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Recollection and the Brain
Reading list
• Yonelinas, A. (2002) The nature of Recollection and Familiarity: A
review of 30 Years of Research. Journal of memory and language, 46,
441-517
• Eichenbaum H. Yonelinas AP, Ranganath C. (2007) The medial
Temporal lobe and recognition memory. Annu Reve Neurosci, 30, 12352
• Souchay, C. and Moulin, CJA. (in press) Memory and Consciousness
in Alzheimer’s disease. Current Alzheimer Research.
Reading list
•
Wheeler, M, Stuss, D. & Tulving, E. (1997) Toward a Theory of Episodic Memory: The
Frontal Lobes and Autonoetic Consciousness. Psychological Bulletin, 121, 331-354
•
Tulving, E. (2002) Episodic memory: From Mind to Brain. Annu. Rev.Psychol, 53, 1-25
•
Habib,R. Nyberg, L & Tulving, E. (2003) Hemispheric asymmetries of memory: The
HERA model revisited. Trends in Cognitive Sciences, 7, 241-245
•
Lepage, M., Habib, R. & Tulving. E (1998) Hippocampal PET activations of memory
encoding and retrieval: the HIPER model. Hippocampus, 8, 313-22
•
Gardiner, J., Ramponi, C. & Richardson-Klavehn (1998) Experiences of Remembering,
Knowing and Guessing, Consciousness and Cognition, 7, 1-26
Aims
• 1. Recollection
• 2. Special populations
• 3. Neuroimaging
Recollection
• 1 Memory and Consciousness
• 2 Episodic and Semantic memory
• 3 Recollection and Familiarity
Memory and Consciousness
•
Long term memory with awareness
– ‘The knowledge of a former state of mind after it has once dropped from
consciousness’ W. James
– Memory consciously retrieved, use our remembrance of past things to guide present
thought and action
•
Long term memory without awareness
– Form of memory that influence our present thinking and behavior while operating
outside awareness.
Memory and Consciousness
Long-term memory systems
Declarative memory
(Explicit)
Episodic
memory
Semantic
memory
Non Declarative memory
(Implicit)
Procedural
memory
Episodic and Semantic Memory
• Episodic / Semantic memory (Tulving, 1972)
– Episodic memory: storage and retrieval of
episodes occurring in a particular place at a
particular moment
– Semantic memory: information about our
stock of knowledge about the world
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Episodic and Semantic Memory
• Autonoetic consciousness vs noetic consciousness (Wheeler et al, 1997)
•Episodic memory = Autonoetic consciouness
–Self-knowing: Capacity that allows adults humans to mentally represent
and to become aware of their protracted existence across subjective time.
Capacity to represent the self’s experience in the past, present and future.
•Semantic memory= Noetic consciousness
–Knowing: when one thinks objectively about something that one knows.
Episodic and Semantic Memory
Scoville and Milner (1957) Patient H.M Impairment of declarative memory (I.e. episodic and semantic memory)
Dominated the minds of researchers in amnesia
•Episodic amnesia versus semantic amnesia
–Nielsen (1958) ‘amnesia is of two types: loss of memory for personal experiences and
loss of memory for acquired facts. Either may be lost without the other’.
–Kapur (1999) distinction between ‘episodic amnesia for personally experienced events
and semantic retrograde amnesia for components of knowledge’
–Tulving (1988) The case of K.C. Closed head injury at the age of 30. Lesion in multiple
cortical and subcortial brain regions including medial temporal lobes. Impaired episodic
memory (autonoetic cs) and spared semantic memory (noetic cs). KC can learn new
semantic information despite impaired episodic memory.
–Vargha-Khadem et al. (1997). Children who became amnesic as a result of anoxic
accidents that produced bilateral hippocampal atrophy. Normal semantic memory,
impaired episodic memory. Normal progress in school.
Episodic memory= Hippocampus
Semantic memory= Left lateral temporal lobe
Episodic and Semantic Memory
•
Episodic memory: Involvement of the frontal lobes
– Recall and recognition tests
• Wheeler, Stuss & Tulving (1995) summary of all lesion work since 1984. Frontal lobe patients
impaired in recall and recognition BUT recall more impaired than recognition
– Source memory
• Source amnesia occurs when a rememberer shows retention of a fact but cannot recollect
where or how the information was learned
• Lesions restricted to the frontal lobes have been associated with Source amnesia
Episodic memory= Frontal lobes
Episodic and Semantic Memory
Neuroimaging studies
•
HERA (Hemispheric Encoding/Retrieval Asymetry)
–
–
–
Left prefrontal cortex differentially more engaged in encoding
episodic information
Right prefrontal cortex differentially more engaged in episodic
memory retrieval
Left prefrontal cortex differentially more engaged in semantic
retrieval because episodic encoding involves semantic
retrieval
Episodic and Semantic Memory
HIPER model: Hippocampal Encoding/Retrieval
(Lepage et al., 1998)
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Rostral region of the hippocampus: episodic encoding
Caudal region of the hippocampus: episodic retrieval
Recollection and Familiarity
•
Recollection: Conscious recall of specific contextual and event details Familiarity: Subjective sense of
having previously encountered a stimulus
Measures of Recollection and Familiarity (Tulving, 1985):
Remember/Know paradigm:
Participants are asked when they retrieve an item to make a ‘Remember’ response if
they are able to bring back to mind some recollection of what occurred at the time the
item was encoded and a ‘Know’ response if they are aware only of the item’s prior
occurrence.
Recollection and Familiarity
•
Interpretation 1: The Dual component views
– Recollection and Familiarity are two independent processes
•
Interpretation 2: The unitary signal detection model
–
The unitary signal detection model maps the two responses (R and K) onto a continuum of trace
strength with two different responses criteria
Recollection and Familiarity
•
The Dual component views
– The Atkinson Model (1973)
• Subjects either make a fast response based on the familiarity of the test item or if the familiarity
process produces an ambiguous response, engage in an extended memory search
– The Mandler Model (1979)
• Familiarity supports recognition and implicit memory, recollection supports recognition and
recall
• Familiarity and recollection are independent and operate in parallel but with familiarity being
faster than recollection
– The Jacoby Model (1983)
• Recollection reflects an analytic, consciously controlled process, familiarity is a relatively
automatic process
Recollection and Familiarity
•
The Dual component views
– The Tulving Model (1985)
• Episodic memory gives rise to the conscious experience of remembering (recollection) and
semantic memory gives rise to the conscious experience of knowing (familiarity)
– The Yonelinas Model (1998)
• Recollection and familiarity differ in terms of the type of information that they provide.
• Familiarity is assumed to reflect the assessment of quantitative memory strength information in a
manner similar to that described by signal detection theory.
• Recollection reflects a threshold retrieval process whereby qualitative information about a
previous event is retrieved.
Recollection
• Measures of Recollection and Familiarity
–
–
–
–
Recall/Recognition methods
Source memory
PDP
Remember/Know procedure
Recollection
• Recall/Recognition
– Recall assimilated to Recollection and Recognition to familiarity
– If a variable has a larger effect on recall than recognition, then it can be said
to have a larger effect on recollection than familiarity
• Source memory
– Recollection reflects the retrieval of qualitative information about the study
event: Source memory is a good way of testing it
Recollection
•
The Process-Dissociation procedure (PDP) Jacoby (1991)
– Recollection is measured as the ability to remember where or when an item was earlier
studied. Familiarity does not support such a discrimination.
•
Remember/Know Tulving (1985)
– Subjects are required to introspect about the basis of their memory judgments and
report whether they recognize items on the basis of remembering (I.e. recollection) or
knowing (I.e. familiarity)
Special Populations
• 1. Amnesia
• 2. Aging
• 3. Frontal lobe lesions
• 4. Alzheimer’s disease
Amnesia
• Recall versus Recognition
– Damage to the hippocampus: recall more impaired than recognition (Baddeley et al.,
2001)
– Damage to the temporal lobe: mixed results
– In Sum: the hippocampus is critical for recollection, the temporal lobe for familiarity
• Source memory
– In comparison to tests of item recognition, amnesics (whithout frontal lobe damage)
perform poorly in tests that require them to remember when an item was presented,
where an item was presented, which modality it was presented in, which list the
item was in, how frequent it was presented
– Same pattern of results observed in Frontal lobe patients (Janowsky et al., 1989)
– In sum: source memory impaired in amnesics and Frontal lobes patients
Amnesia
•
Remember-Know, PDP
– Results from the RK, PDP studies showed that patients with extensive temporal lobe
damage have impaired recollection.
– Left hemisphere temporal lobectomy impairs recollection
– Right hemisphere temporal lobectomy impairs familiarity (Blaxton et al., 1997)
– Patients with extensive temporal lesions show deficits in recollection and familiarity,
patients with selective hippocampal lesions show selective deficits in recollection
(Lazzara et al., 2001)
Hyppocampus critical for recollection
Temporal region critical for familiarity
Aging
•
Recall versus Recognition
– Aging leads to greater recall than recognition deficits (Craik & Jennings, 1992)
•
Source memoy
– Impaired source memory (Schacter et al., 1984)
– Deficits linked to poor executive performance (Glisky et al., 1995)
•
Remember-Know
-
Age effect on Remember responses (Perfect et al., 1995)
PDP and RK procedures indicate that aging leads to a decrease in recollection but does
not influence familiarity
Recollection deficits in aging linked to a decrease in
frontal lobe functioning
Frontal Lobe lesions
•
Recall versus Recognition
– Greater recall than recognition deficits (Janowksy et al., 1989)
– Recognition sometimes relatively normal suggesting that familiarity is preserved
•
Source memory
-Deficits in memory for the source of facts (Janowksy et al., 1989)
-Source memory impaired in patients with dorsolateral prefrontal lobe lesions (Kopelman et
al., 1997)
Frontal lobe lesions
•
Remember-Know
– Levine et al. (1999) Case study.
• Patient with damage to the right ventral prefrontal cortex performed normally on
recall, recognition and source memory BUT correct recognition responses were
associated with fewer remember responses than seen in controls
Lesions to the dorsolateral prefrontal cortex lead to
reductions in recollection but have either smaller or no
effects on familiarity
Alzheimer’s disease
S tu dy
Estim ation m ethods
Adam et al., 2005;
Hudson and
Robertson, 2007;
Knight, 1998;
Koivist o et al., 1998.
[58,59,60,61]
Subjective states
Della Barba (1997)
[63]
Rauchs et al. (2007)
[64]
Piolino et al. (2003)
[65]
Paradi gm
P DP * parad
igm
R/K* paradigm
Fi n di n gs
Impaired controlled processes
(recollection) in AD
Reduced aut omatic processes
(familiarity) in AD
Fewer
R
(recollection)
responses in AD
R/K
paradigm
with Fewer R responses in AD and
justification
for
R fewer justification (contextual
responses
details)
R/K paradigm on an Fewer R responses
aut obiographical memory
task
Alzheimer’s disease
Source m em ory
Gallo et al. (2004)
[68]
Mitchell et al. (1986)
[71]
Dick et al. (1989)
[70]
Dalla Barba et
(1999)
[69]
Multhaup
et
(1997)
[72]
al.
T endolkar
(1999)
[73]
al.
et
al.
Discrimination
between
intact word pairs and
rearranged word pairs
Discrimination
between
words
read
versus
generated
Discrimination
between
words acted and words
non-acted
Discrimination
between
seen
from
imagined
objects
Discrimination
between
read
versus
self
of
experimenter
generated
words
Words
presented
in
different colours
More false alarms to rearranged
pairs in AD
Impaired source discrimination
in AD
Impaired discrimination in AD
Impaired discrimination in AD
Impaired discrimination in AD
AD patients unable t o recall the
correct colours
Alzheimer’s disease
Neuroimaging
• 1. Event-Related Potentials (ERPs)
• 2. TEP and fMRI
ERPs
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ERPs
EEG profiles obtained during various
states of consciousness
After Penfield and Jasper (1954)
ERPs
• Encoding
– Items that are associated with a positive ERP signal (Positivity) are more likely to be
recognized and this effect is more pronounced for items that are later recollected
compared to those recognized on the basis of familiarity
– Effect of positivity (P300) more pronounced for recall than recognition (Paller et al., 1988)
– Effect of positivity (P300) more pronounced for Remember than Know responses
(Friedman & Trott, 2000)
ERPs
• Retrieval
– Recollection is related to an ERP positivity that is maximal over left parietal sites
– Familiarity related to an earlier positivity that has frontal-central distribution
Recollection and familiarity involve distinct neural generators.
Recollection: Parietal lobes
Familiarity: Frontal lobes
Neural activation related to familiarity is observable earlier.
But difficult to determine the location of the neural generators on
the basis of sclap ERPs.
fMRI
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TIFF (Uncompressed) decompressor
are needed to see this picture.
QuickTime™ and a
TIFF (Uncompressed) decompressor
are needed to see this picture.
fMRI
• Encoding
– Activation in prefrontal regions and the medial and inferior temporal lobes
associated with subsequent recognition memory, effects more related to
recollection than familiarity.
– Greater activation in the prefrontal, parahippocampal regions for R than K
• Retrieval
– Hippocampal and parahippocampal regions related to recollection but not
familiarity.
– Prefrontal regions involved in both recollection and familiarity.
– Parietal activation related to recollection
Neuroimaging
Wais P (2008) FMRI signals associated with memory strenght in the
medial temporal lobes: a meta-analysis, Neuropsychologia, 46, 3185-96
to identify patterns of memory-related neural activity in the medial temporal lobes (MTL), a quantitative metaanalysis of 17 functional magnetic resonance imaging (fMRI) studies was performed. The analysis shows that
increased activity in the hippocampus and the parahippocampal cortex predicts subsequent memory strength.
During retrieval, activity in the hippocampus increases in association with strong memory. In the perirhinal
cortex, increased activity predicts subsequent recognition, whether based on weak or strong memory, whereas
during retrieval activity decreases below the level for misses in association with both weak and strong memory.
The results are consistent with the claim that the hippocampus selectively subserves recollection,
whereas adjacent structures subserve familiarity [Eichenbaum, H., Yonelinas, A., & Ranganath, C.
(2007). The medial temporal lobe and recognition memory. The Annual Review of Neuroscience, 30, 123-152].
However, this conclusion depends on a specific dual-process theory of recognition memory that has been used
to interpret the results. An alternative dual-process model holds that the behavioral methods used to
differentiate recollection from familiarity instead separate strong memories from weak memories. When the
fMRI data are interpreted in terms of the alternative theory, the fMRI results do not point to
selective roles for the hippocampus or the adjacent MTL structures.
The fMRI data alone cannot distinguish between these two models, so other methods are needed to
resolve the issue.
Conclusion
• Remembering and the brain….
– Frontal lobes and temporal lobes both involved in recollection and
familiarity
– Familiarity earlier than recollection
– Greater activation of these brain regions for Recollection
Conclusion
T able 1. A contemporary overview of memory: Recollection and familiarity processes
Brain Region
Conscious
Subjective
Mental
state
Resources State
Contextual
Status in
or Source
AlzheimerÕs
Information Disease
Recollection Hippocampus; ÔrememberingÕ Effortful,
Impaired
Slow
Frontal lobes
Familiarity
Aut onoetic Some
P eri-
ÔknowingÕor
Relatively
Hippocampal
finding
aut omatic,
Regions
familiar
Quick
Noetic
None
Relatively
intact