Summary
Neuronal reliability and sensitivity to behaviorally relevant stimulus patterns were investigated in a higher-order nucleus of the diencephalon believed to participate in the jamming avoidance response (JAR) of the weakly electric fish,Eigenmannia. The fish raises or lowers its frequency of electric organ discharge (EOD) to minimize interference from a neighboring fish's EOD. Proper JARs require determination of the sign of the difference frequency (Df) between the neighboring fish's EOD and the fish's own EOD. Bastian and Yuthas (1984) recently described diencephalic neurons within the nucleus electrosensorius that are able to make this determination. In the present study, response properties of such neurons were compared with those of lower-level ‘sign-selective’ cells found in the torus semicircularis and the optic tectum (Heiligenberg and Rose 1985) as well as with properties of the intact behavior.
Most sign-selective cells within the nucleus electrosensorius show a high degree of selectivity for one sign of the difference frequency; cells with either sign preference were found in approximately equal numbers. The sign preference and the degree of sign selectivity is most often independent of the spatial orientation of the jamming stimulus. In contrast, the responses of toral and tectal cells are less robust and consistent and are often highly dependent on the geometry of the jamming stimulus.
Determination of the sign of the difference frequency requires the analysis of amplitude modulations coupled with modulations in phase (timing) differences between pairs of areas of the body surface. The most sensitive cells recorded in the nucleus electrosensorius can determine the sign of the difference frequency with timing differences of 1 μs or less, roughly comparable to the behavioral threshold of 400 ns (Carr et al. 1986). The best toral/tectal response required at least a 16 μs modulation.
Cells within the nucleus electrosensorius thus code the sign of Df with a high degree of reliability and sensitivity. Ambiguities persist, however, which suggest that single cells at this level cannot completely account for the behavioral discrimination. Additional processing may be necessary to transform a still primarily sensory code into a motor program for control of the JAR (Rose et al. 1988).
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Abbreviations
- EOD :
-
electric organ discharge
- JAR :
-
jammning avoidance response
- Df :
-
difference frequency between jamming signal and fish's own EOD
- S 1 :
-
sinusoidal EOD mimic of subject fish
- S 2 :
-
sinusoidal EOD mimic of neighbor
References
Baylis GC, Rolls ET, Leonard CM (1985) Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey. Brain Res 342:91–102
Bastian J (1981) Electrolocation I and II. J Comp Physiol 144:465–494
Bastian J, Heiligenberg W (1980) Neural correlates of the jamming avoidance response ofEigenmannia. J Comp Physiol 136:135–152
Bastian J, Heiligenberg W (1980) Phase-sensitive midbrain neurons inEigenmannia: neural correlates of the jamming avoidance response. Science 209:828–831
Bastian J, Yuthas J (1984) The jamming avoidance response ofEigenmannia. properties of a diencephalic link between sensory processing and motor output. J Comp Physiol A 154:895–908
Bullock TH, Hamstra RH Jr, Scheich H (1972) The jamming avoidance response of high frequency electric fish. I and II J Comp Physiol 77:1–48
Bullock TH (1986) Some principles in the brain analysis of important signals: mapping and stimulus recognition. Brain Behav Evol 28:145–156
Carr CE, Maler L, Heiligenberg W, Sas E (1981) Laminar organization of the afferent and efferent systems of the torus semicircularis of gymnotiform fish: morphological substrates for parallel processing in the electrosensory system. J Comp Neurol 203:649–670
Carr CE, Heiligenberg W, Rose GJ (1986) A time comparison circuit in the electric fish midbrain. I. Behavior and physiology. J Neurosci 6:107–119
Frank K, Becker MC (1964) Microelectrodes for recording and stimulation. In: Nastuk WL (ed) Physical techniques in biological research, vol 5, part A. Academic Press, New York, pp 23–84
Gross CG, Rocha-Miranda CE, Bender DB (1972) Visual properties of neurons in inferotemporal cortex of the macaque. J Neurophysiol 35:96–111
Heiligenberg W (1986) Jamming Avoidance Responses: model systems for neuroethology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 613–650
Heiligenberg W, Bastian J (1980) The controlof Eigenmannia's pacemaker by distributed evaluation of electroreceptive afferences. J Comp Physiol 136:113–133
Heiligenberg W, Rose G (1985) Phase and amplitude computations in the midbrain of an electric fish: Intracellular studies of neurons participating in the jamming avoidance response (JAR) ofEigenmannia. J Neurosci 5:515–531
Heiligenberg W, Rose G (1987) The optic tectum of the gymnotiform electric fish,Eigenmannia: labelling of physiologically identified cells. Neurosci 22:331–340
Kendrick KM, Baldwin BA (1987) Cells in temporal cortex of conscious sheep can respond preferentially to the sight of faces. Science 236:448–450
Margoliash D (1983) Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J Neurosci 3:1039–1057
Margoliash D, Konishi M (1985) Auditory representation of autogenous song in the song system of white-crowned sparrows. PNAS 82:5997–6000
Partridge BL, Heiligenberg W, Matsubara J (1981) The neural basis of a sensory filter in the jamming avoidance response: No grandmother cells in sight. J Comp Physiol 145:153–168
Rolls ET (1984) Neurons in the cortex of the temporal lobe and in the amygdala of the monkey with responses selective for faces. Human Neurobiology 3:209–222
Rose G, Heiligenberg W (1985) Structure and function of electrosensory neurons in the torus semicircularis ofEigenmannia: Morphological correlates of phase and amplitude sensitivity. J Neurosci 5:2269–2280
Rose G, Heiligenberg W (1986a) Neural coding of frequencies in the midbrain of the electric fishEigenmannia: Reading the sense of rotation in an amplitude-phase plane. J Comp Physiol A 158:613–624
Rose G, Heiligenberg W (1986b) Limits of phase and amplitude sensitivity in the torus semicircularis ofEigenmannia. J Comp Physiol A 159:813–822
Rose G, Kawasaki M, Heiligenberg W (1988) ‘Recognition units’ at the top of a neuronal hierarchy? Prepacemaker neurons inEigenmannia code the sign of frequency differences unambiguously. J Comp Physiol 162:759–772
Shumway CA (1986) Physiological differences in the multiple maps of the electrosensory lateral line lobe (ELL): pyramidal cells have different receptive field sizes. Soc Neurosci Abstr 12:201
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Keller, C.H. Stimulus discrimination in the diencephalon ofEigenmannia: the emergence and sharpening of a sensory filter. J. Comp. Physiol. 162, 747–757 (1988). https://doi.org/10.1007/BF00610964
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DOI: https://doi.org/10.1007/BF00610964