Communication and jamming avoidance in electric fish

TINS-August

205

1981

Communication and jamming avoidance in electric fish G. W. Max Westby

may differ from species to species in terms of the number, duration, polarity and relative amplitude of the pulse components. Indeed, it seems that the form of the discharge alone, irrespective of any modulation of the repetition frequency, is sufficient for species identification and serves the vital function of ensuring reproductive isolation among closely related species. O- a

W e a k l y electric fish use their discharges f o r b o t h o b j e c t d e t e c t i o n a n d c o m m u n i c a t i o n . B a c k g r o u n d electrical i n t e r f e r e n c e o r signals f r o m o t h e r fish m a y p r e s e n t s e r i o u s p r o b l e m s , a f f e c t i n g the a c c u r a c y o f electrolocation. I n this art&le, it is d e s c r i b e d h o w species-specific discharges m a y o f f e r s o m e p r o t e c t i o n , b u t r e c e p t o r s p e c i a l i z a t i o n s a n d j a m m i n g - a v o i d a n c e m a n o e u v r e s are also n e e d e d to p r e s e r v e the f i s h ' s e l e c t r o s e n s o r y capability.

Although the electrosensory system of weakly electric fish evolved primarily for electrolocation, there is increasing evidence that it is used for electric communication. In recent T I N S reviews, Moiler TM and Hopkins TM have discussed the main features of the electrosensory system and presented some of the evidence for its twin functions. In this article I shall take a further look at this form of communication and then go on to discuss the problems of interference faced by electric fish, outlining the peripheral and central physiological specializations which have evolved to deal with these difficulties.

dB

Discharge diversity

Sympatric species from the two groups of weakly electric fish, the African Mormyriformes and South American Gymnotoidei produce a wide range of characteristic electric organ discharges (EODs) 9'1°'al. Both groups can be divided into 'wave'* and 'pulse' species (Fig. 1), the majority being of the pulse type. Whilst the range of interpulse intervals is itself a species characteristic, the form of the E O D has attracted the greatest interest. This * Amongthe Mormyriformesthere is onlyone known wave species,Gymnarchas niloticus

-60

01.1 0

i

.......

iO

kHz

b

0.1

Fig. l. Examples o f South American gymnotoid 'wave" and 'pulse'species and their discharges. Head-posilivity up. Top: Eigenmanniavirescens(the green knife fish). The discharge resembles a clipped sine wave. The P/N ratio is the ratio o f the durations o f the head-positive to the head-negative half waves at the DC baseline (shown as a faint horizontal trace). This parameter is sexually dimorphic (see text and Refs 4, 18), being lower in males o f both E. virescensand Sternopygusmacrurus,The discharge rate o f wave fish is generally high and very stable with individuals maintaining constant private frequencies. Bottom: Gymnotus carapo (the banded knife fish). The polyphasic discharge has a spectral peak at about 1.5 kHz. The interpulse interval is relatively long and highly variable in contrast to the wave species. Both the range o f intervals (approx. 15--25 ms) and the form o f the EO D are species-specific characteristics.

........

1 Frequency, kHz

10

Fig. 2. (a) Behavioural thresholds for three Gymnotus carapo to simulated fish pulse trains. The stimuli were emitted by model fish behind mesh screens at the ends o f the arms o f a ' Y" maze. Animals were constrained to the start box at the base o f the ' Y" and then, according to a random sequence, one o f the two modelfish was activated and the door opened. The animals showed a clear preference for the arm with an electrically active model. The abscissa shows the frequency o f the single-cycle sine wave used as the artificial fish pulse. Stimulus repetilion interval was fixed at 18 ms. On the ordinate, thresholds for correct selection o f the arm containing the active model. 0 dB = 320 ~V cm -~. Field strengths are the maximum gradients detectable in the region of the start box where the orientation decision was made. (b) The best behavioural single-cycle frequencies o f the animals ranged from 2.25 to 2.5 kHz (peak spectral power 1.8--2.1 kHz), somewhat higher than the dominant frequency in their EODs, which varied from 1.2 to 1.7 kHz. Due to the broad power spectra the behavioural best frequency is present in the EO D with a relative power o f between - 1 and -3dB. (Westby,

G. W. M. and Whitbread, R. J., unpublished.) Elsevier/North-HollandBiomedicalPress1981 0378- 5gl2t81/000(I 0000/$02.50

206

T I N S - A u g u s t 1981

TheEODandcommunication For electric communication to be of advantage a fish must be able to discriminate between E O D s produced by conspecifics and those produced by sympatric species, i.e. other species of electric fish commonly found in the same habitat. It must also be able to discriminate between its own E O D and that produced by conspecifics and finally, it must be able to discriminate between the sexes. There is impressive peripheral specialization for the detection of species-specific EODs. Hopkins TM has shown that the tuberous electroreceptors of three sympatric wave gymnotoids (Sternopygus mac-

0 dB cf

-5

a

9

2.__

-10

9

2o

4b

ob

50ps

Frequency, kHz

FIIrttS, Eigenmannia virescens and A p t e r o n o t u s albifrons) are very sharply

tuned to the fundamental frequency of each species' EOD. In gymnotoid pulse species such as G y m n o t u s carapo, narrow O' band electroreceptors responding best to juvenile the peak spectral frequency of a con- dB specific's E O D are found in the head -5' regional By testing G. carapo in a Y-maze system (Fig. 2) we have found that the behavioural ~tuning' corresponds well to the narrowband electro-receptor charac-10" teristics. The task was then modified to a choice discrimination between two discharge trains varying only in the spectral frcquency of the synthetic E O D s produced by the two models. The fish demonstrated a fiequency discrimination threshold of Frequency, kHz 1ms about 400 H which on the basis of published field data", would be sufficient to Fig. 3. (a) EOD power spectra and waveforms for adult Pollimyrusisidori. In an analysis of the discharges of 37 discriminate conspecifics from all other individuals. 35 showed the sexual dimorphism evident in the figure. Males have a smaller.first head-posilive phase than second head-positive phase and vice versa [or females. The deviant individuals were on the boedeHine of sympatric species, Whilst therc are central mechanisms equality of the two phases. Furthermore the female discharge is briefer than that o f the male, as shown in the examples of spectra from three males and three females. Female median peak power at27"C was 13.75 kHz and in males designed to distinguish between self- 10.63 kHz. Note also the generally broader spectrum in females, (Data from Westby.G. W. M. and Kirsehbaum, produced and remote E O D s (see below), F_ part of this discrimination can be achieved (b) Power spectrum and waveform of the larval disperipherally. In addition to the difference charge of Pollimyrusisidori, recorded in a 20 day old in amplitude, the wave-form of the fishes (tl ram) ~h. Note the inverted polarity and greatly j/. A.EOD increased duration o f the EO D compared to the adult. EO D varies considerably depending on the The spectrUm shows peaks at 312 and 703 Hz. The low 43 location of the receptor. This is because the frequency content and opposite polarity of the larval electric organ runs along most of the length EOD raise interesting quesaon~ about its function m of the fish. Receptors around the head will parental behaviour and larval group cohesion. (For a be maximally affected by electrical changes (c) The appearance of the adult discharge (.4.EOD) in their vicinity, with the distally produced in a juvenile specimen of and its components suffering greater attenuation. rapid amplitude increase on successive days. Average On the other hand, for a distant conspecific onset time is about 40 days from the first EO D (add 8 44 • ~'~V the pcrceived wave form will be the result for age from spawning). It first appears as a slight in flexion in the baseline, about 0,7 ms al~er each larval of a more-or-less uniform attenuation of discharge ( L.EO D). Its amplitude soon surpa~es that these different E O D components. Thus. of thf L.EO D and rises to ten times its size in 10 days. the frequency characteristics of the local The larval discharge is produced by a larval electric and distant E O D wave form will differ. organsituatedameriorlyinthemedialpartofthedeep )l~...-Until recently the only unambiguous sex lateral musculature, quite distinct from the adult struc45 difference in the E O D of gymnotoids was ture in the caudal peduncle (Denizot, J. P. et al. in Ref, that found in the low frequency wave t 7). A common pacemaker drives separate pools of electromotoneuroncs innervating the electrocytes of the species, Sternopygu~ m a c r u r u s 8. Here two electric organs. The larval electric organ and males discharge at a rate which is about one electromotoneurones degenerate at 80-90 days and the 1 octave below that of females. Conse- larval EOD disappears. (c modifiedfrom Ref. 17.)

--J

unpublished.)

lulldiscussionseeRef.17,) Pollimyrusisidori

b

~ ~.L.EOO

jl/

C

TINS -August

207

1981

Fig. 4. Electric fish can discriminate the temporal pattern o fan EOD waveform as well as its spectral peak. The first major component o.f the E O D o f G. carapo/s head-positive (see Fig. 1). In other words the f~h 's head is initially electrically positive with respect to its tail and then negative during the second half of the discharge. Playback o f aggressive signal sequences (Bursts) through symmetrical dipole models results in the test fish repeatedly butting and biting the electrode showing initial positivity -the apparent head (H). When the simulated EOD is inverted it redirects its attacks to the other end o f the model (right). (From experimentsreported in Westby,G. W. M. (1974)J. Comp. Physiol. 92,327-341 .)

quently it has been assumed that for the majority of species, in which gross sexual differences in E O D do not occur, additional courtship signals are required for sexual identification. However, Gottsehalk and others 4.18 have recently reported sex differences in the E O D waveform of both S t e r n o p y g u s and E i g e n m a n n i a (see Fig. 1 legend), and these may be sufficient for sexual identification. Some mormyrid pulse fish may also have sexually dimorphic EODs 9'17 (Fig. 3A) and it is tempting to speculate that there may be classes of elec-

troreceptors (i.e. the Knollenorgans) whose tuning characteristics allow the fish to discriminate between the sexes. The whole idea of receptor tuning raises some intriguing questions when we look at the parental behaviour of the mormyrid P o l l i m y r u s isidori where the male guards the young in a small nest. Here, the juvenile fish produce EODs which are totally different from those of the adult (Fig. 3B). Their larval E O D has the opposite polarity and approximately 20 times the duration of the adult pulse which

replaces it after about 40 days (Fig. 3C). The spectral peak at around 500 Hz would pose problems for an adult with receptors tuned to adult EODs of 10-14 kHz peak power, unless additional Knollenorgans are found whose sensitivity extends to such low frequencies. The inverted polarity of the larval E O D compared with that of the adult is not apparent, however, from the power spectra since all phase information is lost. Nevertheless, there is evidence that the temporal characteristics of EODs are perceived by electric fish, implying that

208 more is taken into account than just the frequency content of the signal. Playback of simulated fish pulses through physically symmetrical models demonstrates this very well (Fig. 4). Test fish direct their attacks to the apparent (electrical) head of the model as they would to a real fish. Evidently the fish are only using phase information to make this decision. Experiments using continuous phase variation in the related gymnotoid H y p o p o m u s , has shown that these animals are sensitive to much finer deviations from the 'correct' species-specific waveform than this 180 ° inversion TM. With similar findings on the way for mormyrids TM it seems very likely that the Pollimyrus sex and age differences described above are temporal features that the fish are in principle capable of discriminating.

TINS-August

80.

"t i' "1 n

a 4o

0

tb

''

2() ......

Interval

3'0

"

4'0

ms

zok-

b

\ \ Iq

\

\ "~

Interference problems Once a fish has identified and located the correct species~ it can then use the electrical channel to transmit agonistic and courtship messages. This is usually accomplished by means of frequency modulation of the discharge rate 8'n. Characteristic EODs and appropriate receptor tuning, will go a long way to reducing interference from other electric fish. But what of the interference from conspecifics? The problems and solutions are somewhat different for wave and pulse species. As a first line of defence against interference, wave species have the advantage of possessing remarkably constant individual EOD frequencies. In E i g e n m a n n i a viresc e n s frequencies ranging from 250 to 570 Hz have been recorded 4,~8, each anim a l holding its interpulse interval constant to within a few microseconds, Problems arise when a conspecific with a similar private frequency arrives in the vicinity. Artificial jamming stimuli, for example, can seriously degrade electrolocation ~'' but the fish can protect itself with the so-called iamming avoidance response (JAR). When subjected to sine wavc stimulation at a frequency slightly different from the fish's own discharge, E i g e n m a n n i a can maintain its privacy by shifting its EOD rate away from this stimulus frequency. This response serves to space out the frequencies of individuals within communication range. Further details of the JAR in wave species and the underlying physiological mechanisms can be found in excellent recent reviews by Heiligenberg~L While inwave species thc JAR protects lhe fish from similar frequency discharges, inpulsc species it is designed to minimize the probability of EOD coincidences. In a

1981

G.petersii 108ms

"..~ ;: P bovei 12 45ms 1Ok\

\ k

tb Interval, ms

Fig. 5. The echo response in mormyrids is a tendency for one fish to lock its EODs to those o f a neighbour, discharging at a fixed latency o f lO-14 ms for short bouts, The behaviour is best visualized by triggering a poststimulus time interval histogram accumulation off one of the fish. This has the disadvantage o f requiring separation o f each animal's EO Ds. Although information is lost, e.g. who is"echoing to whom, the echo response can be seen very simply for demonstration purposes as in (a) by combining the E O Ds o f the two fish and casting all the intervals into a time interval histogram. The expected distribution o f intervals in this case is approximately flat from 0 to about 70 ms, so any tendency to echo emerges as a peak as shown in this histogram from a 2000 interval sample o f an interaction between a pair o f Gnathonemuspetersii- the echo latency is at just over 10 ms. Bin width 1 ms. Temperature 27°C, By us'ing the same technique on a larger number offish in a communal aquarium as in (b), the expected distribution o f intervals is somewhat different. Here a million intervals were recorded between all the superimposed E O Ds of 6 G. petersiiand 2 Petrocephalttsboveiat a bin width o f 50 Izs. Short intervals become highly probable but the echo peak Ls ~till very clearly present. Since echo latency Ls wecies-speci fic, lhe peak due to the P. bowelcan be seen at that .species' echo latency of l 2--13 ms. "['his technique could well prove usefid for wecies recognition in the field, once tile echo lateneies for more ,~e¢ ie~ are known.

number of gymnotoids predictable EOD rate shifts can be produced by artificial stimulation. Pulses delivered just before the animal's EOD tend to produce a sudden frequency increase (pacemaker excitation) whereas stimulation just after the discharge evokes a decrease (pacemaker inhibition) 6,7,~. In these experiments, stimulus pulses time-locked to the EOD mimic a foreign fish discharging at exactly the same frequency. In the real world other fish will be discharging at different and highly variable frequencies such that their EODs continuously drift through, or

'scan', the test fish's discharges. It can be seen from Fig. 7 that the direction of scan will depend on whether the foreign fish is discharging at a higher or lower frequency. For the fish to avoid impending E O D coincidences and the resultant disruption of electrolocation, it must be able to determine the direction of scan of a neighbouring fish's pulses. This can be done very simply if we assume that the excitatory and inhibitory effects on the pacemaker are themselves mutually inhibitory. Whichever process is activated first would then have the dominant effect6L The model there-

209

TINS August 1981 -

mV/cm 20

fish A 10

0

,

.

,

°

II

II

II

I

80

'IJL

N = 1000

60

o

o

.

.

.

0

.

2

.

.

.

4

.

.

.

.

6

.

8

.

.

=~

.

10

Latency

18.5

.

.

.

12

14

.

16

18

\

.~ 7

1

1()

2"0

so

4'o

50

ms

own detectionthr~hold

dB

.

~, ~

20

ms

]

II

.

"20

-- E 18,0q "~ ~,~>17.5

.

fish B

\

2Ot

- - ~

T

detect,on

window

\

partner~ perceived EOD am~eude

-16 ~ i

.. "~ .~ "~ -12 E 0a

T

1651

,--" ""

..... -.-.

16-0

83T "4

-0

own EOD h*gherfrequency EOD

-10

5

0 __j~ 5 iI --,i

partner's

+ 10 ms

i

lower frequency parmer's

Interval

EOO

,

!

,

Fig. 6. Top lefi: Post-stimulus time interval (latency) histograms o,f synchronization boutS in a pair of G. carapo interacting electrically but resting in their daytime hiding places about 15 cm apart. Periodically the fish synchronize their EO D frequencies,for short boutS o,f up to 120 successive intervals - a maximum o,f about 2 s. Histogram (a) shows 500 latencies o f the socially dominant fish's EOD from the preceding discharge o f the submissive fish. The data are from 38 consecutive synchronization bouts. In histogram (b) 1000 latencies are plotted for the submissive fish's EO D from the preceding dominant fish's EOD. Here the data are for 52 successive boutS on a different occasion. Note that the peaks indicate a tendency for a fixed latency relationship (a kind o f echo) to be taken up during synchronisntion boutS - with the dominant fish's EO D occurring 3--4 ms before that o,f the submissive fish. Bottom leO: Part of a sequential plot o,f the concurrent E O D intervals and latencies o f the two fish during a synchronization bout in which the fish were locked in near antiphase -for over 1 O0 intervals. The animals go into wild EO D frequency oscillations during these bouts until the synchrony is broken. Fish A is the dominant fish. See Fig. 7,for possible interpretation. ( Reproduced from Westby, G. W. M, (1979) Behav. Ecol. SociobioL 4, 381-393.) Fig. 7. Top right: Schematic representation o,fa synchronization bout in G. carapo of the type illustrated in Fig. 6. Fish A "s EO D is shown as a thin line whereas that of fish B (the dominant animal) is shown as a thick line. Experiments with phase-locked stimuli16 showed that the fish's sensitivity to -foreign discharges varied in the ratio of 100:1 over the inter-pulse interval, being maximal just afier the EO D and dropping to a low level about 5 ms before the expected occurrence of the next discharge. This cyclic variation in sensitivity to -foreign pulses is shown in the diagram from the point of view o f each fish. Note that fish B's pulses fall into the region of low threshold -for each o,ffish A's discharges -the period during which disruption o,f A's electrolocation is likely to occur. This is because Burst Duration Coder receptor responses to the foreign pulse will contaminate the 'correct' BDC response to the fish's own EOD ~7. Fish B, however, is protected from similar interference since A's pulses fall in the region of high threshold. We can therefore hypothesize that such a latency relationship is to the advantage o f B -the dominant fish. ( Reproduced from Ref. 16). Bottom right: By measuring the electric field strength at the fish's head in the recording situation described in Fig. 6, it is possible to define a 'detection window' during which the partner's EO D is above threshold. This model enables us to explain why it is that in natural interactions, the fish does not decrease is frequency during right--lefi scans as it does with artificial stimuli. Except at very close range, -foreign EO Ds will be below threshold until they hit the sharp cut-off o,f the attenuation curve (50 dB ms-9, to the right o f the detection window. Therefore these EODs suddenly 'appear" in the low threshold, excitatory, region thereby producing frequency increases from right-left scans. Left-right scans, due to a lower frequency partner, allow gradual detection of encroaching EO Ds because o,f the more gentle (2.5 dB ms-9 roll-off o.f the curve to the le]t o,f the window. Simply maintaining a higher frequency than one's partner might be an advantage for just this reason -impending EOD coincidences can be predicted several cycles in advance and JAR manoeuvres can be implemented. It is interesting in this respect that E OD frequency and dominance are highly positively correlated in G. carapo*. (Reproduced from Westby, G. W. M. (1979) Behav. EcoL Sociobiol. 4, 381-393.)

fore explains the finding that stimulation with lower frequency foreign pulses leads to a frequency increase (left--fight scan) and a higher frequency to a frequency decrease (right-left s c a n ) - a qualitatively

similar result to the J A R in wave species, Actual coincidences are reduced by this method as the J A R causes the fish's pulse to 'jump over' the encroaching foreign discharge. Recent neurophysiological work

by Baker x has demonstrated that specific classes of primary afferents may be involved in the discrimination of left-right from right-left scans. Coincidences can also be avoided by

210 producing very short pulses. This may explain why brief discharges are more commonly found among gregarious speciesL for here conspecific interference is most intense. In mormyrids E O D rates are more variable than in the gymnotoid pulse species, so the prediction of discharge coincidence will be much more difficult. Mormyrids have developed another mechanism for reducing the probability of E O D coincidences known as the "echo response'a*L For short periods thcsc species are able to lock their EODs to those of a conspecific, discharging at fixed latenties of 10-I 4 ms the exact value depending on the species (Fig. 5). An added feature of this behaviour is that the echo-latency corresponds to a gap in the fish's interpulse interval histogram. This means that an echoing fish "knows" that he is firing his electric organ at the precise moment when his partner is least likely to discharge. Similar E O D synchronizations have been observed in gymnotoids, both in pulse (Fig. 6) and wave species. In the latter case extremely precise phase-coupling is maintained for prolonged periodsL

The problem of self-identification For successful JARs or phase-locking to occur, the fish must not be fooled into thinking that its own E O D is coming from another fish. It must therefore have a way of recognizing its own EOD, and this is not as simple as it might first appear. In mormyrids the command to fire the electric organ from the pacemaker in the medulla is used to ~gate' signals passing through the first relay of the electrosensory system, the nucleus of the posterior lateral line lobe (nPLLL)Z'°,'L Input from the highly sensitive Knollenorgans is blocked during the fish's own discharge but is available to higher centres for communication purposes during the interpulsc interval. On the other hand, electroreceptive information about distortion in the fish's field is coded by the less sensitive Mormyromast receptors, and appears to be available only during the E O D *'7. The system is therefore beautifully designed to time-share the twin functkms of electrolocation and electrocommunication.

TINS-August

Functionally similar types of receptor are fl~und in pulse gymnotoids but no physiological or anatomical evidence for a comParable electric-organ commandrelated signal has been found in thcsc species2"~L Pulse marker receptors, like the Knoltenorgans of mormyrids, fire only a single spike irrespective of stimulus intensity whereas burst-duration coder (BDC) receptors are used to measure the electric field strength for electrolocation, like the Mormyromasts. One genus, H y p o p o m u s , has pulse markers which a,'e much less sensitive than the BDCs. By merely 'listening' to the BDC input when the pulse markers are simultaneously activated, this fish would have a way of separating its own from foreign EODs. Only its own electric field would be sufficiently intense to elicit pulse marker responses. In other gymnotoids, such as G y m n o t u s curapo, pulse markers are more, or as sensitive, as BDC units TM'L This is morc in line with the mormyrid solution, allowing high sensitivity for communication. It might seem that this fish is more open to interference from conspecifics than H y p o p o m u s , however the specific spatial pattern of pulse marker activation could be used to discriminate a foreign electric field from its own, irrespective of any threshold considerations.

Interactions between the JAR and communication The particular circumstances in which JAR manoeuvres take place suggest that they may have an important social function. A good example is the echo response in mormyrids discussed above. Bell et al? have shown in G n a t h o n e m u s petersii that the dominant fish in a pair echoes more than its submissive partner. Furthermore, Luecker and Kramer (unpublished) have reported the surprising finding that Pollimyrus isidori males respond to artificial pulse trains by echoing at 12-14 ms but females show a kind of echo 'avoidance" in that they tend not to discharge at the echo latency to the foreign pulse train. These results imply that the echo response may represent a vital component of mormyrid social behaviour. tn G y m n o t u s carapo there is also an

1981

interaction between dominance and the latency at which the fish synchronizes during encounters with conspecifics. An explanatory model based on these findings has been proposed (Fig. 7). The legend describes how the observed latency relationships tend to be to the jamming advantage of the dominant fish. By maintaining a specific EOD synchronization the dominant animal is least affected by his partner's EODs and is able to predict discharge coincidence and successfully implement jamming avoidance manoeuvres,

Reading list 1 Baker, (. L. (1980) J. Comp, Phwsiol. 136, 165 1~41 2 Bell.C. C. ( 1979)J. Physiol. (Paris), 75,361-379 3 Bell, C. C., Myers,J. P. and Russell, (7. J. ( 19741 J. C),np. Physiol. 92, 181-228 4 Gonsehalk. B, ( 1981) in Advances in Physiological Sciences. Vol, 31 (T. Szaboand G. ('zeh, eds). Pergamon Press.Oxfordpp. 255-277 5 Gonschalk, B. and Scheich, H. (19791 Behav. Ecol. Sociobiol. 4, 395~1.118 .5 Heiligenberg.W. (1977) in Studim of Brain Function (Braitenberg, V., ed.). Vol. 1, pp. 1-85, Springer, Berlin 7 Heiligenberg, W.(I980)Naturwi,~senschafien,67,

499-507 8 Hopkins, C D. (1977) in Hog, Animat~ Communicate (Sebeok. T.A., ed.), pp. 263-289, Indiana UniversityPress. Bloomington 9 [[opkins,C. D. (1980) Behav. Ecol, Socmbiol. 7, 113 10 Hopkins,C, D. (b)81) Trend~ NeuroSei. 4, 4-6 11 Hopkins, (. D, and Heiligenberg, W. (1978) Behuv. Ecol. Soeiobiol. 3. 113-134 12 Kramer,B, (1974)J. Comp. Physiol. 93, 2/13-235 13 Mollcr. P. ( 198111Trends NeuroSei. 3, 105-i119 14 Szabo,T. and Fessard, A. (I 974) in thmdbook of Sen~ory Physiology (Fessard. A, ¢d.). Vol. IlI/3. Springer,Berlin, pp. 59-124 15 Watson, D, and Bastian, J. 119791 J. (¥~mp. Physiol. 134, 191 2112 16 Westby,G. W. M. (1975) J. Cornp. Phwiol. 134, 191-202 17 Westby, G, W. M. and Kirsehbaum, F. 119771 J. C¥)mp. Physiol. 122, 251-271 : ibM 127, 45-59 18 Westby.G. W. M. and Kirschbaum.F. t1981) in Advances in Ph3wiological Sciences. Vol. 31 (T, Szabo and G. Czeh, eds). Pergamon Press, Oxfi~rd, pp. 17t~- 194 Max Westhy receivedhis Ph. D. in l~ychology ]rom the University of Reading in 1972 after which he worked as an SRC post-doctoral fellow in Thomas Szabo's laboratory at the CNRS. Gif-sur-Yvette, France. He g now I,ecturer at the Department of Psychology, University of Sheffield, Sheffield SI 0 2 TN, U K.