Implicit memory

1
Implicit memory

• Schacter and many other researchers distinguish
  between implicit and explicit memory
• This lecture will begin by surveying some
  historical observations regarding implicit memory
• It will then focus on a particular type of
  implicit memory, habits or skills, that are
  mediated by the basal ganglia
• Particular attention will be given to lesion
  studies and studies of patients with Parkinsons
  disease, which is associated with impaired basal
  ganglia functioning

2
Implicit memory

• implicit memory
• occurs when previous experiences facilitate
  performance on a task that does not require
  conscious recollection of those experiences
• explicit memory
• occurs when the task requires conscious
  recollection of past experiences

3
Implicit memory

• Historical survey
• Maine de Biran proposed that after sufficient
  repetition a habit can be executed automatically
  and unconsciously without awareness of the act
  itself or of the previous episodes in which the
  habit was learned
• Maine de Biran also developed a form of multiple
  memory system

4
Implicit memory

• Historical survey
• Carpenter (1874) noted the importance of
  autobiographical recognition or awareness in
  normal memory
• Neurology
• Korsakoff noted that amnesic patients were
  affected by previously experienced events even
  though they were consciously unaware of these
  events
• Claparede refusal of amnesic to shake hands after
  he had pricked her hand

5
Implicit memory

• Historical survey
• Neurology
• Schneider 1912 showed that amnesics required less
  information across learning trials to identify
  fragmented pictures

6
Implicit memory

• Historical survey
• Psychiatry
• Freud and Janet investigated patients suffering
  hysterical amnesia as a result of emotional
  trauma
• these patients could not explicitly remember the
  traumatic event, but their memories of these
  events were expressed indirectly (implicitly)
• Janet --hysterical amnesia consists of 1. the
  inability of a subject to evoke memories
  consciously and voluntarily and 2. Automatic,
  compelling, and untimely activation of these
  memories

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Implicit memory

• Modern research on implicit memory
• effects of subliminally encoded stimuli
• several studies have shown that stimuli that are
  not represented in subjective awareness
  (consciously) are nevertheless processed to high
  levels by the perceptual system

8
Implicit memory

• e.g., Kunst-Wilson Zajonc (1980)
• presented geometric shapes for 1 ms claimed it
  was too brief a period of time to permit its
  perception subsequently tested recognition
  (forced choice) and preference (forced choice)
• Results recognition (RN) was at chance Subjects
  preferred the previously presented geometric shape

9
Implicit memory

• e.g., Bargh Pietromonaco (1982)
• presented hostile words and then later had
  participants rate a target person
• results showed that explicit recognition memory
  of hostile words was at chance, although
  ratings of the target person were more negative
  than those who did not receive prior exposure
• e.g., divided attention study of Eich (1984)

10
Implicit memory

• e.g., divided attention study of Eich (1984)
• auditory divided attention task
• unattended channel -- presented homophones (e.g.,
  taxi fare)
• subsequently participants showed no explicit RN
  memory in yes/no task, but tended to spell
  homophones in biased direction compared to
  baseline performance

11
Implicit memory

• Learning and conditioning without awareness
• participants learn rules or contingencies without
  explicit memory for them
• this phenomenon was studied in multitrial
  learning experiments and in classical
  conditioning experiments

12
Implicit memory

• Implicit learning studies of Reber
• subjects were presented letter strings that were
  organized according to rules of an artificial
  grammar
• Reber reported that subjects could categorize
  these strings correctly even though they were
  unable to consciously aware of the rules

13
Implicit memory

• Repetition priming effects
• facilitation in processing of a stimulus as a
  function of recent prior exposure to the same
  stimulus
• note repetition priming has been observed under
  a wide variety of test conditions, none of which
  require explicit reference to a prior study
  episode
• lexical decision (word/nonword) -- DV latency
• word identification
• word stem or fragment completion (e.g., __
  ss__ss__)

14
Implicit memory

• Repetition priming effects
• 1. used to study nature of lexical representation
• e.g., studied the effects of auditory
  presentation on subsequent word identification
  and lexical decision tasks
• results showed little or no priming
• e.g., morphologically similar words (e.g., seen)
  facilitate priming of (sees), but visually
  similar words do not prime each other (e.g.,
  seen) versus (seed)

15
Implicit memory

• Repetition priming effects
• 2. used to study relation of implicit to explicit
  memory
• stimulated by studies of Warrington and
  Weiskrantz on amnesics
• this study showed that amnesics showed excellent
  retention when they were asked to complete
  three-letter stems of recently presented words
  even though their yes/no recognition memory was
  impaired

16
Implicit memory

• Repetition priming effects
• 2. used to study relation of implicit to explicit
  memory
• several studies have shown that variations in
  level or type of study processing have
  differential effects on priming versus
  remembering
• e.g., Jacoby Dallas (1981) showed that
  answering questions about the meaning of a target
  word improved yes/no recognition memory relative
  to answering questions about presence of a
  letter, but that word identification was
  unaffected

17
Implicit memory

• Repetition priming effects
• 2. used to study relation of implicit to explicit
  memory
• modality shift
• Jacoby Dallas (1981) showed that changing from
  auditory (at study) to visual (at test) severely
  attenuated priming effects as assessed by word
  identification, but had little effect on yes/no
  recognition performance

18
Implicit memory

• Repetition priming effects
• 2. used to study relation of implicit to explicit
  memory
• other factors that have been manipulated
• study-test delay--variable effects
• manipulations that affect retroactive and
  proactive interference (and hence explicit
  memory) have little effect on word-stem or word
  fragment completion

19
Implicit memory

• Repetition priming effects
• 2. used to study relation of implicit to explicit
  memory
• other factors that have been manipulated
• study-test delay--variable effects
• manipulations that affect retroactive and
  proactive interference (and hence explicit
  memory) have little effect on word-stem or word
  fragment completion

20
Implicit memory

• Habit or skilled learning
• Several lines of evidence suggest that the
  caudate nucleus mediates a particular type of
  implicit memory, habit memory or memory for
  skills, that are incrementally acquired
• This type of memory can be dissociated from
  explicit memory
• Caudate nucleus is part of the basal ganglia

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Implicit Memory
Explicit Memory
Priming
Nonassociative Learning
Neocortex
Reflex Pathways
Facts (Semantic Memory)
Events (Episodic Memory)
Skills and Habits
Simple Classical Conditioning
Striatum
Medial Temporal Lobe
Emotional Response
Skeletal Musculature
Amygdala
Cerebellum
Squire and Knowlton (1994) Squire (1987)
Declarative vs. procedural memory
22
Habits and skills

• Characteristics of habits and skills
• Habits are learned (acquired via experience
  dependent plasticity)
• Habits are performed repeatedly over time
• Habits are performed almost automatically and
  nonconsciously
• Habits tend to involve an ordered, structured,
  action sequence
• Habits are elicited by a particular context or
  sequence (either internal or external)
• Habits can be habits of thought and habits of
  motor expression

23
Habits and skills

• Background
• Anatomy
• Basal ganglia (BG) plays an important role in
  normal voluntary movement
• Input to BG received from cerebral cortex and
  output sent to brain stem and via the thalamus
  back to the prefrontal, premotor, and motor
  cortices

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BG in relation to brain structures

• Basal ganglia receives i/p from cerebral cortex
• o/p from BG goes from thalamus back to cerebral
  cortex
• o/p also goes to spinal cord

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Habits and skills

• Background
• Basal ganglia
• Consists of 4 major nuclei
• Caudate nucleus
• Putamen
• Globus pallidus
• Subthalamic nucleus
• Striatum consists of caudate nucleus, putamen,
  and ventral striatum

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BG

• Coronal view of BG in relation to surrounding
  structures
• Medial view of BG note left side is anterior
  right side is posterior

27
Habits and skills

• Background (circuits in BG)
• There are several circuits connected to
  prefrontal regions of the cortex these include
• Dorsolateral prefrontal circuit
• Involved in executive function
• Lateral orbitofrontal circuit
• Plays a major role in mediating empathic,
  socially appropriate responses
• Anterior cingulate circuit
• Appears to play an important role in motivated
  behavior

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Habits and skills

• Background (diseases associated with BG deficits)
  
• Movement disorders associated with basal ganglia
• Parkinsons disease (described by Parkinson 1817)
• Hypokinetic disorder
• Impaired initiation of movement (akinesia)
• Reduced amplitude and velocity of movement
  (bradykinesia)
• Involuntary tremulous movement
• Lessened muscular power
• Increased muscle tone (rigidity)
• Shuffling gait

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Habits and skills

• Parkinsons disease (described by Parkinson 1817)
• Results from an insufficiency of a
  neurotransmitter (dopamine) in the substantia
  nigra
• It has been shown that px with PD have a
  deficiency in dopamine in the striatum, most
  particularly in the putamen
• in 1960s it was shown that injection of L-DOPA,
  the precursor of dopamine led to a reversal of
  symptoms temporarily (for about 5 years)
• Huntingtons disease
• Hyperkinetic disorder
• Excessive movements
• Heritable and results from a gene defect

30
Habits and skills

• Role of BG in learning and memory
• BG is involved in S-R association formation or
  the formation of habits or skills, and this form
  of memory is dissociable from declarative memory
• Animal lesion study (see Eichenbaum, 2002 for
  further information)
• This has been investigated in an 8-arm radial
  maze with different task requirements (e.g.,
  McDonald White, 1993)

31
Habits and skills

• Animal lesion study
• Win-shift maze
• maze is put in a room and the rat is permitted to
  encode stimuli around the room to provide spatial
  cues
• on every trial a food reward is placed at the end
  of the maze rat is released from centre of maze
  and is allowed to retrieve food
• optimal performance occurs if the rat enters each
  arm only once. This means the rat must have
  memory for the mazes that were previously entered

32
Habits and skills

• Role of BG in learning and memory
• Win-stay maze
• 8-arm radial maze used, but maze surrounded by a
  curtain, and lamps were used to illuminate 4
  randomly selected arms of the maze
• food was baited in the illuminated mazes only
  when an arm was entered for first time, the maze
  was rebaited after second time the light was
  turned off and no more food was provided
• task was to associate a particular stimulus
  (light) with food across all trials and it was
  expected that declarative memory was not
  required, but habit memory was required

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radial arm mazes

• Radial arm maze configurations to illustrate
  win-shift and win-stay procedures
• rewarded arm

34
Habits and skills

• Results
• Win-shift
• Rats with hippocampal damage made more errors
  than controls by visiting previously visited maze
  arms
• Rats with striatal damage were unimpaired
  compared to normal animals (controls)
• Win-stay
• Normal control rats learned strategy over several
  sessions
• Rats with hippocampal damage learned somewhat
  faster than controls
• Rats with striatal damage were badly impaired and
  were at about chance levels of performance even
  after extended practice

35
Habits and skills

• Conclusions
• Selective damage to the hippocampus impairs
  performance on a task requiring declarative
  memory
• Selective damage to the striatum interferes with
  habit learning

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Sequence learning

• Human research
• Further support for the dissociation between
  habit memory and declarative memory
• Sequence learning

37
Sequence learning

• Human research
• Evidence suggests that amnesics are unimpaired in
  manual sequence learning (Reber Squire (1998).
  Journal of Cognitive Neuroscience 10, 248-265
• This perceptual-motor habit was investigated in a
  serial response time (SRT) task paradigm
• SRT task. Participants are shown a visual cue in
  1 of 4 locations by pressing a key corresponding
  to the location of the cue
• Cues follow a repeating sequence of locations (n
  12 124313214234)

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Sequence learning

• Amnesics and controls and controls were given SRT
  training. Other unimpaired control groups
  (Memory) memorized the sequence of responses (see
  Table for details). All groups had their implicit
  and explicit memory tested
• The Memory control groups memorized the sequence
  of responses by watching the computer screen and
  attempting to memorize the sequence of responses

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Sequence learning
40
Sequence learning

• Results
• Amnesics and controls had decreasing SRT RTs to
  practiced SRT across trial blocks
• Next figure presents implicit memory performance
  by group
• Note amnesics and controls were the only groups
  to show implicit memory

41
Sequence learning

• Top panel. Open bars present RT for sequence S1
  (practiced by amn and con) open bars shaded bar
  presents RT for N1 (unpracticed)
• Bottom paneldifference between S1 and N1
  (measure of implicit memory

42
Sequence learning

• This Figure presents for each group explicit
  memory performance, assessed by recognition
  memory performance of 5 sequences (1 target and 5
  lures) on a scale from 0 to 100

43
Sequence learning

• Results
• Note amnesics showed little evidence of explicit
  memory, in comparison to other groups
• Memory controls (esp. young) showed explicit
  memory performance

44
Sequence Learning

• Filled squares amnesic
• Open square combined performance of young
  subjects
• Open triangle controls
• Open circle Mem old participants
• Note cross-over interaction

45
Sequence learning

• Conclusions
• Proposed that cross-over interaction shown in
  Figure 5 reflects encapsulation of implicit and
  explicit memory in different memory systems
• Explicit memory mediated by hippocampal/diencephal
  ic brain structures
• Implicit memory mediated by motor cortex,
  neostriatal, supplementary motor area

46
Sequence learning

• Human research (PD)
• Wilkinson 2009, Neuropsychologia, 47, 2564-2573
• Investigated implicit explicit memory in SRT
  task in PDs and controls
• Hypothesized that PDs would be impaired in their
  implicit memory for SRTs and would also be
  impaired in their explicit memory for explicitly
  presented SRTs

47
Sequence learning

• Human research (PD)
• Wilkinson 2009, Neuropsychologia, 47, 2564-2573
• Exp. 1 implicit SRT
• Sequence was presented probabilistically to
  introduce noise and decrease opportunities for
  explicit learning
• E.g., one group of Ps were shown
  3-1-4-3-2-4-2-1-3-4-1-2, 85 of the time and
  4-3-1-2-4-1-3-2-1-4-2-3, 15 of the time
• 10 blocks of trials each block with 120 trials of
  SRT task

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Sequence learning

• Human research (PD)
• Implicit sequence learning assessed by comparing
  difference between probable and improbable
  sequence Reaction time

49
Sequence learning

• PDs shown in back controls shown in white
• designates blocks in which difference between
  probable and improbable sequence is significant
  (p lt .05)
• Note evidence of implicit learning for controls
  stronger than for PDs

50
Sequence learning

• Human research (PD)
• Explicit sequence learning
• After final implicit SRT block presented,
  explicit sequence learning was tested
• Inclusion condition participants were presented
  a sequence of 5 cues from probable sequence and
  were instructed to recall the next correct
  response (Inclusion)
• Exclusion condition participants were presented
  sequence of 5 cues from probable sequence and
  were instructed to respond with the next cue that
  was inconsistent with the training sequence

51
Sequence learning

• Results show that for controls and PDs there was
  no significant difference between inclusion
  probable and baseline and between exclusion
  probable and baseline
• Hence no evidence of explicit memory for sequence

52
Sequence learning

• Human research (PD)
• Conclusion Wilkinson data suggest that PDs are
  impaired in probabilistic sequence learning
  relative to controls
• There is no evidence for explicit memory for
  either group
• Findings suggest that BG plays a role in implicit
  sequence learning
• Findings by Reber and Squire, which showed that
  amnesics were not impaired in sequence learning,
  suggest that a form of habit memory was not
  mediated by MTL

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Implicit memory- cognitive habits

• Human research Cognitive habits
• Traditionally the impairment in the basal ganglia
  was known to result in motor deficits based on
  observations of patients with PD and Huntingtons
  disease
• Aside PD affects dopaminergic input to the
  striatum Huntingtons disease affects cells in
  the striatum
• It now appears that BG is involved in acquisition
  of cognitive habits that involve the gradual
  formation of S-R associations

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Implicit memory- cognitive habits

• Human research
• Probabilistic classification learning
• Knowlton and her colleagues have studied px and
  their performance on the probabilistic
  classification task
• weather prediction task
• Participants are presented 1 to 3 of 4 cards and
  task was to predict sunshine or rain based on
  cues presented cards had complex geometric
  shapes
• Each card and card combination was
  probabilistically associated with 2 outcomes
• after making prediction participant was given the
  actual outcome (see next figure)

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Probabilistic classification learning

• Panel A. Probability of sunshine for individual
  cards
• Panel B. conjoint probabilities associated with
  various card combinations and example of trial
  series

56
Implicit memory- cognitive habits

• Human research
• Probabilistic classification learning
• Note task has been designed so that specific
  memory for outcomes associated with card
  combinations is not as useful, first because
  there are several card combinations, and second,
  because any given card combination may have an
  outcome of sunshine or rain associated with
  it
• More useful is a general sense of the
  relationship between cues and outcomes across
  trials

57
Implicit memory- cognitive habits

• Human research
• Probabilistic classification learning
• Results
• Controls
• Over 50 trials normal controls improved from pure
  guessing (50) correct to about 70 correct
  (highest performance possible)
• PD px did not show significant learning and
  performance was worse in px with more severe
  Parkinsonian symptoms (Knowlton, 1994, Science,
  273, 1399-1402)
• After training PD px and controls were given
  questions about the task and nature of the
  stimuli (declarative tasks) performance of the
  two groups did not differ
• Results from amnesics show an opposite
  dissociation unimpaired performance on the
  weather prediction task and impaired performance
  on the declarative memory task (Knowlton, 1994,
  Learning and Memory 1, 106-120 Reber, 1996,
  Behavioral Neuroscience, 110, 859-869)

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Implicit memory- cognitive habits

• Human research
• Interactions between implicit and declarative
  memory
• When task conditions favor implicit learning
  medial temporal activity decreases as striatal
  activity increases (Foerde, 2006 Foerde, 2007)

59
Implicit memory- cognitive habits

• Human research
• Foerde et al. (2006) PNAS, 103, 11778-11783
• This experiment investigated the hypothesis that
  the declarative and habit memory systems compete
  with each other in tasks in which both systems
  are involved
• This raises the possibility that it might be
  possible to modulate the operation of these
  systems by introducing a secondary task
• Previous research has shown that performing a
  secondary task that requires working memory
  should decrease declarative memory and thereby
  bias (increase) the operation of the habit memory
  system

60
Implicit memory- cognitive habits

• Human research
• Prediction then is that dividing attention should
  affect the way in which a task is performed
• Overview of procedure and design (see also next
  figure). Participants were given weather
  prediction training (PCT task) for two different
  cities based on presentation of two sets of cues
  half the cues for a given city were trained under
  single task conditions (ST) and half the cues for
  that city were trained under dual task conditions
  (DT)
• Secondary task was tone counting task in which
  participants counted the number of high tones

61
Implicit memory- cognitive habits

• Human research
• After training participants were given a probe
  run in which participants were shown cues that
  had been trained under ST or DT conditions and
  were required to predict sun or rain (done in
  fMRI) no tone task administered here
• After scanner, participants were given test of
  declarative memory which required flexible
  knowledge about task (e.g., participants shown
  all 4 single cues and asked to select cue most
  likely to be associated with sun task repeated
  for two-cue combinations, and 3-cue combinations)

62
Foerde procedure

• Tone counting
• Train on weather prediction (single, dual)
• In DT condition report number of high tones
• Baseline button push condition
• Probe run predict weather

63
Implicit memory- cognitive habits

• Results
• Behavioral results shown in next figure showed
  that PCT performance during training was higher
  after run 2 than run 1 and marginally higher in
  ST than DT (See a)
• Probe task (see b) no difference between ST and
  DT in weather prediction performance in probe
  task
• Cue selection (test of declarative memory, see c)
  participants were significantly better in the ST
  than DT condition suggesting that a more flexible
  memory representation was obtained

64

• Fig a. PCT performance during training
• Fig b. PCT performance during probe task
• Fig c. declarative memory performance

65
Implicit memory- cognitive habits

• Results
• fMRI results in next figure (see b) showed that
  probe accuracy was correlated with right
  hippocampus activity in ST but not DT condition
• Figure d showed that probe accuracy was
  correlated with left putamen activity in DT but
  not in ST condition
• Recall hippocampus associated with declarative
  memory
• Putamen is part of BG, which is implicated in
  habit memory

66
fMRI results
67
Implicit memory

• Conclusions
• Memory for PCT can be either MTL or striatal
• Declarative memory depends on executive
  functions, but habit learning does not appear to
  depend upon it (recall secondary task effects)
• Although PCT performance can be supported by MTL
  or striatal systems, the type of memory system
  mediating performance affects flexibility of
  memory (recall declarative memory test)

68
Implicit memory

• Conclusions
• In disease states involving dysfunction of the BG
  medial temporal lobe may be present when normally
  striatum activity would dominate (Moody, 2004)