dissociation of neural circuitry for conscious and unconscious processing of personally-significant...
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Dissociation of neural circuitry for conscious and
unconscious processing of personally-significant faces.
María A. Bobes
Center for Neuroscience, Cuba
Many different types of information derived from faces:race, sex, emotional-expressions, age, identity
Bruce and Young, 1986Bruce and Young, 1986
Assoc. prospag..
Faces tell us who is who (e.g. good and bad or friends and enemies)
Face identity hasemotional content !
Emotion-from-identity
Face identity also offers socio-emotional information
Tranel, Damasio & Damasio, JOCN, 1995, 7:432
Double dissociation between identity recognition and emotional processing of face identity
Prosopagnosia
Medial orbitofrontal damage
Capgras
Modified Bruce & Young model to accommodate double dissociations
(Ellis et al)
Assoc. prospag..
Me
dia
l O
rbit
ofr
on
tal
Limitations of purely cognitive models
• Theories are under-constrained• They have poor contact with neurophysiological data• The posited pathways are not informed by
neuroanatomy• Early attempts to make the connections were heavily
criticized because they were based on incomplete data & were difficult to test (recommendation then to ignore anatomy)
FFAOFA
Hasson, Harel, Levy, & Malach, Neuron, 2003
= >
STS
Posterior Superior Temporal Sulcus(pSTS)
Core Area of the Face Processing System
(Haxby et el, 2000) Extended system for familiar faces?
What is unclear• Are there additional areas involved?
• What are the connections of these areas
• What is the functional contribution of each area
• How brain damage disrupt this circuitry
fMRI correlation
DTI. Tractography
Lesions causal inferences
fMRI Event related design
St Duration: 1s
SOA: variable between 4 and 6 s
3 sessions. Each session:•15 acquaintance faces,•15 learned faces, 30 unknown faces•45 houses.
Target (40 %)Standard (60 %)
1.5 Tesla
TR= 2
16 slices
Statistical Analysis: SPM5+ in-house scripts
fMRI analysis
• ROI localization of areas responding to faces
(faces > houses)
• Finite impulse response estimations for each stimuli condition in each ROI
• Permutation t test over the FIR. (Time characterization)
•FFA (L/R)
•OFA (L/R)
•AIT (L/R)
•Post. Cing.(L/R)
•Medial Orb.fr. (L/R)
•Insula
•Dorsolateral Frontal (L)
•Inferoparietal (L)
Activation for faces >houses
Regions of Interest ROIStructural face processing
Emotional processing
Attention
working memory
Semantic processing
FFA d
OFA d
FFA d
OFA dOFA dAcq vs 0
Unfam vs 0
Acq vs Unfam
OFA d
FFA d
OFA d
Fam vs 0
Desc vs 0
Fam vs Desc
FFA d
OFM d
Unknown faces > Houses
FFA
mOFC
OFA
STS
acquaintance > unknown faces
PC
Group analysis
AIT
To Summarize
• BOLD responses to faces of acquaintances were of larger amplitude and longer duration than to faces of strangers in all ROI, especially in the right hemisphere.
• This differential responsiveness increases as one moves from extrastriate areas to PC to lateral and medial prefrontal cortex.
• There are striking differences in BOLD time-courses in different ROI and interestingly for different conditions in the same ROI (excludes local vascular factors or regional differences in the coupling of neural activity) .
• This suggests that different BOLD time-courses could reflect distinct neural patterns of activity.
Basser et al., 1999Mori et al., 1999
Attempt to ‘connect’ voxels
on basis of directional
similarity of coincident
eigenvectors
Catani, Brain, 2005
Classical DTI tractography: tracts defined by ROIs in white matter:-Good “in vivo” reproduction of tracts found by “post-mortem” dissection -Unfortunately relationship with functional areas (e.g. OFA, FFA) not precise-Gets “lost” or stops in GM
SLF
Probabilistic DTI-tractography seeded with fMRI data
• A Monte Carlo simulation (n=200) is run at each seed voxel and at every step of the path construction a direction randomly drawn from a distribution).
• Validity measure calculated for all paths.• Seed ROIs can be placed in GM• Paths can penetrate GM• Here we used clusters of fMRI activation specific to
faces as seeds for the tractography• Average of validity measures for all paths coming
from the same ROI and reaching any voxel was used as an index of connectivity between the ROI and the voxel.
Seed ROI defined by fMRI
OFA
FFA
Voxelwise, T-test, n=30, of connectivity index, FDR=0.05
Additive color map
(pSTS)mOrF
Modified model of the Face Processing System
SLF?
CP
lOrF?
IFL
IFOF
Summary of new findings from normal subjects
1. Core areas have larger BOLD responses to familiar faces but ERPs elicited in these areas are not affected by familiarity: Suggests feedback from later activated areas.
2. The extended face processing system for familiar faces includes the posterior cingulate and medial orbitofrontal cortex.
3. DTI-tractography seeded by fMRI data suggest a massively parallel face processing system, less sequential than posited in original models.
4. V4, OFA and FFA all feed in parallel into the Inferior longitudinal fasciculus and the Inferior Fronto-occipital fasciculus.
• Are all these areas necessary ?
• Need for lesion studies
• Brain injury / bilateral subdural hematomas (trauma).
• Neuropsychology: normal except face recognition• Basic face processing relatively intact (Benton, Bruyer and Warrington test batteries).•Dense associative prosopagnosia (zero recognition of famous people or acquaintances), cannot learn new faces
Severe bilateral damage to ventral occipito-temporal cortex
Case F.E. . (69 year old male)
Person identification relies on voice, gait, clothing
LR
nsp<0.028
8/14 (57 %)
12/14
(86 %)
10/14 (71 %)
Which face is more trustworthy ?
Which face is nicer ?
Which face is more trustworthy ?
Which face is nicer ?
Forced choice face selectionForced choice face selectionForced choice face selectionForced choice face selection
Bobes et al, COGNITIVE NEUROPSYCHOLOGY, 2004, 21
Unknown Acquaintance (family)
p<0.008
Is more familiar ?
Implicit Implicit Overt
Skin Conductance Response (SCR)
F.E. presented larger skin conductance responses to familiar than to unfamiliar faces.
Bobes et al, COGNITIVE NEUROPSYCHOLOGY, 2004
Acquaintances unfamiliar
Voxel-wise Hotelling T2 test, using vector of intravoxel GM, WM and SCF concentration, contrasting FE vs. 237 control
FDR threshold q<0.01
RL
% Damaged voxels in cortical regions defined by AAL atlas
Patient FE. ER-fMRI Acquaintances, Unfamiliar faces, Houses
• ROI (faces > houses)
• Finite impulse response estimations for each stimuli condition in each ROI
• Statistical comparison of the patient´s response to that of the sample of normal controls (Crawford et al, 2006)
OFA OFAFFA
FFA
OFA
OFA
Left Right
x=44 y=-78z=-14
1
PC CA mOFC
mOFCmOFC
x=0 y=34z=10
Left Right
FE:Left mOFC
Controls> FE
Voxel-based tractography (OFA seeds) deficit analysis: voxel-wise ttest, FE vs 30 controls, FDR q=0.01
Deficits in the territory of the right and left ILF
Method limited by large variance of values in some voxels control subjects
>70 % controls
Only F.E.
Overlap F.E. & controls
Combined DTI/fMRI: Probabilistic Tracts with group OFA seeds for controls and individual OFA seeds for F.E.
IFOF Apparently preserved (more on the on the left )Lower branches of IFL leading to AIT cortex and MTL are more affected
(pSTS)mOrF
SLF?
CP
lOrF?
IFL
IFOF
Residual face processing system in FE
X
X
X
X X
(pSTS)mOrF
SLF?
CP
lOrF?
IFOF
Residual face processing system in FE
XX X
(pSTS)mOrF
ERPs ?
Time course of activation
SLF?
CP
lOrF?
IFL
IFOF
Newly-Learned FacesFaces of unknown persons artificially learned in the lab
Unique Identity
Memory engrams
Unique identity based on face structural information
Affective significance
Semantic Information
Similar visually familiarity
Different emotional value
Acquaintance faces Faces of relatives and very close friends
ERP paradigmERP paradigm
120 channels
0.05-30 Hz
10000Onset latency
St Duration: 1sSt Duration: 1s
SOA: 2 sSOA: 2 s
Two blocks : Random presentation of 16 target known faces and 75 standard unknown faces .
In one block known faces were acquaintances and in the other, newly-learned faces.
Task: To discriminate between familiar (acquaintance or learned) and unfamiliar faces by pressing a key
Subjects: 15 normal adults (7 F and 8 M), ages between 21 and 32
P300P300N170 N170
An iAn index of early ndex of early structural analysis of structural analysis of faces faces
An index ofAn index of the availability of relevant the availability of relevant memories for people.memories for people.
P3b. (parieto-central) •P3a . (frontally distributed)
Learned Faces (LF) in normal subjects.
Target LFStandard UF
•No difference in N170 (structural processing)
•P3b. Conscious processing of familiarity
Acquaintance faces (AF) in normal subjects
Target AFStandard UF
•No difference in N170 (structural processing)
•P3b. Conscious processing of familiarity
•Additional P3a. Emotional processing of identity
A
Newly-learned
500-580ms
B Acquaitances460-570 ms
CAcquaitances300-380 ms
•Temp-parietal• Polo temp• Frontal inf.• Frontal dorsal
• Temp-parietal• Polo temp• Frontal inf.• Frontal dorsal
• OFM• Amigdalas• Polo temporal, • Insula
A) P3b. Newly-learned
B) P3b. Acquaitances
C) P3a. Acquaitances
Current source stimation BMA mode.l Average Brain MNI .
Summarizing• The effect of familiarity appears after 300 ms
once the structural processing (indexed by N170 has been completed)
• Learned faces evoke only the parietal positivity
• Acquaintance faces evoke two different components: a large positivity widely distributed and maximal at parietal sites, and an earlier positivity restricted to frontal sites, which is probably generated at OFM and amygdalas.
ERPs. P300
0 % hits
Bobes et al, COGNITIVE NEUROPSYCHOLOGY, 2004, 21
• P3a adicional: Procesamiento emocional de la identidad• P3a adicional: Procesamiento emocional de la identidad
Target AFStandard UF
•No difference in N170 (structural processing)
•An early and fronto-central P3 (P3a). Emotional processing of identity
•No P3b. (Conscious processing of familiarity)
•Metodo. BMA
•Volumen. RMN sujeto FE
OFM, amigdalas, polo temporal
FE. Estimación de fuentes intracraniales. P3a o P3b?
Las fuentes generadoras de P300 en FE coinciden con las de P3a en normales.
ERP• The processing of emotion from identity does
not necessarily occur before identity have been consciously detected.
• Covert recognition of familiar faces in prosopagnosia evoked the P3a component generated in emotional system
Conclusions1. FFA is not necessary for covert recognition of
familiar faces which could be enabled by OFA. Previous work (Rossion et al) has show that FFA activation is not sufficient for familiar face recognition.
2. OFA and med OrbitoFrontal cortex serve as hubs for covert (unconscious) recognition
3. Prosopagnosia not only due to lesion of “core face areas” but also a disconnection syndrome (IFL disruption) that blocks conscious recognition
Conclusions4. Unconscious recognition could be mediated by
the Inferior Occipito-Frontal Fasciculus or by more indirect pathways via the SLF or the Cingulate fasciculus.
5. Multimodal neuroimaging of neuropsychological cases is a powerful constraint for models of cognitive processing.
6. More effort is needed to develop of statistical techniques for multi-modal image comparison of singles cases to normal controls.
Research team Habana, Cuba• Maria A. Bobes• Lorna Garcia• Yasser Iturria• Ileana Quiñones• Yusniel Santos• Lester Melie• Pedro Valdes Hernandez • and many others from CNEURO
Medellin, Colombia• Francisco Lopera• Jose Ascencio