Distribution of muscarinic acetylcholine receptor mRNA in the brain of the weakly electric fish Apteronotus leptorhynchus

Journal of Comparative Neurology

Volumn 521, Issue 5, 2013, Pages 1054-1072

  Toscano Márquez, Brenda ^a   Dunn, Robert J ^b,c   Krahe, Rüdiger ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MONTREAL GENERAL HOSPITAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Acetylcholine; Electrosensory system; In situ hybridization; Neuromodulation; Weakly electric fish

Indexed keywords

MESSENGER RNA; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR; MUSCARINIC RECEPTOR;

ANIMAL TISSUE; APTERONOTUS LEPTORHYNCHUS; ARTICLE; BRAIN STEM; CEREBELLUM; DIENCEPHALON; DORSAL TORUS SEMICIRCULARIS; ELECTRIC FISH; ELECTROSENSORY LATERAL LINE LOBE; ELECTROSENSORY NUCLEUS; FEMALE; GENE EXPRESSION; IN SITU HYBRIDIZATION; MALE; MESENCEPHALON; NONHUMAN; PREEMINENTIAL NUCLEUS; PRIORITY JOURNAL; RHOMBENCEPHALON; RNA PROBE; SUPERIOR COLLICULUS; TELENCEPHALON; TISSUE DISTRIBUTION;

ACETYLCHOLINE; ANIMALS; BRAIN; ELECTRIC FISH; FEMALE; MALE; RECEPTORS, MUSCARINIC; RNA, MESSENGER;

EID: 84873856843     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23218     Document Type: Article

References (122)

1. Asadollahi A, Mysore SP, Knudsen EI. 2010. Stimulus-driven competition in a cholinergic midbrain nucleus. Nat Neurosci 13: 889-895.
2. Bakin JS, Weinberger NM. 1996. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc Natl Acad Sci U S A 93: 11219-11224.
3. Ball GF, Nock B, Wingfield JC, McEwen BS, Balthazart J. 1990. Muscarinic cholinergic receptors in the songbird and quail brain-a quantitative autoradiographic study. J Comp Neurol 298: 431-442.
4. Bastian J. 1982. Vision and electroreception: integration of sensory information in the optic tectum of the weakly electric fish Apteronotus albifrons. J Comp Physiol A 147: 287-297.
5. Bastian J. 1986. Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe. J Neurosci 6: 553-562.
6. Bastian J, Chacron MJ, Maler L. 2004. Plastic and nonplastic pyramidal cells perform unique roles in a network capable of adaptive redundancy reduction. Neuron 41: 767-779.
7. Berman NJ, Maler L. 1999. Neural architecture of the electrosensory lateral line lobe: adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering. J Exp Biol 202: 1243-1253.
8. Bina KG, Rusak B, Semba K. 1993. Localization of cholinergic neurons in the forebrain and brainstem that project to the suprachiasmatic nucleus of the hypothalamus in rat. J Comp Neurol 335: 295-307.
9. Binns KE. 1999. The synaptic pharmacology underlying sensory processing in the superior colliculus. Prog Neurobiol 59: 129-159.
10. Bonner TI, Buckley NJ, Young AC, Brann MR. 1987. Identification of a family of muscarinic acetylcholine-receptor genes. Science 237: 527-532.
11. Bonner TI, Young AC, Brann MR, Buckley NJ. 1988. Cloning and expression of the human and rat M5 muscarinic acetylcholine-receptor genes. Neuron 1: 403-410.
12. Brown D. 2010. Muscarinic acetylcholine receptors (mAChRs) in the nervous system: Some functions and mechanisms. J Mol Neurosci 41: 340-346.
13. Buckley N, Bonner T, Brann M. 1988. Localization of a family of muscarinic receptor mRNAs in rat brain. J Neurosci 8: 4646-4652.
14. Bullock TH, Hopkins CD, Popper AN, Fay RR. 2005. Electroreception. New York: Springer Science.
15. 1 receptors is mediated by inhibition of SK channels. Neuron 68: 948-963.
16. Carr CE, Maler L. 1985. A golgi study of the cell types of the dorsal torus semicircularis of the electric fish Eigenmannia: functional and morphological diversity in the midbrain. J Comp Neurol 235: 207-240.
17. 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.
18. Carr CE, Maler L, Taylor B. 1986. A time-comparison circuit in the electric fish midbrain. II. Functional morphology. J Neurosci 6: 1372-1383.
19. Caulfield MP. 1993. Muscarinic receptors-characterization, coupling and function. Pharmacol Ther 58: 319-379.
20. Chacron MJ, Doiron B, Maler L, Longtin A, Bastian J. 2003. Non-classical receptive field mediates switch in a sensory neuron's frequency tuning. Nature 423: 77-81.
21. Chacron MJ, Maler L, Bastian J. 2005. Feedback and feedforward control of frequency tuning to naturalistic stimuli. J Neurosci 25: 5521-5532.
22. Chalupa LM, Rhoades RW. 1977. Responses of visual, somatosensory, and auditory neurones in the golden hamster's superior colliculus. J Physiol 270: 595-626.
23. Clemente D, Porteros A, Weruaga E, Alonso JR, Arenzana FJ, Aijon J, Arevalo R. 2004. Cholinergic elements in the zebrafish central nervous system: histochemical and immunohistochemical analysis. J Comp Neurol 474: 75-107.
24. de Lacalle S, Hersh LB, Saper CB. 1993. Cholinergic innervation of the human cerebellum. J Comp Neurol 328: 364-376.
25. 3H]N-methyl scopolamine binding. Eur J Pharmacol 119: 9-16.
26. Ellis LD, Krahe R, Bourque CW, Dunn RJ, Chacron MJ. 2007. Muscarinic receptors control frequency tuning through the downregulation of an A-type potassium current. J Neurophysiol 98: 1526-1537.
27. Ellis LD, Maler L, Dunn RJ. 2008. Differential distribution of SK channel subtypes in the brain of the weakly electric fish Apteronotus leptorhynchus. J Comp Neurol 507: 1964-1978.
28. Engler G, Zupanc GKH. 2001. Differential production of chirping behavior evoked by electrical stimulation of the weakly electric fish, Apteronotus leptorhynchus. J Comp Physiol A 187: 747-756.
29. Fortune ES, Rose GJ. 1997. Passive and active membrane properties contribute to the temporal filtering properties of midbrain neurons in-vivo. J Neurosci 17: 3815-3825.
30. Franchina CR, Stoddard PK. 1998. Plasticity of the electric organ discharge waveform of the electric fish Brachyhypopomus pinnicaudatus I. Quantification of day-night changes. J Comp Physiol A 183: 759-768.
31. Francis A, Schechter N. 1980. Regional and subcellular distribution of cholinergic enzyme and receptor activity in goldfish brain. Neuroscience 5: 293-301.
32. Ganz J, Kaslin J, Freudenreich D, Machate A, Geffarth M, Brand M. 2012. Subdivisions of the adult zebrafish subpallium by molecular marker analysis. J Comp Neurol 520: 633-655.
33. Giassi AC, Maler L, Moreira JE, Hoffmann A. 2011. Glomerular nucleus of the weakly electric fish, Gymnotus sp.: cytoarchitecture, histochemistry, and fiber connections-inisights from neuroanatomy to evolution and behavior. J Comp Neurol 19: 1658-1676.
34. Giassi AC, Duarte TT, Ellis W, Maler L. 2012. The organization of the gymnotiform fish pallium in relation to learning and memory: II. Extrinsic connections. J Comp Neurol doi: 10.1002/cne.23109 [March 20 E-pub ahead of print].
35. Giessel AJ, Sabatini BL. 2010. M1 muscarinic receptors boost synaptic potentials and calcium influx in dendritic spines by inhibiting postsynaptic SK channels. Neuron 68: 936-947.
36. Gu Q. 2003. Contribution of acetylcholine to visual cortex plasticity. Neurobiol Learn Mem 80: 291-301.
37. Hagedorn M, Heiligenberg W. 1985. Court and spark: electric signals in the courtship and mating of gymnotoid fish. Anim Behav 33: 254-265.
38. Harvey-Girard E, Tweedle J, Ironstone J, Cuddy M, Ellis W, Maler L. 2010. Long-term recognition memory of individual conspecifics is associated with telencephalic expression of Egr-1 in the electric fish Apteronotus leptorhynchus. J Comp Neurol 518: 2666-2692.
39. Hasselmo ME. 2006. The role of acetylcholine in learning and memory. Curr Opin Neurobiol 16: 710-715.
40. Heiligenberg W. 1991a. Neural nets in electric fish. Cambridge, MA: MIT Press.
41. Heiligenberg W. 1991b. Sensory control of behavior in electric fish. Curr Opin Neurobiol 1: 633-637.
42. 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 of Eigenmannia. J Neurosci 5: 515-531.
43. Heiligenberg W, Rose GJ. 1987. The optic tectum of the gymnotiform electric fish Eigenmannia: labeling of physiologically identified cells. Neuroscience 22: 331-340.
44. Hopkins CD. 1974. Electric communication: functions in the social behavior of Eigenmannia virescens. Behaviour 50: 270-305.
45. Hoss W, Messer JWS, Monsma JFJ, Miller MD, Ellerbrock BR, Scranton T, Ghodsi-Hovsepian S, Price MA, Balan S, Mazloum Z, Bohnett M. 1990. Biochemical and behavioral evidence for muscarinic autoreceptors in the CNS. Brain Res 517: 195-201.
46. Hulme EC, Birdsall NJM, Buckley NJ. 1990. Muscarinic receptor subtypes. Annu Rev Pharmacol Toxicol 30: 633-673.
47. Ikeda M, Houtani T, Ueyama T, Sugimoto T. 1991. Choline acetyltransferase immunoreactivity in the cat cerebellum. Neuroscience 45: 671-690.
48. Ikenaga T, Yoshida M, Uematsu K. 2006. Cerebellar efferent neurons in teleost fish. Cerebellum 5: 268-274.
49. Imeri L, Bianchi S, Angeli P, Mancia M. 1996. Muscarinic receptor subtypes in the medial preoptic area and sleep-wake cycles. Neuroreport 7: 417-420.
50. Johnston SA, Maler L. 1992. Anatomical organization of the hypophysiotrophic systems in the electric fish, Apteronotus leptorhynchus. J Comp Neurol 317: 421-437.
51. Jones SB, King LB. 1995. Muscarinic cholinergic receptors in brain and atrial membranes of adult brook trout (Salvelinus-fontinalis) measured by radioligand binding techniques. Comp Biochem Physiol C 112: 43-50.
52. Jones SVP. 1993. Muscarinic receptor subtypes: modulation of ion channels. Life Sci 52: 457-464.
53. Kilgard MP, Merzenich MM. 1998. Cortical map reorganization enabled by nucleus basalis activity. Science 279: 1714-1718.
54. Kimura F. 2000. Cholinergic modulation of cortical function: a hypothetical role in shifting the dynamics in cortical network. Neurosci Res 38: 19.
55. Kimura F, Baughman RW. 1997. Distinct muscarinic receptor subtypes suppress excitatory and inhibitory synaptic responses in cortical neurons. J Neurophysiol 77: 709-716.
56. Knudsen E. 1982. Auditory and visual maps of space in the optic tectum of the owl. J Neurosci 2: 1177-1194.
57. Kohlmeier KA, Soja PJ, Kristensen MP. 2006. Disparate cholinergic currents in rat principal trigeminal sensory nucleus neurons mediated by M1 and M2 receptors: a possible mechanism for selective gating of afferent sensory neurotransmission. Eur J Neurosci 23: 3245-3258.
58. Koyama Y, Satou M, Oka Y, Ueda K. 1984. Involvement of the telencephalic hemispheres and the preoptic area in sexual behavior of the male goldfish, Carassius auratus: a brain-lesion study. Behav Neural Biol 40: 70-86.
59. Krahe R, Gabbiani F. 2004. Burst firing in sensory systems. Nat Rev Neurosci 5: 13-23.
60. Krahe R, Bastian J, Chacron MJ. 2008. Temporal processing across multiple topographic maps in the electrosensory system. J Neurophysiol 100: 852-867.
61. Lavine N, Reuben M, Clarke PB. 1997. A population of nicotinic receptors is associated with thalamocortical afferents in the adult rat: laminal and areal analysis. J Comp Neurol 380: 175-190.
62. Lázár G, Libouban S, Szabo T. 1984. The mormyrid mesencephalon. III. Retinal projections in a weakly electric fish, Gnathonemus petersii. J Comp Neurol 230: 1-12.
63. Li F, Endo T, Isa T. 2004. Presynaptic muscarinic acetylcholine receptors suppress GABAergic synaptic transmission in the intermediate grey layer of mouse superior colliculus. Eur J Neurosci 20: 2079-2088.
64. Liu C, Gillette M. 1996. Cholinergic regulation of the suprachiasmatic nucleus circadian rhythm via a muscarinic mechanism at night. J Neurosci 16: 744-751.
65. Maler L. 1979. The posterior lateral line lobe of certain gymnotoid fish: quantitative light microscopy. J Comp Neurol 183: 323-363.
66. Maler L. 2009. Receptive field organization across multiple electrosensory maps. II. Computational analysis of the effects of receptive field size on prey localization. J Comp Neurol 516: 394-422.
67. Maler L, Mugnaini E. 1994. Correlating gamma-aminobutyric acidergic circuits and sensory function in the electrosensory lateral line lobe of a gymnotiform fish. J Comp Neurol 345: 224-252.
68. Maler L, Collins M, Mathieson WB. 1981. The distribution of acetylcholinesterase and choline acetyl transferase in the cerebellum and posterior lateral line lobe of weakly electric fish (Gymnotidae). Brain Res 226: 320-325.
69. Maler L, Sas E, Johnston S, Ellis W. 1991. An atlas of the brain of the electric fish Apteronotus leptorhynchus. J Chem Neuroanat 4: 1-38.
70. Marin G, Mpodozis J, Sentis E, Ossandon T, Letelier JC. 2005. Oscillatory bursts in the optic tectum of birds represent re-entrant signals from the nucleus isthmi pars parvocellularis. J Neurosci 25: 7081-7089.
71. Marin G, Salas C, Sentis E, Rojas X, Letelier JC, Mpodozis J. 2007. A cholinergic gating mechanism controlled by competitive interactions in the optic tectum of the pigeon. J Neurosci 27: 8112-8121.
72. Markham MR, McAnelly ML, Stoddard PK, Zakon HH. 2009. Circadian and social cues regulate ion channel trafficking. PLoS Biol 7: e1000203.
73. Marsat G, Proville RD, Maler L. 2009. Transient signals trigger synchronous bursts in an identified population of neurons. J Neurophysiol 102: 714-723.
74. Mehaffey WH, Ellis LD, Krahe R, Dunn RJ, Chacron MJ. 2008. Ionic and neuromodulatory regulation of burst discharge controls frequency tuning. J Physiol (Paris) 102: 195-208.
75. Metzner W, Heiligenberg W. 1991. The coding of signals in the electric communication of the gymnotiform fish Eigenmannia: from electroreceptors to neurons in the torus semicircularis of the midbrain. J Comp Physiol A 169: 135-150.
76. Miranda MI, Ramirez-Lugo L, Bermudez-Rattoni F. 2000. Cortical cholinergic activity is related to the novelty of the stimulus. Brain Res 882: 230-235.
77. Mooney DM, Zhang L, Basile C, Senatorov VV, Ngsee J, Omar A, Hu B. 2004. Distinct forms of cholinergic modulation in parallel thalamic sensory pathways. Proc Natl Acad Sci U S A 101: 320-324.
78. Murakami T, Morita Y. 1987. Morphology and distribution of the projection neurons in the cerebellum in a teleost, Sebastiscus-marmoratus. J Comp Neurol 256: 607-623.
79. Nicholson LFB, Montgomery JC, Faull RLM. 1994. GABA, muscarinic cholinergic, excitatory amino-acid, neurotensin and opiate binding sites in the octavolateralis column and cerebellum of the skate (Raja nasuta, Pisces, Rajidae). Brain Res 652: 40-48.
80. Northcutt RG. 2006. Connections of the lateral and medial divisions of the goldfish telencephalic pallium. J Comp Neurol 494: 903-943.
81. Park E, Lee Y, Kim Y, Lee CJ. 2008. Cholinergic modulation of neural activity in the telencephalon of the zebrafish. Neurosci Lett 439: 79-83.
82. Pepeu G, Giovannini MG. 2004. Changes in acetylcholine extracellular levels during cognitive processes. Learn Mem 11: 21-27.
83. Phan M, Maler L. 1983. Distribution of muscarinic receptors in the caudal cerebellum and electrosensory lateral line lobe of gymnotiform fish. Neurosci Lett 42: 137-143.
84. + channels in electrosensory and cerebellar neurons. J Comp Neurol 441: 234-247.
85. + channels to burst threshold in a sensory neuron. J Neurosci 21: 125-135.
86. Rasmusson DD. 2000. The role of acetylcholine in cortical synaptic plasticity. Behav Brain Res 115: 205-218.
87. Reever CM, Ferrari-DiLeo G, Flynn DD. 1997. The M5 (m5) receptor subtype: fact or fiction? Life Sci 60: 1105-1112.
88. Rodriguez-Moldes I, Molist P, Adrio F, Pombal MA, Perez SE, Yanez J, Mandado M, Marin O, Lopez JM, Gonzalez A, Anadon R. 2002. Organization of cholinergic systems in the brain of different fish groups: a comparative analysis. Brain Res Bull 57: 331-334.
89. Rose G, Heiligenberg W. 1985. Structure and function of electrosensory neurons in the torus semicircularis of Eigenmannia: morphological correlates of phase and amplitude sensitivity. J Neurosci 5: 2269-2280.
90. Sarter M, Parikh V. 2005. Choline transporters, cholinergic transmission and cognition. Nat Rev Neurosci 6: 48-56.
91. Sarter M, Givens B, Bruno JP. 2001. The cognitive neuroscience of sustained attention: where top-down meets bottom-up. Brain Res Rev 35: 146-160.
92. Sas E, Maler L. 1983. The nucleus praeeminentialis: a Golgi study of a feedback center in the electrosensory system of gymnotid fish. J Comp Neurol 221: 127-144.
93. Sas E, Maler L. 1986a. The optic tectum of gymnotiform teleosts Eigenmannia virescens and Apteronotus leptorhynchus: a Golgi study. Neuroscience 18: 215-246.
94. Sas E, Maler L. 1986b. Retinofugal projections in a weakly electric gymnotid fish (Apteronotus leptorhynchus). Neuroscience 18: 247-259.
95. Sas E, Maler L. 1987. The organization of afferent input to the caudal lobe of the cerebellum of the gymnotid fish Apteronotus leptorhynchus. Anat Embryol 177: 55-79.
96. Sas E, Maler L, Weld M. 1993. Connectios of the olfactory bulb in the gymnotiform fish, Apteronotus leptorhynchus. J Comp Neurol 22: 486-507.
97. Sato H, Hata Y, Masui H, Tsumoto T. 1987. A functional role of cholinergic innervation to neurons in the cat visual cortex. J Neurophysiol 58: 765-780.
98. Satou M, Oka Y, Kusunoki M, Matsushima T, Kato M, Fujita I, Ueda K. 1984. Telencephalic and preoptic areas integrate sexual behavior in hime salmon (landlocked red salmon, Oncorhynchus nerka): results of electrical brain stimulation experiments. Physiol Behav 33: 441-447.
99. Semba K. 2000. Multiple output pathways of the basal forebrain: organization, chemical heterogeneity, and roles in vigilance. Behav Brain Res 115: 117-141.
100. Semba K. 2004. Phylogenetic and ontogenetic aspects of the basal forebrain cholinergic neurons and their innervation of the cerebral cortex. Prog Brain Res 145: 3-43.
101. Seo JS, Kim MS, Park EM, Ahn SJ, Kim NY, Jung SH, Kim JW, Lee HH, Chung JK. 2009. Cloning and characterization of muscarinic receptor genes from the nile tilapia (Oreochromis niloticus). Mol Cells 27: 383-390.
102. + channel activity in sympathetic neurons. Life Sci 68: 2481-2487.
103. Shumway CA. 1989. Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. I. Physiological differences. J Neurosci 9: 4388-4399.
104. Sillito AM, Kemp JA. 1983. Cholinergic modulation of the functional organization of the cat visual cortex. Brain Res 289: 143-155.
105. Sillito AM, Kemp JA, Berardi N. 1983. The cholinergic influence on the function of the cat dorsal lateral geniculate nucleus (dLGN). Brain Res 280: 299-307.
106. Skaliora I, Doubell TP, Holmes NP, King AJ. 2004. Functional topography of converging visual and auditory inputs to neurons in the rat superior colliculus. J Neurophysiol 92: 2933-2946.
107. Smiley JF, Levey AI, Mesulam MM. 1999. m2 Muscarinic receptor immunolocalization in cholinergic cells of the monkey basal forebrain and striatum. Neuroscience 90: 803-814.
108. Stoddard PK, Markham MR, Salazar VL, Allee S. 2007. Circadian rhythms in electric waveform structure and rate in the electric fish Brachyhypopomus pinnicaudatus. Physiol Behav 90: 11-20.
109. Szabó A, Nemcsók J, Kása P, Gulya K. 1989. Muscarinic cholinergic components in the carp brain. Neurochem Int 15: 511-516.
110. Tang Y, Mishkin M, Aigner TG. 1997. Effects of muscarinic blockade in perirhinal cortex during visual recognition. Proc Natl Acad Sci U S A 94: 12667-12669.
111. Wang SR, Li Z, Xu HY. 1986. Muscarinic action of acetylcholine in the pigeon optic tectum. Exp Neurol 94: 436-440.
112. Wang Y, Luksch H, Brecha NC, Karten HJ. 2006. Columnar projections from the cholinergic nucleus isthmi to the optic tectum in chicks (Gallus gallus): a possible substrate for synchronizing tectal channels. J Comp Neurol 494: 7-35.
113. Wess J, Blin N, Mutschler E, Blüml K. 1995. Muscarinic acetylcholine receptors: structural basis of ligand binding and G protein coupling. Life Sci 56: 915-922.
114. Williams FE, Messer WS. 2004. Muscarinic acetylcholine receptors in the brain of the zebrafish (Danio rerio) measured by radioligand binding techniques. Comp Biochem Physiol C 137: 349-353.
115. Wong CJH. 1997. Connections of the basal forebrain of the weakly electric fish, Eigenmannia virescens. J Comp Neurol 389: 49-64.
116. Wong CJH. 2000. Electrical stimulation of the preoptic area in Eigenmannia: evoked interruptions in the electric organ discharge. J Comp Physiol A 186: 81-93.
117. Yamamoto N, Ito H. 2008. Visual, lateral line, and auditory ascending pathways to the dorsal telencephalic area through the rostrolateral region of the lateral preglomerular nucleus in cyprinids. J Comp Neurol 508: 615-647.
118. Yang JJ, Wang YT, Cheng PC, Kuo YJ, Huang RC. 2010. Cholinergic modulation of neuronal excitability in the rat suprachiasmatic nucleus. J Neurophysiol 103: 1397-1409.
119. Yu CJ, Debski EA. 2003. The effects of nicotinic and muscarinic receptor activation on patch-clamped cells in the optic tectum of Rana pipiens. Neuroscience 118: 135-144.
120. Zupanc GKH. 1997. The preglomerular nucleus of gymnotiform fish-relay station for conveying information between telencephalon and diencephalon. Brain Res 761: 179-191.
121. Zupanc GKH, Correa SAL. 2005. Reciprocal neural connections between the central posterior/prepacemaker nucleus and nucleus G in the gymnotiform fish, Apteronotus leptorhynchus. Brain Behav Evol 65: 14-25.
122. Zupanc GKH, Horschke I. 1997. Reciprocal connections between the preglomerular nucleus and the central posterior/prepacemaker nucleus in the diencephalon of weakly electric fish, Apteronotus leptorhynchus. Neuroscience 80: 653-667.