Cyborg psychiatry to ensure agency and autonomy in mental disorders. A proposal for neuromodulation therapeutics

Abstract

Neuromodulation therapeutics—as repeated Transcranial Magnetic Stimulation (rTMS) and neurofeedback—are valuable tools for psychiatry. Nevertheless, they currently face some limitations: rTMS has confounding effects on neural activation patterns, and neurofeedback fails to change neural dynamics in some cases. Here we propose how coupling rTMS and neurofeedback can tackle both issues by adapting neural activations during rTMS and actively guiding individuals during neurofeedback. An algorithmic challenge then consists in designing the proper recording, processing, feedback, and control of unwanted effects. But this new neuromodulation technique also poses an ethical challenge: ensuring treatment occurs within a biopsychosocial model of medicine, while considering both the interaction between the patients and the psychiatrist, and the maintenance of individuals' autonomy. Our solution is the concept of Cyborg psychiatry, which embodies the technique and includes a self-engaged interaction between patients and the neuromodulation device.

Full text

PERSPECTIVE ARTICLE
published: 05 September 2013
doi: 10.3389/fnhum.2013.00463
Cyborg psychiatry to ensure agency and autonomy in
mental disorders. A proposal for neuromodulation
therapeutics
Jean-Arthur Micoulaud-Franchi1,2*, Guillaume Fond3and Guillaume Dumas 4,5
1Unité de Neurophysiologie, Psychophysiologie et Neurophénoménologie, Solaris, Pôle de Psychiatrie Universitaire, Hôpital Sainte-Marguerite, Marseille, France
2Laboratoire de Neurosciences Cognitives, UMR CNRS 7291, 31 Aix-Marseille Université, Site St Charles, Marseille, France
3Université Paris Est-Créteil, Pôle de Psychiatrie du Groupe des Hôpitaux Universitaires de Mondor, INSERM U955, Eq Psychiatrie Génétique, Fondation
FondaMental Fondation de Coopération Scientifique en Santé Mentale, Paris, France
4Equipe Cogimage (ex-LENA CNRS UPR 640), CRICM - UPMC/INSERM UMR-S975/CNRS UMR7225, Paris, France
5Human Brain and Behavior Laboratory, Center for Complex Systems and Brain Sciences, Florida Atlantic University, Boca Raton, FL, USA
Edited by:
Elisabeth V. C. Friedrich, University
of Graz, Austria
Reviewed by:
Thorsten O. Zander, Max Planck
Institute for Intelligent Systems,
Germany
Klaus Mathiak, RWTH Aachen
University, Germany
*Correspondence:
Jean-Arthur Micoulaud-Franchi,
Solaris, Pôle de Psychiatrie
Universitaire, Hôpital
Sainte-Marguerite, 270 Bd
Sainte-Marguerite, 13009 Marseille,
France
e-mail: jarthur.micoulaud@
gmail.com
Neuromodulation therapeutics—as repeated Transcranial Magnetic Stimulation (rTMS)
and neurofeedback—are valuable tools for psychiatry. Nevertheless, they currently face
some limitations: rTMS has confounding effects on neural activation patterns, and
neurofeedback fails to change neural dynamics in some cases. Here we propose how
coupling rTMS and neurofeedback can tackle both issues by adapting neural activations
during rTMS and actively guiding individuals during neurofeedback. An algorithmic
challenge then consists in designing the proper recording, processing, feedback, and
control of unwanted effects. But this new neuromodulation technique also poses an
ethical challenge: ensuring treatment occurs within a biopsychosocial model of medicine,
while considering both the interaction between the patients and the psychiatrist, and the
maintenance of individuals’ autonomy. Our solution is the concept of Cyborg psychiatry,
which embodies the technique and includes a self-engaged interaction between patients
and the neuromodulation device.
Keywords: brain computer interface, neurofeedback, non-invasive brain stimulation, transcranial magnetic
stimulation, brain-state-dependent stimulation, mental disorder, psychiatry, neurocognitive networks
NON-INVASIVE ELECTROPHYSIOLOGICAL INTERVENTIONS
IN PSYCHIATRY
A new therapeutic approach in psychiatry is to modulate neu-
ral networks of the brain in order to induce neural plasticity
(Peled, 2005; Linden, 2006; Schneider et al., 2009; Thut and
Pascual-Leone, 2010). However, traditional treatments for men-
tal disorders such as pharmacology and psychotherapy give lit-
tle consideration to the neural network dynamics (Mackey and
Milton, 1987). Psychiatric drugs could have long-term neuroplas-
tic effects but are difficult to adapt to each patient (Fond et al.,
2012). Psychotherapies, in particular Cognitive Behavior Therapy
(CBT), have an adaptive and interactive effect on the brain but
it remains quite indirect (Goldapple et al., 2004). Two non-
invasive electrophysiological interventions, however, are proving
promising in brain therapeutics for mental disorders:
•Electrical brain stimulations devices: Transcranial Magnetic
Stimulation (TMS; Miniussi and Rossini, 2011)and
Transcranial Direct Current Stimulation (tDCS; Polania
et al., 2010)
•Neurofeedback (NF) devices (Coben and Evans, 2011).
Repeated TMS (rTMS) and NF are valuable therapeutics in the
field of psychiatry (Yucha and Montgomery, 2008; Coben and
Evans, 2011), but with rTMS we are confronted with the con-
founding effects of brain-mind states and, with NF, difficulties
to change neural dynamics could be a potential problem. In the
current proposal our aim is twofold: (i) to explain how rTMS
and NF coupling may offer a solution to the two aforementioned
problems, and (ii) to analyze how these neuromodulation tech-
niques may be integrated into an individual’s brain dynamics and
conception of him or herself as an autonomous agent (Glannon,
2013). In effect, we argue that the coupling of rTMS and NF can
pave the way for a direct, adaptive, and interactive brain therapy
in which patients can be self-engaged.
rTMS AND THE EFFECTS OF BRAIN-MIND STATES
Repetitive transcranial magnetic stimulation (rTMS) comprises
a non-invasive and painless way to induce magnetic flux activa-
tion (high frequency) or inhibition (low frequency; Lisanby et al.,
2002). Efficient in the treatment of psychiatric disorders, it has
proved particularly robust for the treatment of major depres-
sive episode (MDE), and results of its use in schizophrenia are
encouraging (Lisanby et al., 2002; Coben and Evans, 2011). rTMS
modifies neuronal activity in the selected superficial brain struc-
ture, but also modulates neural network activity (Lisanby et al.,
2002; Huerta and Volpe, 2009). Thus, basic research carried out
on TMS has led to the concept of “state dependency TMS”
(Silvanto and Pascual-Leone, 2008). This concept suggests that
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HUMAN NEUROSCIENCE

Micoulaud-Franchi et al. Cyborg psychiatry
the activation states of the neural circuits both before and dur-
ing the stimulation influence the pulse effect. Indeed, TMS effect
must be seen, not simply as the result of an applied stimulus,
but as the result of the interaction between the applied stimu-
lus and the level of brain activity (Silvanto and Pascual-Leone,
2008). Thus, the effects of rTMS are dependent on the brain-mind
states of the stimulated subject (Bonnard et al., 2003). Therefore,
current high variability of therapeutic effects of rTMS in mental
disorders may be due in part to its partial account of individuals’
neurodynamics and its effects on distant neural sites, even with
localized stimulations (Vedeniapin et al., 2010).
Basic research suggests that rTMS efficiency could be increased
in psychiatric disorders by triggering patients’ brain activi-
ties during stimulation (Micoulaud-Franchi et al., 2013). Thus
“interactive rTMS protocols” have been proposed (Micoulaud-
Franchi et al., 2013). In NeuroAnalysis 2008 (Peled)said:“a
future potential ‘brain pacemaker’ would probably involve a
multiple-coil TMS device coupled with an EEG-dependent feed-
back mechanism, similar to a cardiac pacemaker set to act
according to the ECG arrhythmias” (Peled, 2008). Thus, a “brain
pacemaker,” commonly referred to as “Brain-State-Dependent
Stimulation” (BSDS; Walter et al., 2012), would comprise an
adaptive TMS coupled to the ongoing brain activity; the stim-
ulation would vary in time, intensity, frequency, and topogra-
phy according to an on-line EEG feedback. EEG coupled TMS
is “a technique that has come of age” (Fitzgerald, 2010)and
offers new possibilities for the treatments of mental disorders
(Thut and Pascual-Leone, 2010; Miniussi and Vallar, 2011).
Priceetal.showthefirstencouragingresultsoftheuseofthis
kind of adaptive/contingent rTMS in the treatment of MDE
(Price et al., 2010).
NEUROFEEDBACK AND THE DIFFICULTIES TO CHANGE NEURAL
DYNAMICS
NF is a non-invasive technique that enables an individual to
learn the cognitive strategies required to change neurophysiolog-
ical activity (i.e., EEG), for the purposes of improving health and
performance (Yucha and Montgomery, 2008). The originality of
NF is that it gives patients a more active role in there own health
care (Yucha and Montgomery, 2008) and comprises a holistic
conception in which cognitive and brain activities are modified
together (Rémond, 1997; Cherici and Barbara, 2007; Coben and
Evans, 2011). For this reason, NF is also referred to as “psy-
choneurotherapy” (Paquette et al., 2009), “brain psychotherapy”
(Micoulaud-Franchi and Vion-Dury, 2011)or“neuroimagery
therapy” (deCharms, 2008). Indeed, NF facilitates an on-line self-
regulation of brain activity and as such may be considered as an
adaptive and interactive brain therapy (Micoulaud-Franchi et al.,
2012).
However, for certain subjects, modifying their neural dynam-
ics through NF can prove very difficult. In a NF study aimed
at investigating to what extent the regulation of excitability in
cortical networks is impaired in epileptic patients, it was found
that performance on NF was initially below healthy subjects and
that “not every patient seemed to be able to achieve this con-
trol” (Rockstroh et al., 1993). This difficulty is also found in
the field of Brain Computer Interface (BCI). BCI was developed,
in particular, as assistive technology for patients with motor
disabilities (Wang et al., 2010). BCI is commanded directly by
brain activity feedback (EEG, MEG or fMRI activities measure-
ments), with EEG activity constituting the most commonly used
brain activity feedback. However, BCI performances show large
variability across individuals, and for a non-negligible propor-
tion of users (estimated at 15–30%), BCI control does not work
(Vidaurre and Blankertz, 2010).
Many solutions have been proposed to optimize NF and BCI.
Solutions based “on the participants” are closed to cognitive and
behavioral therapeutics. The aims are to enhance the motiva-
tion of the participants, to help the participants to try different
strategies, to explicit individual-specific control strategies and
to apply the learned self-regulation skills in real-life situations
(Kotchoubey et al., 2001). Solutions based “on the BCI loop,”
were proposed to optimize BCI performance. We suggest that
some of these solutions could be applied to optimize NF for
treatment of mental illness. The first involves an algorithmic
solution that aims to develop a machine-learning mechanism
(Vidaurre and Blankertz, 2010). It is in line with the concept of
co-adaptation in which the tool becomes functionally involved
in the extraction and definition of the user’s goals: both subject
and the tool are learning (Sanchez et al., 2009). The second solu-
tion comprises a “hybrid BCI,” in which two BCIs are combined,
for example: event-related (de)synchronization (ERD, ERS) of
sensorimotor rhythms and steady-state visual evoked potentials
(SSVEP; Pfurtscheller et al., 2010). The third solution comes
from basic research in animals and invasive BCI. It uses closed-
loop neural interface technology that combines neural ensemble
decoding with simultaneous electrical microstimulation feedback
(Marzullo et al., 2010; Mussa-Ivaldi et al., 2010). However, very
few studies have used this solution to optimize BCI in humans
(Walter et al., 2012). Birbaumer suggested: “The combination of
these stimulation techniques (TMS, tDCS, neurochips) with BCIs
is a largely unexplored field” (Birbaumer and Cohen, 2007), and,
at the same time, research has yielded encouraging results show-
ing that TMS may help participants to increase their brain EEG
response performance in BCI (Kubler et al., 2002; Karim et al.,
2004). This solution is, therefore, worthy of interest in the field of
NF in psychiatry. Indeed, recurrent neuronal networks have been
used to propose an interpretation of several mental dysfunctions
(Pezard and Nandrino, 2001), which is evidence in itself that it
is particularly difficult to modify one’s brain activity when one
has such mental disorders. Thus, rTMS could bring the necessary
energy to break the recurrent neural network dynamics in order
to help the patient explore new neural network dynamics and, by
means of the NF device, change his/her EEG activity in the desired
way to improve health and performance (Micoulaud-Franchi and
Vion-Dury, 2011). tDCS may also enhance the effect of cognitive
remediation techniques (Andrews et al., 2011) and could, thus,
havethesamepositiveeffectonNF(Miniussi and Vallar, 2011).
COUPLING NON-INVASIVE ELECTROPHYSIOLOGICAL
INTERVENTIONS
THE CHALLENGE OF CLOSING THE LOOP
To summarize, firstly TMS may be improved by taking into
account brain activity (particularly EEG activity) to stimulate the
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Micoulaud-Franchi et al. Cyborg psychiatry
brain (Price et al., 2010)and,secondly,NFcouldbeimprovedby
combining it with TMS or tDCS brain stimulation (Kubler et al.,
2002). In addition, further research needs to be undertaken in
this area to replicate the preliminary results in mental disorders
(Price et al., 2010). However, here we propose to investigate the
challenge of neuromodulation techniques that couple these two
aforementioned improvements. We previously proposed the con-
cept of “Neurofeedback rTMS” (Micoulaud-Franchi and Vion-
Dury, 2011): in which the rTMS efficacy is enhanced by the
background EEG, which is self-regulated by subjects through NF,
and, at the same time, the subject is helped by the rTMS to cre-
ate this background EEG. TMS/tDCS-NF coupling can, therefore,
close the loop completely in order to optimize simultaneously
the non-invasive neurostimulation techniques and the NF, See
Figure 1.TMS/tDCS-NFcouplingis,however,confrontedbytwo
challenges: the first is algorithmic, the second is ethic.
The algorithmic challenge involves determining the kind of
brain activity that will be recorded and the kind of feedback that
will be made, how all these data will be treated in real time and
how to control unwanted effects. The first issue is related to the
use of a new diagnostic system correlated to the neural network
disturbance in mental disorders. The “Clinical Brain Profiling”
advanced by Peled is an interesting approach to these novel thera-
peutic hypotheses based on TMS/tDCS-NF coupling (Peled, 2006,
2009). Peled proposed a new etiology-oriented diagnostic system
for psychiatry based on neural network dynamics complexity and
neural plasticity (Peled, 2004). It provides an innovative heuris-
tic for recording brain activity and will soon integrate data from
TMS-EEG research (Ilmoniemi et al., 1997; Thut and Pascual-
Leone, 2010). The second issue related to such approaches is how
to better account for non-linear dynamics in neuroscience. This
is already being tackled at the theoretical levels, but relies, also,
on the development of new methods. One such novel method is
the “dynamic clamp” advanced by Prinz et al. (2004), which con-
sists in dynamically interfacing living cells with their simulated
counterpart. This technique creates a “hybrid network” incorpo-
rating the inherent nonlinearities of most physiological processes
FIGURE 1 | Combination of Brain-State-Dependent Stimulation
(green-red loop) and Neurofeedback rTMS (blue-red loop) as an
example of Cyborg psychiatry device, adapted from Thut and
Pascual-Leone (2010).
(Prinz et al., 2004). Such a concept has been already scaled from
the neural to the behavioral scale with the so-called “Virtual
Partner Interaction” (VPI; Kelso et al., 2009). VPI could constitute
a paradigmatic model for the therapeutic approach described in
the current paper (Werr y et al., 2001).Thelastalgorithmicissueis
related to some problems appearing in closed loop systems (Corke
and Good, 1996). Indeed, a closed loop feedback system based
on NF and rTMS/tDCS could lead to unforeseeable “resonance”
effects in the brain that should be investigated and be taken into
account.
Theethicchallengeisinlinewiththegeneralaimofpsychiatry,
which tries to enable patients to lead a more self-determined life.
Indeed, psychiatry increasingly uses neuromodulation techniques
in the treatment of mental disorders. For example, the Mind
Machine Project (MMP) initiated in 2009 by the Massachusetts
Institute of Technology (MIT) is “looking for advanced applica-
tions of these technologies, such as “non-chemical based” solu-
tions for psychiatric treatments and brain prostheses.” In addition
the concept of neurorehabilitation has been applied in the field
of psychiatry (Bach-Y-Rita, 2003; Miniussi and Rossini, 2011;
Miniussi and Vallar, 2011). Thus, the question is: how can we
ensure that all these techniques restore or enhance a person’s
agency and autonomy? Related to this, we propose a first ethi-
cal issue based on the biopsychosocial model of medicine and a
third person perspective (Glannon, 2013). This issue is related
to the fact that these neuromodulation techniques depend on
the interaction between the learner (subjects) and the trainer
(practitioner/therapist), and are constructed as a process that
occurs within a biopsychosocial context and social constraints
(Glannon, 2013). We also put forward a second, more radical,
ethical issue based on a neurophenomenological point of view
and a first person perspective. Here we suggest that agency and
autonomy depend on the capacity of all these techniques to be
embodied by the patients. Such an approach is already present
in closed loop technology for sensory substitution (Bach-Y-Rita,
2003; Bach-Y-Rita and Kercel, 2003). The ethical issue is ensured
by the fact that the subject used the device as a part of his/her
body. The device has to open up a world to the subject that will
be appropriated by himself or herself. Similarly, TMS/tDCS-NF
coupling could help patients to promote therapeutic neural plas-
ticity using their own brain connectivity and without the direct
intervention a third party (Linden, 2006; Schneider et al., 2009).
Of course, psychiatrists should still help the patients, but the
important point is that the device enables the subject to redis-
cover their own mind-brain world and from their own first person
perspective. This ethical point of view leads us to the concept of
Cyborg.
BACK TO THE CYBORG CONCEPT AS AN HEURISTIC FOR CUTTING
ACROSS MIND, BRAIN AND DEVICES
“Cyborg” is a term coined in 1960s, in the context of the chal-
lenges presented by space flight and travel, with the famous article
entitled “Cyborgs and Space,” by Kline, a psychiatrist at Rockland
State Hospital, and Clynes, a scientist at the Dynamic Simulation
Lab (Clynes and Kline, 1960; Gray, 1995). “Cyborg” combined
the words “cybernetic” and “organism.” The concept involves
devices that enable an organism to live outside its habitat (in
Frontiers in Human Neuroscience www.frontiersin.org September 2013 | Volume 7 | Article 463 |3

Micoulaud-Franchi et al. Cyborg psychiatry
this case: Space): “The Cyborg deliberately incorporates exoge-
nous components extending the self-regulatory control function
of the organism in order to adapt it to new environments” (Clynes
and Kline, 1960). Consequently, a Cyborg is a kind of extended
embodiment, an organism that is, at the same time, natural and
artificial, and, as such, questions the limits between organism,
technology and external environment (Tomas, 1995).
In 1970, Clynes wrote, this time without Kline, a second
Cyborg article entitled “Sentic space travel” (Clynes, 1995). This
Sentic Cyborg involves devices that enable a human “to express
his emotion in accordance with his nature” to enable them to
carry out very long space-flights (Gray, 1995). Initially refused,
Clynes’ proposition is now of theoretical interest in light of the
new possibilities of cognitivo-brain modulation using TMS/tDCS
and NF. Kline and Clynes’ original question, “What are some of
the devices necessary for creating self-regulating man-machine
systems (...) to unconsciously adapt it to new environments?”
(Clynes and Kline, 1960), can now be rephrased as: What are
the devices needed to create self-regulating brain-machine sys-
tems to be used by patients with mental disorders to pro-
mote new brain/mind dynamics? By extending the first Cyborg
hypothesis of Kline and Clynes, the new direct, adaptive, and
interactive brain therapies proposed in this paper could not
only open the door to new ways of interacting with the outside
(Space), but also create new possibilities of dealing with the inside
(brain-mind).
As Clynes suggested in the conclusion of his Sentic Cyborg
hypothesis: “Through understanding our unconscious heritage
consciously, we may be able to teach our automatic systems to
live in harmony with our old heritage, as well as with our new
exploration of outer, and perforce, inner, space” (Clynes, 1995).
The benefit of the cyborg hypothesis is that it leads the psychia-
trist to consider neurostimulation techniques (as TMS or tDCS),
not just as an outside brain constraint, but also as a brain guid-
ance interaction in which the patient’s mind is self-engaged. This
hypothetical point of view is meanly theoretical and need to be
tested with some experimental observations in order to confirm
its effectiveness and its lack of unwanted and side effects as “res-
onant” effects (Corke and Good, 1996). However, we wanted to
stress that the future of neuromodulation treatments for mental
disorders will involve dealing, firstly, with neural network dynam-
ics (Peled, 2006, 2008) and, secondly, with the capacity of the
treatment to exploit the point of view of the patients, to act as
acyborgdevice.
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Conflict of Interest Statement: The
authors declare that the research
was conducted in the absence of any
commercial or financial relationships
that could be construed as a potential
conflict of interest.
Received: 08 February 2013; accepted:
25 July 2013; published online: 05
September 2013.
Citation: Micoulaud-Franchi JA, Fond G
and Dumas G (2013) Cyborg psychia-
try to ensure agency and autonomy in
mental disorders. A proposal for neu-
romodulation therapeutics. Front. Hum.
Neuro sci. 7:463. doi: 10.3389/ fnhum.
2013.00463
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