THE SYSTEMS NEUROSCIENCE OF HUMAN MEMORY

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THE SYSTEMS NEUROSCIENCE OF HUMAN MEMORY

• Rik Henson

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Overview

• A taxonomy of memory
• For each type of memory
• Definition and Common tests
• Neuropsychological evidence
• Neuroimaging evidence
• Summary

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Taxonomy of Memory
Memory
Cohen and Squire, 1980
Declarative
Non-declarative
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Taxonomy of Memory
Memory
Cohen and Squire, 1980
Declarative
Non-declarative

• Available to conscious retrieval
• Can be declared (propositional)
• Examples
• What did I eat for breakfast? (episodic)
• What is the capital of Spain? (semantic)
• What did I just say? (working)

• Experience-induced change in behaviour
• Cannot be declared (procedural)
• Examples
• Subliminal advertising? (priming)
• How to ride a bicycle (skills)
• Phobias (conditioning)

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Taxonomy of Memory
Memory
Declarative
Non-declarative
Semantic
Working
Episodic
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Taxonomy of Memory
Memory
Declarative
Non-declarative
Semantic
Working
Episodic
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Episodic Memory

• Memory for personally experienced events that
  occurred in particular place at a specific time
  (defined by Tulving, 1972)
• Contextual, spatiotemporal, autobiographical,
  remembering
• Direct memory tests
• Encoding Retrieval
• Free recall CAT ?
• DOG ?
• Cued recall CAT DOG EAGLE- ?
• EAGLE NEST CAT- ?
• Recognition CAT CAT ?
• DOG SUN X
• Source Memory CAT CAT bold
• DOG DOG italics

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Episodic Memory
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Episodic Memory - Neuropsychology

• Organic Amnesia
• Intact semantic memory (e.g,
  language) working memory (e.g, mins) nondeclarative memory

Hippocampal / MTL memories consolidated into
neocortex over time, and become
hippocampal-independent (Marr 1971 Alvarez
Squire, 1995)
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Episodic Memory - Neuropsychology
Large lesions of bilateral Hippocampi,
Amygdalae, and Rhinal Cortex produce severe
antero- and retro-grade amnesia, eg, HM (Scoville
Milner, 1957) Circumscribed lesions of CA1
of Hippocampus produce significant anterograde
amnesia (Zola-Morgan et al 1986) Korsakoffs
Patients with diffuse damage to Diencephalon,
Medial Thalamus, Mammillary Nuclei show varied
amnesia (Press et al., 1989) Alzheimers
patients show early signs of amnesia, with first
lesions in Medial Temporal Lobe (Hyman et al
1984) Frontal Patients show confabulation
(Burgess Shallice, 1996), impaired source
memory (Janowsky et al., 1989) and interference
(Shimamura et al., 1995)
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Episodic Memory - Neuroimaging

• MTL activations during episodic encoding
  (Tulving et al 1996) and retrieval (Schacter et
  al. 1996)
• Anterior-Posterior dissociation? (Lepage et
  al. 1998 Schacter et al. 1999)
• Left Frontal during Encoding (Shallice et al.,
  1994), right during Retrieval
• HERA Hemispheric Encoding Retrieval
  Asymmetry (Tulving et al., 1994)
• Posterior cingulate / Precuneus (Fletcher et
  al., 1996)
• Left lateral inferior parietal cortex (Henson
  et al., 1999)
• Network of Frontal - Medial Temporal
  Posterior areas all involved
• Frontal areas control encoding and retrieval of
  memories?
• Posterior association areas store components of
  memories?
• Medial Temporal regions (temporarily) bind
  different components?
• Finer spatial resolution (fMRI) beginning to
  dissociate MTL regions, eg Hippocampus /
  Perirhinal for Recollection / familiarity?
  (Aggleton Brown, 1999)

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Taxonomy of Memory
Memory
Declarative
Non-declarative
Semantic
Working
Episodic
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Semantic Memory

• Memory for facts, general knowledge, word
  meanings
• Acontextual Independent of where or when the
  information was encoded

• Common Tests
• Object Naming e.g. What is this?

Semantic Judgements Which bottom picture
goes best with the top one?
Category Fluency Name as many dog breeds as
possible in 1 minute German Shepard, golden
retriever, . . .
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Semantic Memory - Neuropsychology

• Modality-specific visual Agnosia after Left
  Temporal damage (Warrington, 1975)
• Category-specific, amodal Agnosia following
  Left Medial/Middle Temporal damage, eg, living
  vs. nonliving (Warrington Shallice, 1984)
• category effects reflect visual vs functional
  information?
• Temporal Pole lesions cause deficits in
  person-naming Left Middle Inferior in
  animal-naming and Left Posterior Inferior in
  tool-naming (Damasio et al 1996)
• Semantic Dementia (SD) following
  anterior/inferior Temporal atrophy, with reverse
  Ribot gradients (Graham et al., 2000)
• SD patients demonstrate graded deterioration of
  knowledge (Hodges et al., 1992)

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Semantic Memory - Neuroimaging
Common activation in Left Inferior Frontal,
Inferior Temporal, Angular gyrus and Temporal
pole for semantic judgments to words and pictures
(Vandenberghe et al 1996) Left Inferior
Temporal activations for animal and tool naming,
Temporal Pole for people naming (Damasio et al.,
1996) Left Inferior Temporal activation for
category- versus letter-fluency (Mummery et al
1996) Left Middle Temporal and Premotor
activations for tool vs animal naming, Left
Middle Occipital for animal vs tool naming
(Martin et al 1996) Distributed
representations, with activations reflecting
objects interaction with world? E.g., tool
naming activates motor regions
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Episodic vs Semantic debate
Are episodic/semantic memory just a continuum?
(Watkins, 1974) Does Global Anterograde
Amnesia exist? Inability to acquire new
semantic memories (Gabrieli et al,
1998)... ...yet intact development of semantic
memory despite hippocampal damage (Vargha-Khadem
et al. 1998) Hippocampus proper underlies true
episodic memory? Additional Medial Temporal
areas underlie anterograde semantic memory
impairment?
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Taxonomy of Memory
Memory
Declarative
Non-declarative
Semantic
Working
Episodic
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Working Memory

• The ability to hold information on-line for
  current task (e.g. for comprehension, planning,
  problem solving, Baddeley 1992)
• Short-term memory (cf. long-term episodic /
  semantic memory)
• Verbal vs Visuospatial Maintenance vs
  Manipulation
• Spatial vs Object Storage vs Rehearsal

• Common Tests
• Memory Span (maintenance)
• Digit span Repeat back 8,5,3,2,7,9

• (Sternberg) probe task (maintenance)

• N-back task (manipulation)
• . . . !

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Working Memory - Neuropsychology
Auditory-Verbal maintenance deficit following
Left Supramarginal / Inferior Parietal lesions,
eg KF (Warrington Shallice, 1969)
Visual-spatial maintenance deficit following
Right Inferior Parietal lesion, eg ELD (Hanley et
al 1991) Frontal patients impaired on
manipulating information in Working Memory on
tasks such as card sorting (Milner, 1963) and
selection-without-repetition (Petrides Milner,
1982) Age-related Working Memory deficits
following frontal-striatal decline (Gabrieli,
1996) Modality-specific, passive stores in
posterior parietal/temporal cortex Common
executive processes in frontal cortex
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Working Memory - Neuroimaging
Left Inferior Parietal activation during
verbal storage Left Inferior Frontal and
Premotor activation during verbal rehearsal
(Paulesu et al. 1993) Right Inferior Parietal,
Inferior Frontal, Anterior Occipital, and
Premotor Cortex activated during spatial
maintenance (Jonides et al. 1993) Left
inferior temporal and inferior parietal activated
when object compared to spatial maintenance
(Smith et al. 1995) Dorsolateral Frontal Cortex
activated in N-back task when manipulation
required by N1 (Cohen et al 1997), for both
verbal and spatial material (Owen et al
1998) Ventrolateral (Inferior) Frontal Cortex
involved in maintaining information on-line in
current form Dorsolateral Frontal Cortex
involved in manipulating information into new
forms (Owen 1997 Postle DEsposito, 1999)
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Taxonomy of Memory
Memory
Declarative
Non-declarative
Semantic
Working
Episodic
Priming
Procedural
Conditioning
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Taxonomy of Memory
Memory
Declarative
Non-declarative
Semantic
Working
Episodic
Priming
Procedural
Conditioning
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Priming

• A change in speed, accuracy or bias of processing
  a stimulus owing to prior exposure to that
  stimulus
• Perceptual vs Conceptual
• Example Indirect Memory Tests
• Perceptual Identification Gollin Figures -

• Stem/Fragment Completion
• (SMILE) SMI_ _
• S_ _ L _
• Word Association
• (ROSE) FLOWER - ?
• Speeded Decisions
• (APPLE) Concrete/Abstract?

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Priming - Neuropsychology

• Amnesics with Medial Temporal damage show intact
  Perceptual Priming (Warrington Weiskrantz 1970)
  and intact Conceptual Priming (Graf et al 1985)
• Huntingtons patients with Basal Ganglia damage
  show intact priming (Heindel et al 1989)
• Alzheimers patients with diffuse Temporal Lobe
  damage show intact perceptual priming but
  impaired conceptual priming (Keane et al 1995)
• Patients with right occipital lesions show no
  perceptual priming, but intact conceptual priming
  (Gabrieli et al 1995)

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Priming - Neuroimaging

• Reduced activity in bilateral occipito-temporal
  regions in word-stem completion (Buckner et al.
  1995), independent of explicit memory (Schott et
  al, 2005)
• Reduced activity in left frontal cortex in
  word-association (Blaxton et al 1996)
• Subliminal priming right thru to motor cortex
  (Dehaene et al, 2001) though issues of stimulus
  vs response priming (Dobbins et al, 2004)
• Left frontal cortex involved in
  conceptual/semantic priming
• Occipito-temporal cortex involved in visual
  perceptual priming
• Priming deactivations localised in same areas
  that performed initial processing (Schacter
  Buckner, 1998)
• Deactivations reflect less neural activity
  (lowered thresholds, synaptic change, residual
  activation)? Priming-related increases? (Henson,
  2003)

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Taxonomy of Memory
Memory
Declarative
Non-declarative
Semantic
Working
Episodic
Priming
Procedural
Conditioning
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Procedural Memory

• Skill learning (e.g. riding a bicycle)
• Requires multiple trials
• Indexed by improved accuracy or RTs

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Procedural - Neuropsychology

• Amnesic patients show intact
• Rotary Pursuit (Corkin 1968)
• Serial Reaction Task (Nissen Bullemer 1987)
• Alzheimers patients show intact
• Rotary Pursuit (Gabrieli et al 1993)
• Mirror Tracing (Heindel et al 1989)
• Parkinsons patients impaired on
• Rotary Pursuit (Heindel et al 1989)
• Serial Reaction Task (Ferraro et al 1993)
• Huntingtons patients impaired on
• Rotary Pursuit (Gabrieli et al 1997)
• Serial Reaction Task (Willingham Koroshetz
  1993)
• but not
• Mirror Tracing (Gabrieli et al 1997)
• Cerebellar lesions impair Mirror Tracing (Sanes
  et al 1990)

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Procedural - Neuroimaging

• Rotary Pursuit learning correlates with activity
  in Primary and Secondary Motor Cortex (Grafton et
  al 1992)
• Serial Reaction Task correlates with activity in
  Primary and Secondary Motor Cortex, and Basal
  Ganglia (Hazeltine et al 1997)
• Two hypotheses
• 1. Learning repetitive sequence involves Basal
  Ganglia-Thalamic-Motor Cortical loop
• Learning new visual-motor mappings involves
  Cerebellar-Motor Cortical loop
• 2. Open-loop learning (minimal feedback) Basal
  Ganglia-Thalamic-Motor Cortical loop
• Closed-loop learning (continual
  feedback) Cerebellar-Motor Cortical loop
• Rotary Pursuit and Serial Reaction Task involve
  open-loop motor learning with little visual
  feedback (impaired by Basal Ganglia lesions)
• Mirror Tracing involves much visual feedback
  (impaired by Cerebellar lesions)
• Need to examine nonvisual feedback

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Taxonomy of Memory
Memory
Declarative
Non-declarative
Semantic
Working
Episodic
Priming
Procedural
Conditioning
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Classical Conditioning

• Changes in response (R) to conditioned stimulus
  (CS) after repeated conditioned unconditioned
  stimulus (US) pairing
• Example
• Existing e.g. air puff to eye (US) blink
  reflex (R)
• Training e.g. tone in ear (CS) air puff to
  eye (US)
• Result tone in ear (CS) blink reflex
  (R)
• Delay Conditioning US starts after a CS but
  they co-occur

Trace Conditioning US starts after CS but they
do NOT co-occur
Fear Conditioning CS is neutral (e.g. a light),
US is aversive (e.g. shock) R is
behavioural/physiological (e.g. Galvanic skin
response)
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Conditioning - Neuropsychology

• Delay conditioning (eye-blink)
• Abolished with Cerebellar lesions (Daum et al
  1993)
• Abolished in Alzheimers Disease diffuse
  damage? (Woodruff-Pak et al 1990)
• Impaired in Korsakoffs amnesics diffuse
  damage (McGlinchey-Berroth et al 1995)
• Intact despite Basal-Ganglia lesions in
  Huntingtons (Woodruff-Pak Papka 1996)
• Intact in Medial-Temporal amnesics (Gabrieli et
  al 1995b Clark Squire, 1998)
• Trace conditioning
• Impaired in Medial-Temporal amnesics
  (McGlinchey-Berroth et al 1997)
• Fear conditioning
• Impaired following amygdala resection, despite
  intact declarative memory for contingency (LeBar
  et al 1995)
• Intact in amnesics despite impaired declarative
  memory for contingency (Bechara et al 1995)

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Conditioning - Neuroimaging

• Cerebellar activity correlated with CR during
  Delay Conditioning (Logan Grafton 1995)
• Hippocampus (and amygdala) shows transient
  involvement in Fear Trace Conditioning (Buechel
  et al., 1999)
• Amygdala activity correlates with CS during Fear
  conditioning (Morris et al 1998)
• Cerebellum implicated in delay conditioning
• Amygdala implicated in fear conditioning
• Hippocampus may be involved in trace
  conditioning (development of declarative memory
  for contingency?)
• Future research may benefit from analyses of
  effective connectivity (Buechel et al 1998)

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Taxonomy of Memory
Memory
Declarative
Non-declarative
Semantic
Working
Episodic
Priming
Procedural
Conditioning
What did I just say?
What did I have for breakfast?
What is the capital of France?
Facilitated processing
Reflex response to new stimuli
How to ride a bicycle
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