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Perception and the Medial Temporal Lobe: Evaluating the Current Evidence

Perception and the Medial Temporal Lobe: Evaluating the Current Evidence. Wendy A. Suzuki NYU. Outline. Anatomy of the medial temporal lobe (MTL) Medial temporal lobe memory system (MTLMS) hypothesis Evidence towards MTLMS from humans and non-human primates

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Perception and the Medial Temporal Lobe: Evaluating the Current Evidence

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  1. Perception and the Medial Temporal Lobe: Evaluating the Current Evidence Wendy A. Suzuki NYU

  2. Outline • Anatomy of the medial temporal lobe (MTL) • Medial temporal lobe memory system (MTLMS) hypothesis • Evidence towards MTLMS from humans and non-human primates • Perceptual-mnemonic (PM) hypothesis • Evidence against PM from humans, non-human primates and rats

  3. Human Medial Temporal Lobe (MTL) • Hippocampus • Entorhinal cortex • Perirhinal cortex • Parahippocampal cortex Kandel et al., 2000

  4. Animal MTL Anatomy

  5. Medial Temporal Lobe Memory System (MTLMS) • Traditional view: • MTL is involved in the ability to learn and retain declarative memory • Declarative memory involves information for events, facts and relationships(Eichenbaum and Cohen, 2001; Squire and Zola-Morgan, 1991) • Procedural learning, perceptual priming, and emotional memory are spared

  6. Perceptual-Mnemonic Hypothesis • Novel view: • MTL is involved in declarativememory AND perception (Bussey and Saksida, 2007; Lee et al., 2005; Murray and Wise, 2004) • Specifically, the perirhinal cortex • High feature ambiguity (overlapping features)

  7. Perception in the Lateral Temporal Lobe Dorsal Stream (Vision for Action) Ventral Stream (Vision for Perception) Milner and Goodale, 1995

  8. Wendy Suzuki: Argument I argue that little or no convincing evidence exists in favour of the role of the MTL in perception

  9. MTLMS: Evidence from Human Amnesic Patients • Patient H.M. (Henry Gustav Molaison) • Mostly anterograde amnesia, but also temporally graded retrograde amnesia • Bilateral removal of hippocampus (2/3), amygdala, parahippocampal gyrus, perirhinal and entorhinal cortices • Declarative memory gone, perception spared

  10. MTLMS: Evidence from Non-human Primates • Induce lesions • Large MTL lesions modeled from H.M. (Mishkin, 1978; Zola-Morgan and Squire, 1985) • Selective MTL lesions – perirhinal and entorhinal, just perirhinal (Meunier et al., 1993), or hippocampus (Alvarez et al., 1995; etc) • All involved in declarative/relational memory with online perceptual processing spared • Can still process features (colours/shapes) • Can differentiate between stimuli

  11. MTLMS: Evidence from Non-human Primates • MTL receives inputs from many high-order sensory and association areas • MTL might be sight for integration of perceptual stimuli (Suzuki and Amaral, 1994)

  12. Delayed Nonmatching-to-Sample (DNMS) Task (Mishkin, 1978) Zola-Morgan et al., 1989

  13. Perirhinal Lesions: No Perceptual Deficits in Monkeys • Tested for perceptual generalization (Hampton and Murray, 2002) • Modified stimuli (rotated, enlarged, shrunken, or masked) • Criticism for similarity to Shepard–Metzler • DNMS task (Buffalo et al., 2000) • Two superimposed objects (high overlap) • Short delay (0.5s)

  14. Monkey Perirhinal Lesions: Evidence Against the PM Hypothesis • Studies claiming MTL involvement in perception have: • Confounded impairment in learning/memory • Required working memory in perception tasks • Extent of the lesion not identified

  15. Monkey Perirhinal Lesions: Evidence Against the PM Hypothesis • Bilateral rhinal ablation (Eacott et al., 1994) • Reported perceptual impairment in 0s delay and simultaneous matching conditions • Large stimulus sets • Averaged together • Later reported that some samples were left out • When left out, no difference! Buckely and Gaffan, 1998

  16. Monkey Perirhinal Lesions: Evidence Against the PM Hypothesis • Concept of visual discrimination learning • Can you test perception in animals without engaging memory? • Learning over multiple trials • Studies reported spared ‘elemental’ discriminations, but impaired ‘object’ discrimination (Buckley and Gaffan, 1998; Bussey et al., 2002, 2003) Buckely and Gaffan, 1998

  17. Oddity Discrimination Task • Developed in attempt to tease out perception from memory • No difference in perirhinal lesioned monkeys during easy and moderate discrimination (colours, shapes) • Problems during complex object discrimination • Perhaps implies impairment in visual associative learning to associate multiple face views as one (Messinger et al., 2001; etc) Buckley et al., 2001

  18. Oddity Discrimination Task • Find the scene outlier • Only 10 scenes • Could use long-term memory to recall the identities of each scene. Buckley et al., 2001

  19. Morphing Features • Different stages of morphing flowers • Each one is morphed into previous one (cumulative) • “High feature overlap” • High feature ambiguity must be held in working memory (Bussey, 2006) • Learning over multiple trials(Bussey et al., 2002) • Must retain object/spatial features in working memory Buckley et al., 2001

  20. Rat Perirhinal Lesions: Evidence Against the PM Hypothesis • Bilateral ablation (Bartko et al., 2007) • Simultaneous oddity discrimination task • Impaired discrimination with high feature ambiguity • PROBLEM: large objects used relative to rats

  21. Summary Thus Far: MTLMS • MTL is involved in only declarative memory • No perceptual/procedural deficits • Studies that support PM hypothesis are unconvincing • Do not adequately isolate perceptual demands from declarative/relational learning or memory • Results are inconsistent

  22. Human MTL Lesions • Major advantages of working with humans: • Verbal/written instructions • Probe to ensure instructions are followed • Follow-up of subject’s opinions • However, many contradictory outcomes in the literature exist

  23. Human MTL Lesions: Evidence in Favour of MTLMS Hypothesis • Large bilateral MTL/hippocampal lesions (Stark and Squire, 2000) • Performed same oddity discrimination task as Buckley et al., 2001 • No perceptual impairment • Maybe prefrontal inputs associated with rules of task?

  24. Human MTL Lesions: Evidence Against the PM Hypothesis • Lee et al., 2005 found impaired discrimination in complex face and scene oddity tasks • Larger stimulus sets • Simultaneous presentation of target and test item (faces/VR rooms) • Added trial-unique discrimination task

  25. Reasons for Discrepancies • Different testing procedures in different labs? • Controls performed equally as well in both studies at all five difficulties and in all three tasks • Reproduced lack of perceptual impairment for trial-unique discrimination • Differences in extent/location of lesion? • Some subjects also had anterior temporal, anterior insula, fusiform gyri lesions, and even lateral TE damage • TE involved in high-order visual perception (Squire, personal communication)

  26. Reasons for Discrepancies (cont) • Differences in extent/location of lesion (cont) • Lesion loci were estimated by visual inspection (4/5 rating scale) (Lee et al., 2005) • Single slice through each area (biased?) • Authors mention validation to volumetric analysis (Galton et al., 2001), but provide no details of validation • Squire’s group performed detailed volumetric analysis throughout MTL and LTL • Recently, MTL has been validated (Barense et al., 2007), but LTL has not

  27. Reasons for Discrepancies (cont) • Lee et al. (2005) argue that MTL group has minimal TE damage since they can discriminate colours and moderately complex objects • TE active during high overlap, not colours(Buckley et al, 1997) • TE neurons respond to faces(Alfred et al., 2005; etc) • TE neurons may reflect upstream input into perirhinal cortex

  28. TE vs Perirhinal Neurons • TE neurons respond to brightness of cue (Liu and Richmond, 2000) • Perirhinal neurons respond to visual-reward associative information of cue • Trial schedule independent of cue • TE = perception • Perirhinal = link between perceptual information and memory

  29. Conclusions • MTLMS hypothesis states MTL is involved in declarative/relational learning and memory with little or no contribution to perception • 60 years old • Animal models lack ability to differentiate perception from memory (strategies) • Human MTL lesions are inconsistent (extent and location)

  30. Future Directions • Further pursue findings with rats (Bartko et al., 2007) • Define semantics • Tease out perceptual and working memory differences (possible continuum) • May be due to axonal connections between MTL and LTL • Add muscimol to perirhinal cortex and record from TE (in monkeys) • Look for compensatory activity in humans • fMRI or connectivity analysis (fcMRI, DTI, DSI, Granger causality)

  31. Thank you ;-)

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