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Sensory Hyperacuity in the Jamming Avoidance Response of Weakly Electric Fish Masashi Kawasaki

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Sensory Hyperacuity in the Jamming Avoidance Response of Weakly Electric Fish Masashi Kawasaki 473 Sensory hyperacuity in the jamming avoidance response of weakly electric fish Masashi Kawasaki Sensory systems often show remarkable sensitivities to The jamming avoidance response small stimulus parameters. Weakly electric; fish are able to The South American weakly electric fish Eigenmannia resolve intensity differences of the order of 0.1% and timing and the African weakly electric fish Cymnanhus perform differences of the order of nanoseconds during an electrical electrolocation by generating constant wave-type electric behavior, the jamming avoidance response. The neuronal organ discharges (EODs) at individually fixed frequencies origin of this extraordinary sensitivity is being studied within (250-600Hz) using the electric organ in their tails. Each the exceptionally well understood central mechanisms of this cycle of an EOD is triggered by coherent action potentials behavior. originating from a coupled oscillator, the pacemaker nucleus in the medulla. An alternating current (AC) electric field is thus established around the body, and its Addresses distortion by objects is detected by electroreceptors on the Department of Biology, University of Virginia, Gilmer Hall, Charlottesville, Virginia 22903, USA; e-mail: [email protected] body surface [5,6] (Figure 1). Current Opinion in Neurobiology 1997, 7:473-479 When two fish with similar EOD frequencies meet, http://biomednet.com/elelecref~0959438800700473 their electrolocation systems jam each other, impairing 0 Current Biology Ltd ISSN 0959-4388 their ability to electrolocate. To avoid this jamming, they shift their EOD frequencies away from each other in Abbreviations a jamming avoidance response in order to increase the ELL electrosensory lateral line lobe difference in their frequencies [7-91. During the jamming EOD electric organ discharge avoidance response, a fish determines, without trial and error, whether it should increase or decrease its own EOD frequency relative to that of its neighbor by computing the Introduction sign of the difference between its own and its neighbor’s Human psychophysics and animal behavioral studies often EOD frequency: Af=f2-fl,where Af is the frequency reveal the astonishingly high sensitivity of sensory organs difference, and fl and f2 are the fish’s own and its to various stimulus parameters [l]. Examples of this neighbor’s EOD frequency, respectively. include vernier acuity in human vision (5s of arc) [2], interaural time disparity in human audition (6~s) [3], Behavioral experiments have demonstrated that a fish and thermal sensitivity in snakes (O.OOl”C) [4]. These determines the sign of 4 solely from the mixture of behavioral sensitivities, or hyperacuities, often exceed sensory feedback from its own electric organ and its the resolution of individual sensory receptor neurons by neighbor’s EODs, without referring to the pacemaker orders of magnitude and, thus, must result from central nucleus for information about fl [lO-131. In these studies, processing. As hyperacuity often results from many steps the fish’s EODs were silenced by blocking cholinergic of central processing, elucidation of its central mechanisms synapses at the electric organ and were replaced with has been hampered by the absence of ‘transparent’ artificially generated EODs at arbitrary frequencies. As systems, in which the flow of pertinent information all the electroreceptors on the body surface are exposed processing can be tracked within the CNS, from sensory to a mixture of the fish’s own and its neighbor’s EODs, receptors to behavioral output. and no receptor is uniquely stimulated by one of them, information about the sign of 4must be computed from In weakly electric fish, information processing within the a complex mixture of the two stimuli. central electrosensory and electromotor mechanisms for an electric behavior, the jamming avoidance response, Two sensory cues that are embedded in this complex is well understood. Furthermore, this response also mixture have been identified as essential for the cal- demonstrates sensitivities to extremely small stimulus culation of Af-specifically, amplitude modulation and parameters (amplitude fluctuations of less than 0.1% and differential-phase modulation, both of which are necessary time disparities in the range of nanoseconds). Thus, for a fish to perform a jamming avoidance response. As weakly electric fish provide a transparent system for shown in Figure 2, amplitude modulation is a periodic examining high sensitivities expressed at the behavioral change of stimulus intensity that results from the beating level. This review focuses on research that examines the of two signals. Differential-phase modulation represents central mechanisms of the jamming avoidance response in small phase differences at different areas of the body light of hyperacuity. that are created by the different spatial geometry of 474 Sensory systems (a) Electric organ Gymnarchus / (cl Jamming avoidance response EOD frequency 2Hz f2 : neighbor’s EOD frequency +2 Hz Af -2 Hz 1 min 0 1997 Current Opinion m Neurobiology Electrolocation and jamming avoidance response. (a) figenmannia and Gymnarchus emit EODs from the electric organ in their tail. (b) Distortion of the fish’s electric field in response to an object (dark gray circle) is detected by electroreceptors on the body surface. (c) The top trace depicts a fish’s EOD frequency, displaying a jamming avoidance response, in response to Af (bottom trace), which represents the difference between the fish’s own (ft) and its neighbor’s (f,) EOD frequency. a fish’s own and its neighbor’s EOD field. These two avoidance responses when the amplitude modulation was parameters vary over time at the same frequency, ]Afi, 0.2% and differential-phase modulation was 1 ps. The with different temporal sequences for Af<O and Af> 0 (see most sensitive fish in the study showed weak but accurate Figure Zc,d,e,f). Various behavioral experiments [lO-131 jamming avoidance responses at an amplitude modulation have predicted that the fish’s CNS must be able to detect of 0.02% and a differential-phase modulation of 90ns the modulation time courses of these two parameters (Figure 3). in order to perform a jamming avoidance response. Despite their independent evolution, both Eigenmannia Because both amplitude and differential-phase modulation and Gymnadus have evolved the same computational are necessary for accurate jamming avoidance responses algorithm for the jamming avoidance response [13]. and because the modulation depths for these parameters co-varied in the above experiments, the detection thresh- old for one of these parameters may even be lower than Hyperacuity in the jamming avoidance estimated. The threshold for one of the parameters while response keeping the other suprathreshold has not been tested. The temporal relation between amplitude and differential- phase modulations depicted in Figure Ze,f determines In the behavioral experiments described above [14,15,16”], whether a fish raises or lowers its EOD frequency during a a fish’s response was observed in -30s periods, during jamming avoidance response. Rose and Heiligenberg [ 141 which time each of the amplitude and differential- and Carr et a/. [15] measured the threshold modulation phase sensitive systems may perform temporal averaging. depths of amplitude and differential phase in Eigenmannia. The jamming avoidance response, however, requires the They reduced the diameter of the circular graphs in temporal structure of amplitude and differential-phase Figure Ze,f until the fish failed to respond to a change modulation, which occurs at a rapid rate (-4 Hz); therefore, in the sense of rotation (i.e. the sign of An by shifting any type of temporal averaging over many seconds, their EOD frequencies in the opposite direction. Even which smears the temporal structure of the signal and when the amplitude modulation was 0.1% and the merely detects the presence of amplitude modulation and differential-phase disparity was 400 ns, the fish still shifted differential-phase modulation, could not be employed. their EOD frequencies in the correct direction. Thus, these behavioral experiments suggest that the fish have an internal representation of the temporal pattern Guo and Kawasaki [16**] have recently shown that of extremely small amplitudes and differential-phase Gymnadus exhibits comparable sensitivities. In their modulations. Spatial averaging, however, appears to play experiments, all the fish performed accurate jamming an important role [14]. Sensory hyperacuity Kawasaki 475 Figure 2 (a) (b) Amplitude modulation __---__ Phase modulation (c) (l.0 Af<O Af>O Signal at A Signal at B 0 0 LeadL 0 Lag LeadL 0 Lag Lead Lead Differential phase 0 1997 thnent Opinion in Neurobiology Amplitude modulation and differential-phase modulation-the essential cues of the jamming avoidance response. (a) A mixture of a fish’s own and a neighbor’s EODs creates a beating signal. Amplitude modulation is the periodic change of the signal envelope. Phase modulation is the periodic change of zero-crossing times. Small vertical ticks mark would-be zero-crossing times of the fish’s own signal alone. (b) While the frequency of both of these modulations equals the absolute frequency difference Id, the magnitudes, or depths, of the modulations are a function of intensity ratios between the two signals. For example, the intensity ratios at body areas A and B are different because the fish’s own EOD establishes a radial electric field (long arrows) because of the internal location
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