialsnot only code voltage as a parameter but also use voltage asa trigger mechanism to generate impulses. To avoid spikingto even subtle voltage fluctuations, neurons are protected bya threshold for impulse initiation. Threshold, on the otherhand, reduces the capacity for differentiation between dif-ferent events coded by voltages below the threshold value.
Passive decremental conduction can only be performedover certain distances. It has, however, the great advantageofan extremely rapid conduction velocity, which is importantfor rapid information processing. Projection neurons withlarge axons must depend on impulse conduction, which ismuch slower in its propagation speed compared to a non-spiking system.
Several of these mechanosensory neurons in the crayfishhave been shown to respond selectively to particular direc-tions and frequencies of oscillatory water currents. In par-ticular, neurons have been shown to respond preferentially toeither "headward" or "tailward" water currents (6). Inaddition, a feed-forward lateral inhibitory pathway involvingan identified nonspiking neuron generates a side-specific biasas well (7, 8). In the present study, we attempt to investigatethe directional characteristic of sensitivity (DCS) of theseneurons in more detail, with specific emphasis given to thequestion of what information is coded by the spiking and bythe nonspiking components of the responses and why bothkinds ofneurons may be involved in the central processing ofmechanical stimuli.
In this study, we have examined two of the identifiedmechanosensory interneurons in the crayfish. These are,according to nomenclature of Reichert and coworkers (7, 9),the nonspiking local directionally selective (LDS) neuronand, postsynaptic to it, the spiking caudal photoreceptor(CPR; ref. 10), which has its output region in the brain of thecrayfish (11, 12). The CPR, in addition to being a mechan-oreceptive interneuron, produces action potentials in re-sponse to direct illumination (10).
METHODSAnimal Care. Orconectes limosus were obtained from a
local supplier and maintained in large aerated tanks and fedad libitum. Animals ranged in size from 4 to 10 cm (rostrumto tailfan).
Stimuli. The experimental chamber consisted of a 15-litertank in which the preparation could be suspended. Theisolated tailfan with the attached ventral cord was mounteddorsal-side down on the underside of a platform that wassecured in the tank. The abdominal nervous system wasthreaded through an opening in the platform onto a piece ofwax. Small pins were used to fasten the abdominal gangliainto place.The water current stimulus consisted of a constant stream
of saline directed toward the center of the tailfan via a small
Abbreviations: CPR, caudal photoreceptor; LDS, local directionallyselective; DCS, directional characteristic of sensitivity; PST, peri-stimulus time; EPSP, excitatory postsynaptic potential; IPSP, inhib-itory postsynaptic potential.*To whom correspondence should be addressed.tPresent address: Department of Biological Sciences, Nelson Bio-logical Laboratory, Rutgers University, Piscataway, NJ 08955-1059.
5853
The publication costs of this article were defrayed in part by page chargepayment. This article must therefore be hereby marked "advertisement"in accordance with 18 U.S.C. §1734 solely to indicate this fact.
5854 Neurobiology: Tautz and Plummer
(1 mm o.d. and 0.8 mm i.d.) glass tube. It was controlled byan electric valve that switched the flow from a pressurizedsaline reservoir to the glass tube (stimulus) or to a drain(between stimuli). The characteristics of the flow were mea-sured using laser doppler anemometry. The distance of theoutlet of the tube to the tailfan was set in such a way that theflow was laminar and its velocity was 40 cm/s at the centerof the tailfan. In this situation, turbulences could be detectedafter the water jet passed the tailfan. The duration of thewater jet was 1.0 s. The time course of the stimulus wasrectangular with a constant plateau velocity.The mechanical arrangement of the holder for the glass
tube allowed the tube to be positioned at different distances(up to 10 cm) relative to the tailfan or at different anglesrelative to the axis of the tailfan but always pointing towardthe center of the tailfan. The zero degree direction corre-sponds to a water jet directed onto the tailfan from behindaligned with the long axis of the animal. The + degree anglesare angles to the right and the - degree angles are to the leftif the crayfish is viewed from behind.
Electrical Recordings. Experiments were done at room tem-perature. The experimental preparation has been described inmore detail elsewhere (for the isolated tailfan; ref. 13). Briefly,the tailfan and the ganglionic chain were removed from theanimal leaving the connections of most sixth ganglion rootsintact. Intracellular recordings were obtained using conven-tional microelectrode recording and amplification techniques.The sixth ganglion was first mechanically desheathed to allowpassage of the electrode into the neuropil.The input side of the LDS neuron (soma side; ref. 8) was
established morphologically by filling the neuron ionto-phoretically with horseradish peroxidase subsequent to theintracellular recording. The input side of the CPRs could beestablished directly from the recording site as all neuropilararborizations are restricted to one-half of the ganglion. Nev-ertheless, these cells were also filled with dye.
Extracellular recordings were obtained by splitting the 3-4or the 5-6 abdominal connective into small bundles and by
Ia III
i4Aiij
ii
ii
.v 4'. 5
100
0
a .-I I *- - bu0 500 1000 1500 2000
100
C
0
a -600 500 1000 1500
Time, ms2000
using suction electrodes to record the activity of ascendingmechanosensory neurons. The CPR was identified using amoveable light. It is the only interneuron in this area of thenervous system that responds to direct illumination.Data Collection and Analysis. Data were recorded on an FM
tape recorder for further analysis. Up to three electrophys-iological records together with trigger signals were recorded.Data were analyzed using a signal processor to initially
average and digitize responses. The data were then trans-ferred to a PC computer for further analysis.The spiking response of the CPR recorded extracellularly
was analyzed by counting the number of action potentials[peristimulus time (PST) histograms] with a bin width of 50ms over a 2.5-s PST. This response was then separated intothe peak (maximal response within the first 200 ms afterstimulus onset) and the plateau phase (between 200 ms and800 ms after stimulus onset) as was done for the nonspikingresponse (see below).To better measure the nonspiking part of the intracellularly
recorded CPR response, an average of 10 responses was takenfor each neuron and for each direction tested. This resulted ina smoothing of spiking activity from the records (Fig. 1 a andb) that could then be analyzed as described below.To describe the graded nonspiking response of the CPR
(see above) and of the LDS neuron, we defined a peak and aplateau phase of the response. The initial transient responsewas expressed as the voltage difference between the restingpotential of the neuron (averaged 500 ms before the onset ofthe stimulus) and the maximal depolarization within the first200 ms after stimulus onset. The plateau response refers tothe average depolarization (same reference voltage as in peakresponse) between 200 ms and 800 ms after stimulus onset.
RESULTSFeatures of the Neuronal Responses. The responses re-
corded from all of the sensory interneurons to the water-jetstimulus were separated into different components.
b
E
0 500-. .. .1 2
0 500 1000 1500 2000
d
E
10080604020 E0
-20-40-60
10080604020 E
0
-20-40-60
Time, ms
FIG. 1. Intracellularly recorded nonspiking responses (mV vs. ms) from one CPR (a and b) and one LDS neuron (c and d) to the standardwater-jet stimulus from 40 degrees left (a and c) and 40 degrees right (b and d) onto the tailfan. Stimulus was on at 400 ms and off at 1400 ms.All four plots are 10-times-averaged responses. The average process eliminates the action potentials occurring in the CPR and leaves thenonspiking response.
Proc. Natl. Acad. Sci. USA 91 (1994)
Neurobiology: Tautz and Plummer
The CPR (n = 6), being spontaneously active in theseexperiments with an average of 1.1 ± 0.15 action potentialsper s, responded with excitation to stimuli from a particulardirection. The initial response consisted of a burst of actionpotentials on top of a large excitatory postsynaptic potential(EPSP), followed by maintained firing at a lower rate ridingon a maintained depolarization showing occasionally a minoroff-excitation. Once the stimulus was turned off, the main-tained phase was then sometimes followed by a post-stimulushyperpolarization coupled with cessation of spiking.The CPR was strongly inhibited by stimuli from certain
directions. In these cases, transient inhibitory postsynapticpotentials (IPSPs) and maintained hyperpolarizations wereobserved. Also, the peak portion of the response was absentand rebound depolarization was observed.The intracellular recordings of the CPR (Fig. 1 a and b)
were taken from the neuropilar processes. Synaptic activitywas resolved well, and the action potentials were quite small.
Unlike the CPR, the LDS neuron (n = 5) respondedexclusively with graded depolarizations of different ampli-tudes depending, for any given stimulus strength, on thestimulus direction (Fig. 1 c and d). Simultaneous intracellularrecording from the CPR (with input side to the left) and theLDS neuron (with input side to the right) revealed a simul-taneous appearance of EPSPs in the LDS neuron and IPSPsin the CPR if the stimulus was directed toward the input sideof the LDS neuron.
Quantitative Response Comparison. To compare the re-sponses of the different neurons and of the different responsecomponents, the data were displayed on cartesian coordi-nates. However, the spatial orientation of the LDS neuronresponse has been reversed to line up with the CPR. Thenonspiking response of the CPR preferentially reflected stim-
uli ipsilateral to its axon and showed a sharp cutoff inresponsiveness to contralateral stimuli (Fig. 2 a and b).The LDS neuron, in contrast, showed an entirely different
response. While it did show directional selectivity, the pre-ferred side was contralateral to its output process or "ax-onal" side (see ref. 8). The decrease in responsiveness wasnot as dramatic as that for the CPR (Fig. 2 c and d).The nonspiking data plotted on cartesian coordinates
showed that the peak and the plateau components of theresponse were not equally sensitive to direction. Specifically,when the difference between the minimum and the maximumresponses was used as an indicator of directional selectivity,the plateau of the response was a much better indicator ofdirection than was the peak of the response (Fig. 2).
Since the nonspiking responses ofthe sensory interneuronsshowed clear directional selectivity, it was interesting tocompare this in detail to the DCS of the spiking response ofthe CPR. Therefore, we measured the firing characteristics ofthe CPR using extracellular suction electrodes.
In these recordings transient and maintained excitation aswell as inhibition were observed, which was even more clearin PSTs based upon 10 summed responses (Fig. 3).When the number of extracellularly recorded action po-
tentials was compared to the magnitude of the intracellularvoltage change, two trends emerged (compare Figs. 2 a andb with 4 a and b). (i) The spiking responses were in every casemore directionally sensitive than the nonspiking responses.(ii) Of the spiking responses, the plateau responses oncemore showed the most obvious directional selectivity.
DISCUSSIONA characteristic stimulus-coding property of many mecha-nosensory neurons is their DCS. Implied by this term is the
1 F.
0.90.80 70.60.50.40.30 20 1
03flno').
0 90 80 70 60 50.4-i!
; 03.~~~~~~C
0 201
02-.0 1
Fr% Ar. an anC 7n Qnr. 2-8-7-S6-5-40U30-21J0 0 10 20 30 4i0 50 6u 7u0u U
80 70-650-40-302G-10 C 1 02030 40 50 60C. 80CLJ D;:C,
FIG. 2. Nonspiking responses from the CPR and the LDS neuron tested with the standard waterjet for directions from 80 degrees left (-80)to 80 degrees right (80). Regardless of the orientation of the neuron as it was originally studied, the responses (mV depolarization) for eachexperiment have been scaled (relative mV) such that the maximum response seen in the complete experimental series is equal to a 100% response(1.0 on the y axis). The data are represented as if the axonal or output side of the cell is on the left. Data are the mean and SEM from seven(CPR) and five (LDS) neurons for responses summed 10 times each. (Insets) Morphology of CPR and LDS neuron. Arrow shows input sideof the LDS neuron; dotted lines give symmetry axis of the ganglion.
- -- -- - .- I- ,- - - -. n nr, "'i
5856 Neurobiology: Tautz and Plummer
aI
20 r
15 V
10 F
c
06n 1L0 N
C
A II....La.Ia
0 Lf)
5
0
20
III
Ln6D
I
O LOCD
~~~~~Ld~~~~~~Ll"I
15
10
5
0
N U-)O
0 LOCD
Time. s
FIG. 3. PST histograms for one CPR based upon 10 summed responses to the standard water-jet stimuli applied from 40 degrees right andleft (c and b) and from 80 degrees right and left (d and a) onto the tailfan. Time course of stimulus (starting at 0 and ending at 1 s) is shown bythe bar under the x axis in a.
number of action potentials that are produced by the mech-anoreceptor when it receives a stimulus from different direc-tions. In general practice, a DCS plot results from successivemeasurements of a neuron's response to stimuli applied fromdifferent directions, which, besides direction, also dependson the stimulus intensity.The DCS of mechanosensory cells of hair receptors in
arthropods (14) can be preserved in postsynaptic interneu-rons (15). In the cercal system of crickets (Acheta domesti-cus), central projections of four classes of sensory neurons(originating from singly innervated hairs, each respondingbest to one of four wind directions) are kept separate in thecercal glomerulus where they synapse onto ascending inter-neurons (16) or onto local nonspiking interneurons (17). TheDCS of each one of these interneurons results from theconvergence of sensory neurons having identical DCS ontothe same interneurons. Such a central connectivity preservesthe peripheral categories of directionality. But the output ofa single neuron at any moment is ambiguous as differentcombinations of stimulus intensity and direction can producethe same level of neuronal excitation. This ambiguity can bereduced by parallel processing and comparing the output ofprimary neurons with different DCSs.An alternative strategy would be to use the spatial layout
ofthe receptors to extract information ofbiological relevancewhile neglecting details of the individual receptor responses.The latter strategy seems to be realized in neurons pro-
cessing the input from certain hairs on the tailfan (telson anduropods) of crayfish. Here mechanosensory hairs highlysensitive to even slight water movements are multiply inner-vated and the different neurons from any one hair havedifferent DCSs (18). The primary afferents synapse in the lastabdominal ganglion onto ascending and local interneurons, afew of which have been identified and their stimulus codingproperties investigated (e.g., refs. 7 and 19). For certainascending mechanosensory interneurons with input from thetailfan, it has been shown that electrical stimulation of
sensory axons ipsilateral to the dendritic tree (restricted to ahemiganglion) excites the neuron and contralateral stimula-tion inhibits them (20, 21). This kind of response leads to anextreme sidedness of the DCSs of the interneurons, whichmay reflect use of the geometrical arrangement of receptorsin the sense mentioned above.The ascending CPR and the LDS neuron have proved ideal
for an exploration of this problem of sidedness. Each of thetwo paired nonspiking LDS neurons is presynaptic to one ofthe two paired CPRs, resulting in a feed-forward inhibitionacross the midline (7, 8).The DCS for the CPR to water movements from different
directions onto the tailfan becomes less sharp when thesensory nerves ipsilateral to the soma (contralateral to thedendrites; see also, Fig. 2b Inset) ofthe CPR are severed (22).Not many direct afferent connections could have been dis-rupted by this operation since only very few branches of theprimary afferents do cross the midline ofthe ganglion (23, 24).
In the above experiments, Wilkens (22) used sinusoidalwater movements of uniform intensity across the tailfan.Here we present DCSs for locally applied water jets. Thesestimuli result in DCSs of the CPR that look different than thepublished data (22). Especially, they show much steepergradients. The DCS even shows a "shaped edge" represent-ing a sudden transition from excitation to inhibition (Fig. 4),and this edge corresponds to the animal's axis of symmetry.This specific DCS is not the result of the simple combinationof the DCSs of the sensory neurons but is produced by twomechanisms: (i) the feed-forward inhibition of the LDS ontothe CPR and (ii) the threshold level for initiation of actionpotentials in the CPR. The DCS of the LDS neuron is ratherweak when compared to that of the CPR and stimuli fromdifferent directions are only weakly differentiated. We as-sume that the shape of the DCS of the LDS neuron is causedby lateralization of the excitatory and inhibitory input to theLDS neuron, because electrical stimulation of ipsilateral(relative to the soma) sensory nerves elicited EPSPs and of
20 r
15
10
5
CO
.a)
Cn 20
Fo
15 F
10 F
5
45
Proc. Natl. Acad Sci. USA 91 (1994)
RI
0Lu
Proc. Natl. Acad. Sci. USA 91 (1994) 5857
a0.9 F
0.80.70.60.50403
020.1
-01
-0 2
-0.3-0.4
-80-70-60-50-40-30-20-10 0
Degre10 20 3040 5060 7080
-0.5-80-70-60-50-40-30-20-10 0
Dearc
_ .
1 0 20 30 40 50 60 Mt 8KOS
FIG. 4. CPR spiking output (peak and plateau) to the standard water-jet stimuli applied from 80 degrees left (-80) to 80 degrees right (80)based on PST histograms as shown in Fig. 3. The response was normalized to the maximum response seen in the complete experimental series.Zero on the y axis corresponds to the resting activity ofthe undisturbed neuron; negative values indicate inhibition. Data are the mean and SEMofthe normalized (the largest mean was set as 1) numbers ofaction potentials (summed responses of 10 trials per each of six neurons were countedat a bin width of 50 ms).
the contralateral nerve elicited (depolarizing) IPSPs in theLDS neuron (25). Thus sensory inputs from different sides ofthe tailfan produce different effects in the LDS neuron.The lateral inhibition fed-forward from the LDS neuron
onto the CPR sharpens the DCS of the CPR. The gradeddepolarization of the LDS neuron allows a very preciseinhibition of the CPR that exactly matches the excitation ofthe LDS neuron over its entire dynamic range. The resultingDCS of the generator potential of the CPR (i.e., the nonspik-ing behavior of the CPR) is further sharpened (now as
measured from the spiking response) by the voltage level ofthe threshold for the initiation of action potentials.The DCS ofthe CPR spiking response finally resulting from
these two mechanisms has the important consequence thatstimuli applied to the tailfan as a whole are more weaklydifferentiated than those applied locally [compare the resultsof Wilkens (22) to those presented here].The steepest gradient in the output dynamics of the CPR
would result ifwater movement over the tailfan was directedsimultaneously into opposite directions across the midline ofthe crayfish (26). Local water movements that would produceexactly such a stimulus pattern across the tailfan are spinningvortices produced by swimming fish (27, 28). The detectionoffish, in which the tailfan can play an important role (29-31),is most important for crayfish as they can be prey orpredators for the crayfish. However, the mechanosensorysystem discussed here probably is involved in the receptionof other stimuli of biological relevance as well.
In general, relevant natural stimuli should be manifest incharacteristics of the sensory structures animals use toevaluate their environment in the sense of matched filters(32). Matched filters do not need to code every single detailof a stimulus field (which is certainly very complex for thewater movements taking place in a fish-crayfish interaction)but respond to basic underlying patterns (32). The directionalcharacteristic of sensitivity of the caudal photoreceptor, aprominent ascending interneuron, can be viewed as preciselysuch a "matched filter" responding as it does best to watervortices typically produced by swimming fish.
We thank D. C. Sandeman, W. Gronenberg, and K. Wiese formany valuable suggestions to a first version of the paper and B.H6lldobler for critically reading the manuscript. This work wassupported by the Deutsche Forschungsgemeinschaft (Ta 82/3-2).
1. Loewenstein, W. R. (1971) in Handbook of Sensory Physiology, ed.Loewenstein, W. R. (Springer, Heidelberg), Vol. 1, pp. 269-290.
2. Dowling, J. E. (1979) in The Neurosciences: Fourth Study Program, eds.Schmitt, F. 0. & Worden, F. G. (Massachusetts Institute ofTechnologyPress, Cambridge, MA), pp. 163-181.
3. Bullock, T. H. (1981) in Neurones Without Impulses, eds. Roberts, A. &Bush, B. M. H. (Cambridge Univ. Press, Cambridge, England), pp.269-282.
4. Bush, B. M. H. (1981) in Neurones Without Impulses, eds. Roberts, A.& Bush, B. M. H. (Cambridge Univ. Press, Cambridge, England), pp.147-176.
5. Shaw, S. R. (1981) in Neurones Without Impulses, eds. Roberts, A. &Bush, B. M. H. (Cambridge Univ. Press, Cambridge, England), pp.61-116.
6. Wiese, K., Calabrese, R. & Kennedy, D. (1976) J. Neurophysiol. 39,834-843.
7. Reichert, H., Plummer, M. R. & Wine, J. J. (1983) J. Comp. Physiol. 151,261-276.
8. Reichert, H., Plummer, M. R. & Wine, J. J. (1983b) J. Physiol. (London)78, 786-792.
9. Reichert, H., Plummer, M. R., Hagiwara, G., Roth, R. L. & Wine, J. J.(1982) J. Comp. Physiol. 149, 145-162.
10. Welsh, J. H. (1934) J. Cell Comp. Physiol. 4, 379-388.11. Simon, T. W. & Edwards, D. H. (1990) J. Comp. Physiol. 166, 745-755.12. Hamm, I. (1989) Ph.D. thesis (Universitit Konstanz, Konstanz, F.R.G.).13. Sigvardt, K. A., Hagiwara, G. & Wine, J. J. (1982) J. Comp. Physiol.
148, 143-157.14. Gnatzy, W. & Tautz, J. (1980) Cell Tissue Res. 213, 441-463.15. Camhi, J. (1988) Experientia 44, 401-408.16. Murphey, R. K., Walthall, W. W. & Jacobs, G. A. (1984) J. Exp. Biol.
112, 7-25.17. Bodnar, D. A., Miller, J. P. & Jacobs, G. A. (1991) J. Comp. Physiol.
168, 553-564.18. Wiese, K. (1976) J. Neurophysiol. 39, 816-833.19. Plummer, M. R., Tautz, J. & Wine, J. J. (1986) J. Comp. Physiol. 15,
751-764.20. Wilkens, L. A. & Larimer, J. L. (1972) J. Comp. Physiol. 80, 389-407.21. Calabrese, R. L. (1976) J. Comp. Physiol. 105, 103-114.22. Wilkens, L. A. (1988) Comp. Biochem. Physiol. C 91, 61-68.23. Kondoh, Y. & Hisada, M. (1987) Cell Tissue Res. 247, 17-24.24. Schmitz, B. (1992) in Nervous Systems: Principles of Design and
Function, ed. Naresh Singh, R. (Wiley Eastern, New Delhi, India), pp.69-90.
25. Krenz, W. D. & Reichert, H. (1985) J. Comp. Physiol. 157, 499-507.26. Wiese, K. & Schultz, R. (1982) J. Comp. Physiol. 147, 447-454.27. Blickhan, R., Krick, C., Zehren, D., Nachtigall, W. & Breithaupt, T.
F.R.G.).29. Tautz, J. (1989) Medienbewegung in der Sinneswelt der Arthhropoden:
Fallstudien zu einer Sinnes6kologie (Fischer, Stuttgart), p. 59.30. Tautz, J. (1990a) in Frontiers in Crustacean Neurobiology, eds. Wiese,
K., Krenz, W. D., Tautz, J., Reichert, H. & Mulloney, B. (Birkhaeuser,Basel), pp. 200-206.
31. Tautz, J. (1990b) in Sensory Systems and Communication in Arthropods,eds. Gribakin, F. G., Wiese, K. & Popov, A. V. (Birkhaeuser, Basel),pp. 359-363.
32. Wehnr, R. (1987) J. Comp. Physiol. 161, 511-531.
![The spiny-cheek crayfish, Orconectes limosus (Rafinesque ... · Decapoda: Cambaridae], digs into the UK David Holdich1* and John Black2 ... are unknown it seems likely they were intro-duced](https://static.documents.pub/doc/80x56/5fab5d6194df0a24ac21b348/the-spiny-cheek-crayfish-orconectes-limosus-rafinesque-decapoda-cambaridae.jpg)
