J. comp. Physiol. 127, 267-286 (1978) Journal of Comparative Physiology. A 9 by Springer-Verlag 1978 The Jamming Avoidance Response in Eigenmannia Revisited: The Structure of a Neuronal Democracy Walter Heiligenberg, Curtis Baker, and Joanne Matsubara Neurobiology Unit, Scripps Institution of Oceanography, Universityof California, San Diego, La Jolla, California 92093, USA Accepted July 11, 1978 Summary. The Jamming Avoidance Response (JAR) is a gradual shift in frequency of the fish's electric organ pacemaker in an attempt to increase a small difference, Af, between the fundamental frequency of electric organ discharges (EODs) of a conspecific and that of the animal's own EODs. The JAR can be elicited in curarized animals by replacing the silenced EOD with a periodic electric stimulus, $1, and by simulating EODs of a conspecific with a periodic stimulus, $2, whose frequency differs by Af from the frequency of S~. Similar to the natural JAR, the fre- quency of the pacemaker will rise and fall in response to negative and positive Afs respectively, provided that Sa, but not $2, shares critical features with the EOD of the animal. Ambivalent or even opposite responses (Anti-JARs) may result if S~ lacks critical EOD features (Fig. 1). In search of these features the following results were obtained. 1. To elicit JARs, S~ need not be phaselocked to the pacemaker. The JAR can thus be driven exclu- sively by electroreceptive afference, without reference to the pacemaker. 2. $1 and $2 may be pure sinewaves as long as their field geometries differ sufficiently. Higher har- monics, which may be added to a sinewave to mimic the EOD wave shape, are required only if S~ and $2 have identical geometries, i.e., if they are presented through the same pair of electrodes. The animal may thus use two different strategies to determine the sign of the Af: one which is based on differences in stim- ulus field geometries and one which is based on the presence of higher harmonics. Only the former is con- sidered in the following. 3. The $1, but not the $2, field geometry should approximate the natural EOD field geometry. To the extent that this condition is violated, sufficiently high $2 intensities may elicit Anti-JARs (Fig. 4). 4. Evidence is given that the JAR is controlled, in a cumulative manner, by local interactions of neighboring electroreceptive fields on the animal's body surface which, as a consequence of different $1 and $2 field geometries, experience different degrees of contamination of $1 by $2. Simultaneous stimulations of remote areas of body surface result in almost linear summation of their associated effects on the pacemaker (Figs. 5, 6). Theoretically, no uni- tary central EOD representation is required. 5. Based on the results in 3. und 4., we propose that correct JARs are elicited to the extent that the majority of electroreceptors is predominantly driven by $1, rather than by $2, and this condition is fulfilled to the extent that the $1 field geometry approximates that of the natural EOD. 6. Effective $2 stimuli have a periodicity near that of the EOD (S~) fundamental frequency, f. This in- cludes all stimuli with a power peak at a frequency of n.f+Af, n=1,2,3,... (Fig. 2), with the optimal Afbeing 3 to 8 Hz and identical for all n. Such stimuli cause consistent distortions in successive EODs (S~ pulses), which gradually travel through the EOD ($1) cycle (Fig. 3). This "motion" leads to periodic fluctu- ations in the amplitude of the joint signal, EOD (S~) + $2, and the phase of its positive zero-crossings with regard to those of the EOD ($1) (Fig. 7). The modulation of these two variables can be represented by a motion along a closed graph in a two-dimen- sional state plane (Fig. 8), which is reproduced Af times per s. The direction of motion along this graph reflects the sign of the Af. Evidence is given that this motion is detected by a mechanism comparable to a motion detector in the realm of vision. Introduction The electric fish Eigenmannia discharges its electric organ in a continual quasi-sinusoidal wave-type man- 0340-7594/78/0127/0267/$04.00