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Sleep unconsciousness and breakdown of serial critical intermittency:

New vistas on the global workspace

Paolo Allegrini,1,2 Paolo Paradisi,3 Danilo Menicucci,1,2 Marco Laurino,1,4


Remo Bedini,1,2 Andrea Piarulli,2,5 Angelo Gemignani1,2,4
1 Istituto di Fisiologia Clinica (IFC-CNR), Via Moruzzi 1, 56124 Pisa, Italy
2 Centro EXTREME, Scuola Superiore Sant’Anna, P.zza Martiri della Libertà 7, 56127 Pisa, Italy
3 Istituto di Scienza e Tecnologie dell’Informazione “A. Faedo” (ISTI-CNR), Via Moruzzi 1, 56124 Pisa, Italy
4 Dipartmento di Patologia Chirurgica, Medica, Molecolare e dell’area critica, Università di Pisa, Via Paradisa 2, 56127 Pisa, Italy
5 PERCeptual RObotics laboratory, Scuola Superiore Sant’Anna, P.zza Martiri della Libertà 7, 56127 Pisa, Italy

Abstract
While several mental functions are characterized by parallel computation performed by moduli in the cortex, consciousness is
sustained by a serial global integration: a single scene at a time takes place. Studies on complex systems show that macroscopic
variables, integrating many components activities, undergo fluctuations with an intermittent serial structure when the system is
in a state called “criticality”, characterized by avalanches with inverse-power-law (scale-free) distribution densities of sizes and
inter-event times. Criticality has been established in human brain dynamics during wakefulness. Here we review how the criti-
cal hypothesis is able to explain many recent studies on brain complex dynamics. We focus, in particular, on the global, serial,
intermittent behavior that can be assessed via high-density electroencephalograms, studying transitions between metastable states.
Established as it is during wakefulness, it remained unsolved whether this global intermittent dynamics correlates with conscious-
ness or with a non-task-driven default mode, also present in non-conscious states, like deep (NREM) sleep. Here we show that
in NREM sleep seriality breaks down, and re-establishes during REM sleep (dreams), with unaltered spacial structure, in terms of
complex branching of avalanches. We conjecture that this connectivity is exploited in NREM sleep by neural-bistability waves,
resetting and “parallelizing” portions of the cortex.
Keywords: Consciousness, Sleep, Criticality, Scale-free networks, Intermittency

1. Introduction Thus, studying the differences in neural correlates of NREM


sleep, with respect to wakefulness or dreams, provides a spot-
Defining Consciousness is elusive. Many features of con- light to investigate consciousness. On the other hand, the very
sciousness have been proposed by psychologists and neuro- presence of consciousness remains private, thus impossible to
physiologists, varying from vigilance to the presence or ex- be reduced to a list of features [2]. One way around this philo-
pression of cognitive or emotional functions. Along this line, sophical difficulty is to adopt a different route to scientific re-
consciousness can be studied in an analytical way, namely via duction, namely focusing on the “downwards causation” of an
the study of the various outputs correlating with it. Deep, or emerging complex phenomenon onto measurable features. This
dreamless, sleep is the only physiological state characterized means that output features must be considered necessary, but
by absence of consciousness. Other conditions of lack of con- never sufficient to describe consciousness.
sciousness are typically pathological and range from neural to
cardiovascular till to metabolic dysfunctions (e.g. epilepsy, syn- In this paper, we first review concepts linking conscious-
copes, coma, severe hypoglycemia). ness, seriality, intermittency and criticality. This should help in
On the other hand, there is consensus among psychologists understanding the emergence and quenching of consciousness
that consciousness is fully present during structured oneiric ac- during wakefulness and dreaming on one side, and dreamless
tivity (dreaming with presence and gestalt) typically reported sleep on the other.
after awakenings from REM sleep. Although, according to re-
cent literature (see [1] for a review), mental activity have been Then we present a holistic measure stemming from elec-
reported also in non-REM phases, here for simplicity we rest on troencefalogram (EEG) recording, showing how intermittency
the hypothesis that conscious dreaming is the typical function is lost during non-REM (NREM) sleep, where structured
of REM sleep. We will come back to this point later, near the oneiric activity (gestalt) is thought to be absent. Finally we
end of our paper (specifically in the caption of Fig. 7), where we present a rather simple heuristic view, based on sleep physiol-
will see what kind of activity may be present when the global ogy, that may allow to link consciousness and complexity in
workspace is fragmented. terms of an emerging global workspace.
Preprint submitted to Chaos, Solitons, and Fractals (Accepted on May 21, 2013) May 22, 2013
2. Criticality: Theoretical implications more fundamental postulate than Hebbian learning, that in fact
provides a convenient rule to attain criticality by minimizing
2.1. Entropy issues “resources” in terms of coupling (number and amount of neu-
Evidence is growing that the conscious self is a holistic auto- rotransmitters) or wiring (number of synapses). In other words,
organization phenomenon, to be tackled using the framework of Hebbian plasticity, when expressed at the critical point, fa-
complexity theories, like, for instance, renormalization group vors the emergence and consolidations of a scale-free-network
relations [3] that effectively describe critical phenomena, char- topology.
acterized by diverging correlations in space (or structure) and
time due to rescaling symmetries (autosimilarity). These intro- 2.3. Avalanches
duce “redundancies”, thermodynamically (i.e. for macroscopic Another signature of criticality is the presence of avalanches,
volumes) making the entropy per volume tend to zero. This where the term avalanche denotes the rapid domino-like trans-
actually does not imply a vanishing entropy for the whole sys- mission of excitation from one node to the other, with an
tem, thermodynamically occurring only at absolute-zero tem- inverse-power law distribution of the number of nodes involved,
perature. This means that entropy ceases, at criticality, to be an called avalanche size. This topological scale-free feature was
extensive quantity for the system. This is easily understandable indeed predicted by some authors [12, 13] as a critical-point,
by envisaging entropy in the Gibbs sense (S = log W, where separating a quenched and an explosively expanding behavior
W is the number of possible microstates): structural infinite in the transmission of excitation through layers of neurons. Fi-
correlations prevents different subsystems of a critical system nally, we remark that the critical branching defines another kind
Q
to become statistically independent, so that W , Wi , thus of complex networks and is subtly related to functional connec-
P
S , S i , where i is a subsystem label. tivity. This point will be discussed in some detail in Section
An emphasis on information is gaining momentum to objec- 7.
tively define the eluding concept of consciousness. According
to Tononi’s integrated information theory [4], consciousness
3. Criticality in the brain
is associated with a critical interplay between integration and
segregation in functional neural networks, and, neglecting the As we have seen, dynamical systems posed near the criti-
epistemic problems earlier exposed, a measure of conscious- cal point are characterized by the emergence of collective, self-
ness was proposed, namely the difference Φ between the sum organized behavior. At the critical point the dimension of this
of the local Kolmogorov entropies and the global one. As a re- collective mode is that of the whole system (giant cluster). This
sult, conscious (high-Φ) neural circuits have to be critically bal- is associated with scale-free or power-law behavior and long-
anced between integration and independence [5]. In this way, range correlations. Although these properties, as we shall see,
“consciousness” is low (or absent) both when the system is per- have been reported for brain dynamics, it is important to un-
fectly integrated (synchronicity) or completely segregated (no derstand (i) whether criticality has been assessed for brain dy-
global integration). namics and, in case, (ii) which kind of criticality is taking place
[14]. Given criticality for assessed, however, both in critical
2.2. Scale-free networks phenomena (i.e. second order phase transitions) [15] and in
The dynamical rules implemented in [4], however, are such self-organized criticality [16, 17] we expect similar behaviors.
that the only property that can be responsible of a change in Indeed the system is either posed in, or moves towards, a the
global behavior is a change in topology [6]. In a toy model critical value of a cooperation parameter driving the non-linear
of brain [7] one can start pruning an all-to-all network till to coupling among many individual units. This means that the
recover a first-neighbor one, passing from synchronization to system stays in, or reaches, a critical point, corresponding to a
local segregation: Complex dynamical behavior is seen in be- phase transition from an uncorrelated to a correlated condition.
tween, when the network is complex. This hypothesis for brain dynamics is not new. In his pioneering
We remark that similar models, for virtually every kind of work [18], Turing conjectured that an intelligent system cannot
non-disjoint network, can yield complex behavior. Complex- “live” either in a too much correlated condition (order, super-
ity is established by varying the so called control parameter, critical), or in a too chaotic one (disorder, sub-critical). More
e.g. the neuron-neuron coupling or, alternatively, the noise. Re- recently, theoretical studies have been performed, with similar
markably, at the critical point the functional connectivity de- conclusions (see, e.g., [19] or, more recently, [8, 20, 21]).
velops long-range correlations, resulting in an effective “func- Many authors have investigated the spatial and/or structural
tional” complex scale-free network [8]. Here functional con- complexity of neuronal network models, of in vitro and in vivo
nectivity is defined as the network of above-threshold cross- data and found features in agreement with criticality. These
correlations. Complexity Φ thus reaches its maximum at the properties are (i) scale-free network topology in cross correla-
critical point of any neural-network model (e.g. of Kuramoto tions and (ii) avalanches. Point (i) is advocated, e.g., by the
oscillators, or others [9, 10]), when a fluctuating functional net- authors of Refs. [8], who studied the functional connectivity of
work emerges with scale-free properties. The fixed or slowly- the brain defined through the network of above-threshold cross-
changing “anatomical” topology has the only role of shifting correlations derived from fMRI data, which is again a struc-
the critical point in the control-parameter space [11]. Interest- tural property. They evaluated the degree distribution (the de-
ingly, in [11] it has been hypothesized that the critical point is a gree of a node is the number of links of that node with others),
2
with different thresholds (normalized in terms of total number long time intervals with calm motion and short-time bursting
of links). What they found is that, experimentally, scale-free events. These events, occurring in the temporal evolution of the
network structures stemming from cross-correlation functions order parameter, are crucial, since they are described by a serial
of MRI voxels are indistinguishable from those stemming from fractal point process, i.e., a sequence of intermittent events that:
a paradigmatic model for criticality, i.e. the Ising model for (a) occur randomly in time and (b) display a slow (power-law)
ferromagnetic materials, exactly at the Curie temperature. decay in the distribution of inter-event or Waiting Times (WTs).
As far as point (ii) is concerned, the presence of firing-neuron Type-I intermittency is in agreement with a fast decay of
avalanches have been reported both in vitro and in vivo [22], memory in correspondence of event occurrences. In the lan-
and also at the level of EEG [23]. In particular, the authors guage of stochastic processes, this is described by a renewal
of Refs. [22, 24] found a scale-free distribution of avalanche point process [32], which is defined by the condition of mu-
(or cluster) sizes, which is a signature of spatial and structural tual statistical independence of the events and, consequently,
long-range correlations, in network models and in vitro data. of the WTs. In summary, the macroscopic fluctuations of a
critical system are driven by a renewal point process, which
is the mathematical tool used here to describe intermittency
4. Criticality, intermittency, seriality and consciousness and, in the case of a self-similar of fractal distribution of
WTs, fractal intermittency. The renewal condition is gener-
4.1. Criticality yields intermittency in global fluctuations
ated by burstiness with fast memory decay, and it was found
The above cited studies about criticality in the brain are fo- to well describe the intermittency features of several complex
cused on the spatial or structural complexity. Apart from a vast systems, from blinking quantum dots [33, 34] to turbulence
literature on scale-free dinamics and 1/f spectral properties, that [35, 36, 37] and brain dynamics [38]. The renewal property
have been reported starting from Novikov [25], an often over- seems to play a crucial role in the perturbation of complex sys-
looked property is the temporal complexity. We plan to shift the tems [39, 40, 41, 42, 43] and it is a fundamental assumption in
focus from temporal long-range correlations with power-law the derivation of a new Fluctuation-Dissipation Theorem (FDT)
decay (equivalent to 1/ f noise) to time intermittency, which is based on renewal events [44, 45], whose main prediction is that
defined by the presence of crucial events in the complex/critical two complex systems have a maximum interaction when they
system. Intermittent events are defined as the time instants have similar complexities. The power-law relaxation foreseen
where the system abruptly increases its entropy, due to short by this new FDT was also experimentally validated in the weak
episodes of bursting activity, intermittently separated by qui- turbulence regime of a liquid crystal [46].
escent metastable states. When the distribution density of the
time durations of these metastable states are characterized by 4.2. The emergence of the global workspace
long tails (with infinite second moment) the events are called
crucial, insofar as the overall entropy increase is sublinear, so Basal EEG in healthy people have indeed been shown to pro-
the increase rate (Kolmogorov entropy) is null [26], a signature duce 1/ f noise through “events” associated with a global in-
of complexity. termittent process of activation/deactivation of integrated net-
It was recently proved that the inverse-power-law decaying works [38].
auto-correlation functions (equivalent, according to a general- From a psychophysiological point of view, the presence of a
ized Wiener-Kintchine theorem [27, 28] to 1/ f noise) are typi- global serial intermittent process reconciles the apparent para-
cal of critical points of second-order phase transitions, and are dox of massive parallel computing units in the brain and the
ultimately due to serial intermittent dynamics driving the fluc- presence of a unique stream of consciousness, and corroborates
tuations of those macroscopic variables, called “order param- the theory of a “global workspace” [47]. The concept of global
eters”, averaging microscopic fluctuations. In particular, in- workspace is the most widely accepted psychological and neu-
termittency in critical systems was theoretically established in robiological way of describing consciousness [47, 48]. It has
three dimensions, using a Landau treatment [29], and numeri- been hypothesized that the existence of the workspace is made
cally [30] using a decision-making model, equivalent, at small possible by re-entrant loops in the neural topology [49], with
couplings, to a 2D Ising Monte-Carlo. Remarkably, the results the emergence of a global neural dynamic core, namely a serial
of [30] are robust with respect to changes in anatomical topol- mechanism coordinating a variety of integrated cores working
ogy. In a nutshell, the macroscopic dynamics driving the fluctu- in parallel.
ations in system at the critical points are driven by intermittent Thus, a description of brain dynamics grounded on the
events. physics of critical phenomena explains the long-range neural
The authors of Refs. [30, 29] found that the fluctuations binding, like that well described by Chialvo [8], and provides,
of a random field at the critical point, i.e., the “order pa- as earlier stated, the presence of a unique intermittent serial pro-
rameter” averaging microscopic fluctuations, are described in cess that is essential in the description of consciousness. The
terms of a Type-I intermittent dynamical map similar to the emerging picture is a dynamical pattern of “thoughts” as a serial
well-known Manneville map [31], which describes turbulent conscious output which integrates parallel non-conscious units.
bursting. Again, turbulent bursting is complex, as this kind The serial, operational time [50] is characterized by the system
of dynamical systems is characterized by the presence of a visiting meta-stable states, with information only increasing at
marginally unstable point determining an alternation between the transitions (quakes) between a metastable state and the next.
3
All this can be operatively associated to segmentation in elec- a signature of consciousness, while the lack of fractal features
troencephalogram (EEG) [51, 52, 53], namely to the fact that and the emergence of normal diffusion could characterize non-
EEG signals frequently look like juxtapositions of epochs with conscious states.
stable frequency and amplitude, with abrupt changes, called
rapid transition processes (RTP), from epoch to epoch.
6. Data description and methods of analysis
In Fig. 1 we graphically summarize what we have reviewed
thus far, namely how the hypothesis that awake resting-state A normal night’s sleep consists of a few (from 4 to 6) cy-
brain activity can be successfully described in term of a system cles, each cycle consisting of different phases, defined on the
at a critical point. presence of different “waves”, or graphoelements, and specific
rhythms. After a pre-sleep wakefulness, the first cycle begins
5. Intermittency in brain dynamics with a wake-sleep transition state called N1. As the sleep deep-
ens, due to the diminished presence of various neurotransmit-
The existence of crucial events in the brain is well- ters, sleep phases N2 (shallow sleep) and N3 (deep, or Slow
established, as spontaneous neuronal activity exhibits relatively Wave Sleep, SWS) are visited one or more times, till the Rapid
quiet periods in alternation with chaotic or bursty periods. Eye Movement (REM) phase (typically a dreaming phase) oc-
Such brain events can be extracted from ElectroEncephalo- curs, that marks the end of the cycle. The phases N1, N2 and
Gram (EEG) data with detection algorithms. Events are here N3 (or SWS) are globally referred to as Non-REM (NREM)
defined as abrupt transitions or Rapid Transition Processes phase. At variance with NREM phase, REM is characterized
(RTPs) [51, 52, 53]) to and from metastable states, via multi- by a high level of the acetilcholine (ACh) neurotransmitter. At
channel EEGs [38]. On short time scales brain events typically the end of the first cycle, a second cycle begins, with or without
display a complex structure in terms of neuronal avalanches N1 or wakefulness episodes (Wakefulness After Sleep Onset,
[23, 55]. WASO), with the presence of NREM sleep (AC hagain drops
Exploiting the concept of RTP events, the temporal com- to low values), again ending with a REM phases, and so on.
plexity of brain dynamics, in terms of intermittency features,
has been investigated [38, 23]. It was found that a serial re- Data set. Our data set is composed of 29 whole-night high-
newal process of global integration exists in the human brain density (128 channel, 4ms sampling time) EEG recordings.
during a resting state wake condition and that this renewal pro- Subjects slept two nights with the same experimental setup,
cess has well-defined scaling exponents in both distributions namely after an adaptation night the second one was recorded.
of avalanche sizes and inter-event times [38, 23]. These scal- All subjects signed informed consent according to local ethi-
ing exponents, being a signature of Type-I fractal intermittency, cal committees. Through visual inspection of the polygraphic
confirm the critical brain hypothesis [21]. The scaling expo- traces, namely a selection of few EEG channel plus miogram
nents were evaluated through the diffusion scaling of different (muscle tone intensity) and oculogram (eye movements) all
random walks driven by the RTP events (see details in the next recordings were segmented into different cycles and phases.
Section 6). This approach based on diffusion scaling allowed For the purpose of the present paper, however, we will fo-
to get a robust estimation of the intermittency exponent or com- cus on global properties of sleep in the various phases and we
plexity index µ, i.e., the exponent of the inverse power-law tail will freely make recourse to grand averages over the 29 whole-
in the WT distribution: ψ(τ) ∼ 1/τµ . It is worth noting that night recordings. Artifacts were semiautomatically removed,
similar approaches, based on brain events and point processes, and only artifact-free segments of time duration longer than 3
have been recently applied, confirming the robust and univer- minutes were kept for the RTP detection. We use only segments
sal critical behavior of brain dynamics and neuronal networks of the first cycle, as signal quality decreased in subsequent cy-
[55, 56]. cles.
Is intermittency related to consciousness? All the above find-
ings lead to the idea that consciousness is related with the emer- Rapid Transition Processes. Herein, for each EEG channel,
gence of criticality and fractal intermittency. However, this pass-band filtered between 0.3 and 40 Hz (Chebyshev II filter
is just a hypothesis as it is not yet clear if this renewal frac- algorithm), RTPs are extracted as a “significant” selection of in-
tal process is uniquely associated with consciousness or with a tersection between two different moving averages of the Hilbert
non-task-driven default mode activity [57], also present in non- transform of the signal modulus. Moving averages have win-
conscious states like deep sleep. dows of 5 and 125 ms, respectively. By significant we mean
In the following we clarify this point by evaluating the event- that we select only the points where the intersection between
driven diffusion scaling of EEG data collected from the obser- the two curves is above a threshold angle. To do this we select
vation of healthy human subjects during sleep. The statistical a 125 ms window surrounding the intersection and compute the
analysis we use is essentially the same as in Ref. [38]. In Sec- sum of the modulus of the difference between the two curves.
tion 6 we describe the dataset and the methods of data analysis. For each channel significant RTPs are those in the highest decile
In particular, we will introduce the diffusion scaling method. (the ones higher than 90% are chosen). Notice that the choice of
In Section 7 we show our results and we discuss the hypoth- RTPs described above is both different from that used by Ka-
esis that the emergence of intermittent events described by a plan [52] and from our group’s original recipe (see Fig. 1 of
(serial) renewal fractal process and of anomalous diffusion is [23]). We however proved in [58] that our subsequent analysis
4
Brain at critical point

(a) Intermittency (b) Correlational (i. e. functional) (c) At criticality the


in fluctuations of connectivity of resting brain MRI is entropy per volume
order parameter that of a ferromagnet at criticality tends to zero

(d) Small
Serial intermittency Complex networks Worlds in Entropy reduction
the brain

Features of consciousness
(e) Global Workspace explained by the hypothesis (g) high Φ

(f) Operational Modules that awake resting-state brain (integrated information)

works at a critical point

Figure 1: Conceptual map of the literature analysis that represents the minimal background on which the present work is based. Dark boxes with white letters
represent concepts, while arrowed gray boxes with black letters represent results well established in scientific literature of different fields (with different readerships).
Examples of (a) are the works of Diakonos and Contoyiannis and of Turalska et al. [29, 30]; for (b) we make reference to the recent works of Chialvo, for instance
[8]; (c) is a classic result of the theory of critical phenomena, see e.g. the book of Stanley [54]; there is a vast literature about result (d), see e.g. the work of Sporn
[6, 7]; for (e) see the reviews of Baars and Edelman et al. [47]; for (f) we refer to the recent review of Fingelkurts et al. [50]. Finally, literature (g) refers to the
Tononi’s Integrated Information Theory [4, 5]

is robust with respect to a variation of event definition, and also changes value only in correspondence of event occurrences. In
in the presence of superimposed noise [59]. Figs. 2 and 3 a sketch of the two signals ξ(t) is reported. The
We are here interested on global events, i.e., on the “simul- times t0 , t1 , t2 , ... correspond to the occurrence of the events
taneous” occurrences of RTP in different EEG channels. For 0, 1, 2, ..., while τ1 , τ2 , ... are the WTs, i.e., the time interval
each EEG recording, the sequence of coincidences, or (concur- between the events 0 and 1, the events 1 and 2 and so on. In
rent) Multi-Channel RTPs (MC-RTPs), is obtained from single- particular, we have:
channel RTPs via the introduction of two thresholds: The first
(a) Asymmetric Jump (AJ) rule:
one, ∆tc , defines the maximum time distance for two single-
the walker makes a positive jump (ξ(tn ) = 1) in correspon-
channel RTPs (from different channels) to be considered con-
dence of each event n, otherwise it stands (ξ(t) = 0). Then,
current; the second one, Nt , defines the minimum number of
ξ(t) is a sequence of pulses of constant intensity.
concurrent single-channel RTPs required for a MC-RTPs to be
recorded as a global event. Since events that have a distance less (b) Symmetric Jump (SJ) rule:
than ∆tc are considered to be simultaneous, ∆tc must be small. as in the AJ rule, but the walker can make positive or nega-
We herein use ∆tc = 4 ms, equal to the instrumental sampling tive jumps in correspondence of an event: ξ(tn ) = ±1. The
time, and Nt = 5. Nt < 5 suffered from first-neighbor effects, sign ± is chosen with a coin tossing prescription.
and Nt > 5 resulted behavior similar to that reported, but with
decreased statistics. +1 +1

Event-driven random walks and diffusion scaling. The ran-


dom walks driven by renewal events [38, 37] are inspired to
t1 t3
the Continuous Time Random Walk (CTRW) of Montroll and
t0 t2
co-workers [60, 61]. In CTRW it is allowed to have random
τ1 τ2 τ3
time steps, corresponding to a sequence of WTs from a renewal
process. Here, the WT sequences derived from the EEG record- −1 −1
ings are used to define two different CTRWs driven by the same
RTP global events. Firstly, we introduce a discrete artificial Figure 2: The SJ walking rules for the “velocity signal” ξ(t).
signal ξ(t), i.e., a kind of random discontinuous velocity that
5
+1 +1 +1 +1
The joint use of these walking rules can be used to evaluate
τ2 the value of the µ by inverting the expressions given in Eqs. (3-
τ1 τ3
4). It can be seen from Fig. 4 that HAJ (µ) is not an invertible
function, as the same value of H corresponds to two distinct
t0 t1 t2 t3 values of µ, one smaller and the other greater than 2. When
HS J < 1/2 it results µ < 2 and both rules, i.e., the associated
Figure 3: The AJ walking rules for the “velocity signal” ξ(t).
values of µ derived from AJ and SJ rules, could be compared to
each other. On the contrary, for HS J = 1/2, a value of µ cannot
be derived from the SJ rule, but we can assume µ > 2. For this
1 reason, the SJ rule could be used to discriminate between µ < 2
H and µ > 2, overcoming the ambiguity of AJ rule.
AJ

0.5
Detrended Fluctuation Analysis. The diffusion scaling H of
the two random walks introduced above is estimated by means
SJ of Detrended Fluctuation Analysis (DFA) [62]. We briefly re-
call the main steps of this method:
0
1 2 3 µ • For a discrete time L = 4, 5, ..., the time series of the dif-
fusion process X(t) is split into not-overlapping time win-
Figure 4: Diffusion scaling H vs. complexity index µ for SJ and AJ walking dows of length L: [kL + 1, kL + L]. The window number is
rules: AJ (continuous line), SJ (dotted-dashed line).
given by [M/L], i.e., the integer part of M/L, being M the
total length of the time series.
Then, from the artificial signal ξ(t) the diffusion variable of the
• For each time window [kL+1, kL+ L] (k = 0, 1, ..., [M/L]),
CTRW is defined as follows:
the local trend is evaluated with a least-squares straight
j=t
X line fit: X k,L (t) = ak,L t + bk,L ; kL < t ≤ (k + 1)L.
X(t) = X0 + ξ( j) ∆t , (1)
j=0 • The fluctuation is derived in the usual way: X ek,L (t) = X(t)−
X k,L (t) = X(t) − ak,L t − bk,L ; kL < t ≤ (k + 1)L.
being ∆t the sampling time of the experimental time series.
The scaling properties of these random walks were exten- • For a given time scale L, the mean-square deviation of the
sively investigated in several papers (see [38, 36, 37] for a brief fluctuation is calculated over every window:
review) by applying the analytical methods of CTRW. Here we
are interested in the scaling exponent H of the second moment (k+1)L (k+1)L
1 X e2 1 X  2
F 2 (k, L) = Xk,L (t) = X(t) − X k,L (t) (5)
 2 L t=kL+1 L t=kL+1
σ2 (t) = h X(t) − X i ∼ t2H , (2)

where X is the mean value of X(t). • Finally, an average over the windows is performed:
Analytical expressions of the scaling H as a function of the [M/L]
complexity index µ were determined in the case of renewal WTs 1 X
F (L) =
2
F 2 (k, L) (6)
with inverse power-law tail: ψ(τ) ∼ 1/τµ . These expressions [M/L] k=0
H = H(µ) are reported in Fig. 4 and summarized in the follow-
ing: H
In the case of a self-similar process, it results: F(L) ∼ L . Then,

 µ/2 ; 1<µ<2 by defining z = log(F(L)) and y = log(L), it is possible to apply
a least-squares straight line fit:



HAJ =  2 − µ/2 ; 2≤µ<3

(AJ) (3)

z = Hy + C ,


 (7)
µ≥3

 1/2 ;
where C is a constant.
 (µ − 1) /2 ; 1<µ<2


HS J = 

(SJ) (4) Improvement of statistical accuracy in DFA. Given a time
 1/2 ; µ≥2

series of total length L, the DFA evaluation is reliable up to
Both rules give a normal scaling H = 1/2 for µ ≥ 3, corre- about L/10 and this is due to the lack of statistics in the long-
sponding to normal (Gaussian) diffusion. For the SJ rule this is time regime. However, we do not have only one time series, but
true also in the range 2 < µ ≤ 3, while AJ rule is super-diffusive several independent time segments, each one separated from the
(H > 1/2) in all the interval 1 < µ < 3. On the contrary, the SJ others by at least one artifact or phase shift in the original EEG
rule is sub-diffusive (H < 1/2) for 1 < µ < 2. We note that, if recording. Several DFA curves can be obtained, one for each
the WTs comes from a Poisson process, the value of H is again time segment, and then averaged to get a mean DFA curve. In
1/2 and, in the long-time, we have a Gaussian diffusion. this way, we are able to compute DFA up to a time given by the
6
maximum among the values Li /10, that is maxi (Li /10), where i a time from an underlying set of parallel scenes, and only
runs over all time segments and Li is the total duration time of this selected scene comes into consciousness;
the i-th time segment. Actually, the statistical accuracy remains
stable up to a time given by mini (Li /10) and then decreases for 4. In conscious states, there’s a competition among cooper-
longer time scales. In fact, the number of segments entering ative global integration and autonomous fragmentation;
the average decreases very rapidly when approaching the time the interplay of these two components constitutes the
scale maxi (Li /10). A common method to improve the statistics metastable regime of brain dynamics and determines the
is glueing different segments together, in order to have a reliable complex intermittent behavior in the EEG field [50, 64, 5].
P
DFA curve up to a time ( i Li )/10. This was done for instance 5. the renewal fractal process derived from EEG data, which
for coding segments in DNA [62]. is defined by the sequence of renewal RTP events, is a par-
We improved the statistical accuracy on longer time scales, ticular serial process, as only a global metastable state (gi-
without the risk of making the running window explore spu- ant cluster) at a time takes place and the short-time RTP
rious signal, i.e. that belong to different segments. Firstly, events mark the death of a metastable state and the birth of
for each sleep phase, we evaluated the minimal duration time: a new one [38, 23].
Lm = mini (Li ); then, for each segment, we computed the DFA
up to time Lm ; finally, we performed the average over all the From the above observations, we are then lead to make the fol-
segments. Note that Lm is not only 10 times greater than lowing assumption:
mini (Li /10), but it is also greater than maxi (Li /10). With this The renewal point process describing fractal intermit-
approach, a much better accuracy on long time scales is ob- tency, which is experimentally defined in EEG data by the
tained. In fact, even if the statistical accuracy is low for the sequence of global RTP events with inverse power-law dis-
segments with the shortest duration times, the number of seg- tributed WTs, is a correlate of consciousness.
ments entering the average is greatly increased in the time range We validate this assumption by comparing different states of
between mini (Li /10) and Lm = mini (Li ), as all segments always consciousness in healthy subjects during sleep. In Section 6
enter in the average operation. we have already given a description of the dataset and of the
methods used to analyze the EEG data, which can be summa-
rized as follows: (a) segmentation and artifact removal; (b) RTP
7. Results and discussion
detection, global brain events (c) computation of event-driven
Criticality has been found both in neuronal networks (models random walks (SJ and AJ) and estimation of second moment
and in vitro, see Refs. [22, 24]) and human brain [8] by inves- scaling H by applying DFA.
tigating the spatial and structural complexity, while temporal The diffusion scaling H of the SJ rule is definitively H =
complexity, i.e., time intermittency, in brain EEG was investi- 0.5 for all time segments and subjects (data not shown for the
gated in our previous papers (see Refs. [38, 23]). In particular, sake of conciseness). This is a signature that the complexity
from the analysis of EEG data in resting state (wakefulness) index µ is greater than 2. In Fig. 5 we show the square root
condition we found that the brain (RTP) events introduced by of the second moment σ(t) for the AJ rule, averaged over all
the authors of Refs. [51, 52] are driven by an underlying re- subjects and nights and over the time segments of sleep cycle I
newal fractal point process with well-defined scaling proper- as explained at the end of Section 6.
ties (fractal intermittency). As already said, it is not clear The second moment scaling H switches from an anomalous
if fractal intermittency is uniquely associated with conscious- diffusion scaling (H = 0.75) in the case of (pre-sleep) wake
ness or with a non-task-driven default mode activity [57], also and REM phases to a normal diffusion scaling (H = 0.5) in
present in non-conscious states like deep (NREM) sleep. To deep (SWS) sleep. Inverting Eq. 3, this means that in wake
clarify this point, let us summarize some observations about and REM phases, which are conscious states, we get an aver-
consciousness: age value µ = 2.5, thus giving fractal intermittency and long-
range correlations, whereas in the deep (SWS) sleep phase we
1. the conscious brain is associated with an emerging “gi- get µ > 3. We recall that normal diffusion (H = 0.5) is also
ant cluster” or Global Workspace [47]) that co-exist with in agreement with a Poisson condition, i.e., with exponentially
clusters of any size having scale-free size distribution, in distributed WTs or, more realistically, with an exponential cut-
analogy with what happens in critical systems (see e.g. off emerging at relatively short WTs and, thus, with short-time
[22, 24] for dynamical avalanches, or [63] for oscillator correlations.
synchronization); The normal diffusion regime during SWS phase could be ex-
2. conscious scenes are unitary and occur serially: only one plained in terms of the fragmentation of the Global Workspace
scene at a time takes place [47]; into local, independent, functional units working in parallel,
which is a condition known to be associated with the lack of
3. consciousness is a sequence of metastable states (giant consciousness. Notice that the fragmentation is related to the
clusters), which reflect rapidly adaptive selection mech- large number of Sleep Slow Oscillations (SSOs) during SWS
anisms in perception and memory; in the consciousness [65, 66], which determine a reset of the neuronal activity by
theory of Baars [47], the Global Workspace is an emerging means of a hyper-polarizing wave putting most neurons in a
serial process that, in some way, selects only one scene at down-state, i.e., a state far from the activation threshold of the
7
100 100
10 P(N)
σ(t)
10-1
1

0.1 10-2
10
0.01
10
0 2
10
3
10 10
4 5
10 10-3
t (ms) REM
SWS
10-4 WAKE
WAKE N2
REM i=1.9
1 SWS 10-5
H=0.75
H=0.5 10-6
1 10 N 100
3 4 5
10 10 t (ms) 10
Figure 6: Probability density function P(N) of the number of concurrent events
Figure 5: Asymptotic time range in the DFA computed for AJ rule applied to for different stages, limited to the first sleep cycle. Concurrency is defined in
different sleep phases (cycle I). Continuous and dashed lines are a guide to the the text, and holds within a tolerance time ∆t, i.e. adopting the prescriptions
eye for the slopes H = 0.75 and H = 0.5, respectively. In the inset we report of previous works [22, 38, 23]. Here ∆t = 4.0 ms. WAKE refers to pre-sleep
the entire time range over which the DFA has been computed. Notice that, in wakefulness. REM, N2 and SWS correspond to the different sleep stages as
the short-time range, the DFA of the three phases (WAKE, REM and SWS) are described in the section ”Methods”. Dashed line is a guide to the eye corre-
essentially superposed, all displaying normal diffusion. sponding to an inverse-power law with index ν = 1.9.

membrane potential. This is also called “electrical silence”. Fi- of N electrodes as follows
nally, from a purely descriptive point of view, we can conclude X X
that the result of Fig. 5 demonstrates that the scaling H, and the CN ≡ ξt(i) ξt( j) · · · ξt(k) , (9)
t i< j···<k
associated complexity index µ, could be proposed as a reliable
indicator of conscious states. The interpretation of these results where we consider all N-uples {i, j, · · · , k} of electrodes, so that
deserve further investigations that, however, will be the focus
of future research work. CN
P(N) = P . (10)
Surprisingly, the distribution of avalanche sizes does not N CN
change when comparing wakefulness, NREM and REM sleep. The result of P(N) illustrated in Fig. 6 thus suggests that the
This means that, at variance with the intermittent behavior, wakefulness functional connectivity is preserved both during
the global topological features of the brain neuronal network NREM and REM sleep. We can rigorously state that even in
are independent from the particular brain condition (wakeful- deep sleep spontaneous patterns emerge, with the same size dis-
ness, REM, NREM). Fig. 6 illustrates the distribution P(N) of tribution of those emerging during wakefulness or REM sleep.
avalanche sizes N, namely the number of electrodes simultane-
ously undergoing an RTP, within time tolerance ∆t = 4.0ms.
The distribution, confirming previous results [23], decays as 8. Heuristic explanation based on physiology
1/N ν with ν . 2. No difference in the distribution is visible
as a function of sleep phases. In [67] it was shown how neural functional connectivity de-
Let us see heuristically how distribution P(N) is related to the creases in deep sleep, compared to wakefulness, after sublim-
topology of functional connectivity. We recall that this prop- inal Trans-cranial Magnetic Stimulation (TMS). It was there-
erty is classically derived from cross-correlation functions. Let fore hypothesized that a pruned or simplified functional topol-
us for simplicity omit the role of ∆t, and consider concurrences ogy was responsible for the lack of consciousness, as it makes
as if the events in different electrodes were exactly at the same the system drifts away from the critical integration/segregation
time. Since our signal is given by the dichotomous time series balance towards a more segregated state. Along this line, [71]
ξ(t) corresponding to the AJ rule, we only have a nonzero con- recently reported that during NREM sleep the dynamics over
tribution for pairwise correlation functions only when we have different brain areas show an higher degree of independency
a concurrence of events among electrodes. Defining C2 as the (parallel computation) with respect to wakefulness and REM
sum of the integrals of all pairwise correlation functions sleep. An even more recent paper confirms this behavior in
XX anesthesia, i.e. during propofol-induced loss of consciousness
C2 ≡ ξt(i) ξt( j) , (8) [72]. Combining these important experimental results with the
t i< j increasing evidence of criticality in brain functioning (at least
during wakefulness) may lead to think that during NREM sleep
where ξt(i) is the dichotomous signal stemming from channel i the system drifts away from the critical regime. Does lack of
at time t, we can generalize this correlation measure for clusters consciousness mean that the system become supercritical or
8
   
   
   
   
   
   
   
   
   
   
   
   
   
   
   
   
   
   

Event:  integra,ng  excita,ons   Downwards  causa,on  or  SSO-­‐driven  reset  (long  arrow)  

Figure 7: Schematic description of circular causation with and without consciousness. Left panel describes a classic scheme of circular causation in critical systems.
Downwards arrows denote the dynamics of order parameters or, equivalently, the dynamic emergence of organized activity at a given level of description, which
generates an organized structure at a larger-scale level. Upwards arrows denote the constraints imposed by the emergence of structures within a level to a smaller-
scale level. The figure is inspired by Fig.1 of [50], where the smallest scale level is the microscopic one, either associated to neural small structures or to qualia (the
atoms of cognition); the second level is mesoscopic, associated to larger neural formations or to cognitive objects; the third is associated to a macroscopic neural
level, or to phenomenal scenes. Here a further level is introduced, making it explicit the fact that, at criticality, activity clusters continuously form (events) and
break, with only one giant cluster present at the time. Conversely, it also explicits the unitary nature of consciousness, and the emergence of a global workspace. In
the right panel we see the modifications induced by the possibility of neural bistability, which is normally induced by large fluctuations: Till the level of phenomenal
scenes the circular causation described by criticality is conserved; when a giant cluster is being formed the consequential large fluctuations directly reset the system
at the microscopic neural level (long downwards arrow). As a consequence the global workspace never survives in its unitarity. This is graphically underlined by
the use of a dashed line for the largest-scale.

subcritical? The question, at the light of our results, is a lit- coupling among neurons. As a result, it is also possible that the
tle more complicated and further aspects have to be taken into system stays globally critical, drifting from a critical condition
proper consideration. The explanation we propose, illustrated to another. As a matter of fact, an indication of global critical-
in Fig. 7 aims at conciling the results presented herein and the ity is given by the distribution P(N) of quake sizes that remains
known literature, also taking into account that in biology a new unaltered throughout all sleep phases.
form of criticality may take place, i.e. the extented criticality The stability of P(N) with respect to sleep phases may be at
advocated by Bailly and Longo [73]. According to this view, odds with the results of [67]. It has to be said, however, that we
some form of criticality always takes place in biological sys- are herein looking at spontaneous dynamics involving networks
tems, that continuously drift from a critical point to another (for also composed of thalamic neurons, rather than stimulated in a
a review see [74]). top-down fashion, hence shunting the thalamus, via TMS as in
The onset of sleep is characterized by a reduction of neuro- [67].
transmitters and hence of neural activity in the reticular ascend- Sleeping brain is characterized by cellular bi-stability. Neu-
ing system, connecting the brain stem to the cortex. This is fol- rons during sleep are able, due to the opening of calcium-
lowed by a sensory deafferentation. Both mechanisms reduce dependent potassium channels, to hyper-polarize down to nega-
the high frequency activity in the cell yielding a reduction in the tive potentials as low as −80mV. This state, is normally referred
amount of random activity onto synapses, or, in other words, to as “down state” or “electrical silence”. The reason of this be-
of fluctuations. We expect therefore that the system becomes havior is under debate. Some explanations are given by differ-
super-critical, i.e. more synchronized. On the other hand, the ent amounts of chemicals at the end of a prolonged wakefulness
reduction in neurotransmitters may also decrease the effective (s-process) [75]. For our purposes it is sufficient to recognize
9
that after the onset of sleep certain neurons live in a thermody- be devoted to the study of pathological forms of unconscious-
namic state such that an afferent activity may locally generate ness, as it is not clear whether the route to unconsciousness due
the down state. When a coordinated pool of nearby neurons to sleep may be a good model for understanding these condi-
globally undergo the electrical silence, a giant EEG event takes tions. It is foreseeable that epileptic-related unconsciousness
place, called Sleep Slow Oscillation (SSO) [65, 66] which is may share some mechanisms with sleep, while for other con-
able to diffuse to a large portion of the scalp. SSO events mark ditions like traumatic brain injuries (with wide-spread axonal
the death of metastable states, and can be safely assumed to be injury) this similarity is expected to break down.
renewal, since they reset the memory in vast areas of the scalp.
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