The Electro Sense

1452J. D. PETTIGREWElectroreception in monotremes1453abilities involve moving along isopotential lines to find thedipole: the ‘approach algorithm’ (Kalmijn, 1997; Hopkins,1999). The platypus seems to be able to detect the field nonuniformitydirectly. This difference may owe something to thecomplex curved shape of the platypus bill and the enormousrepresentation in the neocortex of the 100 000 electroreceptorsand mechanoreceptors distributed over the bill. Time-of-arrivaldifferences in electroreception, from one side of the bill to theother, would be three orders of magnitude too small to bedetectable, even if the platypus had the incredible 100 ns timeresolution of Gymnarchus sp. (Kawasaki, 1997). As for passiveelectroreception in elasmobranchs (Kalmijn, 1997), thedetermination of directionality would, therefore, require acomplete spatial reconstruction of the shape of the electric fieldat the array of electroreceptors, so that the system could ‘placean arrow’ orthogonal to the field lines, pointing to the source‘up’ the field gradient.Such a reconstruction could be achieved by the S1 corticalrepresentation, where there is a detailed topographicrepresentation of the bill surface combined with arepresentation of different field strengths at each location on thebill. This point-by-point map of the electroreceptors on the bill,combined with different neurons at each point with differingpreferred field sensitivity, would enable a reconstruction of theshape of the field lines over the bill. This would provide anoutput that moved the head in a direction orthogonal to the fieldlines and, therefore, towards the electrical source. Theparasagittal arrays of electroreceptors (Fig. 2B) might explainwhy the platypus is most sensitive to electrical fields thatproduce field lines parallel to the long axis of the bill and thatdecay across the bill. This pattern of sensitivity would also beless subject to the field induced by the platypus’ ownneuromuscular activity (Fjällbrant et al., 1998).HyperacuityThe whole platypus does much better at detecting smallelectrical signals than individual receptors. For a criterion of aone-to-one relationship between stimulus phase and a singlespike discharge, platypus electroreceptors have thresholds ofapproximately 1–2 mV cm −1 (Gregory et al., 1988). The wholeplatypus can, however, detect stimuli with fields as low as20 µV cm −1 , given the appropriate conditions (Fjällbrant et al.,1998). The highly directional response of the platypus headsaccades suggests that it must be performing very sophisticatedsignal processing of the electrical image over large numbers ofelectroreceptors, some of which must be responding to evenlower fields than the 20 µV cm −1 threshold (Pettigrew et al.,1998).This large improvement by the whole animal over theperformance of its individual electroreceptors is also seen inelasmobranchs (in which the whole-animal threshold reachesa record low of less than 5 nV cm −1 ; Montgomery andBodznick, 1999), in mormyrids, in gymnotids (in which thewhole-animal threshold varies widely around the microvoltrange) and in paddlefish (Wilkens et al., 1997).Distance judgementElectric fish can judge distance by comparing the amplitudeand gradient of the voltage distribution (von der Emde, 1999).Platypus also appear to be able to judge prey distance, althoughno behavioural data are available, but only by comparingmechanoreception and electroreception.The unique specialisation of the S1 cortical representationof the bill has focused attention on the role ofmechanoreception. If the mechanoreceptors are used for thedirect tactile encounter of the bill with prey, why is there suchintimate cross-talk with the electrosensory system whose rolemight be expected to be over once contact had been made withthe prey?A clue was provided by recent observations of the activeopening of receptor pores when the bill of the platypus isimmersed. It is eminently reasonable that the pore of theTrigeminalnucleusMechanoreceptiveTrigeminal ThalamusS1 cortexCO organisation in layer IIIPush-rod mechanoreceptorMucous gland electroreceptorElectroreceptive‘Far’ bimodal neurondetects long intervalbetween mechanoandelectro-latencies‘Near’ bimodalneuron detectsshort intervalbetweenmechano- andelectro-latenciesFig. 7. Integrative processing of mechanoreceptive andelectroreceptive information in the stripe-like array that represents thebill skin in platypus S1 neocortex. Bimodal neurons respond both toelectrical stimuli and to mechanical stimuli in the water, with sometuning for the delay between inputs. Along with the directionalityalready demonstrated for platypus electroreception, this array couldprovide direct information about prey distance (taken from PettigrewThe ElectroSensemucous gland electroreceptors should close when the bill is outof water and open once again, to secrete mucous, when the billis immersed (Manger et al., 1998). Such a mechanism wouldavoid deleterious drying and reduced sensitivity of theelectroreceptors when the platypus leaves the water. But whatcan be made of the fact that the push-rod mechanoreceptors alsoopen upon immersion (Manger et al., 1998)? This observationmade us wonder whether the mechanoreceptors are primarilydesigned for the detection of water-borne disturbance ratherthan direct contact with prey. This idea is further supported bythe fact that push-rods in platypus are free to rotate about theirbase, in contrast to the same structures in the terrestrial echidnasand star-nosed mole, where they are tethered distally to thewalls of the pore in a way that would reduce their sensitivityand increase their impedance for lateral displacements. Thesehints that mechanoreceptors are specialised for the detection ofwater disturbances led us to test whether bothmechanoreception and electroreception cooperate in the longdistancedetection of prey (Pettigrew et al., 1998).Although the final demonstration may not be forthcomingsoon, the evidence collected so far supports an arrangement inthe S1 cortex in which distant prey produce a mechanicaldisturbance that arrives some time after the electrical signalfrom the same prey’s movement (Fig. 6) (Pettigrew et al.,1998). Bimodal neurons in the S1 cortex are sensitive to thetime-of-arrival differences, so the stripe-like array wouldprovide a direct read-out of prey distance. An alciopidpolychaete worm has two retinas with different spectralsensitivities that it uses in a similar bimodal trick to judge depthbelow the surface (Wald and Rayport, 1977), and scorpions usethe difference between near-field and far-field ground-bornevibration to judge distance (Babu and Jacobdoss, 1994). Theseexamples from invertebrates illustrate the principle of usingtwo sensory systems with different characteristics to obtain a‘fix’ in depth. The unusual combined array of electroreceptiveand mechanorecepive neurons in platypus S1 neocortex mayprovide the most direct read-out of distance using two differentsensory inputs so far seen in a vertebrate.This work was supported by grants from the AustralianResearch Council and the National Health and MedicalResearch Council of Australia.ReferencesAndres, K. H. and von During, M. 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