Studies of Boolean recurrent neural networks are briefly introduced with an emphasis on the attractor dynamics determined by the sequence of distinct attractors observed in the limit cycles. We apply this framework to a simplified model of the basal ganglia-thalamocortical circuit where each brain area is represented by a “neuronal” node in a directed graph. Control parameters ranging from neuronal excitability that affects all cells to targeted local connections modified by a new adaptive plasticity rule, and the regulation of the interactive feedback affecting the external input stream of information, allow the network dynamics to switch between stable domains delimited by highly discontinuous boundaries and reach very high levels of complexity with specific configurations. The significance of this approach with regard to brain circuit studies is briefly discussed.

1.
J. P.
Segundo
, “
Nonlinear dynamics of point process systems and data
,”
Int. J. Bifurcat. Chaos
13
,
2035
2116
(
2003
).
2.
J. P.
Segundo
,
G. P.
Moore
,
L. J.
Stensaas
, and
T. H.
Bullock
, “
Sensitivity of neurones in Aplysia to temporal pattern of arriving impulses
,”
J. Exp. Biol.
40
,
643
667
(
1963
), available at http://jeb.biologists.org/content/40/4/643.full.pdf.
3.
H. L.
Bryant
and
J. P.
Segundo
, “
Spike initiation by transmembrane current: A white-noise analysis
,”
J. Physiol.
260
,
279
314
(
1976
).
4.
M.
Abeles
, Local Cortical Circuits. An Electrophysiological Study, Studies of Brain Function Vol. 6 (Springer-Verlag, Berlin, 1982).
5.
A. E. P.
Villa
and
M.
Abeles
, “
Evidence for spatiotemporal firing patterns within the auditory thalamus of the cat
,”
Brain Res.
509
,
325
327
(
1990
).
6.
A. E. P.
Villa
and
J. M.
Fuster
, “
Temporal correlates of information processing during visual short-term memory
,”
Neuroreport
3
,
113
116
(
1992
).
7.
M.
Abeles
,
H.
Bergman
,
E.
Margalit
, and
E.
Vaadia
, “
Spatiotemporal firing patterns in the frontal cortex of behaving monkeys
,”
J. Neurophysiol.
70
,
1629
1638
(
1993
).
8.
I. V.
Tetko
and
A. E. P.
Villa
, “
A pattern grouping algorithm for analysis of spatiotemporal patterns in neuronal spike trains. 2. Application to simultaneous single unit recordings
,”
J. Neurosci. Methods
105
,
15
24
(
2001
).
9.
P. E.
Rapp
,
I. D.
Zimmerman
,
A. M.
Albano
,
G. C.
Deguzman
, and
N. N.
Greenbaun
, “
Dynamics of spontaneous neural activity in the simian motor cortex: The dimension of chaotic neurons
,”
Phys. Lett. A
110
,
335
338
(
1985
).
10.
G. J.
Mpitsos
,
R. M.
Burton, Jr.
,
H. C.
Creech
, and
S. O.
Soinila
, “
Evidence for chaos in spike trains of neurons that generate rhythmic motor patterns
,”
Brain Res. Bull.
21
,
529
538
(
1988
).
11.
A.
Celletti
and
A. E. P.
Villa
, “
Low-dimensional chaotic attractors in the rat brain
,”
Biol. Cybern.
74
,
387
393
(
1996
).
12.
A.
Celletti
,
V. M. B.
Lorenzana
, and
A. E. P.
Villa
, “
Correlation dimension for paired discrete time series
,”
J. Stat. Phys.
89
,
877
884
(
1997
).
13.
A.
Babloyantz
,
J. M.
Salazar
, and
C.
Nicolis
, “
Evidence of chaotic dynamics of brain activity during the sleep cycle
,”
Phys. Lett. A
111
,
152
155
(
1985
).
14.
E.
Başar
, “Chaotic dynamics and resonance phenomena in brain function: Progress, perspectives, and thoughts,” in Chaos in Brain Function, edited by E. Başar (Springer, Berlin, 1990), pp. 1–30.
15.
Y.
Asai
and
A. E. P.
Villa
, “
Reconstruction of underlying nonlinear deterministic dynamics embedded in noisy spike trains
,”
J. Biol. Phys.
34
,
325
340
(
2008
).
16.
J.
Iglesias
and
A. E. P.
Villa
, “
Recurrent spatiotemporal firing patterns in large spiking neural networks with ontogenetic and epigenetic processes
,”
J. Physiol. Paris
104
,
137
146
(
2010
).
17.
W.
Little
, “
The existence of persistent states in the brain
,”
Math. Biosci.
19
,
101
120
(
1974
).
18.
M. I.
Rabinovich
,
P.
Varona
,
A. I.
Selverston
, and
H. D. I.
Abarbanel
, “
Dynamical principles in neuroscience
,”
Rev. Mod. Phys.
78
,
1213
1265
(
2006
).
19.
J. J.
Knierim
and
K.
Zhang
, “
Attractor dynamics of spatially correlated neural activity in the limbic system
,”
Annu. Rev. Neurosci.
35
,
267
285
(
2012
).
20.
J. J.
Hopfield
, “
Neural networks and physical systems with emergent collective computational abilities
,”
Proc. Natl. Acad. Sci. U.S.A.
79
,
2554
2558
(
1982
).
21.
D. J.
Amit
,
Modeling Brain Function: The World of Attractor Neural Networks
, 2nd ed. (
Cambridge University Press
,
1992
).
22.
G.
Schöner
, “
Timing, clocks, and dynamical systems
,”
Brain Cogn.
48
,
31
51
(
2002
).
23.
S.
Thorpe
,
A.
Delorme
, and
R.
Van Rullen
, “
Spike-based strategies for rapid processing
,”
Neural. Netw.
14
,
715
725
(
2001
).
24.
E. D.
Adrian
and
Y.
Zotterman
, “
The impulses produced by sensory nerve-endings: Part II. The response of a single end-organ
,”
J. Physiol.
61
,
151
171
(
1926
).
25.
V. B.
Mountcastle
,
G. F.
Poggio
, and
G.
Werner
, “
The relation of thalamic cell response to peripheral stimuli varied over an intensive continuum
,”
J. Neurophysiol.
26
,
807
834
(
1963
).
26.
W.
Bialek
,
R.
de Ruytervan Steveninck
,
F.
Rieke
, and
D.
Warland
,
Spikes: Exploring the Neural Code
(
MIT Press
,
1999
).
27.
S.
Grossberg
, “
Pavlovian pattern learning by nonlinear neural networks
,”
Proc. Natl. Acad. Sci. U.S.A.
68
,
828
831
(
1971
).
28.
T.
Kohonen
, “
Self-organized formation of topologically correct feature maps
,”
Biol. Cybern.
43
,
59
69
(
1982
).
29.
P. J.
Werbos
, “
Generalization of backpropagation with application to a recurrent gas market model
,”
Neural. Netw.
1
,
339
356
(
1988
).
30.
V.
Del Prete
,
L.
Martignon
, and
A. E. P.
Villa
, “
Detection of syntonies between multiple spike trains using a coarse-grain binarization of spike count distributions
,”
Network
15
,
13
28
(
2004
).
31.
J.
Cabessa
and
A. E. P.
Villa
, “
A hierarchical classification of first-order recurrent neural networks
,”
Chin. J. Physiol.
53
,
407
416
(
2010
).
32.
J.
Cabessa
and
A. E. P.
Villa
, “
An attractor-based complexity measurement for boolean recurrent neural networks
,”
PLoS One
9
,
e94204
(
2014
).
33.
J. J.
Hopfield
and
D. W.
Tank
, “
Computing with neural circuits: A model
,”
Science
233
,
625
633
(
1986
).
34.
H. T.
Siegelmann
and
E. D.
Sontag
, “
Analog computation via neural networks
,”
Theor. Comput. Sci.
131
,
331
360
(
1994
).
35.
H.
Siegelmann
and
E.
Sontag
, “
On the computational power of neural nets
,”
J. Comput. Syst. Sci.
50
,
132
150
(
1995
).
36.
J.
Cabessa
and
A. E.
Villa
, “
The expressive power of analog recurrent neural networks on infinite input streams
,”
Theor. Comput. Sci.
436
,
23
34
(
2012
).
37.
J.
Cabessa
and
J.
Duparc
, “
Expressive power of nondeterministic recurrent neural networks in terms of their attractor dynamics
,”
Int. J. Unconv. Comput.
12
,
25
50
(
2016
), available at http://www.oldcitypublishing.com/pdf/7589.
38.
J.
Cabessa
and
A. E. P.
Villa
, “
Expressive power of first-order recurrent neural networks determined by their attractor dynamics
,”
J. Comput. Syst. Sci.
82
,
1232
1250
(
2016
).
39.
F.
Pasemann
and
N.
Stollenwerk
, “
Attractor switching by neural control of chaotic neurodynamics
,”
Network
9
,
549
561
(
1998
).
40.
M.
Cencini
,
M.
Falcioni
,
D.
Vergni
, and
A.
Vulpiani
, “
Macroscopic chaos in globally coupled maps
,”
Phys. D
130
,
58
72
(
1999
).
41.
S.
Wu
,
K.
Hamaguchi
, and
S.-I.
Amari
, “
Dynamics and computation of continuous attractors
,”
Neural. Comput.
20
,
994
1025
(
2008
).
42.
K.
Kaneko
, “
From globally coupled maps to complex-systems biology
,”
Chaos
25
,
097608
(
2015
).
43.
S.-I.
Amari
, “
Learning patterns and pattern sequences by self-organizing nets of threshold elements
,”
IEEE Trans. Comput.
100
,
1197
1206
(
1972
).
44.
G.
Palm
, Neural Assemblies: An Alternative Approach to Artificial Intelligence, Studies of Brain Function Vol. 7 (Springer-Verlag, Berlin, 1982).
45.
G. J.
Mpitsos
, “
Attractors: Architects of Network Organization?
,”
Brain Behav. Evol.
55
,
256
277
(
2000
).
46.
K.
Kaneko
and
I.
Tsuda
,
Complex Systems Chaos and Beyond: A Constructive Approach with Applications in Life Sciences
(
Springer
,
Berlin
,
2001
).
47.
K.
Kaneko
and
I.
Tsuda
, “
Chaotic itinerancy
,”
Chaos
13
,
926
936
(
2003
).
48.
S. C.
Kleene
, “Representation of events in nerve nets and finite automata,” in Automata Studies, edited by C. Shannon and J. McCarthy (Princeton University Press, Princeton, NJ, 1956), pp. 3–41.
49.
M. L.
Minsky
,
Computation: Finite and Infinite Machines
(
Prentice-Hall, Inc.
,
Englewood Cliffs, NJ
,
1967
).
50.
J.
Cabessa
and
H. T.
Siegelmann
, “
The super-Turing computational power of plastic recurrent neural networks
,”
Int. J. Neural. Syst.
24
,
1450029
(
2014
).
51.
D. J.
Amit
and
S.
Fusi
, “
Learning in neural networks with material synapses
,”
Neural. Comput.
6
,
957
982
(
1994
).
52.
W. C.
Abraham
and
A.
Robins
, “
Memory retention—the synaptic stability versus plasticity dilemma
,”
Trends Neurosci.
28
,
73
78
(
2005
).
53.
H. T.
Siegelmann
and
L. E.
Holzman
, “
Neuronal integration of dynamic sources: Bayesian learning and Bayesian inference
,”
Chaos
20
,
037112
(
2010
).
54.
A.
Knoblauch
,
G.
Palm
, and
F. T.
Sommer
, “
Memory capacities for synaptic and structural plasticity
,”
Neural Comput.
22
,
289
341
(
2010
).
55.
D.
Malagarriga
,
A. E. P.
Villa
,
J.
Garcia-Ojalvo
, and
A. J.
Pons
, “
Consistency of heterogeneous synchronization patterns in complex weighted networks
,”
Chaos
27
,
031102
(
2017
).
56.
C. C.
Bell
,
V. Z.
Han
,
Y.
Sugawara
, and
K.
Grant
, “
Synaptic plasticity in a cerebellum-like structure depends on temporal order
,”
Nature
387
,
278
281
(
1997
).
57.
H.
Markram
,
J.
Lübke
,
M.
Frotscher
, and
B.
Sakmann
, “
Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs
,”
Science
275
,
213
215
(
1997
).
58.
D. E.
Feldman
, “
The spike-timing dependence of plasticity
,”
Neuron
75
,
556
571
(
2012
).
59.
J.
Cabessa
and
A. E. P.
Villa
, “
Attractor dynamics driven by interactivity in boolean recurrent neural networks
,”
Lecture Notes Comp. Sci.
9886
,
115
122
(
2016
).
60.
Handbook of Basal Ganglia Structure and Function, 2nd ed., edited by H. Steiner and K. Y. Tseng, Handbook of Behavioral Neuroscience Vol. 24 (Elsevier, 2017), pp. i–xxiii, pp. 1–1012.
61.
M. L.
Perreault
,
A.
Hasbi
,
B. F.
O’Dowd
, and
S. R.
George
, “
The dopamine D1-D2 receptor heteromer in striatal medium spiny neurons: Evidence for a third distinct neuronal pathway in basal ganglia
,”
Front. Neuroanat.
5
,
31
(
2011
).
62.
F.
Sato
,
M.
Parent
,
M.
Levesque
, and
A.
Parent
, “
Axonal branching pattern of neurons of the subthalamic nucleus in primates
,”
J. Comp. Neurol.
424
,
142
152
(
2000
).
63.
E. D.
Lumer
,
G. M.
Edelman
, and
G.
Tononi
, “
Neural dynamics in a model of the thalamocortical system. I. Layers, loops and the emergence of fast synchronous rhythms
,”
Cereb. Cortex
7
,
207
227
(
1997
).
64.
M.
Salami
,
C.
Itami
,
T.
Tsumoto
, and
F.
Kimura
, “
Change of conduction velocity by regional myelination yields constant latency irrespective of distance between thalamus and cortex
,”
Proc. Natl. Acad. Sci. U.S.A.
100
,
6174
6179
(
2003
).
65.
C. R.
Stoelzel
,
Y.
Bereshpolova
,
J.-M.
Alonso
, and
H. A.
Swadlow
, “
Axonal conduction delays, brain state, and corticogeniculate communication
,”
J. Neurosci.
37
,
6342
6358
(
2017
).
66.
A.
Villa
and
I.
Tetko
, “Spatio-temporal patterns of activity controlled by system parameters in a simulated thalamo-cortical neural network,” in Supercomputing in Brain Research: From Tomography to Neural Networks, edited by H. Herrmann, D. Wolf, and E. Poppel (World Scientific, 1995) pp. 379–388.
67.
W. S.
McCulloch
and
W.
Pitts
, “
A logical calculus of the ideas immanent in nervous activity
,”
Bull. Math. Biophys.
5
,
115
133
(
1943
).
68.
S. L.
Foote
and
J. H.
Morrison
, “
Extrathalamic modulation of cortical function
,”
Annu. Rev. Neurosci.
10
,
67
95
(
1987
).
69.
D. A.
McCormick
and
H. C.
Pape
, “
Noradrenergic and serotonergic modulation of a hyperpolarization-activated cation current in thalamic relay neurones
,”
J. Physiol.
431
,
319
342
(
1990
).
70.
A. E. P.
Villa
,
I. V.
Tetko
,
P.
Dutoit
, and
G.
Vantini
, “
Non-linear cortico-cortical interactions modulated by cholinergic afferences from the rat basal forebrain
,”
Biosystems
58
,
219
228
(
2000
).
71.
B. E.
Jones
, “
From waking to sleeping: Neuronal and chemical substrates
,”
Trends Pharmacol. Sci.
26
,
578
586
(
2005
).
72.
S.
Spiga
,
A.
Lintas
, and
M.
Diana
, “
Altered mesolimbic dopamine system in THC dependence
,”
Curr. Neuropharmacol.
9
,
200
204
(
2011
).
73.
T. S.
Turova
and
A. E. P.
Villa
, “
On a phase diagram for random neural networks with embedded spike timing dependent plasticity
,”
Biosystems
89
,
280
286
(
2007
).
74.
Y.
Baram
, “
Developmental metaplasticity in neural circuit codes of firing and structure
,”
Neural. Netw.
85
,
182
196
(
2017
).
75.
J.-T.
Lu
,
C.-y.
Li
,
J.-P.
Zhao
,
M.-m.
Poo
, and
X.-h.
Zhang
, “
Spike-timing-dependent plasticity of neocortical excitatory synapses on inhibitory interneurons depends on target cell type
,”
J. Neurosci.
27
,
9711
9720
(
2007
).
76.
E.
Fino
and
L.
Venance
, “
Spike-timing dependent plasticity in the striatum
,”
Front. Synaptic. Neurosci.
2
,
6
(
2010
).
77.
X.
Ji
,
S.
Saha
,
J.
Kolpakova
,
M.
Guildford
,
A. R.
Tapper
, and
G. E.
Martin
, “
Dopamine receptors differentially control binge alcohol drinking-mediated synaptic plasticity of the core nucleus accumbens direct and indirect pathways
,”
J. Neurosci.
37
,
5463
5474
(
2017
).
78.
S. M.
Vogt
and
U. G.
Hofmann
, “
Neuromodulation of STDP through short-term changes in firing causality
,”
Cogn. Neurodyn.
6
,
353
366
(
2012
).
79.
T. P.
Vogels
,
R. C.
Froemke
,
N.
Doyon
,
M.
Gilson
,
J. S.
Haas
,
R.
Liu
,
A.
Maffei
,
P.
Miller
,
C. J.
Wierenga
,
M. A.
Woodin
,
F.
Zenke
, and
H.
Sprekeler
, “
Inhibitory synaptic plasticity: Spike timing-dependence and putative network function
,”
Front. Neural. Circuits
7
,
119
(
2013
).
80.
R. R.
Kerr
,
D. B.
Grayden
,
D. A.
Thomas
,
M.
Gilson
, and
A. N.
Burkitt
, “
Coexistence of reward and unsupervised learning during the operant conditioning of neural firing rates
,”
PLoS One
9
,
e87123
(
2014
).
81.
M.-L.
Wang
and
J.-S.
Wang
, “
Dynamical balance between excitation and inhibition of feedback neural circuit via inhibitory synaptic plasticity
,”
Acta. Phys. Sin.
64
,
108701
(
2015
).
82.
N.
Maurice
,
J. M.
Deniau
,
A.
Menetrey
,
J.
Glowinski
, and
A. M.
Thierry
, “
Prefrontal cortex-basal ganglia circuits in the rat: Involvement of ventral pallidum and subthalamic nucleus
,”
Synapse
29
,
363
370
(
1998
).
83.
A.
Lintas
,
I. G.
Silkis
,
L.
Albéri
, and
A. E.
Villa
, “
Dopamine deficiency increases synchronized activity in the rat subthalamic nucleus
,”
Brain Res.
1434
,
142
151
(
2012
).
84.
W. D.
Hutchison
,
R. J.
Allan
,
H.
Opitz
,
R.
Levy
,
J. O.
Dostrovsky
,
A. E.
Lang
, and
A. M.
Lozano
, “
Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson’s disease
,”
Ann. Neurol.
44
,
622
628
(
1998
).
85.
F.
Njap
,
J. C.
Claussen
,
A.
Moser
, and
U. G.
Hofmann
, “
Modeling effect of GABAergic current in a basal ganglia computational model
,”
Cogn. Neurodyn.
6
,
333
341
(
2012
).
86.
B.
Hu
,
Y.
Guo
,
X.
Zou
,
J.
Dong
,
L.
Pan
,
M.
Yu
,
Z.
Yang
,
C.
Zhou
,
Z.
Cheng
,
W.
Tang
, and
H.
Sun
, “
Controlling mechanism of absence seizures by deep brain stimulus applied on subthalamic nucleus
,”
Cogn. Neurodyn.
12
,
103
119
(
2018
).
87.
A. E. P.
Villa
,
I. V.
Tetko
,
P.
Dutoit
,
Y.
De Ribaupierre
, and
F.
De Ribaupierre
, “
Corticofugal modulation of functional connectivity within the auditory thalamus of rat, guinea pig and cat revealed by cooling deactivation
,”
J. Neurosci. Methods
86
,
161
178
(
1999
).
88.
G.
Le Masson
,
S.
Renaud-Le Masson
,
D.
Debay
, and
T.
Bal
, “
Feedback inhibition controls spike transfer in hybrid thalamic circuits
,”
Nature
417
,
854
858
(
2002
).
89.
C. K. E.
Moll
,
A.
Sharott
,
W.
Hamel
,
A.
Münchau
,
C.
Buhmann
,
U.
Hidding
,
S.
Zittel
,
M.
Westphal
,
D.
Müller
, and
A. K.
Engel
, “
Waking up the brain: A case study of stimulation-induced wakeful unawareness during anaesthesia
,”
Prog. Brain Res.
177
,
125
145
(
2009
).
90.
L.
Albéri
,
A.
Lintas
,
R.
Kretz
,
B.
Schwaller
, and
A. E.
Villa
, “
The calcium-binding protein parvalbumin modulates the firing properties of the reticular thalamic nucleus bursting neurons
,”
J. Neurophysiol.
109
,
2827
2841
(
2013
).
91.
J.
Cannon
,
N.
Kopell
,
T.
Gardner
, and
J.
Markowitz
, “
Neural sequence generation using spatiotemporal patterns of isnhibition
,”
PLoS Comput. Biol.
11
,
e1004581
(
2015
).
92.
K.
Rajan
,
C. D.
Harvey
, and
D. W.
Tank
, “
Recurrent network models of sequence generation and memsory
,”
Neuron
90
,
128
142
(
2016
).
93.
J.
Cabessa
and
H. T.
Siegelmann
, “Evolving recurrent neural networks are super-Turing,” in 2011 International Joint Conference on Neural Networks (IJCNN) (IEEE, 2011), pp. 3200–3206.
94.
J.
Cabessa
and
A. E. P.
Villa
, “
Recurrent neural networks and super-Turing interactive computation
,”
Springer Series in Bio-/Neuroinformatics
,
4
,
1
29
(
2015
).
95.
J. M.
Young
,
W. J.
Waleszczyk
,
C.
Wang
,
M. B.
Calford
,
B.
Dreher
, and
K.
Obermayer
, “
Cortical reorganization consistent with spike timing—but not correlation-dependent plasticity
,”
Nat. Neurosci.
10
,
887
895
(
2007
).
96.
J. G.
Mikhael
and
R.
Bogacz
, “
Learning reward uncertainty in the basal gasnglia
,”
PLoS Comput. Biol.
12
,
e1005062
(
2016
).
97.
G.
Rodriguez
,
M.
Sarazin
,
A.
Clemente
,
S.
Holden
,
J. T.
Paz
, and
B.
Delord
, “
Conditional bistability, a generic cellular mnemonic mechanism for robust and flexible working memory computations
,”
J. Neurosci.
(
2018
).
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