Electrosensory processing in Apteronotus albifrons: implications for general and specific neural coding strategies across wave-type weakly electric fish species.
Understanding how the brain processes sensory input to generate behavior remains an important problem in neuroscience. Towards this end, it is useful to compare results obtained across multiple species to gain understanding as to the general principles of neural coding. Here we investigated hindbrain pyramidal cell activity in the weakly electric fish Apteronotus albifrons We found strong heterogeneities when looking at baseline activity. Additionally, ON- and OFF-type cells responded to increases and decreases of sinusoidal and noise stimuli, respectively. While both cell types displayed band-pass tuning, OFF-type cells were more broadly tuned than their ON-type counterparts. The observed heterogeneities in baseline activity as well as the greater broadband tuning of OFF-type cells were both similar to those previously reported in other weakly electric fish species, suggesting that they constitute general features of sensory processing. However, we found that peak tuning occurred at frequencies ∼15 Hz in A. albifrons, which is much lower than values reported in the closely related species Apteronotus leptorhynchus and the more distantly related species Eigenmannia virescens In response to stimuli with time-varying amplitude (i.e., envelope), ON- and OFF-type cells displayed similar high-pass tuning curves characteristic of fractional differentiation and possibly indicate optimized coding. These tuning curves were qualitatively similar to those of pyramidal cells in the closely related species A. leptorhynchus In conclusion, comparison between our and previous results reveals general and species-specific neural coding strategies. We hypothesize that differences in coding strategies, when observed, result from different stimulus distributions in the natural/social environment.
Department of Physiology, McGill University, Montreal, Quebec, Canada.
Diana
0000-0003-0982-4092
D
Martinez
Department of Physiology, McGill University, Montreal, Quebec, Canada.
Michael G
MG
Metzen
Department of Physiology, McGill University, Montreal, Quebec, Canada maurice.chacron@mcgill.ca.
Maurice J
MJ
Chacron
D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D004555:Electric Fish / Q000502:physiology*; D004557:Electric Organ / Q000166:cytology* / Q000502:physiology; D005260:Female; D008297:Male; D008959:Models, Neurological; D009068:Movement; D009622:Noise; D017966:Pyramidal Cells / Q000145:classification* / Q000502:physiology*; D012677:Sensation / Q000502:physiology*; D013045:Species Specificity; D013997:Time Factors
behavior; envelopes; neural coding; tuning
J Neurosci. 1989 Dec;9(12):4388-99
2593005
Neuron. 2014 Sep 17;83(6):1256-8
25233308
Nat Rev Neurosci. 2011 Jun 20;12(7):415-26
21685932
J Neurophysiol. 2009 Aug;102(2):714-23
19474165
PLoS Comput Biol. 2012;8(7):e1002564
22807662
Nat Rev Neurosci. 2015 Dec;16(12):733-44
26558527
Phys Rev E Stat Nonlin Soft Matter Phys. 2015 Apr;91(4):042717
25974537
Curr Opin Neurobiol. 2009 Aug;19(4):439-44
19647992
J Chem Neuroanat. 1991 Jan-Feb;4(1):1-38
2012682
J Neurophysiol. 2006 May;95(5):2933-46
16495358
J Neurosci. 2013 Aug 21;33(34):13758-72
23966697
J Exp Biol. 2012 Dec 1;215(Pt 23):4196-207
23136154
J Neurophysiol. 2008 Aug;100(2):852-67
18509073
Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14798-803
9405693
Nat Neurosci. 2013 Jul;16(7):942-8
23749146
J Neurophysiol. 2016 Apr;115(4):2158-75
26843601
Nature. 2003 May 1;423(6935):77-81
12721628
ILAR J. 2009;50(4):361-72
19949252
Behav Brain Res. 2010 Mar 5;207(2):368-76
19874855
J Exp Biol. 2012 May 1;215(Pt 9):1567-74
22496294
J Neurosci. 1989 Dec;9(12):4400-15
2556508
Front Neural Circuits. 2016 Jul 26;10:54
27507937
Nat Rev Neurosci. 2005 May;6(5):389-97
15861181
J Neurophysiol. 2009 Oct;102(4):2273-87
19675292
J Exp Biol. 2007 Jul;210(Pt 14):2501-9
17601954
J Comp Neurol. 1981 Jan 1;195(1):87-139
7204653
PLoS Comput Biol. 2015 Jan 08;11(1):e1004034
25569283
J Comp Neurol. 1979 Jan 15;183(2):323-63
762262
J Exp Biol. 1999 May;202(# (Pt 10)):1267-79
10210667
Physiol Rep. 2014 Mar 20;2(3):e00253
24760508
Curr Opin Neurobiol. 2012 Aug;22(4):686-92
22326255
Trends Neurosci. 2015 May;38(5):273-8
25800324
Proc Natl Acad Sci U S A. 2015 Apr 14;112(15):4791-6
25825717
J Physiol Paris. 2002 Sep-Dec;96(5-6):451-8
14692493
Elife. 2016 Jun 21;5:
27328322
J Neurosci. 2012 Apr 18;32(16):5510-24
22514313
J Neurosci. 2015 Feb 18;35(7):3124-38
25698748
Elife. 2016 Apr 29;5:
27128376
Nat Commun. 2016 Apr 18;7:11353
27088670
J Neurosci. 2001 Jul 15;21(14):5328-43
11438609
Proc Natl Acad Sci U S A. 2013 Nov 26;110(48):19609-14
24218585
Zoolog Sci. 2009 Sep;26(9):587-99
19799509
J Neurosci. 1998 Sep 15;18(18):7599-611
9736677
J Neurosci. 1998 Mar 15;18(6):2283-300
9482813
Arch Neurol. 2012 Aug;69(8):987-93
22473771
Curr Opin Neurobiol. 2011 Oct;21(5):752-60
21683574
J Neurosci. 2005 Jun 8;25(23):5521-32
15944380
Neuroscience. 2011 Jan 13;172:270-84
21035523
J Exp Biol. 2008 May;211(Pt 10):1657-67
18456893
Curr Opin Neurobiol. 2014 Feb;24(1):13-21
24492073
Elife. 2015 Aug 04;4:e08163
26238277
J Neurosci. 2002 Mar 15;22(6):2374-82
11896176
Nat Neurosci. 2008 Nov;11(11):1335-42
18931665
J Neurophysiol. 2008 Apr;99(4):1825-35
18256161
Nature. 1996 Dec 12;384(6609):564-7
8955269
J Comput Neurosci. 2000 Mar-Apr;8(2):95-112
10798596
Neural Comput. 2001 Apr;13(4):717-49
11255566
J Neurophysiol. 2011 Dec;106(6):3102-18
21940609
PLoS Comput Biol. 2015 Oct 16;11(10):e1004430
26474395
J Exp Biol. 2013 Jul 1;216(Pt 13):2393-402
23761464
J Neurosci. 1996 Jan;16(1):380-91
8613805
Nat Neurosci. 2009 Apr;12(4):463-73
19287389
Ann N Y Acad Sci. 1971 Dec 3;188:242-69
4331616
J Neurosci. 2016 Sep 21;36(38):9859-72
27656024
Nat Rev Neurosci. 2007 Sep;8(9):700-11
17704812
J Exp Biol. 2014 Apr 15;217(Pt 8):1381-91
24363423
J Neurosci. 2000 Sep 1;20(17):6672-83
10964972
J Comput Neurosci. 2008 Aug;25(1):1-24
18176850
J Neurosci. 2002 Apr 1;22(7):2737-47
11923439
Proc Natl Acad Sci U S A. 2006 Sep 26;103(39):14596-601
16983081
Sci Rep. 2016 Jun 28;6:28716
27349635
Network. 1996;7(1):61-85
29480147
J Neurophysiol. 2001 Jan;85(1):10-22
11152701