Neural maps in the electrosensory system of weakly electric fish

Current Opinion in Neurobiology

Volumn 24, Issue 1, 2014, Pages 13-21

  Krahe, Rüdiger ^a   Maler, Leonard ^b  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BODY SURFACE; BRAIN MAPPING; ELECTRIC FISH; ELECTRORECEPTOR; ELECTROSENSORY LATERAL LINE LOBE; ELECTROSENSORY SYSTEM; INTERPERSONAL COMMUNICATION; LATERAL LINE SYSTEM; MESENCEPHALON; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW; RHOMBENCEPHALON; SENSORY STIMULATION; SENSORY SYSTEM; SPATIOTEMPORAL ANALYSIS;

ANIMALS; BRAIN; ELECTRIC FISH; LATERAL LINE SYSTEM; NERVE NET;

EID: 84883641163     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2013.08.013     Document Type: Review

References (59)

1. Mountcastle V.B. The columnar organization of the neocortex. Brain 1997, 120:701-722.
2. McCreery D.B. Spatial organization of receptive fields of lateral lemniscus neurons of the lateral line lobe of the catfish Ictalurus nebulosus. J Comp Physiol A 1977, 113:341-353.
3. Wojtenek W., Pei X., Wilkens L.A. Paddlefish strike at artificial dipoles simulating the weak electric fields of planktonic prey. J Exp Biol 2001, 204:1391-1399.
4. Gillis J.A., Modrell M.S., Northcutt R.G., Catania K.C., Luer C.A., Baker C.V.H. Electrosensory ampullary organs are derived from lateral line placodes in cartilaginous fishes. Development 2012, 139:3142-3146.
5. Modrell M.S., Bemis W.E., Northcutt R.G., Davis M.C., Baker C.V.H. Electrosensory ampullary organs are derived from lateral line placodes in bony fishes. Nat Commun 2011, 2.
6. Alves-Gomes J. The evolution of electroreception and bioelectrogenesis in teleost fish: a phylogenetic perspective. J Fish Biol 2001, 58:1489-1511.
7. Bullock T.H., Hopkins C.D., Popper A.N., Fay R.R. Electroreception 2005, Springer, New York.
8. Bell C.C., Maler L. Central neuroanatomy of electrosensory systems in fish. Electroreception 2005, 68-111. Springer, Springer Handbook of Auditory Research. T.H. Bullock, C.D. Hopkins, A.N. Popper, R.R. Fay (Eds.).
9. New J.G., Singh S. Central topography of anterior lateral line nerve projections in the channel catfish, Ictalurus punctatus. Brain Behav Evol 1994, 43:34-50.
10. Carr C.E., Maler L., Sas E. Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish. J Comp Neurol 1982, 211:139-153.
11. Lannoo M.J., Maler L., Tinner B. Ganglion cell arrangement and axonal trajectories in the anterior lateral line nerve of the weakly electric fish Apteronotus leptorhynchus (Gymnotiformes). J Comp Neurol 1989, 280:331-342.
12. Chacron M.J., Longtin A., Maler L. Efficient computation via sparse coding in electrosensory neural networks. Curr Opin Neurobiol 2011, 21:752-760.
13. Marsat G., Longtin A., Maler L. Cellular and circuit properties supporting different sensory coding strategies in electric fish and other systems. Curr Opin Neurobiol 2012, 22:686-692.
14. Maler L. Receptive field organization across multiple electrosensory maps. I. Columnar organization and estimation of receptive field size. J Comp Neurol 2009, 516:376-393.
15. Bastian J., Chacron M.J., Maler L. Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J Neurosci 2002, 22:4577-4590.
16. Chacron M.J. Nonlinear information processing in a model sensory system. J Neurophysiol 2006, 95:2933-2946.
17. Bastian J., Chacron M.J., Maler L. Plastic and nonplastic pyramidal cells perform unique roles in a network capable of adaptive redundancy reduction. Neuron 2004, 41:767-779.
18. Marsat G., Maler L. Preparing for the unpredictable: adaptive feedback enhances the response to unexpected communication signals. J Neurophysiol 2012, 107:1241-1246.
19. Maler L. Receptive field organization across multiple electrosensory maps. II. Computational analysis of the effects of receptive field size on prey localization. J Comp Neurol 2009, 516:394-422.
20. Krahe R., Bastian J., Chacron M.J. Temporal processing across multiple topographic maps in the electrosensory system. J Neurophysiol 2008, 100:852-867.
21. Mehaffey W.H., Maler L., Turner R.W. Intrinsic frequency tuning in ELL pyramidal cells varies across electrosensory maps. J Neurophysiol 2008, 99:2641-2655.
22. Nelson M.E., MacIver M.A. Prey capture in the weakly electric fish Apteronotus albifrons: Sensory acquisition strategies and electrosensory consequences. J Exp Biol 1999, 202:1195-1203.
23. Bol K., Marsat G., Harvey-Girard E., Longtin A., Maler L. Frequency-tuned cerebellar channels and burst-induced LTD lead to the cancellation of redundant sensory inputs. J Neurosci 2011, 31:11028-11038.
24. Middleton J.W., Longtin A., Benda J., Maler L. Postsynaptic receptive field size and spike threshold determine encoding of high-frequency information via sensitivity to synchronous presynaptic activity. J Neurophysiol 2009, 101:1160-1170.
25. Ellis L.D., Mehaffey W.H., Harvey-Girard E., Turner R.W., Maler L., Dunn R.J. SK channels provide a novel mechanism for the control of frequency tuning in electrosensory neurons. J Neurosci 2007, 27:9491-9502.
26. Benda J., Longtin A., Maler L. A synchronization-desynchronization code for natural communication signals. Neuron 2006, 52:347-358.
27. Turner R.W., Lemon N., Doiron B., Rashid A.J., Morales E., Longtin A., Maler L., Dunn R.J. Oscillatory burst discharge generated through conditional backpropagation of dendritic spikes. J Physiol (Paris) 2002, 96:517-530.
28. Gabbiani F., Metzner W., Wessel R., Koch C. From stimulus encoding to feature extraction in weakly electric fish. Nature 1996, 384:564-567.
29. Krahe R., Gabbiani F. Burst firing in sensory systems. Nat Rev Neurosci 2004, 5:13-23.
30. Metzner W., Koch C., Wessel R., Gabbiani F. Feature extraction by burst-like spike patterns in multiple sensory maps. J Neurosci 1998, 18:2283-2300.
31. Marsat G., Proville R.D., Maler L. Transient signals trigger synchronous bursts in an identified population of neurons. J Neurophysiol 2009, 102:714-723.
32. Marsat G., Maler L. Neural heterogeneity and efficient population codes for communication signals. J Neurophysiol 2010, 104:2543-2555.
33. Ávila-Ǻkerberg O., Krahe R., Chacron M.J. Neural heterogeneities and stimulus properties affect burst coding in vivo. Neuroscience 2010, 168:300-313.
34. Ellis L.D., Krahe R., Bourque C.W., Dunn R.J., Chacron M.J. Muscarinic receptors control frequency tuning through the downregulation of an A-type potassium current. J Neurophysiol 2007, 98:1526-1537.
35. Toscano Márquez B., Dunn R.J., Krahe R. Distribution of muscarinic acetylcholine receptor mRNA in the brain of the weakly electric fish, Apteronotus leptorhynchus. J Comp Neurol 2013, 521:1054-1072.
36. Deemyad T., Maler L., Chacron M.J. Inhibition of SK and M channel-mediated currents by 5-HT enables parallel processing by bursts and isolated spikes. J Neurophysiol 2011, 105:1276-1294.
37. Summers C.H., Winberg S. Interactions between the neural regulation of stress and aggression. J Exp Biol 2006, 209:4581-4589.
38. Metzner W., Juranek J. A sensory brain map for each behavior. Proc Natl Acad Sci U S A 1997, 94:14798-14803.
39. Carr C.E., Maler L., Heiligenberg W., Sas E. 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 1981, 203:649-670.
40. Heiligenberg W., Rose G. 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 1985, 5:515-531.
41. Rose G., Heiligenberg W. Structure and function of electrosensory neurons in the Torus semicircularis of Eigenmannia: morphological correlates of phase and amplitude sensitivity. J Neurosci 1985, 5:2269-2280.
42. Rose G., Heiligenberg W. Neural coding of difference frequencies in the midbrain of the electric fish Eigenmannia: reading the sense of rotation in an amplitude-phase plane. J Comp Physiol A: Sensory Neural Behav Physiol 1986, 158:613-624.
43. Metzner W., Heiligenberg W. 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: Sensory Neural Behav Physiol 1991, 169:135-150.
44. McGillivray P.M., Vonderschen K., Fortune E.S., Chacron M.J. Parallel coding of first- and second-order stimulus attributes by midbrain electrosensory neurons. J Neurosci 2012, 32:5510-5524.
45. Vonderschen K., Chacron M.J. Sparse and dense coding of natural stimuli by distinct midbrain neuron subpopulations in weakly electric fish. J Neurophysiol 2011, 106:3102-3118.
46. Khosravi-Hashemi N., Fortune E.S., Chacron M.J. Coding of movement direction by burst firing in electrosensory neurons. J Neurophysiol 2011, 106:1954-1968.
47. Khosravi-Hashemi N., Chacron M.J. Bursts and isolated spikes code for opposite movement directions in midbrain electrosensory neurons. PLoS ONE 2012, 7:e40339.
48. Bastian J. Vision and electroreception: integration of sensory information in the optic tectum of the weakly electric fish Apteronotus albifrons. J Comp Physiol A: Sensory Neural Behav Physiol 1982, 147:287-297.
49. Sas E., Maler L. The optic tectum of gymnotiform teleosts Eigenmannia virescens and Apteronotus leptorhynchus: a Golgi study. Neuroscience 1986, 18:215-246.
50. Hupé G.J., Lewis J.E. Electrocommunication signals in free swimming brown ghost knifefish, Apteronotus leptorhynchus. J Exp Biol 2008, 211:1657-1667.
51. Yu N., Hupé G.J., Garfinkle C., Lewis J.E., Longtin A. Coding conspecific identity and motion in the electric sense. PLoS Comp Biol 2012, 8:e1002564.
52. Stamper S., Fortune E.S., Chacron M.J. Perception and coding of envelopes in weakly electric fishes. J Exp Biol 2013, 216:2393-2402.
53. Fotowat H., Harrison R.R., Krahe R. The statistics of the electrosensory input in the freely swimming weakly electric fish Apteronotus leptorhynchus. J Neurosci 2013, 33:13758-13772.
54. Heiligenberg W., Rose G.J. The optic tectum of the gymnotiform electric fish, Eigenmannia: labeling of physiologically identified cells. Neuroscience 1987, 22:331-340.
55. Giassi A.C.C., Duarte T.T., Ellis W., Maler L. Organization of the gymnotiform fish pallium in relation to learning and memory: II. Extrinsic connections. J Comp Neurol 2012, 520:3338-3368.
56. Giassi A.C.C., Ellis W., Maler L. Organization of the gymnotiform fish pallium in relation to learning and memory: III. Intrinsic connections. J Comp Neurol 2012, 520:3369-3394.
57. Harvey-Girard E., Tweedle J., Ironstone J., Cuddy M., Ellis W., Maler L. Long-term recognition memory of individual conspecifics is associated with telencephalic expression of Egr-1 in the electric fish Apteronotus leptorhynchus. J Comp Neurol 2010, 518:2666-2692.
58. Harvey-Girard E., Giassi A.C.C., Ellis W., Maler L. 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. J Comp Neurol 2012, 520:3395-3413.
59. O'Keefe J. Hippocampal neurophysiology in the behaving animal. The hippocampus book 2007, 475-584. Oxford University Press. P. Anderson, R. Morris, D. Amaral, T. Bliss, J. O'Keefe (Eds.).