Transcript Declarative Memory

Language, memory, and brain:
A cognitive neuroscience
perspective on
first and second language
Michael T. Ullman
Departments of Neuroscience, Linguistics,
Psychology and Neurology
Georgetown University
[email protected]
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Collaborators and Funders
Georgetown
Laura Babcock (now at Trieste, Italy)
Harriet Bowden (now at Univ. of Tennessee)
Claudia Brovetto (now at Montevideo, Uruguay)
John Drury (now at SUNY Stony Brook)
Cristina Dye (now at Newcastle, UK)
Matthew Gelfand
Sarah Grey (now at Penn State)
Joshua Hartshorne (now at MIT)
Darlene Howard
Kaitlyn Litcofksy (now at Penn State)
Jarrett Lovelett
Christopher Maloof
Robbin Miranda (now at Shafer Corp)
Kara Morgan-Short (now at UIC)
Elizabeth Pierpont (now at Wisconsin)
Elizabeth Prado (now at UC Davis)
Mariel Pullman
Cristina Sanz
Karsten Steinhauer (now at McGill)
Kaitlyn Tagarelli
Peter Turkeltaub
Joao Verissimo (now at Potsdam)
Matthew Walenski (now at Northwestern)
Main collaborators
Stefano Cappa (Milan, Italy)
Gina Conti-Ramsden (Manchester, UK)
Laurie Cutting (Vanderbilt)
Ingrid Finger (Porto Alegre, Brazil)
Myrna Gopnik (McGill, emeritus)
Martina Hedenius (Uppsala, Sweden)
Jarrad Lum (Melbourne, Australia)
Stewart Mostofksy (KKI, Johns Hopkins)
Helen Neville (Univ of Oregon)
Dezso Nemeth (Hungary)
Aaron Newman (Dalhousie)
Steven Pinker (Harvard)
Anu Shankar (Harvard)
Bruce Tomblin (U. of Iowa)
Heather van der Lely (Harvard; deceased)
Funding
NIH: R01 MH58189; R01 HD049347 (& -09S3); R03 HD050671;
R21 HD087088
NSF: SBR-9905273; BCS-0519133; BCS-0001961; BCS-1124144;
BCS-1439290
Defense: DAMD-17-93-V-3018/3019/3020, DAMD-17-99-2-9007
Foundations: McDonnell Foundation; National Alliance for Autism
Research; Simons Foundation; Mabel Flory Trust
Corporations: Pfizer, Inc.
International: US-Israel Binational Science Foundation; 2
Grand Challenges Canada
Motivation and Approach
Evolution and biology re-use existing systems for new functions
• Air bladder in fish evolved into the lung; limbs became wings, hands, …
• The wing may be used to swim, shade prey, …
Therefore:
Language should depend in part on pre-existing brain systems
• We focus on two systems: Declarative memory and procedural memory
Approach:
• Test if and how various aspects of language depend on these systems
Advantages of this approach:
• From animal and human studies we know a lot about these systems
(their computational, anatomical, molecular, genetic, etc. substrates)
• Thus we can make specific novel testable predictions that might be
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unwarranted in the more circumscribed study of language
Bottom Line
Converging evidence suggests:
• Language depends on both memory systems
• Lexical and grammatical knowledge depend differentially on the two systems
The learning and
processing of
Idiosyncratic
(lexical)
knowledge
Rule-governed
(grammatical)
knowledge
Declarative Memory
Yes
Yes, to a fair extent, as a function of
subject, item, and other factors...
(eg, females, L2, SLI,
higher frequency items)
Procedural Memory
?
Yes
The two memory systems play at least partially redundant roles
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Declarative Memory System
Characteristics:
•
•
•
•
Knowledge for “what”: remembering an event (episodic); knowing a fact (semantic)
Specialized for learning arbitrary bits of information and associating them
Learning rapid in this system (single presentation of information)
Knowledge not just explicit, but also implicit
Functional Neuroanatomy:
• Hippocampus, other medial temporal lobe structures: Learning and consolidation
• Neocortex, especially in temporal lobes: Long-term storage
• Frontal regions (BA 45/47): Recall
Biological substrates:
• The neurotransmitter acetylcholine; the hormone estrogen
(females better than males)
• Various genes play a role, including for the proteins BDNF, APOE, others
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Procedural Memory System
Characteristics:
• Knowledge for “how”: Learning and processing of motor and cognitive skills
• Examples: typing, riding a bike, sequences, categories, rules, route-learning (navigation)
• May be specialized for aspects of sequences and rules (possibly: learning to predict)
• Learning gradual; once learned, skills applied rapidly and reliably; excellent retention
• Knowledge apparently only implicit
Functional Neuroanatomy:
• Frontal/basal-ganglia circuits; other structures (cerebellum)
• Basal ganglia (caudate nucleus): important for learning & consolidation
• Frontal (BA 44, (pre)motor cortex): more important for processing
Biological substrates:
• The neurotransmitter dopamine
• Possible genes include those for the proteins FOXP2, DARPP-32
The Two Memory Systems Interact
Cooperatively: redundant mechanisms
• Some functions are learnable only by one or the other system
• Declarative memory: arbitrary bits of information and their relations
• Procedural memory: possibly motor skills
• Others can be learned by both systems, but generally in different ways
• Route-learning (navigation), sequences, categories, rules
• Various factors affect which system is relied on more (eg, functionality)
Competitively: see-saw effect
• Dysfunction of one system may enhance the functionality of the other
• Estrogen enhances declarative memory and inhibits procedural memory
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Declarative/Procedural Theory
of Language
Lexical
Grammar
Memory
Relative reliance
Rule-governed
of Memory
grammar
hierarchical
store:
on each
(at memory
least)
& sequential
system
Subject factors:
(de-)composition
sex,
all word-specific
L2 vs. L1, of
procedural
complex
information:
system
forms: dysfunction
Item factors: the frequency
-syntax
-simple
(the
of complex
words
cat; NP
(cat)
forms
VP)
Input factors: how
-morphology
much
-irregulars:
L2 (regulars:
input,(dig-dug)
immersion
walk -ed)
vs. instruction
-complements
-phonology (novel
(devour
forms:
[direct
blick)
obj])
Declarative Memory
(Ullman, 2001, 2004, 2008, 2013, in press)
Procedural Memory
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Converging Evidence
Behavioral/Psycholinguistic
• Correlational evidence
• Evidence for storage: frequency, imageability, similarity effects
• Evidence for composition: working memory, priming effects
Neurological
• Developmental disorders: SLI, dyslexia, autism, TS, ADHD
• Neurodegenerative disease: AD, PD, HD, semantic dementia
• Aphasia, amnesia
Neuroimaging
• fMRI
• PET
Electrophysiological
• Event-Related Potentials
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The rest of the talk:
Evidence
First language: Behavioral, neurological, neuroimaging, electrophysiological
Second language: Behavioral, neurological, neuroimaging, electrophysiological
Neurodevelopmental disorders (SLI): Behavioral, neuroimaging, electrophysiological
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First Language
Behavioral Evidence:
Correlational
Meta-analysis of correlational studies
Children (ages 4-13): 9 studies, 27 correlations, 554 children
Correlations
Declarative Memory
Procedural Memory
Lexicon
r = .41, p < .001
r = .04, p = .727
Grammar
(syntax, morphology)
r = .13, p = .096
r = .22, p = .005
(Hamrick, Lum and Ullman, in preparation)
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First Language
Neurological Evidence
Medial Temporal
Lobe Amnesia
Specific Language
Impairment
Medial Temporal
Abnormal
Normal
Declarative Memory
Abnormal
Relatively Normal
Word (Learning)
Abnormal
Relatively Normal
Basal Ganglia
Normal
Abnormal
Procedural Memory
Normal
Abnormal
Grammar (Learning)
Normal
Abnormal
• Similar dissociations between Alzheimer’s & Parkinson’s diseases
(Ullman & Pierpont, 2005; Ullman, Pullman, Lovelett, Pierpont & Turkeltaub, Under Rev.; Ullman, 2004;
Lum, Conti-Ramsden, Page, and Ullman, 2012; Kensinger, Ullman & Corkin, 2001; Postle & Corkin, 12
1998;
Meulemansa & Linden, 2003; Reber et al, 2003; Ferreira et al 2008)
First Language
Neuroimaging Evidence
Medial Temporal
(hippocampus)
Basal Ganglia
(caudate nucleus)
Activation
Word Learning
Artificial
Grammar
Learning
?
Activation during
chunk-learning
Activation during
rule-learning
(Brietenstein et al, 2005; Lieberman et al, 2004; Forkstam et al, 2006; Moro et al, 2001; Wong et al. 2013;
Folia et al, 2011; Karuza et al, 2013)
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First Language
Electrophysiological Evidence:
Event-Related Potentials (ERPs)
N400
LAN
Lexical anomalies
Consistently
No
Grammatical anomalies
Rarely
Reasonably often
• Also elicited by nonverbal semantic stimuli
• Linked to temporal lobe
structures
• Declarative Memory
• Also elicited by nonverbal sequences
• Automatic, early
• Linked to frontal regions
• Procedural Memory
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Second Language Hypotheses
- Declarative memory improves during childhood, and plateaus in adolescence
and early adulthood
- The developmental trajectory of procedural memory is less clear, but it
seems to be established early, and may attenuate during childhood
- Therefore: earlier language learners (L1, early L2 learners) should rely more
on procedural memory, and later learners more on declarative memory, for
those tasks and functions (including grammar) than can rely on either system
- However, procedural memory should only be somewhat attenuated in adults.
With enough exposure (perhaps of the right type: immersion?) at least some
proceduralization of the grammar should occur (contra critical period)
(Ullman, 2001, 2005, 2012, 2015, in press)
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Second vs. First Language (L2 vs. L1):
Predictions
Declarative Memory
Procedural Memory
Lexical Memory:
L1 and L2
Grammar
L2 > L1
L2: lower > higher exposure
Grammar
L1 > L2
L2: higher > lower exposure
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Second Language
Behavioral Evidence:
Correlational
Meta-analysis of correlational studies
Adult learned L2: 6 studies, 17 correlations, 181 learners
Correlations
Grammar at low
exposure/proficiency
Grammar at high
exposure/proficiency
Declarative Memory
Procedural Memory
r = .48, p < .001
r = -.17, p = .155
r = .19, p = .181
r = .43, p < .001
(Hamrick, Lum and Ullman, in preparation)
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Second Language
Neurological Evidence
Lesion
Temporal Lobe
(Alzheimer’s disease)
Frontal or Basal Ganglia
(Parkinson’s disease, stroke)
L1 = L2
Lexical
Not Available
L2 < L1
Grammatical
L2 higher exposure =
L2 lower exposure
L1 < L2
L2 higher exposure <
L2 lower exposure
(Fabbro and Paradis, 1995; Fabbro, 1999; Hyltenstam and Stroud, 1989; Zanini et al 2004; Johari et al, 2013;
Ullman, 2001)
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Second Language
Neuroimaging Evidence
Activation Likelihood Estimation (ALE) meta-analysis:
• 22 fMRI/PET studies, with a total of 432 subjects
• Preliminary analyses:
1) Lexical/semantics: L1 and L2 similar (e.g., BA 45/47, temporal pole,
superior temporal, fusiform) but more bilateral in L2
2) Grammar: L1 and L2 similar (e.g., BA 44, BA 6) but more bilateral in L2, and
different: basal ganglia, especially caudate (head), only in L2
(Ullman, Tagarelli, Grey,
& Turkeltaub, in prep.)
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Second Language
Electrophysiological Evidence: ERPs
Lexical/semantic
anomalies
L1
N400
Syntactic
anomalies
LAN
Low exposure L2 N400
No LAN
High exposure L2 N400
LAN
Sometimes N400
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(Ullman, 2001; Ullman, 2005; Ullman, 2012; Morgan-Short and Ullman, 2012; Bowden et al 2013; McLaughlin et
al 2010; Osterhout et al 2008; Tanner et al 2013; Weber and Lavric 2008; Friederici et al 2002; Morgan-Short,
Steinhauer, Sanz & Ullman 2012; Morgan-Short, Finger, Grey & Ullman 2012)
Neurodevelopmental Disorders:
A Neurocognitive Hypothesis
Hypothesis: Various developmental disorders result (at least in part)
• from abnormalities of brain structures underlying procedural memory
• whereas declarative memory remains largely normal, and compensates
These disorders may include (at least):
1) Specific Language Impairment (SLI)
2) Dyslexia
3) Autism
4) Tourette syndrome
5) ADHD
This hypothesis may explain a wide range of behavioral and brain
patterns in these disorders, and their comorbidities with one another
(Ullman & Gopnik, 1999; Ullman 2004, 2008; Ullman & Pierpont, 2005; Walenski, Tager-Flusberg & Ullman, 2006;
Walenski, Mostofsky & Ullman, 2007; Ullman, Pullman, Lovelett, Pierpont & Turkeltaub, under rev; Ullman,21Pullman,
Tagarelli & Curchack, in prep; Ullman & Pullman, 2015)
Specific Language Impairment
(SLI):
What is it?
Developmental language disorder in the absence of hearing impairments,
environmental deprivation, emotional problems, deficient IQ, and gross
neurological damage.
Grammatical aspects of language, in particular syntax, morphology, and
phonology, are especially affected.
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SLI
Explanatory Accounts
Previous Explanatory Hypotheses:
•
•
SLI is due to grammar-specific deficits
SLI is due to a processing deficit (e.g., of working memory)
Procedural Deficit Hypothesis (PDH):
1) SLI can be largely explained by abnormalities of brain structures
underlying procedural memory, in particular of frontal/basal ganglia,
especially Broca’s region and the caudate nucleus.
2) These abnormalities lead to impairments of procedural memory,
including grammar, and will also likely result in problems with other
functions dependent on these structures, including working memory
3) These grammatical and other deficits will be at least partly
compensated for by declarative memory
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(Ullman 2004; Ullman & Pierpont, 2005; Ullman, Pullman, Lovelett, Pierpont & Turkeltaub, under rev.;
Ullman & Pullman, 2015)
SLI
SLI: Overview of
Behavioral and Neuroanatomical
Evidence
Neuroanatomy
Learning/Memory
Language
Other Cognition
Relatively Normal
Abnormal
Medial Temporal
Basal Ganglia (Caudate)
Declarative Memory
Procedural Memory
Lexical Memory
Grammar
Often Impaired:
Motor Skills
Working Memory
Rapid Temporal Processing
(Ullman 2004; Ullman and Pierpont, 2005; Ullman, Pullman, Lovelett, Pierpont & Turkeltaub, under rev) 24
SLI
Behavioral: Procedural Learning
A Meta-Analysis
•
•
8 SRT studies: 186 individuals with SLI, 203 typical controls
Findings: Significant SRT learning deficits in SLI
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(Lum, Morgan, Conti-Ramsden, and Ullman, 2014)
SLI
Frontal and Caudate
Abnormalities
Neuroanatomical Meta-analysis of SLI:
• New meta-analysis technique: Co-localization Likelihood Estimation
• 25 studies: 270 individuals with SLI, 265 typically-developing controls
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(Ullman, Pullman, Lovelett, Pierpont and Turkeltaub, under rev)
SLI
Frontal and Caudate Abnormalities
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(Ullman, Pullman, Lovelett,
Pierpont & Turkeltaub, under rev.)
SLI
Declarative Memory Remains
Relatively Normal
Learning new
information
• Normal for non-verbal material
• Relatively normal for verbal material, especially
once language and working memory impairments
are controlled for
Long-term
knowledge
• Lexical knowledge relatively spared (any lexical
impairments appear primarily due to working
memory, phonological, and recall deficits)
(for a review, see Ullman and Pullman, 2015. Also: see Ullman and Pierpont, 2005; Lum, Conti-Ramsden, Page,
and Ullman, 2012; Riccio et al., 2007; Dewey and Wall, 1997)
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SLI
Declarative Memory Compensation:
Behavioral Evidence
1) Individuals with SLI memorize complex forms as chunks (“walked”,
“the cat”), rather than implicitly combining their parts (“the” + “cat”)
2) Individuals with SLI learn explicit grammar rules
3) Grammatical abilities correlate with procedural memory in typicallydeveloping children, but with declarative memory in children with SLI
(for reviews, see Ullman and Pierpont, 2005; Ullman and Pullman, 2015;
Also see: Oetting and Horohov, 1997; Ullman and Gopnik, 1999; Lum, Conti-Ramsden, Page, and Ullman,29
2012)
SLI
Declarative Memory Compensation:
Behavioral Evidence: Correlational
Typically developing children:
Correlations Declarative Memory
Vocabulary
Grammar
Procedural Memory
r = .480**
r = .233
r = .235
r = .305*
Children with SLI:
Correlations Declarative Memory
Procedural Memory
Vocabulary
r = .394*
r = -.008
Grammar
r = .305*
r = .112
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(Lum, Conti-Ramsden, Page, and Ullman, 2012)
SLI
Declarative Memory Compensation:
Electrophysiological Evidence:
Event-Related Potentials
Children
Lexical/semantic
anomalies
Syntactic
anomalies
N400
LAN
N400
N400
Typically
Developing
SLI
(Fonteneau & Van der Lely, 2008)
Overall: Summary
Converging behavioral, neurological, neuroimaging and electrophysiological
evidence suggests:
• Language depends on both memory systems
• Lexical and grammatical knowledge depend differentially on the two systems
The learning and
processing of
Idiosyncratic
(lexical)
knowledge
Rule-governed
(grammatical)
knowledge
Declarative Memory
Yes
Yes, to a fair extent, as a function of
subject, item, and other factors...
Subject:
good declarative memory (eg, ♀, L2)
bad procedural memory (eg, SLI, L2)
Item: (eg, higher frequency)
Procedural Memory
?
Yes
The two memory systems play at least partially redundant roles
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Some Implications
And Future Directions
Second Language:
Enhancing L2 learning/retention may be achieved via interventions (e.g., behavioral,
pharmacological) that enhance learning/retention in the memory systems
Specific Language Impairment (and other neurodevelopmental disorders):
Translational implications - diagnostic:
• Possible early diagnosis via neural markers of caudate dysfunction (but with caution)
• Better diagnosis via tests that do not allow for declarative memory compensation
Translational implications - therapeutic:
• Predicted therapeutic improvements with interventions (behavioral, pharmacological)
that enhance learning/retention in the memory systems
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