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 Parkinson’s disease, which is associated with impaired basal ganglia functioning

Implicit memory implicit memory explicit 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

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

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

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

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

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

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

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

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

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

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 not consciously aware of the rules

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__)

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)

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

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

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

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

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 striatum and basal ganglia

[Squire (1987): Declarative vs. procedural memory] Implicit Memory Explicit Memory Priming Nonassociative Learning Neocortex Reflex Pathways Facts (Semantic Memory) Events (Episodic Memory) Skills and Habits Simple Classical Conditioning Striatum Reed p.138 Going into the different memory systems Medial Temporal Lobe Emotional Response Skeletal Musculature Amygdala Cerebellum Squire and Knowlton (1994) [Squire (1987): Declarative vs. procedural memory]

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

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

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

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

BG

BG Bottom figure shows coronal view of BG in relation to surrounding structures Top figure shows medial view of BG: note left side is anterior; right side is posterior

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

Habits and skills Background (diseases associated with BG deficits) Movement disorders associated with basal ganglia Parkinson’s 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

Habits and skills Parkinson’s disease Huntington’s disease Results from an insufficiency of a neurotransmitter (dopamine) in the substantia nigra It has been shown that px with Parkinson’s disease (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) Huntington’s disease Hyperkinetic disorder Excessive movements Heritable and results from a gene defect

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)

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

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

radial arm mazes Radial arm maze configurations to illustrate win-shift and win-stay procedures; + = rewarded arm

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

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

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

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)

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

Sequence learning

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

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 panel—difference between S1 and N1 (measure of implicit memory

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

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

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

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/diencephalic brain structures Implicit memory mediated by motor cortex, neostriatal, supplementary motor area

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

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

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

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

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

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

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

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 Huntington’s disease Aside PD affects dopaminergic input to the striatum; Huntington’s 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

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)

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

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

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)

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)

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

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

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)

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

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

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

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

fMRI results

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)

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)