social neuroscience: insights from neuropsychology · 2015-09-13 · social neuroscience: insights...

Social Neuroscience: Insights fromneuropsychology

Dana SamsonUniversité catholique de Louvain

Theoryof Mind: Insights fromcognitiveneuropsychology

Dana SamsonUniversité catholique de Louvain

Two topics…

� Part 1: What can cognitive neuropsychologytell us about ToM?

� Part 2: Implicit and Explicit ToM?

Part 1: What can neuropsychology tell us?� Functional Necessity

� Is language necessary for ToM?� Are executive functions necessary for ToM?

� Neural Necessity� Which parts of the ToM brain network are

essential/necessary?

� Cognitive and Neural Architecture� What are the ToM building blocks?

Functional necessity

Functional Necessity

� Children usually pass FB tests from the ageof 4 (Wimmer & Perner, 1983), i.e. at a time when they acquire more sophisticated language and executive function abilities

� Non-humans do not pass FB tests (Call & Tomasello, 2008)

� Are language and executive function necessary for belief reasoning?

Necessaryfor what?

Necessaryfor what?

� (1) To deal with the incidental processingdemands?� Belief problems are complex, we need

language and executive function to processthe incidental task demands (understandingthe words describing the situation, remembering the events etc.)

� Not the most interesting relation…but needs to be taken into account to be ruled out as sole link..

Necessaryfor what?

� (2) To develop a ToM?(Scaffolding hypothesis)� LANGUAGE:

� verbal interactions

� could allow children to learn about mental states, for example via the description that parents give about their mental states (e.g., Sabbagh & Callanan, 1998)

� the mastering of complex grammar � could give them the means to discover the properties of

propositional mental states such as beliefs (e.g., de Villiers & Pyers, 2002)

Necessaryfor what?

� (2) To develop a ToM? (Scaffolding hypothesis)� EXECUTIVE FUNCTION:

� being able to disengage from salient information (i.e., inhibitory control), could help children

� understand that other people may have different mental states to theirs,

� that beliefs do not necessarily match the outside world (e.g., Carlson & Moses, 2001; Russell, 1996)

Necessaryfor what?

� (3) For reasoning per se?� LANGUAGE:

� the use of complex grammar could be necessary to represent beliefs (de Villiers, & Pyers, 2002)

Necessaryfor what?

� (3) For reasoning per se?� EXECUTIVE FUNCTION:

� working memory could be necessary to hold in mind multiple perspectives (Gordon & Olson, 1998)

� inhibitory control could be necessary for the mental flexibility needed when reasoning about other people’s mental states (Russell, 1996).

Necessaryfor what?

� Developmental studies have found correlations between language and/or executive function abilities, and performance on ToM tasks (Astington & Jenkins, 1999;Carlson, Moses, & Breton, 2002; de Villiers, & Pyers, 2002; Ruffman, Slade, Rowlandson, Rumsey, & Garnham, 2003; Sabbagh, Moses, &

Shiverick, 2006).

� BUT:� For scaffolding or reasoning per se?

� � need to investigate adults� Correlation and causality…

� � need for a more direct causal test

Causal test

� What happens if language or executive function is unavailable in an adult?� Temporary unavailability in healthy subjects:

dual task paradigm� More enduring unavailability in patients with

acquired brain damage: patients withlanguage or executive function deficits

Necessaryfor what?

� For reasoning per se?� LANGUAGE:

� the use of complex grammar could be necessary to represent beliefs (de Villiers, & Pyers, 2002)

The functional necessityof language

� Two published studies tested the necessity of language for ToM in healthy adults with the dual task paradigm (Newton & de Villiers, 2007; Forgeot

d’Arc & Ramus, 2011).

� Language shadowing task � no specific language ability was targeted

� Conflicting results

� What about patients with grammatical processing deficits?

� Hypothesis: grammar plays a fundamental role� Sally thinks that the marble is in the basket

�Embedded complement clauses (de Villiers & Pyers, 2002)

� He pushes the man that shouted at the woman� Embedded relative clauses, i.e. more general role of embedded grammatical structures (Smith, Apperly, & White, 2003)

� Evidence for a link comes mainly from developmental psychology

Languageand Belief reasoning

� Can agrammatic patients infer and represent beliefs?(preliminary indication: yes, Varley & Siegal, 2000;

Varley et al., 2001)

The functional necessityof language

PH (male, age=33, stroke)Left fronto-temporal lesions

Severe anomiaDeep dyslexia and deep dysgraphia

Relatively spared lexico-semantic processing

(Apperly et al., 2006)

Palpa test 55 – sentence/picture matching

Oral: 67% correct overall (50% correct on reversible sentences)

Written: 70% correct overall (55% correct on reversible sentences)

“The dog is followed by the man ”PH’s interpretation: “the dog is following the man”

� extracts meaning by following the order of the words rather than taking into account grammar

Grammatical processing


New grammatical test specifically testing embedded relative clauses

The woman shook the man that drank the water

(+ control sentences)


The woman shook the man that drank the water.


New grammatical test specifically testing embedded relative clauses

The woman shook the man that drank the water Embedded relative clause sentence


7/14

Nonverbal ToM tasks


Video false belief task – indirect/low self salience

Video false belief task – direct/high self salience

2nd order nonverbal false belief task (woman 1 wrongly thinks that woman 2 wrongly thinks the object is in the left box)

12/12

11/12

12/12


Verbal false belief inference task 10/12

Jeremy is eating out at a restaurant. Inside therestaurant, Jeremy hangs his coat on the standby the door, and leaves his bag underneath. Thewaitress shows Jeremy to his table and tells himabout today’s special dishes. When she comesback, the waitress notices Jeremy’s bag beneaththe coat stand by the door. She decides that it isunsafe for the bag to stay there, as it would beeasy for someone to steal. Leaving the coat onthe coat stand, she locks the bag in the storecupboard.Where does Jeremy think the bag is? On the chair or in the store cupboard?

Verbal ToM tasks


Embedded complement clauses (no belief inference)

he thinks there is a red ball in the boxbut

really there is a yellow ball in the box

Verbal ToM tasks


he thinks there is a red ball in the boxbut

really there is a yellow ball in the box

Verbal ToM tasks

3/12Embedded complement clauses (no belief inference)

Functional necessityof language

� Can agrammatic patients infer and represent beliefs?� YES!

� Grammar is not necessary to infer and reason about beliefs as such

� But grammar plays an important role to understand verbally presented contexts (input to belief reasoning )

Necessaryfor what?

� For reasoning per se?� EXECUTIVE FUNCTION:

Evidence frompatients

� Co-occurrence of deficits in many studies

� But not for all types of ToM tasks and not all type of EF tasks (e.g., Bibby, & McDonald, 2005; Channon & Crawford, 2000; Gregory et al,. 2002; Happé, Malhi, & Checkley, 2001; McDonald & Pearce, 1996; Rowe, Bullock, Polkey, & Morris, 2001; Shamay-tsoory, Tomer, Berger, & Aharon-peretz, 2003).

Evidence frompatients

� There have been also reports of dissociations, with impaired performance on ToM tasks without deficits on standard executive function tasks (e.g., Lough, Gregory, & Hodges, 2001; Lough & Hodges, 2002) or vice versa (Blair & Cipolotti, 2000; Bird, Castelli, Malik, Frith, & Husain, 2004).

Necessaryfor what?



� inhibitory control could be necessary for resisting interference from one’s own perspective/knowledge of reality (Russell, 1996).

WorkingMemoryand ToM

� Dual task in healthy adults:� Concurrent working memory task has

detrimental effects on 2nd order more than 1st order false belief reasoning (McKinnon and Moscovitch, 2007).

� Brain damaged patients:� Performance on a working memory task

predicted performance on a 2nd order but not 1st order false belief task (Bibby and McDonald, 2005).

Inhibition and ToM

� Dual task in healthy adults and neuropsychological studies: � quite messy results….� no control for the critical “inhibitory” aspect of

ToM

Inhibition and ToM

SeriousAshamedAlarmed

Bewildred

Inhibition and ToM

Tony puts some Coke in the cabinet. Then he leaves the room. Maria comes along and moves the Coke from the cabinet into the refrigerator to chill. Later, Tony comes back in.

Where does Tony think the Coke is?

Necessaryfor what?



� inhibitory control could be necessary for resisting interference from one’s own perspective/knowledge of reality (Russell, 1996).

� Need to show specific relation between inhibition and ToM tasks in which there is a need to inhibit one’s own perspective

High Self-perspective Inhibition demands

Self-perspective inhibition


Low Self-perspective Inhibition demands


WBA, male, age=61, strokePW, male, age=75, stroke

Cognitive control problem: perseveration of thoughts

Voxel-based morphometry analysisresults

WBA PW

0

2

4

6

8

10

12

Num

ber c

orre

ct

Samson et al., 2005, Brain





� Do all frontal patients with executive function(inhibition) deficits have difficulties inhibitingtheir own perspective?

� Do patients with a deficit in self-perspective inhibition have difficulties inhibiting any type of information?

WBA, male, age=61, strokePW, male, age=75, stroke

Cognitive control problem: perseveration of thoughts

GA, male, age=52, herpes encephalitisSP, male, age=53, herpes encephalitis

Cognitive control problem: distractibility

WBA & PW versus SP & GALesions common to WBA, PW, SP & GA

What colour would Simon want the next card to be?

Participant

Desirereasoningtask

Participant

Simon

?

What does Simon want the next card to be?� Not red, bue (disengagement from self-perspective)

0

2

4

6

8

10

12

WBA PW GA SP

Num

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orre

ct

Thoughtperseveration

(problems inhibitinginternal information)

Distractibility(problems inhibitingexternal information)

Houthuys et al., in prep

What colour would Simon want the next card to be? (win/approach)

Participant

Simon

?

Participant

Simon

?

What do you want the next card to be?� Not red, bue (disengagement from salient card)

0

2

4

6

8

10

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WBA PW GA SP

Num

ber c

orre

ct

Thoughtperseveration

(problems inhibitinginternal information)

Distractibility(problems inhibitingexternal information)

What colour would Simon want the next card to be? (win/approach)

What colour would You want the next card to be? (loose/avoidance)

Houthuys et al., in prep


� Do all frontal patients with executive function(inhibition) deficits have difficulties inhibitingtheir own perspective?

� Do patients with a deficit in self-perspective inhibition have difficulties inhibiting any type of information?

� Self-perspective inhibition and inhibition of internally-generated information?

Functional necessity: conclusions (I)

� Enduring role of domain-general cognitive processes for ToM? � Working memory may be necessary to hold

multiple perspectives� Inhibition seems necessary to resist

interference from one’s own perspective BUT:� Grammar does not appear to be necessary to

hold in mind propositional mental states such as beliefs.

Functionnecessity: conclusions (II)

� Language or executive function or ToMshould not be considered as unitary functions�careful task analyses are necessary to identify what the demands of a given task are likely to be � need and scope for within-task manipulations

Neural Necessity

� Which parts of the classic ToM are essential?

Lateral view

TPJ

TP

Medial view

MPF

C

PCC

The medial prefrontal cortex

� Frontal variant of fronto-temporal dementia (fvFTD)

� Brain atrophy most marked in the medial prefrontal cortex (Williams, Nestor, & Hodges, 2005)

� Severe problems in social conduct


Gregory et al. (2002)


� Problem: lesions can often extend into the dorsolateral prefrontal cortex as well as the temporal cortex

� not straightforward to link the impairment solely to the ventromedial prefrontal cortex


� 62 year old woman� Stroke� Dysexecutive syndrome

Bird et al., 2004


� No clear evidence that the region is necessary for ToM tasks

� What is then the role of the medial prefrontal cortex and why do we find it so often activated when healthy adults reason about mental states?


� Hypothesis 1:

� the medial prefrontal cortex could be activated because when adults are presented with ToM problems, these often also trigger reasoning about social characteristics of the protagonists other than their mental states such as their personality traits (e.g., Van Overwalle, 2009)


� Hypothesis 2:

� because participants not only infer the mental state but also think about the behavioural or emotional consequences of the protagonists’mental states (e.g., Aichhorn, Perner, Kronbichler, Staffen, & Ladurner, 2006)

� Hypothesis 3:

� Medial prefrontal cortex would be recruited when the situation is ambiguous (e.g. Jenkins & Mitchell, 2010)

� Independent evidence that patients with medial prefrontal cortex deficits have only problems when they have to deal with “ill-structured” situations (Burgess, Gilbert, & Dumontheil, 2007)


� Both the left and the right temporo-parietal junction have been associated with ToM (Saxe

& Powell, 2006). � RTPJ: more specific to beliefs

� LTPJ: also activated when adults reason about non-social representation of the world such as false signs (Aichhorn et al., 2009).

The temporo-parietal junction

� So far, no documented report of the effects of a lesion to the RTPJ on ToM performance.

� However, lesions to the LTPJ leads to an impaired performance on a false belief reasoning task (Samson, et al., 2004).



PF, female, age=55, stroke

DB, male, age=68, stroke

RH, male, age=70, stroke

Samson et al., 2004


Where is the green object?


Samson et al., 2004


Where is the green object?


Apperly et al., 2007


� Thus, LTPJ is necessary for belief reasoning

� And for reasoning about other forms of representations

The temporal poles

� These brain regions are usually thought to be involved in semantic processing, particularly for integrating various sources of knowledge about objects or the world (Patterson, Nestor & Rogers, 2007).

� This had led to the hypothesis that the temporal poles would be involved in the retrieval of social conceptual knowledge (Frith & Frith, 2003; Ross & Olson, 2010).

The temporal poles

� Temporal variant of fronto-temporal dementia (tvFTD)� severe atrophy of the temporal poles� major changes in the patients’ social conduct � the amount of problems noticed by family and

friends in terms of perspective taking and empathic concern (as measured by the Interpersonal Reactivity Index (IRI), Davis, 1983) has been found to positively correlate with the amount of atrophy in the temporal poles (Rankin

et al., 2006).

The temporal poles(amygdala)

� Acquired damage to the amygdala which often occurs alongside damage to the temporal poles � Some authors found ToM impairments (Stone,

Baron-Cohen, Calder, Keane, & Young, 2003) while others found only a slight impairment especially for lesions acquired in childhood (Shaw et al., 2004).

The temporal poles(amygdala)

Stone et al., 2003

Faux Pas Reading the Mind in the eyes

Shaw et al., 2004

The temporal poles

CM, degenerative temporal pole atrophy, especially on the left (semantic dementia)60 years old manPicture Naming: 21/80, 26%, correct (mean controls: 74.2/80)

Michel et al., in prep

The temporal poles


CM, degenerative temporal pole atrophy, especially on the left side (semantic dementia)60 years old man

The temporal poles


Social semantics: synonym judgment tasks

Disdainful

Arrogant Indecent

Abondant

Diffuse Opulent

Personality traitsMental states Non-social

The temporal poles


Social semantics: synonym judgment tasks

Disdainful

Arrogant Indecent

Abondant

Diffuse Opulent

CM= 24/48 (50%) CM= 15/48 (31%)

Average performance of matched controls: >90%Below control performance, p<0.01

The temporal poles


Social semantics: discrimination of mental state expressions

Je suggère que l’objet est dans cette boîte

Je confirme que l’objet est dans cette boîte

The temporal poles


Social semantics: discrimination of mental state expressions

CM= 55/72 (76%)

Average performance of matched controls: >90%Below control performance, p<0.01

The temporal poles


Social semantics:

The patient is impaired compared to controlsBUTNo more so for mental than non-mental states

The temporal poles

Theory of Mind: Intention reasoning (Sarfati et al., 2003)


The temporal poles

Theory of Mind: Intention reasoning


02468

10121416182022242628

Intention items Control items

Num

ber

corr

ect

Within control rangep=0.18

The temporal poles

Theory of Mind: source of knowledge reasoning


stapler

post-it

We look for the stapler

Qui sait ?Who knows where it is?

02468

1012141618202224

2 modalities 4 modalities

Num

ber

corr

ect

The temporal poles

Theory of Mind: source of knowledge reasoning

Seeing vs. weighting


Seeing vs. touchingvs. smelling vs.

tasting

Controls 22-24/24

The temporal poles

Theory of Mind: Belief reasoning




The temporal poles

Theory of Mind: Belief reasoning


Low Inhibition High Inhibition

0123456789

101112

Num

ber c

orrect

False Belief

Memory Control

Controls 11-12/12

The temporal poles

Theory of Mind:

The patient performs very close to or within normal rangefor intention reasoningfor source of knowledge inferencefor false belief reasoning

The temporal poles

� These findings suggest that the left TP � is not specifically dedicated to the storage of

social concepts � is not necessary for inferring mental states.

� Right TP?

The temporal poles

� No clear evidence for the necessity of the temporal poles for ToM

� Perhaps ToM problems tested are too simple, temporal poles may only be recruited when more complex social knowledge is recruited

Other areas?

� Posterior cingulate/precuneus� self-reflective thoughts (Johnson et al., 2002),

� autobiographical memory (Summerfield, Hassabis, & Maguire, 2009)

� egocentric spatial representations (Weniger, Ruhleder, Wolf, Lange, & Irle, 2009).

�However, there is so far no direct evidence that these areas are necessary to solve ToMproblems.

Neural necessity: conclusions

� Except for TPJ: results are mixed

� Current tasks may not be fine grainedenough to show subtle deficits

� Perhaps different parts within the network can compensate for one another

Cognitive and Neural Architecture


Emotion, desire, intention, belief

TEMPORARY AND CONSCIOUSREPRESENTATION OF SOMEONE’S

MENTAL STATE

Self-perspectiveinhibition

Role of the right lateral prefrontal cortex

WBA PW

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Num

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Samson et al., 2005, Brain







MENTAL STATE

Self-perspectiveinhibition Social

knowledge andtheory of mind

LONG-TERMKNOWLEDGE

Top-down

Top-down

Role of the temporo-parietal junction?

Self-perspective inhibition demands do not predict errors in TPJ patients

PF DB RH

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10

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Num

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orre

ct



WBA PW

0

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Right frontal lesion patients Temporo-parietal lesion patients

TPJ patients do not necessarily makeegocentric errors

Right frontallesion patients

Temporo-parietallesion patients

0

10

20

30

40

50

60

70

80

90

100

WBA PF

Per

cent

age

Other errors

Egocentric errors

Distribution of errors

Samson et al., 2007

Monitoring the environment




MENTAL STATE

Self-perspectiveinhibition Social

knowledge andtheory of mind

LONG-TERMKNOWLEDGE

Top-down

Top-down

Two main conclusions

1. Distinction between theory of mind use and theory of mind knowledge� The patients reported here could solve theory

of mind tasks in some situations but not others� � their theory of mind knowledge seemed

intact� � their difficulties relate to the “use” of that

knowledge

� The question is more complex than “having” or “not having” a ToM

Two main conclusions

1. Distinction between theory of mind use and theory of mind knowledge

2. Distinct theory of mind use processes� Qualitative differences in deficits indicating

that the use of one’s ToM does not rely on a unitary process

� Self-perspective inhibition� Orientating attention to the relevant elements in

the environment� Detecting relevant cues� Inhibition of salient distractors in the

environment� Integration of various information/cues

Methodological implications

1. Need for new tasks, with within/between-task manipulations to isolate processing demands



2. Heterogeneity of deficits: caution about group averages

PF DB RH

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WBA PW

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High Inhibition

Low Inhibition



2. Heterogeneity of deficits: caution about group averages

Group

0

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6070

80

90100

Num

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High Inhibition

Low Inhibition

Part 2: Implicit and Explicit ToM?

Current puzzle in the literature…

Is belief reasoningdifficult?


More than 30 years of research: Only from the age of 4, children pass false belief tasks


More than 30 years of research: from the age of 4, children pass false belief tasks

Recent findings:Infants are sensitive to another person’s false beliefFrom 24 months (Onishi & Baillargeon, 2005)

From 7 months (Kovacs et al., 2010)

Is belief reasoningautomatic?

Main taskMain taskMain taskMain task: follow where the object is

Secondary taskSecondary taskSecondary taskSecondary task: respond yes/no to the question:BELIEF QUESTION : She thinks it is in the left/right boxREALITY QUESTION: It is true that it is in the left/right box

Two experimental conditionsTwo experimental conditionsTwo experimental conditionsTwo experimental conditions:(1) No explicit instruction to track beliefs(2) Explicit instructions to track beliefs

Question

Apperly et al.,2006



Apperly et al.,2006


Kovacs et al.,2010

Question


Low level processes?

Consistent perspectives

Self sees 1Other sees 1


How many discs does the other see?

Inconsistent perspectives

Samson et al.,2010



How many discs do you see?

Samson et al., 2010

Consistent perspectives Inconsistent perspectives

+

HE

2

Samson et al.,2010

+

YOU

2

Samson et al.,2010

Egocentric biases

Consistent Perspectives

Inconsistantes Perspectives

Samson et al.,2010

Altercentric biases

Consistent Perspectives

Inconsistent Perspectives

Samson et al.,2010

� We can’t prevent ourselves from computingwhat the other person sees even when it has detrimental effects on our performance

� In some conditions, we are quicker at judgingthe other person’s perspective than our ownperspective

Altercentric biases

+

YOU

2

Bip Bip

�

1x

Bip

�

2x

Secondary task

Qureshi et al., 2010

Dual task paradigm

VOLET 1: processus de bas niveau

Prise de perspective visuelle

Qureshi et al., 2010

� We can’t prevent ourselves from computingwhat the other person sees even when it has detrimental effects on our performance

� In some conditions, we are quicker at judgingthe other person’s perspective than our ownperspective

� We compute what other people seeeffortlessly

Altercentric biases

Top-down

Top-downBottom-up

Samson, 2009

Desire representation

Belief representation

Self/Otherdistinction

TEMPORARYREPRESENTATION

Social knowledge andtheory of mind

LONG-TERMKNOWLEDGE

Top-down

Motor state

Emotional state

Visual experience

Bottom-up

Top-down

Bottom-up

Bottom-up

Top-downBottom-up

Desire representation

Belief representation

Self/Otherdistinction

TEMPORARYREPRESENTATION

Social knowledge andtheory of mind

LONG-TERMKNOWLEDGE

Samson, 2009

Thanks to…

� All the patients� Collaborateurs

� Ian Apperly (University of Birmingham)� Glyn Humphreys (University of Oxford)

� Past lab members� Sarah Houthuys� Adam Qureshi � Sarah Boldey Scott � Eleanor Limback� Sanni Quadflieg

� Funding bodies� MRC, Lerhulme Trust, Stroke Association, FNRS, FSR

www.springlab.org

� Current lab members� Henryk Bukowski� François Maurage� Gaëlle Meert� Caroline Michel � Richard Ramsey� Andrew Surtess

social neuroscience: insights from neuropsychology · 2015-09-13 · social neuroscience: insights...

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