Sensory hyperacuity in the jamming avoidance ... - web.pdx.edu
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Sensory hyperacuity in the jamming avoidance response of weakly electric fish Masashi Kawasaki
Sensory systems often show remarkable sensitivities to small stimulus parameters. Weakly electric; fish are able to resolve intensity differences of the order of 0.1% and timing differences of the order of nanoseconds during an electrical behavior, the jamming avoidance response. The neuronal origin of this extraordinary sensitivity is being studied within the exceptionally well understood central mechanisms of this behavior.
Addresses Department of Biology, University of Virginia, Gilmer Hall, Charlottesville, Virginia 22903, USA; e-mail: [email protected] Current Opinion in Neurobiology 1997, 7:473-479 http://biomednet.com/elelecref~0959438800700473 0 Current Biology Ltd ISSN 0959-4388 Abbreviations electrosensory lateral line lobe ELL electric organ discharge EOD
Introduction Human psychophysics and animal behavioral studies often reveal the astonishingly high sensitivity of sensory organs to various stimulus parameters [l]. Examples of this include vernier acuity in human vision (5s of arc) [2], interaural time disparity in human audition (6~s) [3], and thermal sensitivity in snakes (O.OOl”C) [4]. These behavioral sensitivities, or hyperacuities, often exceed the resolution of individual sensory receptor neurons by orders of magnitude and, thus, must result from central processing. As hyperacuity often results from many steps of central processing, elucidation of its central mechanisms has been hampered by the absence of ‘transparent’ information systems, in which the flow of pertinent processing can be tracked within the CNS, from sensory receptors to behavioral output. In weakly electric fish, information processing within the central electrosensory and electromotor mechanisms for an electric behavior, the jamming avoidance response, is well understood. Furthermore, this response also demonstrates sensitivities to extremely small stimulus parameters (amplitude fluctuations of less than 0.1% and time disparities in the range of nanoseconds). Thus, weakly electric fish provide a transparent system for examining high sensitivities expressed at the behavioral level. This review focuses on research that examines the central mechanisms of the jamming avoidance response in light of hyperacuity.
The jamming
avoidance
response
The South American weakly electric fish Eigenmannia and the African weakly electric fish Cymnanhus perform electrolocation by generating constant wave-type electric organ discharges (EODs) at individually fixed frequencies (250-600Hz) using the electric organ in their tails. Each cycle of an EOD is triggered by coherent action potentials 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 distortion by objects is detected by electroreceptors on the body surface [5,6] (Figure 1). When two fish with similar EOD frequencies meet, their electrolocation systems jam each other, impairing their ability to electrolocate. To avoid this jamming, they shift their EOD frequencies away from each other in a jamming avoidance response in order to increase the difference in their frequencies [7-91. During the jamming 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 sign of the difference between its own and its neighbor’s EOD frequency: Af=f2-fl, where Af is the frequency difference, and fl and f2 are the fish’s own and its neighbor’s EOD frequency, respectively. Behavioral experiments have demonstrated that a fish determines the sign of 4 solely from the mixture of sensory feedback from its own electric organ and its neighbor’s EODs, without referring to the pacemaker nucleus for information about fl [lO-131. In these studies, the fish’s EODs were silenced by blocking cholinergic synapses at the electric organ and were replaced with artificially generated EODs at arbitrary frequencies. As all the electroreceptors on the body surface are exposed to a mixture of the fish’s own and its neighbor’s EODs, and no receptor is uniquely stimulated by one of them, information about the sign of 4must be computed from a complex mixture of the two stimuli. Two sensory cues that are embedded in this complex mixture have been identified as essential for the calculation of Af-specifically, amplitude modulation and differential-phase modulation, both of which are necessary for a fish to perform a jamming avoidance response. As shown in Figure 2, amplitude modulation is a periodic change of stimulus intensity that results from the beating of two signals. Differential-phase modulation represents small phase differences at different areas of the body that are created by the different spatial geometry of
474
Sensory systems
(a)
Gymnarchus
Electric organ /
Jamming avoidance response
(cl 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 parameters vary over time at the same frequency, ]Afi, with different temporal sequences for Af 0 (see Figure Zc,d,e,f). Various behavioral experiments [lO-131 have predicted that the fish’s CNS must be able to detect the modulation time courses of these two parameters in order to perform a jamming avoidance response. Despite their independent evolution, both Eigenmannia and Gymnadus have evolved the same computational algorithm for the jamming avoidance response [13].
Hyperacuity in the jamming avoidance response The temporal relation between amplitude and differentialphase modulations depicted in Figure Ze,f determines whether a fish raises or lowers its EOD frequency during a jamming avoidance response. Rose and Heiligenberg [ 141 and Carr et a/. [15] measured the threshold modulation depths of amplitude and differential phase in Eigenmannia. They reduced the diameter of the circular graphs in Figure Ze,f until the fish failed to respond to a change in the sense of rotation (i.e. the sign of An by shifting their EOD frequencies in the opposite direction. Even when the amplitude modulation was 0.1% and the differential-phase disparity was 400 ns, the fish still shifted their EOD frequencies in the correct direction. Guo
and
Kawasaki [16**] have recently shown that exhibits comparable sensitivities. In their all the fish performed accurate jamming experiments, Gymnadus
avoidance responses when the amplitude modulation was 0.2% and differential-phase modulation was 1 ps. The most sensitive fish in the study showed weak but accurate jamming avoidance responses at an amplitude modulation of 0.02% and a differential-phase modulation of 90ns (Figure 3). Because both amplitude and differential-phase modulation are necessary for accurate jamming avoidance responses and because the modulation depths for these parameters co-varied in the above experiments, the detection threshold for one of these parameters may even be lower than estimated. The threshold for one of the parameters while keeping the other suprathreshold has not been tested. In the behavioral experiments described above [14,15,16”], a fish’s response was observed in -30s periods, during which time each of the amplitude and differentialphase sensitive systems may perform temporal averaging. The jamming avoidance response, however, requires the temporal structure of amplitude and differential-phase modulation, which occurs at a rapid rate (-4 Hz); therefore, any type of temporal averaging over many seconds, which smears the temporal structure of the signal and merely detects the presence of amplitude modulation and differential-phase modulation, could not be employed. Thus, these behavioral experiments suggest that the fish have an internal representation of the temporal pattern of extremely small amplitudes and differential-phase modulations. Spatial averaging, however, appears to play an important role [14].
Sensory hyperacuity Kawasaki
475
Figure 2
(a)
(b)
Amplitude modulation __---__
Phase modulation
(l.0
(c)
Af>O
AfO. While traces for A and B both show phase modulation, their depths are different, thus creating differential-phase modulation. (e,f) The temporal patterns of these modulations are different for different signs of Af. The amplitude envelope (top traces) and differential phase (bottom traces) both modulate at the same frequency 14, but their temporal relations are different, as revealed by the opposite senses of rotation in the Lissajous graphs depicted on the top right.
Emergence nuclei
of behavioral
accuracies in brain
In Eigenmannia, the chain of neuronal structures involved in the jamming avoidance response has been well characterized physiologically and anatomically [17,18] (Figure 4). Neuronal acuity to amplitude and phase have been measured in the different nuclei involved in the
avoidance response. While behavioral sensitivity to amplitude modulation is largely accomplished at the first brain station, acuity to phase information improves progressively along the neuronal chain.
jamming
Amplitude information is sampled by P-type electroreceptors, which encode stimulus amplitude by the probability
476
Sensory
systems
Fiaure 3
W
(a) Differential-phase modulation: 2.8ps Amplitude modulation: 0.58%
_A0
Differential-phase modulation: 92.6 ns
I
._._Q
-Da
m ’ ’ ’ “,‘I
0.1
m - ’ ’ “,‘I
1 .o
’ v
10
Mean differential-phase modulation @s.)
1 min
0.01
0.1
10
Mean amplitude modulation (%) ,
0 1887 Currenl Opinion in Nsurcbiilogy
Jamming avoidance response of Gymnarchus in hyperacuity conditions. (a) The sense of rotation (Af0) in the circular Lissajous graphs in Figure 2 was switched every 30s (dotted vertical lines). The diameter of the circular graph (i.e. depth of modulation) was made progressively smaller to determine the behavioral thresholds for the modulations. The frequency traces are not averaged; depicted here are the results of a single trial consisting of eight 30 s segments. This particular individual showed weak but correct jamming avoidance responses (JARS) at amplitude modulation of 0.0192% and differential-phase modulation of 92.6 ns. (b) Collective data from eight individuals. Different symbols represent different individuals. Unconnected symbols represent the percentage of correct responses in the eight sessions; connected symbols represent the magnitude of the JAR. Adapted from [16*‘1.
of firing of action potentials. Although the responses of P-type electroreceptor afferents to a very small amplitude modulation have not been recorded, Scheich et a/. [19] have reported that a step increase of stimulus amplitude by a factor of 4% induced an additional single action potential in a primary afferent fiber that was firing at -SOspikes/s. Taking noise and fluctuations in firing probability into consideration, representation of amplitude modulation at a level of 0.1% in an individual P-type afferent fiber is weak. The primary afferent fibers from P-type electroreceptors project to the basilar pyramidal cells via direct excitatory connections and to nonbasilar pyramidal cells via indirect inhibitory connections in the electrosensory lateral line lobe (ELL) in the medulla [ZO]. Shumway [Zl] measured the threshold of both types of pyramidal cells in the ELL. The mean threshold of neurons in the most sensitive subdivision of the ELL (lateral map) was -3%, and the most sensitive neuron’s threshold was 0.3%. In a closely related gymnotiform fish, Apteronotus, which also perform jamming avoidance responses, both basilar and nonbasilar pyramidal cells gave good responses to amplitude modulation of 0.3%, which was the smallest amplitude modulation tested [Z?]. Sensitivity to amplitude modulation at this first sensory processing stage seems to be remarkably improved over that of primary afferents. This large increase of sensitivity requires (statistically) a lbfold larger sample size. This is probably achieved by
anatomical convergence of afferent fibers to ELL neurons [ZZ]. Descending pathways from the midbrain nucleus back to the ELL appear to have no effect on sensitivity enhancement in ELL neurons [23,24]. These ELL neurons project to the torus semicircularis (torus hereafter) in the midbrain [25,26]. When Rose and Heiligenberg [27] examined the threshold for amplitude modulation in amplitude-sensitive neurons in the torus, they found that the median was 2%, and the most sensitive of 28 neurons showed a threshold response to 0.1% of amplitude modulation. Thus, there appear to be small improvements of amplitude sensitivity in this nucleus. Whereas amplitude sensitivity (as demonstrated at the behavioral level) is achieved largely at earlier stages in the neuronal chain, sensitivity to phase is improved progressively, involving many nuclei (as described below). Phase, or zero-crossing time of sensory signals, is sampled by T-type electroreceptors, which fire one action potential at each zero-crossing of the signal [19]. Afferents from T-type electroreceptors terminate on the spherical cells in the medulla, which in turn project to giant cells in the torus. As these cells are phase-lockedthat is, they respond with one action potential to a particular phase of one cycle of sensory stimulithe phase of the sensory signal is represented by action potential times of giant
Sensory hyperacuity Kawasaki
/
Pacemaker
477
nucleus
Nucleus electrosensorius Prepacemaker nucleus
Sublemniscal prepacemaker nucleus
\ Primary afferents from electroreceptors
0 1997 Current Opinm
Brain nuclei involved in the jamming avoidance
response
of Eigenmannia. The physiological
properties
in Neurobiology
of some of these neurons have
been reported: electric organ/behavior [14,15,16’*1; primary afferents from electroreceptors 1191; sublemniscal prepacemaker nucleus 1321; prepacemaker nucleus [36]; nucleus electrosensorius [31]; torus semicircularis 127-301; electrosensory lateral line lobe (ELL) [21,22,27-301.
neurons in the torus. Carr eta/. [ 151 measured the accuracy of action potentials in these phase-locked neurons and showed that it progressively improved due to anatomical convergence. While the T-type afferents show average jitter of -30 ps (range of 10-100 s), jitter of midbrain neurons was -11 ps, on average (range of 4-32 s). Phase differences between giant cells and inputs from spherical cells are detected by small cells in the torus, which project to other differential-phase-sensitive neurons [Z&29]. When Rose and Heiligenberg [30] examined the threshold for differential-phase modulation in differential-phase-sensitive neurons in the torus, they found that the threshold median was lops, and the most sensitive of 37 neurons showed a threshold response to 6ps of differential-phase modulation. These differential-phase-sensitive neurons encode the time course of differential-phase modulation by their timing of action potential bursts. Thus, temporal encoding is not constrained by the timing accuracy of individual action potentials, allowing higher-order neurons to further improve accuracy. Neurons
in the torus that are sensitive to the sign of projections from amplitude-sensitive neurons and differential-phase-sensitive neurons [27], but the scarcity of such neurons and the difficulty of recording from them prevent examination of their sensory threshold [31]. Neurons in the subsequent processing area, the nucleus electrosensorius, have been recorded under hyperacuity conditions. Neurons in this nucleus discriminate the sign of Af, even when amplitude modulation is
-0.2% and differential-phase modulation is -1 ps [31]. In the one of two final nuclei for jamming avoidance response processing [32], the prepacemaker nucleus [33-3.51, individual neurons are almost as accurate as the behavioral output [36], culminating in the improvement of the accuracy for small modulations along the neuronal chain.
Mechanisms
of differential-phase
comparison
Although we know that small cells in the torus extract differential-phase information in Eigenmannia [29,37], little is known about the cellular mechanisms of differentialphase detection. How do small cells detect time disparities of microseconds from phase-locked action potentials of longer duration! The small size of the neurons in the torus has precluded routine intracellular recordings so that postsynaptic potential could be studied. In a context of comparative studies [38*,39], Kawasaki and Guo [40**] discovered a phase comparison circuitry in the medullary structure of Gymnanh, in which neurons are also sensitive to differential-phase modulation in the range of microseconds and are relatively large (12-15 pm).
4 have convergent
In my laboratory, we are using in oivo whole-cell recordings to measure postsynaptic potentials in neurons that receive phase-locked inputs and are sensitive to differential phase. We have also described the complex response dynamics of these neurons [40**], suggesting that differential-phase comparison is performed not only by simple coincidence detection but also by a complex adaptation mechanism. In
478
Sensory systems
a recent paper [16”], we showed that phase accuracy of primary afferent fibers is somewhat better in Gymnarzhs (-6~s) than in Eigenmannia (-3Ops), reflecting the fact that differential-phase computation is performed one step earlier in Gymnadus.
Temporal hyperacuity
in other systems
Mormyrid electric fish use temporal information in the range of microseconds for species and individual recognition [41]. The neuronal mechanisms for temporal analysis in these species show interesting parallels with Eigenmannia and Gymnarchs [39,42-114]. Remarkable sensitivity (-5 nV/cm) to low-frequency electrosensory signals has also been reported in elasmobranch fish [45], but nothing is known about the central mechanisms for this hyperacuity. Two specialists in audition, echolocating bats and the barn owl, are of particular interest in examining hyperacuity. Simmons et a/. [46] reported that the threshold for echo delay detection is as small as 12 ns in an echolocating bat. They propose that neurons in the inferior colliculus deal with the very small temporal signals by time expansion in which nanosecond temporal codes are expressed by multiple unit potentials of millisecond range [47,48’]. Barn owls can localize a sound source in elevation using interaural intensity differences and in azimuth using interaural time differences; in behavioral experiments, Knudsen, Blasdel and Konishi (491 determined that the accuracy of localizing sound is approximately 2” both in elevation and azimuth. These values correspond roughly to interaural intensity difference of 5% and interaural time differences of -5 ps [SO].
Condusions The study of the electrosensory system of weakly electric fish shows how sensory acuity expressed in behavior is shaped along a neuronal chain of processing areas. While amplitude sensitivity is largely accomplished by one processing area (the ELL), sensitivity to small phase differences emerges from successive processing by many brain areas. This difference reflects perhaps a difference in the complexity of neuronal processing for these two parameters. Persistence of the electrical behavior and accessibility of all involved brain nuclei in neurophysiological preparations of electric fish have greatly facilitated a systems-level analysis of behavioral hyperacuity, which could not be accomplished by studying individual steps of neuronal processing in reduced preparations. Our understanding of the neuronal mechanisms for hyperacuity is limited, however, in two ways. First, we have not expIained how signals of small magnitude are processed within each component neuron, because postsynaptic potentials for subthreshold signals have been difficult to record. Second, more detailed studies are needed to determine the anatomy of neuronal connections, particularly those beyond the midbrain.
These two limitations are attributable to difficulties of standard intracellular recording and labeling in the small neurons of the fish brain. Recently, however, in &JO whole-cell recording techniques [Sl’], which allow long-term intracellular recording of postsynaptic potentials and reliable tract tracing, have been applied successfully in electrosensory systems and hold much promise for further study. Future studies of the detailed mechanisms of the jamming avoidance response should continue to provide fruitful ground for understanding not only hyperacuity but also the neural substrate of behavior in general.
Acknowledgements Work reported from the author’s laboratory was supported by National Insritutes of Health grants RZ9MH48115-05 and K02MH01256-01. I thank Cameron McLaughlin for editing my English and Yasuko Kawasaki for preparation of the figures.
References
and recommended
reading
Papers of particular interest, published within the annual period of review, have been highlighted as: . l
0
of special interest of outstanding interest
1.
Autrum H: Performance limits of sensory organs. lnterdisciplin Sci Rev 1966, 13:27-39.
2.
Westheimer G: Visual hyperacuity. 1 :l -30.
3.
Tobias JV: Curious binaural phenomena In Foundations of Modern Auditory Theory, vol 2. Edited by Tobias JV. New York: Academic Press; 1972:465-466.
4.
De Cock Buning T: Threshold of infrared sensitive tectal neurons in Python retiw/atus, Boa wnstrictor and Agkistrvdon rhodostcme. J Comp Physioll983, 151:461-467.
5.
Bastian J: EIectrolocatIon. Behavior, anatomy, and physlology. In Electroreception. Edited by Bullock TH, Heiligenberg W. New York: Wiley & Sons; 1966:577-612.
6.
Lissmann HW, Machin KE: The mechanism of object location in Gymnarchus nilotiws and similar fish. J Exp Biol 1956, 35:451466.
7.
Watanabe A, Takeda K: The change of discharge frequency by AC. stimulus in a weakly electric fish. J Exp Biol 1963, 40:5766.
6.
Heiiigenberg W: Principles of Electrolocation and Jamming Avoidance in E/e&c Fish -A Neuroethological Approach, vol I. New York: Springer-Vet-lag; 1977.
9.
Bullock TH, Hamstra RH, Scheich H: The jamming avoidance response of high frequency electric fish. I. General features. J Comp Physioll972, 77~1-22.
10.
Heiiigenberg W, Baker C, Matsubara J: The jamming avoidance response in Eigenmennia revisited: the structure of a neuronal democracy. J Comp Physioll976, 127:267-266.
11.
Heiligenberg W, Bastian J: The control of Eigenmennids pacemaker by distributed evaluation of electroreceptive afferences. J Comp Physioll960, 136:113-l 33.
12.
Bastian J, Heiligenberg W: Neural correlates of the jamming avoidance response in Eigenmannia. J Comp Physioll960, 136:135-l 52.
13.
Kawasaki M: Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish, Gymnanhus nilotiws. J Comp Physiol 1993, 173:9-22.
14.
Rose GJ, Heiiigenberg W: Temporal hyperacuity sense of fish. Nature 1965, 316:176-l 60.
15.
Carr CE. Heiligenberg W, Rose GJ: A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology. J Neurosci 1966, 6:107-l 19.
Prog Sensory Physioll961,
in the electric
Sensory
16.
Guo Y. Kawasaki M: Repreoentetlon of accurate temooral information in the electrosensory system of the Af&an electric fish, Gymnarchus niloticus. J Neurosci 1997, 17:1761-l 768. The acuity of the phase processing system in Gymnarc!tus was measured usina hiahlv orecise stimulus and recordinn methods. The iitter of ohaselooked ~ou&s was -6~s. The stability 07 the electric organ discharges was also measured and their jitter was less than 1 ps. This stability of electric organ discharge, however, is not required for hyperacuity.
..
1 7.
Heiligenberg W: Neural Ners in Electric Fish. Cambridge, Massachusetts: MIT Press; 1991.
18.
Heiligenberg W: Jamming avoidance responses: model systems for neuroethology. In Elecfroreception. Edited by Bullock TH, Heiligenberg W. New York: Wiley & Sons; 1986:613649.
19.
Scheich H, Bullock TH, Hamstra RH: Coding properties of two classes of afferent nerve fibers: high-frequency electroreceptors in the electric fish, Eigenmacnia. J Neurophysiol 1973, 36:39-60.
20.
Maler L, Sas E, Rogers J: The cytology of the posterior lateral line lobe of high frequency weekly electric fish (Gymnotidee). Dendritic differentiation and synaptic specificity in a simple cortex. J Comp Neural 1981, 195:67-139.
21.
Shumway CA: Multiple electrosensory maps in the medulla of weakly electric gymnotlform fish. I. Physiological differences. J Neurosci 1989, g:4368-4399.
22.
Bastion J: Electrolocation. II. The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells in Apteronotus a/bifrons. J Comp Physiol 1961, 144:481-494.
23.
Bastian J, Bratton B: Descending control of electroreception. I. Properties of nucleus praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe. J Neurosci 1990, IO:1 226-l 240.
24.
25.
Bastian J: Gain control in the electrosensory by descending inputs to the electrosenoory J Neurosci 1906, 6:553-562.
system mediated lateral line lobe.
Carr CE, Maler L, Heiligenberg W, Sas E: Laminar organization of the afferent and efferent systems of the torus semicircularis of Gymnotlform fish: morphological substrates for parallel processing in the electrosensory system. J Comp Neural 1961, 203:649-670.
35.
hyperacuityKawasaki
Kawasaki M: Comperetlve studies on the motor control mechanisms for electro-communicetfon in gymnotiform J Comp Physioll993, 173:726-728.
479
fishes,
36.
Kawasaki M, Rose GJ, Heiligenberg W: Temporel hypemcuity in single neurons of electric fish. Nature 1988, 336:173-l 76.
37.
Heiligenberg W, Rose G: phase end amplitude computetfons in the midbrein of an electric fish: intracellular studies of neurons partlclpetlng In the jamming evoldance response of Eigenmannia. J Neurosci 1965,5:515-531.
38. .
Kawasaki M: Comparative analysis of the jamming avoidance response in Africen and South Amerlcen wave-type flshen Biol Bull 1996, 191 :103-108. Two phylogenetically unrelated groups of fishes perform electrolocation. Not only do they share this basic function, but both fishes perform jamming avoidance responses of identical form. Moreover, they share rather complex computational algorithms. Different brain areas, however, are used to perform a certain step of neuronal computation. Comparative implications are discussed. 39.
Hopkins C: Convergent designs for electrogenesls end electroreception. Curr Opin Neurobiol 1995, 5:769-777.
40. ..
Kawasaki M, Guo Y-X: Neuronal circuitry for comperison of timing in the electrosensory lateral line lobe of an Afrlcen wave-type electric fish, Gymnanzhus niloticus. J Neurosci 1996, 16:300-391. Intracellular recording and labeling were performed in a neural circuit that detects ohase differences in the microsecond raoae. Phase-locked neurons spread &on terminals in both halves of a medulltistructure, the electrosensory lateral line lobe. Neurons sensitive to phase differences are found in the inner cellular layer of this structure. These neurons respond to changes in smell phase differences, but ignore steady-state differences in phase. 41.
Hopkins CD, Bass AH: Temporal coding of species recognition signals in an electric fish. Science 19131, 21265-87.
42.
Friedman MA, Hopkins CS: Neural substrate for species recognition in the time-coding elecbosensory pathway of mormyrid electric fish J Neurosci 1997. in press.
43.
Amagai S, Friedman MA, Hopkins CD: Time-coding in the midbrain of mormyrid electric fish. I. physiology end anatomy of cells in the nucleus exterolateralis pars anterior (ELa). J Comp Physiol IA] 1997, in press.
44.
Amagai S: Time-coding in the midbrain of mormyrid electric fish. II. Stimulus selectivity in the nucleus exterolaterelis pars posterior (ELp). J Comp Physiol fAj 1997, in press.
26.
Shumway CA: Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. II. Anatomical differences. J Neurosci 1989, 9:4400-4415.
45.
Kalmijn A: Electric and magnetic field detection in elasmobranch fishes. Science 1982, 218:916-918.
46.
27.
Rose GJ, Heiligenberg W: Neural coding of difference frequencies in the midbrain of the electric fish Eigenmannia: reading the sense of rotation in en amplitude-phese plane. J Comp Physiol 1966, 159:613-624.
Simmons J, Ferragamo M, Moss C, Stevenson S, Altes R: Discrimination of jittered sonar echoes by the echolocating bat Eptesicus fuscus: the shape of terget images in echolocation. J Comp Physiol IA1 1990, 167:569-616.
47.
28.
Bastian J, Heiligenberg W: Phase-sensitive midbrain neurons In Eigenmannia: neural correlates of the jamming avoidance response. Science 1980, 209:826-831.
Simmons J, Saillant P, Ferragamo M, Haresign T, Dear S, Fritz J, McMullen T: Auditory computations for biosonar target imaging in bats. In Auditory Computation. Springer Handbook of Auditory Research Edited by Hawkins H, McMullen T, Popper A, Fay R. New York: Springer-Verlag; 1995:401-468.
29.
Carr CE. Maler L. Tavlor , B: A time-comoarison circuit in the electric fish midbrain. II. Functional morphology. J Neurosci 1986, 6:1372-l 363.
30.
Rose GJ, Heiligenberg W: Limits of phase and amplitude sensitivity in the torus semlcirculsris of Eigenmannia. J Comp Physiol IA1 1986, 15g:al3-822.
31.
Keller CH: Stimulus discrimination In the diencephalon of Eigenmannia: the emergence and sharpening of a sensory filter. J Comp Physioll996, t62:747-757.
32.
Metzner W: The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways. J Neurosci i 993, 13:i 862-i 878.
33.
34.
Kawasaki M, Maler L, Rose GJ, Heiligenberg W: Anatomical and functlonel organization of the prepacemaker nucleus in gymnotiform electric fish: the accommodation of two behaviors in one nucleus. J Comp Neural 1988, 276:113-l 31. Kawasaki M, Heiligenberg W: Different classes of glutamate receptors and GABA medlate distinct modulations In the firing pattern of a neuronal oscllletor, the medullary pacemaker of gymnotlform electric flsh. J Neurosci 1990, 10:3896-3904.
48. .
Simmons J, Dear S, Ferragamo M, Haresign T, Fritz J: Representation of perceptual dimensions of insect prey during terminal pursuit by echolocating bats. Biol Bull 1996, 191 :I 09121. On the basis of multiunit recording data in the inferior colliculus of a bat, Eptesicus, the authors have developed a new theory that bats’ hyperacuity is endowed by time expansion. Latency of multiple unit response peaks to pulse-echo pairs changes by l OO-200~s as echo delay changes by about 5 us. 49.
Knudsen El, Blasdel GG, Konishi M: Sound localization barn owl (Tyto a/be). J Comp Physiol 1979, 133:13-21.
50.
Brainard MS, Knudsen El, Esterty SD: Neural derivation of sound source location: resolution of spatial ambiguities in binaural cues. J Acoust Sot Am 1992, 91 :1015-l 027
51. .
by the
Rose G, Fortune E: New techniques for making whole-cell recordings from CNS neurons in ho. Neurosci Res 1996, 26:89-94. A whole-cell recording technique using patch-clamp pipettes is refined for in viva preparation of electric fish. This method permits long-term recording of synaptic potentials as well as action potentials in preparations showing electrical behavior.
Sensory hyperacuity in the jamming avoidance response of weakly electric fish Masashi Kawasaki
Sensory systems often show remarkable sensitivities to small stimulus parameters. Weakly electric; fish are able to resolve intensity differences of the order of 0.1% and timing differences of the order of nanoseconds during an electrical behavior, the jamming avoidance response. The neuronal origin of this extraordinary sensitivity is being studied within the exceptionally well understood central mechanisms of this behavior.
Addresses Department of Biology, University of Virginia, Gilmer Hall, Charlottesville, Virginia 22903, USA; e-mail: [email protected] Current Opinion in Neurobiology 1997, 7:473-479 http://biomednet.com/elelecref~0959438800700473 0 Current Biology Ltd ISSN 0959-4388 Abbreviations electrosensory lateral line lobe ELL electric organ discharge EOD
Introduction Human psychophysics and animal behavioral studies often reveal the astonishingly high sensitivity of sensory organs to various stimulus parameters [l]. Examples of this include vernier acuity in human vision (5s of arc) [2], interaural time disparity in human audition (6~s) [3], and thermal sensitivity in snakes (O.OOl”C) [4]. These behavioral sensitivities, or hyperacuities, often exceed the resolution of individual sensory receptor neurons by orders of magnitude and, thus, must result from central processing. As hyperacuity often results from many steps of central processing, elucidation of its central mechanisms has been hampered by the absence of ‘transparent’ information systems, in which the flow of pertinent processing can be tracked within the CNS, from sensory receptors to behavioral output. In weakly electric fish, information processing within the central electrosensory and electromotor mechanisms for an electric behavior, the jamming avoidance response, is well understood. Furthermore, this response also demonstrates sensitivities to extremely small stimulus parameters (amplitude fluctuations of less than 0.1% and time disparities in the range of nanoseconds). Thus, weakly electric fish provide a transparent system for examining high sensitivities expressed at the behavioral level. This review focuses on research that examines the central mechanisms of the jamming avoidance response in light of hyperacuity.
The jamming
avoidance
response
The South American weakly electric fish Eigenmannia and the African weakly electric fish Cymnanhus perform electrolocation by generating constant wave-type electric organ discharges (EODs) at individually fixed frequencies (250-600Hz) using the electric organ in their tails. Each cycle of an EOD is triggered by coherent action potentials 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 distortion by objects is detected by electroreceptors on the body surface [5,6] (Figure 1). When two fish with similar EOD frequencies meet, their electrolocation systems jam each other, impairing their ability to electrolocate. To avoid this jamming, they shift their EOD frequencies away from each other in a jamming avoidance response in order to increase the difference in their frequencies [7-91. During the jamming 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 sign of the difference between its own and its neighbor’s EOD frequency: Af=f2-fl, where Af is the frequency difference, and fl and f2 are the fish’s own and its neighbor’s EOD frequency, respectively. Behavioral experiments have demonstrated that a fish determines the sign of 4 solely from the mixture of sensory feedback from its own electric organ and its neighbor’s EODs, without referring to the pacemaker nucleus for information about fl [lO-131. In these studies, the fish’s EODs were silenced by blocking cholinergic synapses at the electric organ and were replaced with artificially generated EODs at arbitrary frequencies. As all the electroreceptors on the body surface are exposed to a mixture of the fish’s own and its neighbor’s EODs, and no receptor is uniquely stimulated by one of them, information about the sign of 4must be computed from a complex mixture of the two stimuli. Two sensory cues that are embedded in this complex mixture have been identified as essential for the calculation of Af-specifically, amplitude modulation and differential-phase modulation, both of which are necessary for a fish to perform a jamming avoidance response. As shown in Figure 2, amplitude modulation is a periodic change of stimulus intensity that results from the beating of two signals. Differential-phase modulation represents small phase differences at different areas of the body that are created by the different spatial geometry of
474
Sensory systems
(a)
Gymnarchus
Electric organ /
Jamming avoidance response
(cl 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 parameters vary over time at the same frequency, ]Afi, with different temporal sequences for Af 0 (see Figure Zc,d,e,f). Various behavioral experiments [lO-131 have predicted that the fish’s CNS must be able to detect the modulation time courses of these two parameters in order to perform a jamming avoidance response. Despite their independent evolution, both Eigenmannia and Gymnadus have evolved the same computational algorithm for the jamming avoidance response [13].
Hyperacuity in the jamming avoidance response The temporal relation between amplitude and differentialphase modulations depicted in Figure Ze,f determines whether a fish raises or lowers its EOD frequency during a jamming avoidance response. Rose and Heiligenberg [ 141 and Carr et a/. [15] measured the threshold modulation depths of amplitude and differential phase in Eigenmannia. They reduced the diameter of the circular graphs in Figure Ze,f until the fish failed to respond to a change in the sense of rotation (i.e. the sign of An by shifting their EOD frequencies in the opposite direction. Even when the amplitude modulation was 0.1% and the differential-phase disparity was 400 ns, the fish still shifted their EOD frequencies in the correct direction. Guo
and
Kawasaki [16**] have recently shown that exhibits comparable sensitivities. In their all the fish performed accurate jamming experiments, Gymnadus
avoidance responses when the amplitude modulation was 0.2% and differential-phase modulation was 1 ps. The most sensitive fish in the study showed weak but accurate jamming avoidance responses at an amplitude modulation of 0.02% and a differential-phase modulation of 90ns (Figure 3). Because both amplitude and differential-phase modulation are necessary for accurate jamming avoidance responses and because the modulation depths for these parameters co-varied in the above experiments, the detection threshold for one of these parameters may even be lower than estimated. The threshold for one of the parameters while keeping the other suprathreshold has not been tested. In the behavioral experiments described above [14,15,16”], a fish’s response was observed in -30s periods, during which time each of the amplitude and differentialphase sensitive systems may perform temporal averaging. The jamming avoidance response, however, requires the temporal structure of amplitude and differential-phase modulation, which occurs at a rapid rate (-4 Hz); therefore, any type of temporal averaging over many seconds, which smears the temporal structure of the signal and merely detects the presence of amplitude modulation and differential-phase modulation, could not be employed. Thus, these behavioral experiments suggest that the fish have an internal representation of the temporal pattern of extremely small amplitudes and differential-phase modulations. Spatial averaging, however, appears to play an important role [14].
Sensory hyperacuity Kawasaki
475
Figure 2
(a)
(b)
Amplitude modulation __---__
Phase modulation
(l.0
(c)
Af>O
AfO. While traces for A and B both show phase modulation, their depths are different, thus creating differential-phase modulation. (e,f) The temporal patterns of these modulations are different for different signs of Af. The amplitude envelope (top traces) and differential phase (bottom traces) both modulate at the same frequency 14, but their temporal relations are different, as revealed by the opposite senses of rotation in the Lissajous graphs depicted on the top right.
Emergence nuclei
of behavioral
accuracies in brain
In Eigenmannia, the chain of neuronal structures involved in the jamming avoidance response has been well characterized physiologically and anatomically [17,18] (Figure 4). Neuronal acuity to amplitude and phase have been measured in the different nuclei involved in the
avoidance response. While behavioral sensitivity to amplitude modulation is largely accomplished at the first brain station, acuity to phase information improves progressively along the neuronal chain.
jamming
Amplitude information is sampled by P-type electroreceptors, which encode stimulus amplitude by the probability
476
Sensory
systems
Fiaure 3
W
(a) Differential-phase modulation: 2.8ps Amplitude modulation: 0.58%
_A0
Differential-phase modulation: 92.6 ns
I
._._Q
-Da
m ’ ’ ’ “,‘I
0.1
m - ’ ’ “,‘I
1 .o
’ v
10
Mean differential-phase modulation @s.)
1 min
0.01
0.1
10
Mean amplitude modulation (%) ,
0 1887 Currenl Opinion in Nsurcbiilogy
Jamming avoidance response of Gymnarchus in hyperacuity conditions. (a) The sense of rotation (Af0) in the circular Lissajous graphs in Figure 2 was switched every 30s (dotted vertical lines). The diameter of the circular graph (i.e. depth of modulation) was made progressively smaller to determine the behavioral thresholds for the modulations. The frequency traces are not averaged; depicted here are the results of a single trial consisting of eight 30 s segments. This particular individual showed weak but correct jamming avoidance responses (JARS) at amplitude modulation of 0.0192% and differential-phase modulation of 92.6 ns. (b) Collective data from eight individuals. Different symbols represent different individuals. Unconnected symbols represent the percentage of correct responses in the eight sessions; connected symbols represent the magnitude of the JAR. Adapted from [16*‘1.
of firing of action potentials. Although the responses of P-type electroreceptor afferents to a very small amplitude modulation have not been recorded, Scheich et a/. [19] have reported that a step increase of stimulus amplitude by a factor of 4% induced an additional single action potential in a primary afferent fiber that was firing at -SOspikes/s. Taking noise and fluctuations in firing probability into consideration, representation of amplitude modulation at a level of 0.1% in an individual P-type afferent fiber is weak. The primary afferent fibers from P-type electroreceptors project to the basilar pyramidal cells via direct excitatory connections and to nonbasilar pyramidal cells via indirect inhibitory connections in the electrosensory lateral line lobe (ELL) in the medulla [ZO]. Shumway [Zl] measured the threshold of both types of pyramidal cells in the ELL. The mean threshold of neurons in the most sensitive subdivision of the ELL (lateral map) was -3%, and the most sensitive neuron’s threshold was 0.3%. In a closely related gymnotiform fish, Apteronotus, which also perform jamming avoidance responses, both basilar and nonbasilar pyramidal cells gave good responses to amplitude modulation of 0.3%, which was the smallest amplitude modulation tested [Z?]. Sensitivity to amplitude modulation at this first sensory processing stage seems to be remarkably improved over that of primary afferents. This large increase of sensitivity requires (statistically) a lbfold larger sample size. This is probably achieved by
anatomical convergence of afferent fibers to ELL neurons [ZZ]. Descending pathways from the midbrain nucleus back to the ELL appear to have no effect on sensitivity enhancement in ELL neurons [23,24]. These ELL neurons project to the torus semicircularis (torus hereafter) in the midbrain [25,26]. When Rose and Heiligenberg [27] examined the threshold for amplitude modulation in amplitude-sensitive neurons in the torus, they found that the median was 2%, and the most sensitive of 28 neurons showed a threshold response to 0.1% of amplitude modulation. Thus, there appear to be small improvements of amplitude sensitivity in this nucleus. Whereas amplitude sensitivity (as demonstrated at the behavioral level) is achieved largely at earlier stages in the neuronal chain, sensitivity to phase is improved progressively, involving many nuclei (as described below). Phase, or zero-crossing time of sensory signals, is sampled by T-type electroreceptors, which fire one action potential at each zero-crossing of the signal [19]. Afferents from T-type electroreceptors terminate on the spherical cells in the medulla, which in turn project to giant cells in the torus. As these cells are phase-lockedthat is, they respond with one action potential to a particular phase of one cycle of sensory stimulithe phase of the sensory signal is represented by action potential times of giant
Sensory hyperacuity Kawasaki
/
Pacemaker
477
nucleus
Nucleus electrosensorius Prepacemaker nucleus
Sublemniscal prepacemaker nucleus
\ Primary afferents from electroreceptors
0 1997 Current Opinm
Brain nuclei involved in the jamming avoidance
response
of Eigenmannia. The physiological
properties
in Neurobiology
of some of these neurons have
been reported: electric organ/behavior [14,15,16’*1; primary afferents from electroreceptors 1191; sublemniscal prepacemaker nucleus 1321; prepacemaker nucleus [36]; nucleus electrosensorius [31]; torus semicircularis 127-301; electrosensory lateral line lobe (ELL) [21,22,27-301.
neurons in the torus. Carr eta/. [ 151 measured the accuracy of action potentials in these phase-locked neurons and showed that it progressively improved due to anatomical convergence. While the T-type afferents show average jitter of -30 ps (range of 10-100 s), jitter of midbrain neurons was -11 ps, on average (range of 4-32 s). Phase differences between giant cells and inputs from spherical cells are detected by small cells in the torus, which project to other differential-phase-sensitive neurons [Z&29]. When Rose and Heiligenberg [30] examined the threshold for differential-phase modulation in differential-phase-sensitive neurons in the torus, they found that the threshold median was lops, and the most sensitive of 37 neurons showed a threshold response to 6ps of differential-phase modulation. These differential-phase-sensitive neurons encode the time course of differential-phase modulation by their timing of action potential bursts. Thus, temporal encoding is not constrained by the timing accuracy of individual action potentials, allowing higher-order neurons to further improve accuracy. Neurons
in the torus that are sensitive to the sign of projections from amplitude-sensitive neurons and differential-phase-sensitive neurons [27], but the scarcity of such neurons and the difficulty of recording from them prevent examination of their sensory threshold [31]. Neurons in the subsequent processing area, the nucleus electrosensorius, have been recorded under hyperacuity conditions. Neurons in this nucleus discriminate the sign of Af, even when amplitude modulation is
-0.2% and differential-phase modulation is -1 ps [31]. In the one of two final nuclei for jamming avoidance response processing [32], the prepacemaker nucleus [33-3.51, individual neurons are almost as accurate as the behavioral output [36], culminating in the improvement of the accuracy for small modulations along the neuronal chain.
Mechanisms
of differential-phase
comparison
Although we know that small cells in the torus extract differential-phase information in Eigenmannia [29,37], little is known about the cellular mechanisms of differentialphase detection. How do small cells detect time disparities of microseconds from phase-locked action potentials of longer duration! The small size of the neurons in the torus has precluded routine intracellular recordings so that postsynaptic potential could be studied. In a context of comparative studies [38*,39], Kawasaki and Guo [40**] discovered a phase comparison circuitry in the medullary structure of Gymnanh, in which neurons are also sensitive to differential-phase modulation in the range of microseconds and are relatively large (12-15 pm).
4 have convergent
In my laboratory, we are using in oivo whole-cell recordings to measure postsynaptic potentials in neurons that receive phase-locked inputs and are sensitive to differential phase. We have also described the complex response dynamics of these neurons [40**], suggesting that differential-phase comparison is performed not only by simple coincidence detection but also by a complex adaptation mechanism. In
478
Sensory systems
a recent paper [16”], we showed that phase accuracy of primary afferent fibers is somewhat better in Gymnarzhs (-6~s) than in Eigenmannia (-3Ops), reflecting the fact that differential-phase computation is performed one step earlier in Gymnadus.
Temporal hyperacuity
in other systems
Mormyrid electric fish use temporal information in the range of microseconds for species and individual recognition [41]. The neuronal mechanisms for temporal analysis in these species show interesting parallels with Eigenmannia and Gymnarchs [39,42-114]. Remarkable sensitivity (-5 nV/cm) to low-frequency electrosensory signals has also been reported in elasmobranch fish [45], but nothing is known about the central mechanisms for this hyperacuity. Two specialists in audition, echolocating bats and the barn owl, are of particular interest in examining hyperacuity. Simmons et a/. [46] reported that the threshold for echo delay detection is as small as 12 ns in an echolocating bat. They propose that neurons in the inferior colliculus deal with the very small temporal signals by time expansion in which nanosecond temporal codes are expressed by multiple unit potentials of millisecond range [47,48’]. Barn owls can localize a sound source in elevation using interaural intensity differences and in azimuth using interaural time differences; in behavioral experiments, Knudsen, Blasdel and Konishi (491 determined that the accuracy of localizing sound is approximately 2” both in elevation and azimuth. These values correspond roughly to interaural intensity difference of 5% and interaural time differences of -5 ps [SO].
Condusions The study of the electrosensory system of weakly electric fish shows how sensory acuity expressed in behavior is shaped along a neuronal chain of processing areas. While amplitude sensitivity is largely accomplished by one processing area (the ELL), sensitivity to small phase differences emerges from successive processing by many brain areas. This difference reflects perhaps a difference in the complexity of neuronal processing for these two parameters. Persistence of the electrical behavior and accessibility of all involved brain nuclei in neurophysiological preparations of electric fish have greatly facilitated a systems-level analysis of behavioral hyperacuity, which could not be accomplished by studying individual steps of neuronal processing in reduced preparations. Our understanding of the neuronal mechanisms for hyperacuity is limited, however, in two ways. First, we have not expIained how signals of small magnitude are processed within each component neuron, because postsynaptic potentials for subthreshold signals have been difficult to record. Second, more detailed studies are needed to determine the anatomy of neuronal connections, particularly those beyond the midbrain.
These two limitations are attributable to difficulties of standard intracellular recording and labeling in the small neurons of the fish brain. Recently, however, in &JO whole-cell recording techniques [Sl’], which allow long-term intracellular recording of postsynaptic potentials and reliable tract tracing, have been applied successfully in electrosensory systems and hold much promise for further study. Future studies of the detailed mechanisms of the jamming avoidance response should continue to provide fruitful ground for understanding not only hyperacuity but also the neural substrate of behavior in general.
Acknowledgements Work reported from the author’s laboratory was supported by National Insritutes of Health grants RZ9MH48115-05 and K02MH01256-01. I thank Cameron McLaughlin for editing my English and Yasuko Kawasaki for preparation of the figures.
References
and recommended
reading
Papers of particular interest, published within the annual period of review, have been highlighted as: . l
0
of special interest of outstanding interest
1.
Autrum H: Performance limits of sensory organs. lnterdisciplin Sci Rev 1966, 13:27-39.
2.
Westheimer G: Visual hyperacuity. 1 :l -30.
3.
Tobias JV: Curious binaural phenomena In Foundations of Modern Auditory Theory, vol 2. Edited by Tobias JV. New York: Academic Press; 1972:465-466.
4.
De Cock Buning T: Threshold of infrared sensitive tectal neurons in Python retiw/atus, Boa wnstrictor and Agkistrvdon rhodostcme. J Comp Physioll983, 151:461-467.
5.
Bastian J: EIectrolocatIon. Behavior, anatomy, and physlology. In Electroreception. Edited by Bullock TH, Heiligenberg W. New York: Wiley & Sons; 1966:577-612.
6.
Lissmann HW, Machin KE: The mechanism of object location in Gymnarchus nilotiws and similar fish. J Exp Biol 1956, 35:451466.
7.
Watanabe A, Takeda K: The change of discharge frequency by AC. stimulus in a weakly electric fish. J Exp Biol 1963, 40:5766.
6.
Heiiigenberg W: Principles of Electrolocation and Jamming Avoidance in E/e&c Fish -A Neuroethological Approach, vol I. New York: Springer-Vet-lag; 1977.
9.
Bullock TH, Hamstra RH, Scheich H: The jamming avoidance response of high frequency electric fish. I. General features. J Comp Physioll972, 77~1-22.
10.
Heiiigenberg W, Baker C, Matsubara J: The jamming avoidance response in Eigenmennia revisited: the structure of a neuronal democracy. J Comp Physioll976, 127:267-266.
11.
Heiligenberg W, Bastian J: The control of Eigenmennids pacemaker by distributed evaluation of electroreceptive afferences. J Comp Physioll960, 136:113-l 33.
12.
Bastian J, Heiligenberg W: Neural correlates of the jamming avoidance response in Eigenmannia. J Comp Physioll960, 136:135-l 52.
13.
Kawasaki M: Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish, Gymnanhus nilotiws. J Comp Physiol 1993, 173:9-22.
14.
Rose GJ, Heiiigenberg W: Temporal hyperacuity sense of fish. Nature 1965, 316:176-l 60.
15.
Carr CE. Heiligenberg W, Rose GJ: A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology. J Neurosci 1966, 6:107-l 19.
Prog Sensory Physioll961,
in the electric
Sensory
16.
Guo Y. Kawasaki M: Repreoentetlon of accurate temooral information in the electrosensory system of the Af&an electric fish, Gymnarchus niloticus. J Neurosci 1997, 17:1761-l 768. The acuity of the phase processing system in Gymnarc!tus was measured usina hiahlv orecise stimulus and recordinn methods. The iitter of ohaselooked ~ou&s was -6~s. The stability 07 the electric organ discharges was also measured and their jitter was less than 1 ps. This stability of electric organ discharge, however, is not required for hyperacuity.
..
1 7.
Heiligenberg W: Neural Ners in Electric Fish. Cambridge, Massachusetts: MIT Press; 1991.
18.
Heiligenberg W: Jamming avoidance responses: model systems for neuroethology. In Elecfroreception. Edited by Bullock TH, Heiligenberg W. New York: Wiley & Sons; 1986:613649.
19.
Scheich H, Bullock TH, Hamstra RH: Coding properties of two classes of afferent nerve fibers: high-frequency electroreceptors in the electric fish, Eigenmacnia. J Neurophysiol 1973, 36:39-60.
20.
Maler L, Sas E, Rogers J: The cytology of the posterior lateral line lobe of high frequency weekly electric fish (Gymnotidee). Dendritic differentiation and synaptic specificity in a simple cortex. J Comp Neural 1981, 195:67-139.
21.
Shumway CA: Multiple electrosensory maps in the medulla of weakly electric gymnotlform fish. I. Physiological differences. J Neurosci 1989, g:4368-4399.
22.
Bastion J: Electrolocation. II. The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells in Apteronotus a/bifrons. J Comp Physiol 1961, 144:481-494.
23.
Bastian J, Bratton B: Descending control of electroreception. I. Properties of nucleus praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe. J Neurosci 1990, IO:1 226-l 240.
24.
25.
Bastian J: Gain control in the electrosensory by descending inputs to the electrosenoory J Neurosci 1906, 6:553-562.
system mediated lateral line lobe.
Carr CE, Maler L, Heiligenberg W, Sas E: Laminar organization of the afferent and efferent systems of the torus semicircularis of Gymnotlform fish: morphological substrates for parallel processing in the electrosensory system. J Comp Neural 1961, 203:649-670.
35.
hyperacuityKawasaki
Kawasaki M: Comperetlve studies on the motor control mechanisms for electro-communicetfon in gymnotiform J Comp Physioll993, 173:726-728.
479
fishes,
36.
Kawasaki M, Rose GJ, Heiligenberg W: Temporel hypemcuity in single neurons of electric fish. Nature 1988, 336:173-l 76.
37.
Heiligenberg W, Rose G: phase end amplitude computetfons in the midbrein of an electric fish: intracellular studies of neurons partlclpetlng In the jamming evoldance response of Eigenmannia. J Neurosci 1965,5:515-531.
38. .
Kawasaki M: Comparative analysis of the jamming avoidance response in Africen and South Amerlcen wave-type flshen Biol Bull 1996, 191 :103-108. Two phylogenetically unrelated groups of fishes perform electrolocation. Not only do they share this basic function, but both fishes perform jamming avoidance responses of identical form. Moreover, they share rather complex computational algorithms. Different brain areas, however, are used to perform a certain step of neuronal computation. Comparative implications are discussed. 39.
Hopkins C: Convergent designs for electrogenesls end electroreception. Curr Opin Neurobiol 1995, 5:769-777.
40. ..
Kawasaki M, Guo Y-X: Neuronal circuitry for comperison of timing in the electrosensory lateral line lobe of an Afrlcen wave-type electric fish, Gymnanzhus niloticus. J Neurosci 1996, 16:300-391. Intracellular recording and labeling were performed in a neural circuit that detects ohase differences in the microsecond raoae. Phase-locked neurons spread &on terminals in both halves of a medulltistructure, the electrosensory lateral line lobe. Neurons sensitive to phase differences are found in the inner cellular layer of this structure. These neurons respond to changes in smell phase differences, but ignore steady-state differences in phase. 41.
Hopkins CD, Bass AH: Temporal coding of species recognition signals in an electric fish. Science 19131, 21265-87.
42.
Friedman MA, Hopkins CS: Neural substrate for species recognition in the time-coding elecbosensory pathway of mormyrid electric fish J Neurosci 1997. in press.
43.
Amagai S, Friedman MA, Hopkins CD: Time-coding in the midbrain of mormyrid electric fish. I. physiology end anatomy of cells in the nucleus exterolateralis pars anterior (ELa). J Comp Physiol IA] 1997, in press.
44.
Amagai S: Time-coding in the midbrain of mormyrid electric fish. II. Stimulus selectivity in the nucleus exterolaterelis pars posterior (ELp). J Comp Physiol fAj 1997, in press.
26.
Shumway CA: Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. II. Anatomical differences. J Neurosci 1989, 9:4400-4415.
45.
Kalmijn A: Electric and magnetic field detection in elasmobranch fishes. Science 1982, 218:916-918.
46.
27.
Rose GJ, Heiligenberg W: Neural coding of difference frequencies in the midbrain of the electric fish Eigenmannia: reading the sense of rotation in en amplitude-phese plane. J Comp Physiol 1966, 159:613-624.
Simmons J, Ferragamo M, Moss C, Stevenson S, Altes R: Discrimination of jittered sonar echoes by the echolocating bat Eptesicus fuscus: the shape of terget images in echolocation. J Comp Physiol IA1 1990, 167:569-616.
47.
28.
Bastian J, Heiligenberg W: Phase-sensitive midbrain neurons In Eigenmannia: neural correlates of the jamming avoidance response. Science 1980, 209:826-831.
Simmons J, Saillant P, Ferragamo M, Haresign T, Dear S, Fritz J, McMullen T: Auditory computations for biosonar target imaging in bats. In Auditory Computation. Springer Handbook of Auditory Research Edited by Hawkins H, McMullen T, Popper A, Fay R. New York: Springer-Verlag; 1995:401-468.
29.
Carr CE. Maler L. Tavlor , B: A time-comoarison circuit in the electric fish midbrain. II. Functional morphology. J Neurosci 1986, 6:1372-l 363.
30.
Rose GJ, Heiligenberg W: Limits of phase and amplitude sensitivity in the torus semlcirculsris of Eigenmannia. J Comp Physiol IA1 1986, 15g:al3-822.
31.
Keller CH: Stimulus discrimination In the diencephalon of Eigenmannia: the emergence and sharpening of a sensory filter. J Comp Physioll996, t62:747-757.
32.
Metzner W: The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways. J Neurosci i 993, 13:i 862-i 878.
33.
34.
Kawasaki M, Maler L, Rose GJ, Heiligenberg W: Anatomical and functlonel organization of the prepacemaker nucleus in gymnotiform electric fish: the accommodation of two behaviors in one nucleus. J Comp Neural 1988, 276:113-l 31. Kawasaki M, Heiligenberg W: Different classes of glutamate receptors and GABA medlate distinct modulations In the firing pattern of a neuronal oscllletor, the medullary pacemaker of gymnotlform electric flsh. J Neurosci 1990, 10:3896-3904.
48. .
Simmons J, Dear S, Ferragamo M, Haresign T, Fritz J: Representation of perceptual dimensions of insect prey during terminal pursuit by echolocating bats. Biol Bull 1996, 191 :I 09121. On the basis of multiunit recording data in the inferior colliculus of a bat, Eptesicus, the authors have developed a new theory that bats’ hyperacuity is endowed by time expansion. Latency of multiple unit response peaks to pulse-echo pairs changes by l OO-200~s as echo delay changes by about 5 us. 49.
Knudsen El, Blasdel GG, Konishi M: Sound localization barn owl (Tyto a/be). J Comp Physiol 1979, 133:13-21.
50.
Brainard MS, Knudsen El, Esterty SD: Neural derivation of sound source location: resolution of spatial ambiguities in binaural cues. J Acoust Sot Am 1992, 91 :1015-l 027
51. .
by the
Rose G, Fortune E: New techniques for making whole-cell recordings from CNS neurons in ho. Neurosci Res 1996, 26:89-94. A whole-cell recording technique using patch-clamp pipettes is refined for in viva preparation of electric fish. This method permits long-term recording of synaptic potentials as well as action potentials in preparations showing electrical behavior.
