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  1. THE SYSTEMS NEUROSCIENCE OF HUMAN MEMORY Rik Henson

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

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

  4. 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)

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

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

  7. 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

  8. PATIENTS CONTROLS Copy Delayed Recall (15 mins) Rempel-Clower et al., 1996 Episodic Memory

  9. Anterograde Amnesia Retrograde Amnesia Episodic memories time Trauma “Ribot” gradient Episodic Memory - Neuropsychology • Organic Amnesia • Intact: semantic memory (e.g, language) working memory (e.g, <5 mins) nondeclarative memory Hippocampal / MTL memories ‘consolidated’ into neocortex over time, and become hippocampal-independent (Marr 1971; Alvarez & Squire, 1995)

  10. 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) • Korsakoff’s Patients with diffuse damage to Diencephalon, Medial Thalamus, Mammillary Nuclei show varied amnesia (Press et al., 1989) • Alzheimer’s 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)

  11. 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)

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

  13. Pyramid and Palm Tree Test (Howard & Patterson 1992) 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, . . .

  14. 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)

  15. McClelland and Rogers, 2003 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 object’s interaction with world? E.g., tool naming activates motor regions

  16. 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?

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

  18. Corsi Block span … … 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) • . . . $ % ^ ! * & * +

  19. 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

  20. 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 N>1 (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 & D’Esposito, 1999)

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

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

  23. Priming Perceptual Priming (Gollin Figures) Warrington & Weiskrantz, 1970 • 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?

  24. Priming - Neuropsychology • Amnesics with Medial Temporal damage show intact Perceptual Priming (Warrington & Weiskrantz 1970) and intact Conceptual Priming (Graf et al 1985) • Huntington’s patients with Basal Ganglia damage show intact priming (Heindel et al 1989) • Alzheimer’s 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)

  25. 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)

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

  27. Serial Reaction Task (e.g. Hazeltine et al., 1997) Rotary–Pursuit (e.g. Gabrieli et al., 1997) Mirror Tracing (e.g. Corkin, 1968) Procedural Memory • Skill learning (e.g. riding a bicycle) • Requires multiple trials • Indexed by improved accuracy or RTs

  28. Procedural - Neuropsychology • Amnesic patients show intact: • Rotary Pursuit (Corkin 1968) • Serial Reaction Task (Nissen & Bullemer 1987) • Alzheimer’s patients show intact: • Rotary Pursuit (Gabrieli et al 1993) • Mirror Tracing (Heindel et al 1989) • Parkinson’s patients impaired on: • Rotary Pursuit (Heindel et al 1989) • Serial Reaction Task (Ferraro et al 1993) • Huntington’s 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)

  29. 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

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

  31. CS US CS US 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)

  32. Conditioning - Neuropsychology • Delay conditioning (eye-blink): Abolished with Cerebellar lesions (Daum et al 1993) Abolished in Alzheimer’s Disease: diffuse damage? (Woodruff-Pak et al 1990) Impaired in Korsakoff’s amnesics: diffuse damage (McGlinchey-Berroth et al 1995) Intact despite Basal-Ganglia lesions in Huntington’s (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)

  33. 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)

  34. Lateral Frontal Parietal and occipital Many cortical regions… Lateral Temporal / Frontal lobes Basal Ganglia Cerebellum Motor cortex Medial temporal Diencephalon Mammillary bodies Frontal lobe Cerebellum/ Amygdala (MTL?) Taxonomy of Memory Memory Declarative Non-declarative Episodic Semantic Working Priming Procedural Conditioning What did I have for breakfast? What is the capital of France? What did I just say? Facilitated processing How to ride a bicycle Reflex response to new stimuli

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