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First published online February 20, 2004
Journal of Experimental Biology 207, 1073-1084 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00851
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Central control of electric signaling behavior in the mormyrid Brienomyrus brachyistius: segregation of behavior-specific inputs and the role of modifiable recurrent inhibition

Bruce A. Carlson* and Carl D. Hopkins

Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA



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  		Fig. 1. (A) Sagittal schematic showing the functional neuroanatomy of the mormyrid electromotor system, based on Bell et al. (1983Go), Carlson (2002bGo, 2003Go) and von der Emde et al. (2000Go). Excitatory terminals are identified by flat lines, inhibitory terminals by solid circles. Red denotes medullary electromotor nuclei, blue denotes mesencephalic and diencephalic electromotor nuclei (topic of the current study), and green denotes corollary discharge nuclei. BCA, bulbar command-associated nucleus; C3, third cerebellar lobule; CN, command nucleus; DP, dorsal posterior nucleus of the thalamus; EGp, eminentia granularis pars posterior; EL, exterolateral nucleus of the torus semicircularis; ELL, electrosensory lateral line lobe; EMN, electromotor neurons; IL, inferior lobe of the hypothalamus; MCA, mesencephalic command-associated nucleus; MRN, medullary relay nucleus; OB, olfactory bulb; PCN, precommand nucleus; Tel, telencephalon; TM, tectum mesencephali; Val, valvula of the cerebellum; VPd, dorsal subdivision of the ventroposterior nucleus of the torus semicircularis. (B) Examples of the three burst display types produced by freely behaving Brienomyrus brachyistius. Quantitative analysis indicates that they fall into distinct categories based on unique temporal patterns of EOD production (Carlson and Hopkins, unpublished observations).

 


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  		Fig. 2. Localization of iontophoresis sites. (A) The precommand nucleus (PCN). (B) The dorsal posterior nucleus (DP). (C) The ventroposterior nucleus (VP). The first column shows photomicrographs of transverse sections with retrogradely labeled neurons against a background of cresyl violet counterstain, taken from the anatomical study by Carlson (2002bGo). In A and B, the label results from an injection of neurobiotin into the command nucleus (CN), while in C it results from an injection of neurobiotin into PCN. The second column shows photomicrographs of transverse sections with alcian blue staining against a background of neutral red counterstain, at the same approximate rostro-caudal locations as the first column. The small blue dots provide a precise marker of electrode location, which was always accurately placed into one of the three nuclei. In the third column, continuous voltage traces of electromotor neuron (EMN) activity are shown, with each spike corresponding to a single EMN volley. Iontophoretic injections of L-glutamate (L-Glu; 500 ms pulses of –500 nA) occurred during the times represented by horizontal green lines below each series of traces. Each example is taken from the site shown in the second column, with 0 µm corresponding to the exact location of the alcian blue marker. The effects of L-Glu iontophoresis at 50 µm and 100 µm dorsal and ventral to these sites are also shown. CP, central posterior nucleus of the thalamus; FR, fasciculus retroflexus; Hyp, hypothalamus; IL, inferior lobe of the hypothalamus; L, lateral nucleus of the torus semicircularis; ll, lateral lemniscus; MV, medioventral nucleus of the torus semicircularis; nLR, nucleus of the lateral recess; pc, posterior commissure; PGc, caudal subdivision of the preglomerular nucleus; PGm, medial subdivision of the preglomerular nucleus; tc, tectocerebellar tract; tt, toro-praeeminential tract; v, ventricle. Scale bars, 200 µm in A, 50 µm in B and 200 µm in C.

 


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  		Fig. 3. Effects of varying L-glutamate (L-Glu) iontophoretic current magnitudes on electromotor neuron (EMN) intervals in the dorsal posterior (DP), precommand (PCN) and ventroposterior nuclei (VP). (A) One example from each nucleus in a single fish. EMN intervals are plotted against time. The timing of L-Glu iontophoresis is indicated by the horizontal bars beneath the plots, with the current magnitude increasing from –100 nA to –900 nA in steps of –200 nA. (B) Dose–response curves of the effects of varying current magnitude on median EMN intervals. Values shown are means ± S.E.M.

 


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  		Fig. 4. Three representative examples of the effects of L-glutamate (L-Glu) iontophoresis on electromotor neuron (EMN) output in the dorsal posterior (DP), precommand (PCN) and ventroposterior nuclei (VP). Each row corresponds to a single fish. The first column shows the effects of L-Glu iontophoresis in DP, the second column shows the effects of L-Glu iontophoresis in PCN, and the third column shows the effects of L-Glu iontophoresis in VP. In each case, iontophoretic currents consisted of –1 µA for 20 s, which is indicated by the horizontal bar beneath each column.

 


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  		Fig. 5. Differences in electromotor neuron (EMN) output patterns in response to L-glutamate (L-Glu) iontophoresis in the dorsal posterior (DP) and precommand nuclei (PCN). Each row corresponds to a single fish. The three representative examples for each nucleus show an expanded view of the period from 31 s to 34 s of the data shown in Fig. 4.

 


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  		Fig. 6. The effects of L-glutamate (L-Glu) iontophoresis in the dorsal posterior (DP) and precommand nuclei (PCN) on the coefficient of variation in electromotor neuron (EMN) interval (A), the minimum EMN interval (B) and the maximum EMN interval (C). Only those fish with data from both nuclei are included. Values shown are means ± S.E.M. Asterisks represent statistically significant differences (Wilcoxon matched pairs test; P<0.05).

 


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  		Fig. 7. Three representative examples of the effects of {gamma}-amino-butyric acid (GABA) iontophoresis on electromotor neuron (EMN) output in the dorsal posterior (DP), precommand (PCN) and ventroposterior nuclei (VP). Each row corresponds to a single fish. In each case, iontophoretic currents consisted of +1 µA for 20 s, which is indicated by the horizontal bar beneath each column.

 


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  		Fig. 8. (A) One example each of the effects of bicuculline methiodide (BMI) iontophoresis in the dorsal posterior (DP) and precommand nuclei (PCN), and the effects of L-glutamate (L-Glu) iontophoresis immediately before and immediately after BMI iontophoresis. L-Glu iontophoretic currents consisted of –1 µA for 20 s, while BMI iontophoretic currents consisted of +100 nA for 4 min, each of which is shown as a horizontal bar beneath each column. (B) Excerpts from A of examples of different burst types occurring during BMI iontophoresis in DP and PCN. (C) Number of different burst types induced by BMI iontophoresis in DP and PCN. Values shown are means ± S.E.M. There were no significant differences in the numbers of any of the three burst types.

 


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  		Fig. 9. The effects of L-glutamate (L-Glu) iontophoresis in the dorsal posterior (DP) and precommand nuclei (PCN) before and after bicuculline methiodide (BMI) iontophoresis on the coefficient of variation (CV) in electromotor neuron (EMN) interval (A), the minimum EMN interval (B), and the maximum EMN interval (C). Values shown are means ± S.E.M. Asterisks represent statistically significant differences (Mann–Whitney U test; P<0.05).

 

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© The Company of Biologists Ltd 2004