Distribution of the cholinergic nuclei in the brain of the weakly electric fish, Apteronotus leptorhynchus: Implications for sensory processing.

acetylcholine electrosensory system gymnotiform neuromodulation tract tracing weakly electric fish

Journal

The Journal of comparative neurology
ISSN: 1096-9861
Titre abrégé: J Comp Neurol
Pays: United States
ID NLM: 0406041

Informations de publication

Date de publication:
06 2021
Historique:
revised: 14 10 2020
received: 16 06 2020
accepted: 15 10 2020
pubmed: 23 10 2020
medline: 11 1 2022
entrez: 22 10 2020
Statut: ppublish

Résumé

Acetylcholine acts as a neurotransmitter/neuromodulator of many central nervous system processes such as learning and memory, attention, motor control, and sensory processing. The present study describes the spatial distribution of cholinergic neurons throughout the brain of the weakly electric fish, Apteronotus leptorhynchus, using in situ hybridization of choline acetyltransferase mRNA. Distinct groups of cholinergic cells were observed in the telencephalon, diencephalon, mesencephalon, and hindbrain. These included cholinergic cell groups typically identified in other vertebrate brains, for example, motor neurons. Using both in vitro and ex vivo neuronal tracing methods, we identified two new cholinergic connections leading to novel hypotheses on their functional significance. Projections to the nucleus praeeminentialis (nP) arise from isthmic nuclei, possibly including the nucleus lateralis valvulae (nLV) and the isthmic nucleus (nI). The nP is a central component of all electrosensory feedback pathways to the electrosensory lateral line lobe (ELL). We have previously shown that some neurons in nP, TS, and tectum express muscarinic receptors. We hypothesize that, based on nLV/nI cell responses in other teleosts and isthmic connectivity in A. leptorhynchus, the isthmic connections to nP, TS, and tectum modulate responses to electrosensory and/or visual motion and, in particular, to looming/receding stimuli. In addition, we found that the octavolateral efferent (OE) nucleus is the likely source of cholinergic fibers innervating the ELL. In other teleosts, OE inhibits octavolateral hair cells during locomotion. In gymnotiform fish, OE may also act on the first central processing stage and, we hypothesize, implement corollary discharge modulation of electrosensory processing during locomotion.

Identifiants

pubmed: 33089503
doi: 10.1002/cne.25058
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1810-1829

Subventions

Organisme : CIHR
ID : 6027
Pays : Canada

Informations de copyright

© 2020 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC.

Références

Adrio, F., Anadón, R., & Rodríguez-Moldes, I. (2000). Distribution of choline acetyltransferase (ChAT) immunoreactivity in the central nervous system of a chondrostean, the siberian sturgeon Acipenser baeri. Journal of Comparative Neurology, 426, 602-621. https://doi.org/10.1002/1096-9861(20001030)426:4<602::AID-CNE8>3.0.CO;2-7.
Ahrens, K., & Wullimann, M. F. (2002). Hypothalamic inferior lobe and lateral torus connections in a percomorph teleost, the red cichlid Hemichromis lifalili. Journal of Comparative Neurology, 449, 43-64. https://doi.org/10.1002/cne.10264.
Anadón, R., Molist, P., Rodríguez-Moldes, I., López, J. M., Quintela, I., Cerviño, M. C., Barja, P., & González, A. (2000). Distribution of choline acetyltransferase immunoreactivity in the brain of an elasmobranch, the lesser spotted dogfish Scyliorhinus canicula. Journal of Comparative Neurology, 420, 139-170. https://doi.org/10.1002/(sici)1096-9861(20000501)420:2<139::aid-cne1>3.0.co;2-t.
Asadollahi, A., Mysore, S. P., & Knudsen, E. I. (2010). Stimulus-driven competition in a cholinergic midbrain nucleus. Nature Neuroscience, 13, 889-895. https://doi.org/10.1038/nn.2573.
Asadollahi, A., Mysore, S. P., & Knudsen, E. I. (2011). Rules of competitive stimulus selection in a cholinergic isthmic nucleus of the owl midbrain. Journal of Neuroscience, 31, 6088-6097. https://doi.org/10.1523/JNEUROSCI.0023-11.2011.
Baldo, B. A., Pratt, W. E., Will, M. J., Hanlon, E. C., Bakshi, V. P., & Cador, M. (2013). Principles of motivation revealed by the diverse functions of neuropharmacological and neuroanatomical substrates underlying feeding behavior. Neuroscience Biobehavioral Reviews, 37, 1985-1998. https://doi.org/10.1016/j.neubiorev.2013.02.017.
Bastian, J. (1982). Vision and electroreception: Integration of sensory information in the optic tectum of the weakly electric fish Apteronotus albifrons. Journal of Comparative Physiology, 147, 287-297. https://doi.org/10.1007/BF00609662.
Bastian, J. (1999). Plasticity of feedback inputs in the apteronotid electrosensory system. Journal of Experimental Biology, 202, 1327-1337.
Bastian, J., Chacron, M. J., & Maler, L. (2004). Plastic and nonplastic pyramidal cells perform unique roles in a network capable of adaptive redundancy reduction. Neuron, 41, 767-779. https://doi.org/10.1016/s0896-6273(04)00071-6.
Bell, C., & Maler, L. (2005). Central neuroanatomy of electrosensory systems in fish. In T. Bullock, C. Hopkins, A. Popper, & R. Fay (Eds.), Electroreception. Springer.
Berman, N., & Maler, L. (1999). Neural architecture of the electrosensory lateral line lobe: Adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering. Journal of Experimental Biology, 202, 1243-1253.
Briscoe, S. D., & Ragsdale, C. W. (2019). Evolution of the chordate telencephalon. Current Biology, 29, 647-662. https://doi.org/10.1016/j.cub.2019.05.026.
Casini, A., Vaccaro, R., Toni, M., & Cioni, C. (2018). Distribution of choline acetyltransferase (ChAT) immunoreactivity in the brain of the teleost Cyprinus carpio. European Journal of Histochemistry, 62, 2932. https://doi.org/10.4081/ejh.2018.2932.
Castro, A., Becerra, M., Manso, M. J., & Anadón, R. (2006). Calretinin immunoreactivity in the brain of the zebrafish, Danio rerio: Distribution and comparison with some neuropeptides and neurotransmitter-synthesizing enzymes. II. Midbrain, hindbrain, and rostral spinal cord. Journal of Comparative Neurology, 494, 792-814. https://doi.org/10.1002/cne.20843.
Chacron, M. J., Longtin, A., & Maler, L. (2011). Efficient computation via sparse coding in electrosensory neural networks. Current Opinion in Neurobiology, 21, 752-760. https://doi.org/10.1016/j.conb.2011.05.016.
Chan, W., Singh, S., Keshav, T., Dewan, R., Eberly, C., Maurer, R., Nunez-Parra, A., & Araneda, R. (2017). Mice lacking M1 and M3 muscarinic acetylcholine receptors have impaired odor discrimination and learning. Frontiers in Synaptic Neuroscience, 9, 4. https://dx.doi.org/10.3389/fnsyn.2017.00004.
Clarke, S. E., Longtin, A., & Maler, L. (2015). Contrast coding in the electrosensory system: Parallels with visual computation. Nature Reviews in Neuroscience, 16, 733-744. https://doi.org/10.1038/nrn4037.
Clarke, S. E., & Maler, L. (2017). Feedback synthesizes neural codes for motion. Current Biology, 27, 1356-1361. https://doi.org/10.1016/j.cub.2017.03.068.
Clemente, D., Arenzana, F. J., Sanchez-Gonzalez, R., Porteros, A., Aijon, J., & Arevalo, R. (2005). Comparative analysis of the distribution of choline acetyltransferase in the central nervous system of cyprinids. Brain Research Bulletin, 66, 546-549. https://doi.org/10.1016/j.brainresbull.2005.02.017.
Clemente, D., Porteros, A., Weruaga, E., Alonso, J. R., Arenzana, F. J., Aijón, J., & Arévalo, R. (2004). Cholinergic elements in the zebrafish central nervous system: Histochemical and immunohistochemical analysis. Journal of Comparative Neurology, 474, 75-107. https://doi.org/10.1002/cne.20111.
Contestabile, A., Migani, P., & Cristini, G. (1979). Choline acetyltransferase activity in the cerebellum and in centers of lateral line system of teleosts. Brain Research Bulletin, 4, 859-861. https://doi.org/10.1016/0361-9230(79)90023-6.
Cronin, S. R., Khoury, A., Ferry, D. K., & Hampton, R. Y. (2000). Regulation of Hmg-Coa reductase degradation requires the P-type atpase Cod1p/Spf1p. Journal of Cellular Biology, 148, 915-924. https://dx.doi.org/10.1083/jcb.148.5.915.
Danielson, P. D., Zottoli, S. J., Corrodi, J. G., Rhodes, K. J., & Mufson, E. J. (1988). Localization of choline acetyltransferase to somata of posterior lateral line efferents in the goldfish. Brain Research, 448, 158-161. https://doi.org/10.1016/0006-8993(88)91112-2.
de Almeida, L., Idiart, M., Dean, O., Devore, S., Smith, D. M., & Linster, C. (2016). Internal cholinergic regulation of learning and recall in a model of olfactory processing. Frontiers in Cellular Neuroscience, 10, 256. https://doi.org/10.3389/fncel.2016.00256.
Delacalle, S., Hersh, L. B., & Saper, C. B. (1993). Cholinergic innervation of the human cerebellum. Journal of Comparative Neurology, 328, 364-376. https://doi.org/10.1002/cne.903280304.
Diamond, I. T., Fitzpatrick, D., & Conley, M. (1992). A projection from the parabigeminal nucleus to the pulvinar nucleus in galago. Journal of Comparative Neurology, 316, 375-382. https://doi.org/10.1002/cne.903160308.
Dunlap, K. D., Chung, M., & Castellano, J. F. (2013). Influence of long-term social interaction on chirping behavior, steroid levels and neurogenesis in weakly electric fish. Journal of Experimental Biology, 216, 2434-2441. https://doi.org/10.1242/jeb.082875.
Dunn, T. W., Gebhardt, C., Naumann, E. A., Riegler, C., Ahrens, M. B., Engert, F., & del Bene, F. (2016). Neural circuits underlying visually evoked escapes in larval zebrafish. Neuron, 89, 613-628. https://doi.org/10.1016/j.neuron.2015.12.021.
Dutar, P., Bassant, M. H., Senut, M. C., & Lamour, Y. (1995). The septohippocampal pathway: Structure and function of a central cholinergic system. Physiological Reviews, 75, 393-427. https://doi.org/10.1152/physrev.1995.75.2.393.
Ekström, P. (1987). Distribution of choline acetyltransferase-immunoreactive neurons in the brain of a cyprinid teleost (Phoxinus phoxinus L.). Journal of Comparative Neurology, 256, 494-495. https://doi.org/10.1002/cne.902560403.
Ellis, L. D., Krahe, R., Bourque, C. W., Dunn, R. J., & Chacron, M. J. (2007). Muscarinic receptors control frequency tuning through the downregulation of an A-type potassium current. Journal of Neurophysiology, 98, 1526-1537. https://dx.doi.org/10.1152/jn.00564.2007.
Ericsson, J., Silberberg, G., Robertson, B., Wikstrom, M. A., & Grillner, S. (2011). Striatal cellular properties conserved from lampreys to mammals. Journal of Physiology, 589, 2979-2992. https://doi.org/10.1113/jphysiol.2011.209643.
Felsenstein, J. (1989). PHYLIP-Phylogeny inference package. Cladistics, 5, 164-166.
Fernandes, A. M., Larsch, J., Donovan, J. C., Helmbrecht, T. O., Mearns, D., Kölsch, Y., Dal Maschio, M., & Baier, H. (2019). Neuronal circuitry for stimulus selection in the visual system. bioRxiv preprintdoi: https://doi.org/10.1101/598383.
Fournier, G. N., Semba, K., & Rasmusson, D. D. (2004). Modality- and region-specific acetylcholine release in the rat neocortex. Neuroscience, 126, 257-262. https://doi.org/10.1016/j.neuroscience.2004.04.002.
Gallagher, S. P., & Northmore, D. P. M. (2006). Responses of the teleostean nucleus isthmi to looming objects and other moving stimuli. Visual Neuroscience, 23, 209-219. https://doi.org/10.1017/s0952523806232061.
Ganz, J., Kaslin, J., Freudenreich, D., Machate, A., Geffarth, M., & Brand, M. (2012). Subdivisions of the adult zebrafish subpallium by molecular marker analysis. Journal of Comparative Neurology, 520, 633-655. https://doi.org/10.1002/cne.22757.
Giassi, A. C. C., Duarte, T. T., Ellis, W., & Maler, L. (2012). Organization of the gymnotiform fish pallium in relation to learning and memory: II. Extrinsic connections. Journal of Comparative Neurology, 520(3), 338-3368. https://doi.org/10.1002/cne.23109.
Giassi, A. C. C., Ellis, W., & Maler, L. (2012). Organization of the gymnotiform fish pallium in relation to learning and memory: III. Intrinsic connections. Journal of Comparative Neurology, 520(3), 369-3394. https://doi.org/10.1002/cne.23108.
Giassi, A. C. C., Harvey-Girard, E., Valsamis, B., & Maler, L. (2012). Organization of the gymnotiform fish pallium in relation to learning and memory: I. Cytoarchitectonics and cellular morphology. Journal of Comparative Neurology, 520(3), 314-3337. https://doi.org/10.1002/cne.23108.
González, A., Morona, R., Moreno, N., Bandín, S., & López, J. M. (2014). Identification of striatal and pallidal regions in the subpallium of anamniotes. Brain Behavior and Evolution, 83, 93-103. https://doi.org/10.1159/000357754.
Govindasamy, L., Pedersen, B., Lian, W., Kukar, T., Gu, Y., Jin, S., Agbandje-McKenna, M., Wu, D., & McKenna, R. (2004). Structural insights and functional implications of choline acetyltransferase. Journal of Structural Biology, 148, 226-235. https://doi.org/10.1016/j.jsb.2004.06.005.
Harvey-Girard, E., Giassi, A. C. C., Ellis, W., & Maler, L. (2012). Organization of the gymnotiform fish pallium in relation to learning and memory: IV. Expression of conserved transcription factors and implications for the evolution of dorsal telencephalon. Journal of Comparative Neurology, 520(3), 395-3413. https://doi.org/10.1002/cne.23107.
Harvey-Girard, E., Giassi, A. C. C., Ellis, W., & Maler, L. (2013). Expression of the cannabinoid CB1 receptor in the gymnotiform fish brain and its implications for the organization of the teleost pallium. Journal of Comparative Neurology, 521, 949-975. https://doi.org/10.1002/cne.23212.
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. Journal of Comparative Neurology, 518, 2666-2692. https://doi.org/10.1002/cne.22358.
Hasegawa, K., & Ogawa, H. (2007). Effects of acetylcholine on coding of taste information in the primary gustatory cortex in rats. Experimental Brain Research, 179, 97-109. https://doi.org/10.1007/s00221-006-0772-4.
Hasselmo, M. E. (2006). The role of acetylcholine in learning and memory. Current Opinion in Neurobiology, 16, 710-715. https://dx.doi.org/10.1016/j.conb.2006.09.002.
Heiligenberg, W., Keller, C., Metzner, W., & Kawasaki, M. (1991). Structure and function of neurons in the complex of the nucleus electrosensorius of the gymnotiform fish Eigenmannia: Detection and processing of electric signals in social communication. Journal of Comparative Physiology, 169, 151-164. https://doi.org/10.1007/BF00215862.
Heiligenberg, W., & Rose, G. J. (1987). The optic tectum of the gymnotiform electric fish, Eigenmannia: Labeling of physiologically identified cells. Neuroscience, 22, 331-340. https://doi.org/10.1016/0306-4522(87)90224-7.
Heilingoetter, C. L., & Jensen, M. B. (2016). Histological methods for ex vivo axon tracing: A systematic review. Neurological Research, 38, 561-569. https://doi.org/10.1080/01616412.2016.1153820.
Henriques, P. M., Rahman, N., Jackson, S. E., & Bianco, I. H. (2019). Nucleus isthmi is required to sustain target pursuit during visually guided prey-catching. Current Biology, 29, 1771-1786. https://doi.org/10.1016/j.cub.2019.04.064.
Herrero, L., Rodriguez, F., Salas, C., & Torres, B. (1998). Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish. Experimental Brain Research, 120, 291-305. https://doi.org/10.1007/s002210050403.
Hofmann, V., & Chacron, M. J. (2019). Novel functions of feedback in electrosensory processing. Frontiers in Integrative Neuroscience, 13, 52. https://dx.doi.org/10.3389/fnint.2019.00052.
Ichikawa, T., Ajiki, K., Matsuura, J., & Misawa, H. (1997). Localization of two cholinergic markers, choline acetyltransferase and vesicular acetylcholine transporter in the central nervous system of the rat: In situ hybridization histochemistry and immunohistochemistry. Journal of Chemical Neuroanatomy, 13, 23-39. https://doi.org/10.1016/s0891-0618(97)00021-5.
Ikeda, M., Houtani, T., Ueyama, T., & Sugimoto, T. (1991). Choline-acetyltransferase immunoreactivity in the cat cerebellum. Neuroscience, 45, 671-690. https://doi.org/10.1016/0306-4522(91)90280-2.
Imura, K., Yamamoto, N., Sawai, N., Yoshimoto, M., Yang, C. Y., Xue, H. G., & Ito, H. (2003). Topographical organization of an indirect telencephalo-cerebellar pathway through the nucleus paracommissuralis in a teleost, Oreochromis niloticus. Brain Behavior and Evolution, 61, 70-90. https://doi.org/10.1159/000069353.
Ito, H., & Yoshimoto, M. (1990). Cytoarchitecture and fiber connections of the nucleus lateralis valvulae in the carp Cyprinus carpio. Journal of Comparative Neurology, 298, 385-399. https://doi.org/10.1002/cne.902980402.
Jensen-Smith, H., Gray, B., Muirhead, K., Ohlsson-Wilhelm, B., & Fritzsch, B. (2007). Long-distance three-color neuronal tracing in fixed tissue using NeuroVue dyes. Immunological Investigations, 36, 763-789. https://doi.org/10.1080/08820130701706711.
Jones, B. E. (2003). Arousal systems. Frontiers in Bioscience, 8, S438-S451. https://doi.org/10.2741/1074.
Jun, J. J., Longtin, A., & Maler, L. (2016). Active sensing associated with spatial learning reveals memory-based attention in an electric fish. Journal of Neurophysiology, 115, 2577-2592. https://doi.org/10.1152/jn.00979.2015.
Kasashima, S., Muroishi, Y., Futakuchi, H., Nakanishi, I., & Oda, Y. (1998). In situ mRNA hybridization study of the distribution of choline acetyltransferase in the human brain. Brain Research, 806, 8-15. https://doi.org/10.1016/s0006-8993(98)00677-5.
Katz, E., Elgoyhen, A., & Fuchs, P. (2011). Cholinergic inhibition of hair cells. In D. K. Ryugo & R. R. Fay (Eds.), Auditory and vestibular efferents. Springer.
Ke, M., Fujimoto, S., & Imai, T. (2013). Optical Clearing of Fixed Brain Samples Using SeeDB. Nature Neuroscience, 16, 1154-1161. https://doi.org/10.1002/0471142301.ns0222s66.
Kimura, F. (2000). Cholinergic modulation of cortical function: A hypothetical role in shifting the dynamics in cortical network. Neuroscience Research, 38, 19-26. https://doi.org/10.1016/s0168-0102(00)00151-6.
Knudsen, E. I. (2011). Control from below: The role of a midbrain network in spatial attention. European Journal of Neuroscience, 33, 1961-1972. https://doi.org/10.1111/j.1460-9568.2011.07696.x.
Köppl, C. (2011). Evolution of the octavolateral efferent system. In D. K. Ryugo & R. R. Fay (Eds.), Auditory and vestibular efferents. Springer.
Krahe, R., & Maler, L. (2014). Neural maps in the electrosensory system of weakly electric fish. Current Opinion in Neurobiology, 24, 13-21. https://doi.org/10.1016/j.conb.2013.08.013.
Linke, R., Pabst, T., & Frotscher, M. (1995). Development of the hippocamposeptal projection in the rat. Journal of Comparative Neurology, 351, 602-616. https://doi.org/10.1002/cne.903510409.
López, J. M., Perlado, J., Morona, R., Northcutt, R. G., & González, A. (2013). Neuroanatomical organization of the cholinergic system in the central nervous system of a basal actinopterygian fish, the Senegal bichir Polypterus senegalus. Journal of Comparative Neurology, 521, 24-49. https://doi.org/10.1002/cne.23155.
Luque, M. A., Pérez-Pérez, M. P., Herrero, L., & Torres, B. (2005). Involvement of the optic tectum and mesencephalic reticular formation in the generation of saccadic eye movements in goldfish. Brain Research Reviews, 49, 388-397. https://doi.org/10.1016/j.brainresrev.2004.10.002.
Maczko, K. A., Knudsen, P. F., & Knudsen, E. I. (2006). Auditory and visual space maps in the cholinergic nucleus isthmi pars parvocellularis of the barn owl. Journal of Neuroscience, 26, 12799-12806. https://doi.org/10.1523/JNEUROSCI.3946-06.2006.
Maler, L., Collins, M., & Mathieson, W. B. (1981). The distribution of acetylcholinesterase and choline acetyl transferase in the cerebellum and posterior lateral line lobe of weakly electric fish (Gymnotidae). Brain Research, 226, 320-325. https://doi.org/10.1016/0006-8993(81)91106-9.
Maler, L., Sas, E., Carr, C. E., & Matsubara, J. (1982). Efferent projections of the posterior lateral line lobe in gymnotiform fish. Journal of Comparative Neurology, 211, 154-164. https://doi.org/10.1002/cne.902110205.
Maler, L., Sas, E., Johnston, S., & Ellis, W. (1991). An atlas of the brain of the electric fish Apteronotus leptorhynchus. Journal of Chemical Neuroanatomy, 4, 1-38. https://doi.org/10.1016/0891-0618(91)90030-g.
Martinez-Gonzalez, C., Bolam, J. P., & Mena-Segovia, J. (2011). Topographical organization of the pedunculopontine nucleus. Frontiers in Neuroanatomy, 5, 22. https://dx.doi.org/10.3389/fnana.2011.00022.
Meek, J., & Schellart, N. A. (1978). A Golgi study of goldfish optic tectum. Journal of Comparative Neurology, 182, 89-122. https://doi.org/10.1002/cne.901820107.
Mooney, D. M., Zhang, L., Basile, C., Senatorov, V. V., Ngsee, J., Omar, A., & Hu, B. (2004). Distinct forms of cholinergic modulation in parallel thalamic sensory pathways. PNAS, 101, 320-324. https://dx.doi.org/10.1073/pnas.0304445101.
Morona, R., López, J. M., Northcutt, R. G., & González, A. (2013). Comparative analysis of the organization of the cholinergic system in the brains of two holostean fishes, the Florida Gar Lepisosteus platyrhincus and the bowfin Amia calva. Brain Behavior and Evolution, 81, 109-142. https://doi.org/10.1159/000347111.
Mueller, T., Vernier, P., & Wullimann, M. F. (2004). The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio. Brain Research, 1011, 156-169. https://doi.org/10.1016/j.brainres.2004.02.073.
Mueller, T., Wullimann, M. F., & Guo, S. (2008). Early teleostean basal ganglia development visualized by Zebrafish Dlx2a, Lhx6, Lhx7, Tbr2 (eomesa), and GAD67 gene expression. Journal of Comparative Neurology, 507, 1245-1257. https://doi.org/10.1002/cne.21604.
Nieuwenhuys, R. (2009). The forebrain of actinopterygians revisited. Brain Behavior and Evolution, 73, 229-252. https://doi.org/10.1159/000225622.
Northmore, D. P. (1991). Visual responses of nucleus isthmi in a teleost fish Lepomis macrochirus. Vision Research, 31, 525-535. https://doi.org/10.1016/0042-6989(91)90103-C.
Oboti, L., Russo, E., Tran, T., Durstewitz, D., & Corbin, J. (2018). Amygdala Corticofugal input shapes mitral cell responses in the accessory olfactory bulb. eNeuro, 5, ENEURO.0175-ENEU18.2018. https://doi.org/10.1523/ENEURO.0175-18.2018.
Oda, Y. (1999). Choline acetyltransferase: The structure, distribution and pathologic changes in the central nervous system. Pathology International, 49, 921-937. https://doi.org/10.1046/j.1440-1827.1999.00977.x.
Ohno, K., Tsujino, A., Brengman, J. M., Harper, C. M., Bajzer, Z., Udd, B., Beyring, R., Robb, S., Kirkham, F. J., & Engel, A. G. (2001). Choline acetyltransferase mutations cause myasthenic syndrome associated with episodic apnea in humans. PNAS, 98, 2016-2022. https://doi.org/10.1073/pnas.98.4.2017.
Pérez, S. E., Yáñez, J., Marín, O., Anadón, R., González, A., & Rodríguez-Moldes, I. (2000). Distribution of choline acetyltransferase (ChAT) immunoreactivity in the brain of the adult trout and tract-tracing observations on the connections of the nuclei of the isthmus. Journal Comparative Neurology, 428, 450-474. https://doi.org/10.1002/1096-9861(20001218)428:3%3C450::aid-cne5%3E3.0.co;2-t.
Perez-Perez, M. P., Luque, M. A., Herrero, L., Nunez-Abades, P. A., & Torres, B. (2003). Afferent connectivity to different functional zones of the optic tectum in goldfish. Visual Neuroscience, 20, 397-410. https://doi.org/10.1017/S0952523803204053.
Phan, M., & Maler, L. (1983). Distribution of muscarinic receptors in the caudal cerebellum and electrosensory lateral line lobe of gymnotiform fish. Neuroscience Letters, 42, 137-143. https://doi.org/10.1016/0304-3940(83)90396-8.
Picciotto, M. R., Higley, M. J., & Mineur, Y. S. (2012). Acetylcholine as a neuromodulator: Cholinergic signaling shapes nervous system function and behavior. Neuron, 76, 116-129. https://dx.doi.org/10.1016/j.neuron.2012.08.036.
Salisbury, J. P., Sîrbulescu, R. F., Moran, B. M., Auclair, J. R., Zupanc, G. K. H., & Agar, J. N. (2015). The central nervous system transcriptome of the weakly electric brown ghost knifefish Apteronotus leptorhynchus: de novo assembly, annotation, and proteomic validation. BMC Genomics, 16, 166. https://doi.org/10.1186/s12864-015-1354-2.
Sarter, M., Hasselmo, M. E., Bruno, J. P., & Givens, B. (2005). Unraveling the attentional functions of cortical cholinergic inputs: Interactions between signal-driven and cognitive modulation of signal detection. Brain Research Reviews, 48, 98-111. https://doi.org/10.1016/j.brainresrev.2004.08.006.
Sas, E., & Maler, L. (1983). The nucleus praeeminentialis: A Golgi study of a feedback center in the electrosensory system of gymnotid fish. Journal of Comparative Neurology, 221, 127-144. https://doi.org/10.1002/cne.902210202.
Sas, E., & Maler, L. (1986a). Identification of a nucleus isthmi in the weakly electric fish Apteronotus leptorhynchus (Gymnotiformes). Brain Behavior and Evolution, 28, 170-185. https://doi.org/10.1159/000118701.
Sas, E., & Maler, L. (1986b). The optic tectum of gymnotiform teleosts Eigenmannia virescens and Apteronotus leptorhynchus: A Golgi study. Neuroscience, 18, 215-246. https://doi.org/10.1016/0306-4522(86)90190-9.
Sas, E., & Maler, L. (1987). The organization of afferent input to the caudal lobe of the cerebellum of the gymnotid fish Apteronotus leptorhynchus. Anatomy and Embryology, 177, 55-79. https://doi.org/10.1007/BF00325290.
Sas, E., Maler, L., & Weld, M. (1993). Connections of the olfactory bulb in the gymnotiform fish, Apteronotus leptorhynchus. Journal of Comparative Neurology, 335, 486-507. https://doi.org/10.1002/cne.903350403.
Sato, H., Hata, Y., Masui, H., & Tsumoto, T. (1987). A functional-role of cholinergic innervation to neurons in the cat visual-cortex. Journal of Neurophysiology, 58, 765-780. https://doi.org/10.1152/jn.1987.58.4.765.
Schmidt, J. T. (1995). The modulatory cholinergic system in goldfish tectum may be necessary for retinotopic sharpening. Visual Neuroscience, 12, 1093-1103. https://doi.org/10.1017/s095252380000674x.
Sillito, A. M., & Kemp, J. A. (1983). Cholinergic modulation of the functional-organization of the cat visual-cortex. Brain Research, 289, 143-155. https://doi.org/10.1016/0006-8993(83)90015-X.
Sillito, A. M., Kemp, J. A., & Berardi, N. (1983). The cholinergic influence on the function of the cat dorsal lateral geniculate-nucleus (DLGN). Brain Research, 280, 299-307. https://doi.org/10.1016/0006-8993(83)90059-8.
Silva, A. C., Perrone, R., Zubizarreta, L., Batista, G., & Stoddard, P. K. (2013). Neuromodulation of the agonistic behavior in two species of weakly electric fish that display different types of aggression. Journal of Experimental Biology, 216, 2412-2420. https://doi.org/10.1242/jeb.082180.
Smith, R. S., Hu, R., DeSouza, A., Eberly, C. L., Krahe, K., Chan, W., & Araneda, R. C. (2015). Differential muscarinic modulation in the olfactory bulb. Journal of Neuroscience, 35, 10773-10785. https://doi.org/10.1523/JNEUROSCI.0099-15.2015.
Stephenson-Jones, M., Ericsson, J., Robertson, B., & Grillner, S. (2012). Evolution of the basal ganglia: Dual-output pathways conserved throughout vertebrate phylogeny. Journal of Comparative Neurology, 520, 2957-2973. https://doi.org/10.1002/cne.23087.
Tomchik, S. M., & Lu, Z. (2006). Auditory physiology and anatomy of octavolateral efferent neurons in a teleost fish. Journal of Comparative Physiology, 192, 51-67. https://doi.org/10.1007/s00359-005-0050-0.
Toscano-Márquez, B., Dunn, R. J., & Krahe, R. (2013). Distribution of muscarinic acetylcholine receptor mRNA in the brain of the weakly electric fish Apteronotus leptorhynchus. Journal of Comparative Neurology, 521, 1054-1072. https://doi.org/10.1002/cne.23218.
Toscano-Márquez, B., Krahe, R., & Chacron, M. J. (2013). Neuromodulation of early electrosensory processing in gymnotiform weakly electric fish. Journal of Experimental Biology, 216, 2442-2450. https://doi.org/10.1242/jeb.082370.
Wallach, A., Harvey-Girard, E., Jun, J. J., Longtin, A., & Maler, L. (2018). A time-stamp mechanism may provide temporal information necessary for egocentric to allocentric spatial transformations. eLife, 7, e36769. https://doi.org/10.7554/elife.36769.
Walz, H., Hupe, G. J., Benda, J., & Lewis, J. E. (2013). The neuroethology of electrocommunication: How signal background influences sensory encoding and behaviour in Apteronotus leptorhynchus. Journal of Physiology Paris, 107, 13-25. https://doi.org/10.1016/j.jphysparis.2012.07.001.
Wang, S. R. (2003). The nucleus isthmi and dual modulation of the receptive field of tectal neurons in non-mammals. Brain Research Reviews, 41, 13-25. https://doi.org/10.1016/S0165-0173(02)00217-5.
Wang, Y., Luksch, H., Brecha, N. C., & Karten, H. J. (2006). Columnar projections from the cholinergic nucleus isthmi to the optic tectum in chicks (Gallus gallus): A possible substrate for synchronizing tectal channels. Journal of Comparative Neurology, 494, 7-35. https://doi.org/10.1002/cne.20821.
Wong, C. J. H. (1997). Connections of the basal forebrain of the weakly electric fish, Eigenmannia virescens. Journal of Comparative Neurology, 389, 49-64. https://doi.org/10.1002/(SICI)1096-9861(19971208)389:1<49::AID-CNE4>3.0.CO;2-E.
Woolf, N. J., & Butcher, L. L. (2011). Cholinergic systems mediate action from movement to higher consciousness. Behavioral Brain Research, 221, 488-498. https://doi.org/10.1016/j.bbr.2009.12.046.
Wullimann, M. F., & Mueller, T. (2004). Teleostean and mammalian forebrains contrasted: Evidence from genes to behavior. Journal of Comparative Neurology, 475, 143-162. https://doi.org/10.1002/cne.20183.
Wullimann, M. F., Rupp, B., & Reichert, H. (1996). The brain of the zebrafish Danio rerio: A neuroanatomical atlas. In Neuroanatomy of the Zebrafish brain. Birkhäuser Verlag.
Xue, H. G., Yamamoto, N., Yoshimoto, M., Yang, C. Y., & Ito, H. (2001). Fiber connections of the nucleus isthmi in the carp (Cyprinus carpio) and tilapia (Oreochromis niloticus). Brain Behavior and Evolution, 58, 185-204. https://doi.org/10.1159/000057563.
Xue, H. G., Yang, C. Y., Yamamoto, N., Ito, H., & Ozawa, H. (2005). An indirect trigeminocerebellar pathway through the nucleus lateralis valvulae in a perciform teleost, Oreochromis niloticus. Neuroscience Letters, 390, 104-108. https://doi.org/10.1016/j.neulet.2005.08.007.
Yáñez, J., Souto, Y., Piñeiro, L., Folgueira, M., & Anadón, R. (2017). Gustatory and general visceral centers and their connections in the brain of adult zebrafish: A carbocyanine dye tract-tracing study. Journal of Comparative Neurology, 525, 333-362. https://doi.org/10.1002/cne.24068.
Yang, C. Y., Yoshimoto, M., Xue, H. G., Yamamoto, N., Imura, K., Sawai, N., Ishikawa, Y., & Ito, H. (2004). Fiber connections of the lateral valvular nucleus in a percomorph teleost, tilapia (Oreochromis niloticus). Journal of Comparative Neurology, 474, 209-226. https://doi.org/10.1002/cne.20150.
Yasuyama, K., & Salvaterra, P. M. (1999). Localization of choline acetyltransferase-expressing neurons in Drosophila nervous system. Microscopy Research and Technique, 45, 65-79. https://doi.org/10.1002/(sici)1097-0029(19990415)45:2<65::aid-jemt2>3.0.co;2-0.
Yoshida, K., Rutishauser, U., Crandall, J. E., & Schwarting, G. A. (1999). Polysialic acid facilitates migration of luteinizing hormone-releasing hormone neurons on vomeronasal axons. Journal of Neuroscience, 19, 794-801. https://doi.org/10.1523/jneurosci.19-02-00794.1999.
Zottoli, S. J., Rhodes, K. J., Corrodi, J. G., & Mufson, E. J. (1988). Putative cholinergic projections from the nucleus isthmi and the nucleus reticularis mesencephali to the optic tectum in the goldfish (Carassius auratus). Journal of Comparative Neurology, 273, 385-398. https://doi.org/10.1002/cne.902730309.

Auteurs

Brenda Toscano-Márquez (B)

Department of Biology, McGill University, Montreal, Quebec.

Livio Oboti (L)

Humboldt-Universität zu Berlin, Institut für Biologie, Berlin, Germany.

Erik Harvey-Girard (E)

Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Ontario, Canada.

Leonard Maler (L)

Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Ontario, Canada.

Rüdiger Krahe (R)

Department of Biology, McGill University, Montreal, Quebec.
Humboldt-Universität zu Berlin, Institut für Biologie, Berlin, Germany.

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