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Journal of Cognitive Enhancement

, Volume 2, Issue 4, pp 335–347 | Cite as

How Brain Stimulation Techniques Can Affect Moral and Social Behaviour

  • C. Di Nuzzo
  • R. Ferrucci
  • E. Gianoli
  • M. Reitano
  • D. Tedino
  • F. Ruggiero
  • Alberto Priori
Original Article

Abstract

Brain stimulation techniques, such as transcranial direct current stimulation (tDCS), transcranial magnetic stimulation (TMS), and deep brain stimulation (DBS) are used to treat psychiatric and neurological diseases. It elicits physical, cognitive, and mood benefits by promoting neuroplasticity. However, at the same time, several studies showed that these techniques could also alter moral judgment and social behaviour, leading to aggressive and prosocial behaviour; thus, there arises an ethical consideration about their effects and usability. Morality has been debated over centuries as the social behaviour regulator in our society. It is required for cognitive executive functions, problem solving, consequence anticipation, conflict management, and emotional evaluation. From an anatomical point of view, in addition to its philosophical and psychological complexity, we know that morality involves different brain areas and neural circuits both cortical and subcortical. In this mini-review, we report a number of recent results related to the use of brain stimulation techniques for modulating moral and social behaviour in human beings.

Keywords

Morality Brain stimulation tDCS TMS DBS Moral brain Moral behaviour Social behaviour Neurostimulation 

Abbreviations

A tDCS

anodal tDCS

A TMS

active TMS

AON

action observation network

AQ

Aggression Questionnaire

C tDCS

cathodal tDCS

CIT

concealed information detection test

cTBS

continuous theta burst stimulation

DBS

deep brain stimulation

DG

dictator game

DGp

dictator game with punishment option

DLPFC

dorsolateral prefrontal cortex

DRE

drug-resistant epilepsy

ECG

echocardiogram

EEG

electroencephalogram

EMG

electromyography

FAD

faked-action-discrimination tasks

fMRI

functional magnetic resonance imaging

GKT

guilty knowledge task

GnGT

go no go task

Hz

Hertz

IAB

intractable aggressive behaviour

IED

intermittent explosive disease

IFC

inferior frontal cortex

IQ

intelligence quotient

IRI

Interpersonal Reactivity Index

L.

left

M1

primary motor cortex

mA

milliampere

MADRS

Montgomery-Åsberg Depression Rating Scale

MEPs

motor evoked potentials

Min

minutes

Mm

millimeters

MMSE

Mini Mental State Examination

MOAS

Modified Overt Aggression Scale

MoCA

Montreal Cognitive Assessment

mPFC

medial prefrontal cortex

NIBS

non-invasive brain stimulation

OAS

Overt Aggression Scale

OFC

orbitofrontal cortex

PD

Parkinson’s disease

PFC

prefrontal cortex

PMH

posteromedial hypothalamus

PPI

Psychopatic Personality Inventory

R.

right

RPQ

Reactive Proactive Aggression Questionnaire

RT

reaction times

rTMS

repetitive transcranial magnetic stimulation

S tDCS

sham tDCS

SCR

skin conductance response

SDS-17

Social Desirability Scale-17

SI

primary somatosensory cortex

SOP

social orientation paradigm

STN

subthalamic circuit

tACS

transcranial alternating current stimulation

TAP

Tayor Aggression Paradigm

TCI

transcallosal inhibition

tDCS

transcranial current direct stimulation

TG

trust game

TMS

transcranial magnetic stimulation

ToM

theory of mind

TPJ

temporoparietal junction

UG

ultimatum game

VAMS

Visual Analog Mood Scale

VAS

Visual Analogue Scales

VAT

vision attention task

VLPFC

ventrolateral prefrontal cortex

Introduction

In the past few decades, a mounting number of studies have demonstrated that brain stimulation techniques can affect moral behaviour, one of the most sophisticated features of human judgment and the mind. For centuries, morality has been debated as the regulator of social behaviour in society due to its impact on emotions and cognition and its implications for the theory of the mind (ToM) (Greene et al. 2004). In reality, morality describes the principles that govern behaviour concerning the standards of right, acceptable, or wrong behaviour or actions (Harris 2011). Other social behaviors related to morality, such as aggressiveness and prosocial behaviour, which form the basis for human interactions. In fact, the majority of scientific studies investigating healthy individuals have explored human behaviour in problematic situations―more specifically, by using moral dilemmas in which individuals are asked to judge the appropriateness of a moral violation, such as killing someone, to obtain a great reward or to save other lives. Studies involving patients have, instead, focused on some forms of aggressive and violent behaviour that can be considered “amoral.” In several psychiatric and neurological conditions, such as Parkinson’s disease (PD), intellectual disability or epilepsy, abnormal and aggressive behaviors are often exhibited (Fumagalli and Priori 2012). In some cases, drug treatment or behavioral therapies are not always sufficient; therefore, it is necessary to resort to neurosurgical treatment. It is evident that morality, in addition to its philosophical and psychological complexity, involves neuroanatomical structures, both cortical and subcortical (Fumagalli and Priori 2012).

It has long been known that the brain affects human behaviour, as explained by the famous and historical case of Phineas Gage. This case demonstrates how significant personality changes can occur after a serious brain injury involving the frontal lobe. In the absence of language, movement or learning deficits, lesion(s) in the frontal lobe cause behavioural alterations as if “Gage was no longer Gage,” such as irreverence, disinhibition, and blasphemy (Harlow 1848). After Gage’s death, Damasio (2000) confirmed that the injured part(s) of the brain corresponded with cortical structures that mediate the emotional and cognitive aspects of behaviour, translating into moral decisions and choices.

In the past few decades, neuroscientific studies have begun to clarify specific anatomical brain structures that are most directly involved in behaviour and moral judgment (Fumagalli and Priori 2012). The frontal lobe controls emotions, behavioural regulation, and planning; hence, dysfunction may lead to impulsive and aggressive behaviour. The temporal lobe is involved in empathy and ToM; therefore, dysfunction is often involved in psychopathy. Only a few evidence-based reports have demonstrated the involvement of the inferior parietal lobe in moral judgment in healthy subjects; however, the parietal lobe appears to have an “assistive role” in all the other brain regions that are directly engaged in moral judgment (Pascual et al. 2013). Subcortical structures are also engaged in moral behaviour: the amygdala, hippocampus, and basal ganglia play an important role in the elaboration of negative emotion and behavioural evaluation of moral dilemma(s) (Decety et al. 2011).

In this scenario, interest in the role of brain stimulation techniques is growing to understand the mechanisms by which moral and social behaviours are modulated. Brain stimulation techniques involve the activation or inhibition of brain activity (Darby and Pascual-Leone 2017). This is made directly possible with the application of electrical current, which can be supplied non-invasively through electrodes placed on the scalp, as in transcranial direct current stimulation (tDCS), or from electrodes implanted in the brain during deep brain stimulation (DBS). Electric current can also be induced using magnetic fields applied to the head, such as with transcranial magnetic stimulation (TMS). While these types of techniques are frequently used for the treatment of some mental disorders and neurological diseases, they are also promising therapies to treat abnormal moral behaviour. However, what are the ethical implications of altering human behaviour using neuromodulation techniques? The present mini-review aimed to answer this question by reporting recent results and debating how brain stimulation techniques can affect moral and social behaviour from a new perspective.

Methods

Articles published in the Medline (PubMed) database were searched through June 20, 2018, using the terms “brain stimulation,” “tDCS” OR “transcranial direct current stimulation,” “TMS” OR “transcranial magnetic stimulation,” “DBS” OR “deep brain stimulation,” in combination with “morality” OR “moral behaviour,” “aggressive behaviour” OR “aggressivity,” “prosocial behaviour” OR “empathy.” Only published studies examining moral behaviour modulated using brain stimulation were included. Therefore, only studies in which tDCS, TMS, and DBS produced or influenced behaviour in humans―either in healthy or clinical samples―were examined. Three external authors manually screened and selected potentially eligible articles, and only studies published in English were included.

Outcome Measures

The Medline (PubMed) database was systematically searched for studies that clearly measured moral and ethical outcomes using brain stimulation techniques, as well as single cases and studies with significant results. The following information was extracted from each article: type and parameters of the brain stimulation technique (tDCS, TMS, DBS); brain target; sample characteristics (number, sex, age, and clinical and/or healthy participants); outcomes; and results.

Results

The search resulted in the retrieval of 172 studies. Review articles, letters to the editor, and reports without clear moral outcomes were excluded. From this search, 39 studies specifically investigated the use of brain stimulation techniques on moral or social behaviour, in either healthy or clinical samples. The articles were grouped into two categories: “moral behaviour” and “social behaviour.”

Moral behaviour included moral judgment and dilemma, while social behaviour addressed aggressiveness and prosocial behaviour. In each category, studies were divided based on the type of brain stimulation technique used (i.e. tDCS, TMS, or DBS). All articles were published between 2008 and 2018.

Moral Behaviour Studies

A small number of studies investigated the role of brain stimulation techniques in moral behaviour (n = 12) (Table 1). Five studies used tDCS; five used TMS; and two explored DBS.
Table 1

Modulation of moral behaviour using non-invasive and invasive brain stimulation techniques

Moral behaviour

Author and year

Brain stimulation parameters

Target location

Sample (mean ± standard deviation years)

Outcomes

Relevant results

Transcranial direct current stimulation (tDCS)

 Sellaro et al. 2015

Anodal/cathodal sham

Intensity = 1 mA

Duration = 20 min

R. TPJ

N = 60 healthy subjects (21 males, range 19–29 years)

Moral judgment task

(Young et al. 2010)

A-tDCS of R.TPJ led to diminished moral blame for accidental harms

 Kuehne et al. 2015

Anodal/cathodal sham

Intensity = 2 mA

Duration = 20 min

L. DLPFC

N = 54

(30 males, range 20–29 years)

Moral personal dilemmas

(adapted from Greene et al. 2004)

Anodal stimulation of L.DLPFC led to less utilitarian responses

 Ye et al. 2015

Anodal/cathodal sham

Intensity = 2 mA

Duration = 20 min

L. or R. TPJ

N = 54 healthy subjects

(22 males, range 19–30 years)

Moral judgment task A

Moral judgment task B

(adapted from Young et al. 2010)

Cathodal R.TPJ reduced blame for attempted but unsuccessful harms

Cathodal L.TPJ increased blame for accidental harms

 Yuan et al. 2017

Anodal/sham

Intensity = 1.5 mA

Unknown duration

mPFC

N = 64 healthy subjects

(38 males, 23.57 ± 2.1 years)

Moral and immoral picture stimuli patterns

(Harenski and Hamann 2006)

mPFC plays an important role in moral judgments while modulating ratings of moral violations

 Zheng et al. 2018

Anodal/cathodal sham

Intensity = 2 mA

Duration = 20 min

R and L DLPFC

R and L TPJ

N = 100 healthy subjects

(48 males, range 17–30 years)

Computer moral judgment task

(adapted from Greene et al. 2001)

A-tDCS on R.DLPFC and C-tDCS on L.DLPFC led to less utilitarian judgments, especially in moral-personal conditions.

Bilateral stimulation of TPJ altered the moral response in non-moral, moral-impersonal and moral-personal dilemmas.

Transcranial magnetic stimulation (TMS)

 Baumgartner et al. 2013

rTMS

Frequency: 1 Hz

Time: 20 min

L. or R. TPJ

N = 36 healthy subjects

(all males; 24.3 ± 4.2 years)

Morality and social dominance orientation questionnaires

Reciprocity and injustice sensitivity scales

1-Hz TMS of R.TPJ decreased punishment of outgroup.

No difference in any scale across treatment groups.

 Buckholtz et al. 2015

rTMS

Frequency: 1 Hz

Time: 30 min

L. or R. DLPFC

N = 66 healthy subjects

(32 males; 18–30 years)

Moral SCENARIOS

(Robinson and Darley, 1995; Robinson

and Kurzban, 2006)

1-Hz R.TMS of either right. or left DLPFC reduced punishment for responsible moral violators

 Jeurissen et al., 2014

TMS

3-pulse inhibition

R. DLPFC

R. TPJ

N = 17 healthy subjects

(8 males; 23.7 years)

Computerized task

RT

TMS-induced disruption of the DLPFC during non-moral, moral-impersonal and personal decisions lead to lower ratings of regret.

 Tassy et al. 2011

rTMS

Frequency: 1 Hz

Time: 15 min

R. DLPFC

N = 24 healthy subjects

(all males)

Moral sense test modified and translated

(Greene et al. 2001)

1-Hz TMS of R.DLPFC reduced utilitarian responses to high conflict personal moral dilemmas

 Young et al. 2010

Exp.1: R.TPJ-TMS

1 Hz

Exp.2: R.TPJ-TMS

10 Hz

R. TPJ

Exp.1 N = 8 (3 males)

Exp.2 N = 12 (5 males)

Range 18–30 years

The moral judgment task

(Young et al. 2010)

1-Hz TMS of R. TPJ increased permissibility for attempted but unsuccessful harms.

Deep brain stimulation (DBS)

 Fumagalli et al. 2011

STN DBS

Bilateral subthalamic

N = 16 with idiopathic PD (8 males; 60 ± 8.6 years, disease duration 11.8 ± 5.2, education 10 ± 3.2)

MMSE and VAS

Moral task (adapted from Greene et al. 2004)

Electrophysiological data

STN responds specifically to conflictual moral stimuli, and could be involved in conflictual decisions of all kinds, not only those for moral judgment.

 Fumagalli et al. 2015

STN DBS

Bilateral subthalamic

N = 11 with idiopathic PD and bilateral STN DBS (5 males, 63 ± 4.8 years)

N = 11 with idiopathic PD without DBS

(6 males; 65 ± 9.2 years)

Computerized moral task (adapted from Greene et al. 2004)

Neuropsychological evaluation

Motor, cognitive, and psychological assessment

No significant results

A-tDCS = anodal tDCS; C-tDCS = cathodal tDCS; Exp = experiment; DG = dictator game; Hz = Hertz; L. DLPFC = left dorsolateral prefrontal cortex; L. TPJ = left temporoparietal junction; mA = milliampere; MEPs = motor evoked potentials; Min = minutes; MMSE = Mini Mental State Examination; mPFC = medial prefrontal cortex; PD = Parkinson’s disease; R. TPJ = left temporoparietal junction; RT = reaction times; rTMS = repetitive transcranial magnetic stimulation; STN DBS = subthalamic circuit deep brain stimulation; TMS = transcranial magnetic stimulation; VAS = visual analogue scale

tDCS and Moral Behaviour

Five studies that investigated how tDCS modulated moral behaviour were selected (Kuehne et al. 2015; Sellaro et al. 2015; Ye et al. 2015; Yuan et al. 2017; Zheng et al. 2018). All of which included healthy samples (total n = 332, 159 males). The largest sample was 100 subjects (Zheng et al. 2018), and the smallest had 54 subjects (Kuehne et al. 2015; Ye et al. 2015).

Four studies compared both anodal and cathodal stimulations (Sellaro et al. 2015; Kuehne et al. 2015; Ye et al. 2015; Zheng et al. 2018). One study examined increased cortical excitability only (Yuan et al. 2017). Direct current from 1 (Sellaro et al. 2015) to 2 mA (Kuehne et al. 2015; Ye et al. 2015; Zheng et al. 2018) was delivered for 20 min. With regard to the brain target, three studies focused on the role of the temporoparietal junction (TPJ) (Sellaro et al. 2015; Ye et al. 2015; Zheng et al. 2018), two on the dorsolateral prefrontal cortex (DLPFC) (Kuehne et al. 2015; Zheng et al. 2018), and one on the medial prefrontal cortex (mPFC) (Yuan et al. 2017).

TMS and Moral Behaviour

Five studies that investigated the modulation of moral behaviour, especially on moral decision-making and judgment, using TMS were selected (Baumgartner et al. 2013; Buckholtz et al. 2015; Jeurissen et al. 2014; Tassy et al. 2011; Young et al. 2010). They involved 163 healthy participants (105 males). The largest sample included 66 subjects (Buckholtz et al. 2015), and the smallest included 17 (Tassy et al. 2011). Three studies used rTMS, which was delivered at a frequency of 1 Hz, explored the roles of the DPLFC (Baumgartner et al. 2013) and TPJ (Buckholtz et al. 2015; Tassy et al. 2011). Single-pulse TMS was used on the right DPLFC and right TPJ (Jeurissen et al. 2014; Young et al. 2010). Modulation of the moral behaviour responses were detected using a self-report scale and reaction time (RT).

DBS and Moral Behaviour

The role of DBS in moral decision-making was investigated in two studies (Fumagalli et al. 2011; Fumagalli et al. 2015) involving 38 patients with PD and 27 with bilateral subthalamic (STN) DBS implants. This brain stimulation technique permitted the exploration of the role of subcortical regions in moral behaviour.

Social Behaviour Studies

A large number of studies investigated the role of brain stimulation techniques in social behaviour, specifically in aggressive or prosocial behaviors (n = 27) (Table 2). Fifteen studies used tDCS, six used TMS, and six investigated DBS.
Table 2

Modulation of social behaviour using non-invasive and invasive brain stimulation techniques

Social behaviour

Author and year

Brain stimulation parameters

Target location

Sample (mean ± standard deviation years)

Outcomes

Relevant results

Transcranial direct current stimulation (tDCS)

Aggressive behaviour

 Choy et al. 2018

Anodal/sham

Intensity: 2 mA

Duration: 20 min

DPLFC

N = 81

(36 males, range ≥ 18 years)

Building language

Psychomotor vigilance task

Iowa gambling task

A-tDCS on DPLFC decreased aggressive intent

 Dambacher et al. 2015a

Anodal/sham

Intensity = 2 mA

Duration 750 s

R. DLPFC

N = 43 healthy subjects

(20 males, 22.14 ± 2 years)

TAP / RPQ

A-tDCS of R DLPFC reduced proactive aggression in men only. TAP correlated positively with RPQ in men, but not in women.

  Dambacher et al. 2015b

Anodal/cathodal

Sham

Intensity = 1.5 mA

Duration = 22 min

L. or R DLPFC

N = 64 healthy subjects

(21.89 ± 3.26 years)

GnGT

TAP/RPQ

No significant results

 Hortensius et al. 2011.

Anodal/cathodal

Sham

Intensity = 2 mA

Duration = 15 min

R. or L. DLPFC

N = 60 healthy subjects

(40 males, age unknown)

Reaction-time game task

TAP

A-tDCS of L.DLPFC increased aggressive responses when individuals were angry

  Riva et al. 2017

Anodal/sham

Intensity = 1.5 mA

Duration = 20 min.

R. VLPFC

N = 79 healthy subjects

(32 males, 21.73 ± 2.38 years)

Violent or non-violent videogame

TAP

A-tDCS on R.VLPFC reduced unprovoked aggression in violent-game players

Prosocial behaviour and empathy

  Coll et al. 2017

Anodal/cathodal

Sham

Intensity = 2 mA

Duration = 20 min.

R. TPJ

N = 48 healthy subjects

(24 males, age unknown)

EEG

SCR/ECG

VAS

A-tDCS stimulation on R.TPJ can decrease the intensity of the pain perceived in others

  Gallo et al. 2018

Anodal/sham

Intensity = 1.5 mA

Duration = 18 min.

L. SI

N = 26 healthy subjects (13 males, 25 ± 4 years

Rating other’s pain

SI influences prosocial decision-making

  Mai et al. 2016

Anodal/cathodal

Sham

Intensity = 1.5 mA

Duration = 20 min.

R. TPJ

N = 68 healthy subjects (33 males, 2.8 ± 2.6 years)

Vollom task

C-tDCS on R. TPJ decreased ToM and cognitive empathy

  Maréchal et al. 2017

Anodal/cathodal

Sham

Intensity = 1.5 mA

Duration = 30 min.

R. DLPFC

N = 145 healthy subjects (73 males, 23 ± 4 years)

Prosocial cheating experiment: N = 156 healthy subjects (68 males; 23 ± 3 years)

DG

Delay discounting ask

tDCS on R. DLPFC reduced cheating when dishonest behaviour

  Nihonsugi et al. 2015

Anodal/sham

Intensity = 2 mA

Duration = 552 s

R. DLPFC

N = 22 healthy subjects

(13 males, 20.5 ± 1.5 years)

TG

A-tDCS on R. DLPFC increases cooperation decisions

  Rêgo et al. 2015

Anodal/cathodal

Sham

Intensity = 2 mA

Duration = 15 min

L. or R. DLPFC

N = 24 healthy subjects

(12 males, 23 ± 2.57 years)

VAMS

Pain stimuli task

Pupil dilation

Self-pain perception

C-tDCS on L.DLPFC and A-tDCS on R.DLPFC reduced emotional valence and arousal ratings to viewing pain in others. Both active DLPFC stimulation decreased self-pain perception

  Ruff et al. 2013

Anodal/cathodal

Sham

Intensity = 1 mA

Unknown duration

R. VLPFC

N = 77 healthy subjects

(All females, 22 ± 0.4 years)

Computerized UG and DG

A-tDCS on R.VLPFC increased giving in UG (+ 33.5%) but decreased in DG.

C-tDCS on R.VLPFC obtained the opposite effect.

 Snowdon and Cathcart., 2018

Anodal/cathodal

Sham

Intensity = 1.5 mA

Duration = 20 min

R. DLPFC

N = 99 healthy subjects (45 males; 23.07 ± 5.36 years)

IRI/SDS-17

Self-report

No significant results

  Wang et al. 2014

Anodal/cathodal

Sham

Intensity = 2 mA

Duration = 5 min

L. DLPFC

N = 27 healthy subjects (9 males, 23.6 ± 2.9 years)

Computerized task

Scale for Pain-related Self-report

A-tDCS on L. DLPFC increased empathic pain ratings

  Wang et al. 2016

Anodal/sham

Intensity = 2 mA

Duration = 15 min

R. OFC

N = 60 healthy subjects (25 males, range 20–25 years)

TG

A-tDCS on R.OFC increased trust and giving

Transcranial magnetic stimulation (TMS)

Aggressive behaviour

  Hofman and Schutter 2009.

TMS/TCI

Frequency = 0.18 ± 0.02 Hz.

Corpus callosum

L. and R. M1

N = 20 healthy subjects (2 males; 21 ± 1.81 years)

EMG

AQ

Selective attention for facial expressions

Increased left-to-right together with reduced right-to-left TCI was associated with a stronger attentional bias for angry faces.

Higher levels of left-to-right TCI significantly correlated with higher AQ scores.

 Perach-Barzilay et al. 2013

cTBS

3-pulse 50 Hz, delivered at

rate of 5 Hz

L. or R. DLPFC

N = 18 healthy subjects (14 males; 28 ± 4.68 years)

SOP

cTBS on R.DLPFC reduces both reactive and proactive aggression

Prosocial behaviour and empathy

 Balconi and Canavesio 2014

TMS

Frequency = 10 Hz

DLPFC

N = 25 healthy subjects (14 males; 23.78 ± 1.16 years)

EMG

Interpersonal scenes

rTMS increased prosocial behaviour

 Fecteau et al. 2008

TMS-induced MEPs

Intensity of 120%

M1

N = 18 healthy subjects (all males; 23.8 ± 3.7 years)

PPI

MEPs

Cortico-spinal excitably modulation was positively correlated with individual PPI scores

 Gallo et al. 2018

rTMS

Frequency = 6 Hz

L. SI hand region

N = 18 healthy subjects (12 males; 25 ± 7 years)

Costly helping paradigm

Correlation between intensity and donation in the Hand condition during active rTMS

 Strang et al. 2014

rTMS

Frequency = 1 Hz

Time = 15 min

L. or R. DLPFC

N = 17 healthy subjects (all males; 23.5 years)

DG /DGp

rTMS reduced giving in both DG and DGp and reduced punishment for low offers

Deep brain stimulation (DBS)

Aggressive behaviour

 Benedetti-Isaac et al. 2015

DBS

Bilateral posterior hypothalamus

N = 5 (all males; range 16–35 years)

Patients with DRE, IAB and below-average IQ

OAS

Follow up after 5 years

Aggressiveness was significantly controlled with evident improvement in the OAS.

Enhancement of the quality of life for patients and their caregivers

  Franzini et al. 2013

DBS

Bilateral posterior hypothalamus

N = 7 (6 males; ages

20–68 years) with below average IQ.

Two patients had refractory generalized multifocal epilepsy.

OAS

Follow-up to 9 years

Reduction in the aggression and disruptive bouts with evident improvement in the OAS

 Giordano et al. 2016

DBS

Subthalamic

Single case

21-year-old patient with IED and MCI

MOAS scores

Follow-up after 22 months

Reduction of aggressive behaviour, with evident improvement in the MOAS.

Enhancement of the quality of life for patients and their caregivers

 Lilleng & Dietrichs, 2008

STN DBS

Bilateral subthalamic

Single case

52-Year patient with PD and previous history of depression and anxiety

MADRS

Patient attempted suicide and developed maniac symptoms after 6 months.

Depressive and manic symptoms were tempered increasing dopaminergic medication

 Papuć et al. 2015

STN DBS

Bilateral subthalamic

Single case

58-year patient with PD

Directed toward family and medical personnel

Aggressive behaviour was absent with stimulation switched off and seemed to be independent of dopaminergic treatment.

 Torres et al. 2013

PMH DBS

Posteromedial hypothalamus

N = 6 (3 males; 28.2 ± 4.8 years)

with medication-resistant erethism and mental retardation

Inventory

Planning general aggressiveness

Follow-up after 46 months

Reduction of aggressive behaviour

in 5 of 6 patients without significant adverse effects.

AQ = Aggression Questionnaire; A-tDCS = anodal tDCS; cTBS = continuous theta burst stimulation: C-tDCS = cathodal tDCS; DBS = deep brain stimulation; DG = dictator game; DGp = dictator game with punishment option; DLPFC = dorsolateral prefrontal cortex; DRE = drug-resistant epilepsy; ECG = echocardiogram; EEG = electroencephalogram; EMG = electromyography; GnGT = go no go task; Hz = Hertz; IAB = intractable aggressive behavior; IED = intermittent explosive disease; IQ = intelligence quotient; IRI = Interpersonal Reactivity Index; L. DLPFC = left DPLFC; L. M1 = left primary motor cortex; L. SI = left primary somatosensory cortex; mA = milliampere; MADRS = Montgomery-Åsberg Depression Rating Scale; MCI = mild cognitive impairment; MEPs = motor evoked potentials; Min = minutes; OAS = Overt Aggression Scale; PD = Parkinson’s disease; PMH DBS = posteromedial hypothalamus DBS; PPI = Psychopatic Personality Inventory; R. DLPFC = right DLPFC; R. M1 = right M1; R. OFC = right orbitofrontal cortex; R. TPJ = right temporoparietal junction; R. VLPFC = right ventrolateral prefrontal cortex; RPQ = Reactive Proactive Aggression Questionnaire; SDS-17 = Social Desirability Scale-17; SOP = social orientation paradigm; STN DBS = subthalamic circuit DBS; TAP = Tayor Aggression Paradigm; TCI = transcallosal inhibition; TG = trust game; TMS = transcranial magnetic stimulation; ToM = theory of mind; VAMS = Visual Analog Mood Scale; VAS = Visual Analogue Scales; UG = ultimatum game

tDCS and Social Behaviour

Fifteen studies that used tDCS to modulate social behaviour were selected (Choy et al. 2018; Coll et al. 2017; Dambacher et al. 2015a; Dambacher et al. 2015b; Gallo et al. 2018; Hortensius et al. 2011; Mai et al. 2016; Maréchal et al. 2017; Nihonsugi et al. 2015; Rêgo et al. 2015; Riva et al. 2017; Ruff et al. 2013; Snowdon and Cathcart 2018; G. Wang et al. 2016; J. Wang et al. 2014). Studies included 799 healthy individuals (375 males), with the largest sample comprising 145 subjects (Maréchal et al. 2017) and the smallest comprising 22 (Nihonsugi et al. 2015).

Nine studies compared both anodal and cathodal stimulations (Coll et al. 2017; Dambacher et al. 2015a; Dambacher et al. 2015b; Hortensius et al. 2011; Mai et al. 2016; Maréchal et al. 2017; Rêgo et al. 2015; Ruff et al. 2013; Snowdon and Cathcart., 2018; Wang et al. 2014), while four used anodal stimulation only (Gallo et al. 2018; Nihonsugi et al. 2015; Riva et al. 2017; Wang et al. 2016). Direct current was delivered at 1 (Ruff et al. 2013), 1.5 (Dambacher et al. 2015b Gallo et al. 2018; Maréchal et al. 2017; Mai et al. 2016; Riva et al. 2017; Snowdon and Cathcart., 2018), or 2 mA (Choy et al. 2018; Coll et al. 2017; Dambacher et al. 2015a; Hortensius et al. 2011; Nihonsugi et al. 2015; Rêgo et al. 2015; Wang et al. 2014; Wang et al. 2016) for maximum 30 min (Maréchal et al. 2017).

Regarding brain target, the majority of studies focused exclusively on the role of the DLPFC (Choy et al. 2018; Dambacher et al. 2015a; Dambacher et al. 2015b; Hortensius et al. 2011; Maréchal et al. 2017; Nihonsugi et al. 2015; Rêgo et al. 2015; Snowdon and Cathcart., 2018; Wang et al. 2014). Other brain targets investigated included the TPJ (Coll et al. 2017; Mai et al. 2016); right ventrolateral prefrontal cortex (rVLPFC) (Riva et al. 2017; Ruff et al. 2013); primary somatosensory cortex (SI) (Gallo et al. 2018); and right orbitofrontal cortex (rOFC) (Wang et al. 2016).

The outcomes were extracted using the ultimatum game (Maréchal et al. 2017; Ruff et al. 2013), dictator game (Maréchal et al. 2017; Ruff et al. 2013), and trust game (Nihonsugi et al. 2015; Wang et al. 2016). Several questionnaires, including the Taylor Aggression Paradigm (TAP) (Dambacher et al. 2015a, 2015b; Hortensius et al. 2011; Riva et al. 2017), self-report (Hortensius et al. 2011; Wang et al. 2014), rating other’s pain (Gallo et al. 2018; Hortensius et al. 2011; Wang et al. 2014), Interpersonal Reactivity Index (IRI) (Wang et al. 2014), Visual Analog Mood Scale (VAMS) (Rêgo et al. 2015), and personality questionnaire (Ruff et al. 2013), were also used. A few studies investigated physiological correlations in moral behaviour by measuring pupil dilatation (Rêgo et al. 2015) or neuropsychological outcomes with RT (Dambacher et al. 2015a; Hortensius et al. 2011).

TMS and Social Behaviour

TMS was used in six studies involving 116 healthy participants (Balconi and Canavesio 2014; Fecteau et al. 2008; Gallo et al. 2018; Hofman and Schutter 2009; Perach-Barzilay et al. 2013; Strang et al. 2014). Repetitive TMS was used in two studies (Gallo et al. 2018; Strang et al. 2014), while only one used continuous theta-burst magnetic stimulation (cTBS) (Perach-Barzilay et al. 2013). In most studies, the frequency delivered was at 1 Hz, with 10 Hz delivered in only one study (Balconi and Canavesio 2014). A large number of studies explored the role of the DPLFC (Balconi and Canavesio 2014; Perach-Barzilay et al. 2013; Strang et al. 2014), whereas the remaining studies investigated the role of the SI (Gallo et al. 2018), primary motor cortex (M1) (Fecteau et al. 2008; Hofman and Schutter 2009), and corpus callosum (Hofman and Schutter 2009).

The outcomes were evaluated using the dictator game (Strang et al. 2014), social orientation task (Perach-Barzilay et al. 2013), and costly helping paradigm (Gallo et al. 2018).

Two studies also used the Aggression Questionnaire (AQ; Hofman and Schutter 2009), Social Orientation Paradigm (SOP; Perach-Barzilay et al. 2013), and Psychopatic Personality Inventory (PPI; Fecteau et al. 2008).

A few studies investigated physiological correlations of moral behaviour by measuring electroencephalogram (EEG) (Gallo et al. 2018), electromyography (EMG) (EMG; Balconi and Canavesio 2014; Hofman and Schutter 2009), motor evoked potentials (MEPs; Fecteau et al. 2008), or neuropsychological outcomes using the selective attention test (Hofman and Schutter 2009).

DBS and Social Behaviour

The role of subcortical structures in social behaviour was investigated in six studies, including 21 patients affected with PD (Lilleeng and Dietrichs 2008; Papuć et al. 2015), epilepsy and intractable aggressive behaviour (IAB) (Benedetti-Isaac et al. 2015; Franzini et al. 2013), medication resistant erethism and mental retardation (Torres et al. 2013), intermittent explosive disease (IED), and mild cognitive impairment (Giordano et al. 2016).

The largest cohort included seven patients with epilepsy and IAB (Franzini et al. 2013), whereas three were single cases (Lilleeng and Dietrichs 2008; Papuć et al. 2015; Giordano et al. 2016). DBS was implanted in specific target locations: the bilateral posterior hypothalamus (Benedetti-Isaac et al. 2015; Franzini et al. 2013), posteromedial hypothalamus (Torres et al. 2013), and bilateral subthalamic nucleus (Giordano et al. 2016; Lilleng & Dietrichs, 2008; Papuć et al. 2015).

Social outcomes were evaluated using the Overt Aggression Scale (OAS; Benedetti-Isaac et al. 2015; Franzini et al. 2013), Modified Overt Aggression Scale (MOAS; Giordano et al. 2016), Montgomery-Åsberg Depression Rating Scale (MADRS; Lilleng & Dietrichs, 2008), and caregivers’ evaluation (Papuć et al. 2015; Torres et al. 2013).

An Overall View

Brain Stimulation Techniques Can Modulate Moral Behaviour

The studies described above provided strong evidence demonstrating how brain stimulation techniques can influence moral responses in both healthy individuals and those with neurological disturbances, making it possible to identify the specific role that cortical and subcortical structures play in morality.

It has been established that brain stimulation techniques enhance cognitive and emotional functions, including attention, memory, and emotional information processing that are involved in morality, leading to modulation of moral decision-making. In fact, when tDCS increased or decreased activity in the DPLFC, the cognitive effort enhanced and contrasted with the non-utilitarian emotional response (Greene et al. 2004). Both cathodal and anodal stimulations led to diminished utilitarian responses in moral tasks (Kuehne et al. 2015; Zheng et al. 2018). On the other hand, if DPLFC activity was interrupted with TMS, an initial emotional response emerged due to the absence of cognitive control; this reduced the punishment for responsible moral violations in personal and impersonal moral dilemmas.

Suppressing the activity in the right or left TPJ disrupted the capacity to use mental states in moral judgment. Application of anodal stimulation to the TPJ decreased moral shame for accidental harm (Sellaro et al. 2015), whereas cathodal stimulation led to an increase (Ye et al. 2015). tDCS could modulate TPJ activity, demonstrating that its suppression provokes the inability to use mental states in moral judgement. The TPJ is commonly associated with ToM and is strongly linked to moral judgment (Young et al. 2010). When its activity was interrupted, the role of beliefs in moral judgements decreased. However, improving cognitive and affective processes could lead to different results in the moral field because behaviours can be improved or made more utilitarian and less desirable according to different situations. TMS stimulation of the rTPJ decreased punishment but increased permissibility for unsuccessful harms.

The mPFC plays a critical role in conflict monitoring and decision-making regarding risk and reward (Bechara and Damasio 2005). Anodal stimulation to the mPFC increased the sense of morality and emotional arousal, leading subjects to rate the severity of moral violations (Yuan et al. 2017).

Regarding the role of subcortical structures, DBS enabled the registration of STN activity. Results demonstrated that this structure was involved in the processes of decision-making regarding moral content, particularly when the subject was required to express a judgment on conflicting moral phrases. Even if the STN is implicated in moral decision-making, it does not have a critical role in morality.

Brain Stimulation Techniques Can Modulate Social Behaviour

Non-invasive brain stimulation enabled the identification of different roles that the frontal lobe plays in aggressive and prosocial behaviors. The use of anodal stimulation of the rDPLFC and rVLPFC reduced proactive aggression in healthy men. Furthermore, social decision-making engaged the SI and rDPLFC, which led to increased prosocial intentions and empathy when modulated by anodal stimulation. Cathodal stimulation, on the other hand, had the reverse effect on both DPLFC and VPLFC.

Stimulating the DLPFC increased prosocial behaviour and decreased aggressiveness. Increased left-to-right, together with reduced right-to-left TCI in M1, was associated with a stronger attention bias for angry faces. Repetitive stimulation on the SI was associated with donation in a prosocial situation.

Another structure closely related to social behaviour, especially aggressiveness, is the hypothalamic region. Its stimulation using DBS induced aggressive behaviour in patients with PD, but improved the behavioral pattern in aggressive patients who benefited from high-frequency stimulation of the posterior hypothalamus. Additionally, patients affected by drug-refractory epileptic syndromes exhibited a decrease in the frequency of epileptic episodes, resulting from DBS, thus reducing drug therapy.

Discussion

Morality is a principle that regulates social relations within society. It underlies disobedience, aggression, psychopathy, and neurological and psychiatric diseases with behavioral disturbances; therefore, the efforts of the scientific community to better understand mechanisms and develop therapies are not surprising.

The present article described studies that used neuromodulation techniques in moral research published in the past decade. Using stimulation techniques to modulate the activity of brain cortices, these studies demonstrated the feasibility of influencing human choices and behaviour related to morality, leading us to assert that it is possible to change individual moral responses.

Non-invasive stimulations techniques, such as tDCS and TMS, have a temporary effect, which are useful in investigating alterations in brain activity in specific cortical areas without negatively affecting the subject undergoing treatment or experimentation. Despite the clinical relevance that emerged, the evidence presented demonstrated that only specific cognitive-affective skills are modulated by modifying certain behaviours in specific tasks (Darby and Pascual-Leone 2017). Neuromodulation can lead to improved empathic abilities by reducing aggressive responses to injustice. At the same time, however, such results may not be desirable in reactive aggression, in which an individual would, instead, want to punish those who acted in an unjust way. This change induced by neurostimulation appears to reduce the autonomy of choice of the individual, leading to a change that may be desirable or undesirable.

Given that morality is a highly complex process influenced by many factors, especially individual differences, future studies should be designed accordingly. Furthermore, another limitation in this field of research is the heterogeneity of the tasks and outcomes used to assess moral behaviour; consequently, comparing results becomes extremely difficult, making it exceedingly difficult to generalize conclusions. Additionally, real-life settings are not always considered in some moral tasks, in which the proposed daily moral situations usually require an abstract evaluation.

Regarding invasive stimulation techniques, such as DBS, modulation occurs in the subcortical region, causing a permanent effect and definitively alters an individual’s response. In the clinical field, drug-resistant aggressive behaviour in difficult patients has been successfully treated using DBS, reducing aggressiveness, and then improving subsequent management in everyday life. In these cases, it is possible to assert that DBS leads to desirable moral and social responses. DBS has also been effectively used to treat motor symptoms. However, a few studies have reported behavioural changes in patients with PD resulting from DBS, such as paedophilia, dependence, and impulsivity (Cyron 2016). These data demonstrate how DBS can also cause undesirable effects, revealing the key role of the subcortical network in morality. Another possible explanation is that DBS for PD indirectly influences moral decision-making by inducing changes in personality and mood, or impulse control disorders (Santens et al. 2018).

Regarding moral research, several variables, such as electrode location, stimulation parameters, pharmacological treatment, and external factors, must be considered to explain their contributions to the development of cognitive and behavioural alterations, eventually resulting in impairment of morality. Furthermore, the number of patients tested in controlled trials is insufficient to draw definitive or generalized conclusions.

Conclusion

In conclusion, we assert that several brain circuits overlapping with other general complex processes support morality, and neuromodulation techniques can be used to influence it. At the same time, modulating the nervous system means altering the human mind, namely treating disturbances, identifying limits of the mind, and promoting and transforming human cognition and behaviours. Due to this manipulative potential to act on the human mind, however, it is not advisable to ignore ethical considerations, which must take into account not only current applications and limitations of these techniques but also their potential. Furthermore, this review raises awareness of the importance of including greater methodological control and homogeneity in moral research.

The use of neurostimulation techniques, both invasive and non-invasive, can provide meaningful insights to delineate the boundaries of morality, which has important clinical and ethical implications. Moreover, understanding the dysfunctional brain structures underlying abnormal moral behaviour can lead to targeted treatments. For example, apart from treating aggression, these techniques may be used for other forms of pathological antisocial behaviour or violence (i.e. sexual assault and pedophilia) when education and/or rehabilitation programs or other treatments fail. Nevertheless, shaping individual morality raises urgent bioethical issues that may be used to inform guideline development and their use while still respecting the human mind.

Notes

Funding Information

The study was partly supported by POR-FESR 2014-2020 (ID247367), by donation in memory of Aldo Ravelli, by the Italian Ministry of Health grant (RC-2017 and GR-2011- 02352807), and Roche Research grant 2017.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that there is no conflict of interest.

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Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • C. Di Nuzzo
    • 1
  • R. Ferrucci
    • 1
    • 2
    • 3
  • E. Gianoli
    • 2
  • M. Reitano
    • 2
  • D. Tedino
    • 2
  • F. Ruggiero
    • 2
  • Alberto Priori
    • 1
    • 3
    • 4
  1. 1.“Aldo Ravelli” Center for Neurotechnology and Experimental Brain Therapeutics, Department of Health SciencesUniversity of Milan Medical SchoolMilanItaly
  2. 2.Neurophysiology UnitIRCCS Ca’ Granda FoundationMilanItaly
  3. 3.UOC Neurologia IASST Santi Paolo e CarloMilanItaly
  4. 4.Università degli Studi di MilanoPolo Ospedaliero San PaoloMilanItaly

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