Neurons can anticipate incoming signals by exploiting a physiological mechanism that is not well understood. This article offers a novel explanation on how a receiver neuron can predict the sender’s dynamics in a unidirectionally-coupled configuration, in which both sender and receiver follow the evolution of a multi-scale excitable system. We present a novel theoretical viewpoint based on a mathematical object, called canard, to explain anticipation in excitable systems. We provide a numerical approach, which allows to determine the transient effects of canards. To demonstrate the general validity of canard-mediated anticipation in the context of excitable systems, we illustrate our framework in two examples, a multi-scale radio-wave circuit (the van der Pol model) that inspired a caricature neuronal model (the FitzHugh-Nagumo model) and a biophysical neuronal model (a 2-dimensional reduction of the Hodgkin-Huxley model), where canards act as messengers to the senders’ prediction. We also propose an experimental paradigm that would enable experimental neuroscientists to validate our predictions. We conclude with an outlook to possible fascinating research avenues to further unfold the mechanisms underpinning anticipation. We envisage that our approach can be employed by a wider class of excitable systems with appropriate theoretical extensions.

1.
H. U.
Voss
, “
Anticipating chaotic sychronization
,”
Phys. Rev. E
61
,
5115
(
2000
).
2.
M.
Ciszak
,
O.
Calvo
,
C.
Masoller
,
C. R.
Mirasso
, and
R.
Toral
, “
Anticipating the response of excitable systems driven by random forcing
,”
Phys. Rev. Lett.
90
,
204102
(
2003
).
3.
F.
Matias
,
P.
Carrelli
,
C. R.
Mirasso
, and
M.
Copelli
, “
Anticipated synchronization in a biologically plausible model of neuronal motifs
,”
Phys. Rev. E
84
,
021922
(
2011
).
4.
M.
Ciszak
,
F.
Marino
,
R.
Toral
, and
S.
Balle
, “
Dynamical mechanism of anticipating synchronization in excitable systems
,”
Phys. Rev. Lett.
93
,
114102
(
2004
).
5.
M.
Hashemi
,
A.
Valizadeh
, and
Y.
Azizi
, “
Effect of duration of synaptic activity on spike rate of a Hodgkin-Huxley neuron with delayed feedback
,”
Phys. Rev. E
85
,
021917
(
2012
).
6.
F. S.
Matias
,
L. L.
Gollo
,
P. V.
Carelli
,
S. L.
Bressler
,
M.
Copelli
, and
C. R.
Mirasso
, “
Modeling positive Granger causality and negative phase lag between cortical areas
,”
NeuroImage
99
,
411
418
(
2014
).
7.
C. R.
Mirasso
,
P.
Carrelli
,
T.
Pereira
,
F.
Matias
, and
M.
Copelli
, “
Anticipated and zero-lag synchronization in motifs of delay-coupled systems
,”
Chaos
27
,
114305
(
2017
).
8.
T.
Pyragienė
and
K.
Pyragas
, “
Anticipating spike synchronization in nonidentical chaotic neurons
,”
Nonlinear Dyn.
74
,
297
306
(
2013
).
9.
C.
Masoller
, “
Anticipation in the synchronization of chaotic semiconductor lasers with optical feedback
,”
Phys. Rev. Lett.
86
,
2782
2785
(
2001
).
10.
M.
Ciszak
,
C. R.
Mirasso
,
R.
Toral
, and
O.
Calvo
, “
Predict-prevent control method for perturbed excitable systems
,”
Phys. Rev. E
79
,
046203
(
2009
).
11.
H.
Weia
and
L.
Li
, “
Estimating parameters with anticipating chaotic synchronization
,”
Chaos
20
,
023112
(
2010
).
12.
C.
Mayol
,
C. R.
Mirasso
, and
R.
Toral
, “
Anticipated synchronization and the predict-prevent control method in the FitzHugh–Nagumo model system
,”
Phys. Rev. E
85
,
056216
(
2012
).
13.
S.
Sivaprakasam
,
E.
Shahverdiev
,
P.
Spencer
, and
K. A.
Shore
, “
Experimental demonstration of anticipating synchronization in chaotic semiconductor lasers with optical feedback
,”
Phys. Rev. Lett.
87
,
154101
(
2001
).
14.
A. N.
Pisarchik
,
R.
Jaimes-Reátegui
, and
J. H.
García-López
, “
Synchronization of coupled bistable chaotic systems: Experimental study
,”
Philos. Trans. R. Soc. Lond. A Math. Phys. Eng. Sci.
366
,
459
473
(
2008
).
15.
J. N.
Blakely
,
M. W.
Pruitt
, and
N. J.
Corron
, “
Time shifts and correlations in synchronized chaos
,”
Chaos
18
,
013117
(
2008
).
16.
Y.
Liu
,
Y.
Takiguchi
,
P.
Davis
,
T.
Aida
,
S.
Saito
, and
J.
Liu
, “
Experimental observation of complete chaos synchronization in semiconductor lasers
,”
Appl. Phys. Lett.
80
,
4306
4308
(
2002
).
17.
S.
Tang
and
J.
Liu
, “
Experimental verification of anticipated and retarded synchronization in chaotic semiconductor lasers
,”
Phys. Rev. Lett.
90
,
194101
(
2003
).
18.
N. J.
Corron
,
J. N.
Blakely
, and
S. D.
Pethel
, “
Lag and anticipating synchronization without time-delay coupling
,”
Chaos
15
,
023110
(
2005
).
19.
L. M.
Pecora
and
T. L.
Carrol
, “
Synchronization in chaotic systems
,”
Phys. Rev. Lett.
64
,
821
(
1990
).
20.
L. M.
Pecora
and
T. L.
Carrol
, “
Driving systems with chaotic signals
,”
Phys. Rev. A
44
,
2374
2383
(
1991
).
21.
K.
Pyragas
and
T.
Pyragienė
, “
Coupling design for a long-term anticipating synchronization of chaos
,”
Phys. Rev. E
78
,
0462217
(
2008
).
22.
F.
Matias
,
P.
Carrelli
,
C. R.
Mirasso
, and
M.
Copelli
, “
Anticipated synchronization in neuronal circuits unveiled by a phase-response-curve analysis
,”
Phys. Rev. E
95
,
052410
(
2017
).
23.
M.
Desroches
,
M.
Krupa
, and
S.
Rodrigues
, “
Inflection, canards and excitability threshold in neuronal models
,”
J. Math. Biol.
67
,
989
1017
(
2013
).
24.
E.
Köksal Ersöz
,
M.
Desroches
, and
M.
Krupa
, “
Synchronization of weakly coupled canard oscillators
,”
Physica D
349
,
46
61
(
2017
).
25.
H. B.
Keller
,
Lectures on Numerical Methods in Bifurcation Problems
(
Springer Verlag
,
1986
).
26.
E.
Benoît
,
J. L.
Callot
,
F.
Diener
, and
M.
Diener
, “
Chasse au canard
,”
Collect Math.
31–32
,
37
119
(
1981
).
27.
M.
Brøns
, “
Bifurcations and instabilities in the Greitzer model for compressor system surge
,”
Math. Eng. Ind.
2
,
51
63
(
1988
).
28.
S. A.
Prescott
,
Y.
De Koninck
, and
T. J.
Sejnowski
, “
Biophysical basis for three distinct dynamical mechanisms of action potential initiation
,”
PLoS Comput. Biol.
4
,
e1000198
(
2008
).
29.
P.
De Maesschalck
and
M.
Desroches
, “
Numerical continuation techniques for planar slow-fast systems
,”
SIAM J. Appl. Dyn. Syst.
12
,
1159
1180
(
2013
).
30.
B.
Ermentrout
and
D.
Terman
,
Mathematical Foundations of Neuroscience
(
Springer
,
2010
).
31.
M.
Diener
, “
The canard unchained or how fast/slow dynamical systems bifurcate
,”
Math. Intell.
6
,
38
48
(
1984
).
32.
W.
Eckhaus
, “
Relaxation oscillations including a standard chase on french ducks
,”
Lect. Notes Math.
985
,
449
494
(
1983
).
33.
F.
Dumortier
and
R.
Roussarie
, “
Canard cycles and center manifolds
,”
Mem. Am. Math. Soc.
121
(577),
x+100
(published online
1996
).
34.
M.
Krupa
and
P.
Szmolyan
, “
Extending geometric singular perturbation theory to nonhyperbolic points—Fold and canard points in two dimensions
,”
SIAM J. Math. Anal.
33
,
286
314
(
2001
).
35.
J.
Mitry
,
M.
McCarthy
,
N.
Kopell
, and
M.
Wechselberger
, “
Exitable neurons, firing threshold manifolds and canards
,”
J. Math. Neurosci.
3
,
1
32
(
2013
).
36.
M.
Krupa
and
P.
Szmolyan
, “
Relaxation oscillation and canard explosion
,”
J. Differ. Equ.
174
,
312
368
(
2001
).
37.
M.
Itoh
and
R.
Tomiyasu
, “Canards and irregular oscillations in a nonlinear circuit,” in IEEE International Symposium on Circuits and Systems (IEEE, Singapore, 1991), pp. 850–853.
38.
P.
Strizhak
, and
M.
Menzinger
, “
Slow passage through a supercritical Hopf bifurcation: Time-delayed response in the Belousov-Zhabotinsky reaction in a batch reactor
,”
J. Chem. Phys.
105
,
10905
(
1996
).
39.
C.
Chicone
, “
Inertial and slow manifolds for delay equations with small delays
,”
J. Differ. Equ.
190
,
364
406
(
2003
).
40.
S. A.
Campbell
,
E.
Stone
, and
T.
Erneux
, “
Delay induced canards in high speed machining
,”
Dyn. Syst.
24
,
373
392
(
2009
).
41.
M.
Krupa
and
J. D.
Touboul
, “
Canard explosion in delay differential equations
,”
J. Dyn. Diff. Equ.
28
,
471
491
(
2016
).
42.
Y.
Hayashi
,
S. J.
Nasuto
, and
H.
Eberle
, “
Renormalized time scale for anticipating and lagging synchronization
,”
Phys. Rev. E
93
,
052229
(
2016
).
43.
E. J.
Doedel
,
A. R.
Champneys
,
F.
Dercole
,
T.
Fairgrieve
,
Y.
Kuznetsov
,
B. E.
Oldeman
,
R.
Paffenroth
,
B.
Sandstede
,
X. J.
Wang
, and
C.
Zhang
, AUTO-07P: Continuation and bifurcation software for ordinary differential equations, 2007, see http://cmvl.cs.concordia.ca/auto.
44.
S.
Baer
and
T.
Erneux
, “
Singular hopf bifurcation to relaxation oscillations
,”
SIAM J. Appl. Math.
46
,
721
739
(
1986
).
45.
S.
Baer
and
T.
Erneux
, “
Singular hopf bifurcation to relaxation oscillations ii
,”
SIAM J. Appl. Math.
52
,
1651
1664
(
1992
).
46.
J.
Moehlis
, “
Canards for a reduction of Hodgkin-Huxley equations
,”
J. Math. Biol.
52
,
141
153
(
2006
).
47.
G.
Ermentrout
,
Simulating, Analyzing, and Animating Dynamical Systems: A Guide to XPPAUT for Researchers and Students
(
SIAM
,
2002
).
48.
A.
Sharp
,
M.
O’Neil
,
L.
Abbott
, and
E.
Mander
, “
The dynamic clamp: Artificial conductances in biological neurons
,”
Trends Neurosci.
6
,
389
394
(
1993
).
49.
A. A.
Prinz
and
R.
Cudmore
, “
Dynamic clamp
,”
Scholarpedia
6
,
1470
(
2011
).
50.
T.
Bozhi
,
T.
Cohen-Karni
,
Q.
Qing
,
X.
Duan
,
P.
Xie
, and
C. M.
Lieber
, “
Three-dimensional, flexible nanoscale field-effect transistors as localized bioprobes
,”
Science
329
,
830
834
(
2010
).
51.
J.
Sieber
,
A.
Gonzalez-Buelga
,
S. A.
Nield
,
D. J.
Wagg
, and
B.
Krauskopf
, “
Experimental continuation of periodic orbits through a fold
,”
Phys. Rev. Lett.
100
,
244101
(
2008
).
52.
T.
Netoff
,
M.
Banks
,
A.
Dorval
,
C.
Acker
,
J.
Haas
,
N.
Kopell
, and
J.
White
, “
Synchronization in hybrid neuronal networks of the hippocampal formation
,”
J Neurophysiol.
93
,
1197
1208
(
2005
).
53.
S.
Wang
,
L.
Chandrasekaran
,
F.
Fernandez
,
J.
White
, and
C.
Canavier
, “
Short conduction delays cause inhibition rather than excitation to favor synchrony in hybrid neuronal networks of the entorhinal cortex
,”
PLoS Comput. Biol.
8
,
1002306
(
2012
).
54.
A.
Messé
,
M.-T.
Hütt
, and
C. C.
Hilgetag
, “
Toward a theory of coactivation patterns in excitable neural networks
,”
PLoS Comput. Biol.
14
,
e1006084
(
2018
).
55.
K. J.
Friston
, “
The labile brain. I. Neuronal transients and nonlinear coupling
,”
Philos. Trans. R. Soc. B
355
,
215
236
(
2000
).
56.
K. J.
Friston
, “
The labile brain. II. Transients, complexity and selection
,”
Philos. Trans. R. Soc. Lond. B
355
,
237
252
(
2000
).
57.
K. J.
Friston
, “
The labile brain. III. Transients and spatio-temporal receptive fields
,”
Philos. Trans. R. Soc. Lond. B
355
,
253
265
(
2000
).
58.
M.
Desroches
,
A.
Guillamon
,
E.
Ponce
,
R.
Prohens
,
S.
Rodrigues
, and
A. E.
Teruel
, “
Canards, folded nodes and mixed-mode oscillations in piecewise-linear slow-fast system
,”
SIAM Rev.
58
,
653
691
(
2016
).
59.
M.
Desroches
,
M.
Krupa
, and
S.
Rodrigues
, “
Spike-adding in parabolic bursting: The role of folded-saddle canards
,”
Physica D
331
,
58
70
(
2016
).
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