Neuropsychology of Memory
• Types of memory problems
– a pure amnesia is relatively rare
– memory problems commonly occur after a
traumatic brain injury (TBI)
TBI results in brain damage of two sorts:
lesions
twisting and shearing of brain structures and
damage from bony protuberances of brain,
particularly of the temporal lobes
Neuropsychology of Memory
• Memory problems following TBI
– post-traumatic amnesia
– retrograde amnesia
– anterograde amnesia
Neuropsychology of Memory
• Memory problems following TBI
– post-traumatic amnesia
after severe TBI, individuals typically lose
consciousness
after they begin to regain consciousness, there is
often a gradual recovery during which patients
have difficulty keeping tracking of and
remembering ongoing events, though there may
be islands of lucidity and memory
Neuropsychology of Memory
• Memory problems following TBI
– retrograde amnesia
refers to difficulty remembering events that
occurred prior to injury
the duration of amnesia varies but can extend
back for several years
duration of retrograde amnesia typically shrinks as
time passes
Neuropsychology of Memory
• retrograde amnesia
– duration of retrograde amnesia typically shrinks
as time passes
e.g., Russell (1959) described case of TBI as a
result of a motorcycle accident
1 week post accident patient had lost 11 years of
memory extending back from injury
2 weeks post accident patient had last 2 years of
memory
about 10 weeks post injury memories of the last
two years gradually returned
Neuropsychology of Memory
• Memory problems following TBI
• retrograde amnesia
– this pattern of results suggests that retrograde
amnesia is a retrieval problem
– the pattern of damage/recovery -- from most
distant to most recent -- has been argued by
some to reflect a failure of consolidation (Ribot’s
Law)
Neuropsychology of Memory
• Memory problems following TBI
• retrograde amnesia
– formal testing of amnesics using famous
faces/famous events has shown that there
appears to be recall and recognition for old
faces/events
Neuropsychology of Memory
• retrograde amnesia
– Butters & Cermak (1986) reported a case study
of an eminent scientist (born 1914) who had
written his autobiography only two years prior to
becoming amnesic
– tested him by asking him questions all drawn
from his autobiography
Neuropsychology of Memory
Percent recall
Recall of information from PZ autobiography
80
70
60
50
40
30
20
10
0
Recall
19161930
19301940
19401950
19501960
19601970
19701980
Neuropsychology of Memory
• retrograde amnesia
– the pattern of results in some individuals appear to
depend upon the nature of the retrieval cue presented
– Warrington and McCarthy (1988) showed that an amnesic
patient was impaired when shown faces of famous people
and asked to recall them
– however, performance was normal when tested using
recognition procedures
Neuropsychology of Memory
• retrograde amnesia (RA)
– pattern of memory gradient varies across patients (See
Moscovitch et al. 2006)
– If lesion restricted to hippocampus, RA extends back a
few years only
– When lesion includes entire hippocampal formation or
extends to adjacent regions, severe ungraded RA
(ungraded means that memory loss is equivalent at all
time periods since acquisition); some labs have reported
graded retroactive amnesia (recent memories are poorer
than more remote memories)
Neuropsychology of Memory
• Memory problems following TBI
– anterograde amnesia
refers to problems of learning new facts
although sometimes amnesia is specific to
learning of verbal material (following LHD) or
visuo-spatial material (following RHD) amnesia
usually affects learning of many types of new
information
Neuropsychology of Memory
• Amnesic syndrome
– dense form of memory deficit (as assessed by
standardized testing)
– relatively spared performance in other domains
Neuropsychology of Memory
• Causes of amnesia
Korsakoff’s syndrome: drinking too much, eating
too little, resulting in a thiamine deficiency and
brain damage
damage to brain following viral infection (e.g., viral
encephalitis)
lesion to critical brain regions -- e.g., HM
anoxia following heart attack, suicide attempt, etc.
Neuropsychology of Memory
• Korsakoff’s syndrome
– History
1881, a neurologist Carl Wernicke described a
syndrome involving ataxia, oculomotor problems (gaze
palsies and nystagmus), peripheral neuropathy, and
confusion. This condition came to be known as
Wernicke's encephalopathy
Korsakoff identified several patients with confusion,
confabulation, sensory loss (especially of the feet),
and anterograde amnesia
Neuropsychology of Memory
• Korsakoff’s syndrome
– Terminology
Ataxia– problems of muscular coordination; e.g.,
people ‘duck walk’, feet apart, stiff-legged
 oculomotor problems (gaze palsies and nystagmus);
abnormal eye movements—palsy = paralysis;
nystagmus = involuntary rapid eye movements
 peripheral neuropathy = functional disturbance of
peripheral nervous system
Neuropsychology of Memory
• Korsakoff’s syndrome
– History
1901 Bonhoffer realized Korsakoff’s patients had
passed through the Wernicke's encephalopathy stage
today syndrome is called alcoholic Korsakoff
syndrome. There are seven primary defining features
of this disease:
Neuropsychology of Memory
• Defining features of alcoholic Korsakoff
syndrome
a. a retrograde amnesia with a temporal gradient
(i.e., better preserved memories from the remote
than from the more recent past)
b. anterograde amnesia, meaning a nearly
complete inability to learn new information from
the time of the disease onset onward.
Neuropsychology of Memory
c. confabulation, which is a tendency to "fill in
the gaps" of one's memories with plausible madeup stories.
confabulations are rare among chronic Korsakoff
patients who've had the disease for more than 5
years. Patients in the chronic stage are more likely
to say "I don't know" or remain silent when faced
with memory failures rather than to invent stories.
Neuropsychology of Memory
d. generally preserved IQ, including a normal
digit span.
e. personality changes, the most common of
which is apathy, passivity and indifference
inability to formulate and follow through a series of
plans
f. lack of insight into their condition.
How can someone with a shattered memory
remember that he has become unable to
remember?
Neuropsychology of Memory
– Korsakoff’s syndrome
worst impairments are on episodic memory tests,
including list learning of words, figures, or faces,
paragraph recall.
relatively preserved semantic memory, including
normal verbal fluency, vocabulary, rules of syntax,
and basic arithmetic operations
intact sensori-motor memory (mirror tracing,
mirror reading, pursuit rotor)
intact performance on implicit memory tests
Neuropsychology of Memory
– Neuropathology of Korsakoff’s syndrome
most sources attribute the amnesia to combined
lesions in two diencephalic structures: regions of
the thalamus and the mammillary bodies of the
hypothalamus
Neuropsychology of Memory
– HM, Hippocampal man
– prototype of amnesia attributable to hippocampal
damage
bilateral mesial temporal lobe resection extending
8 cm. back from the temporal tips, including the
uncus and amygdala, and destroying the anterior
two-thirds of the hippocampus and hippocampal
gyrus, for the treatment of intractable epilepsy in
1954.
surgery led to a permanent, severe anterograde
amnesia, limited retrograde amnesia, and normal
intelligence.
Neuropsychology of Memory
• HM, Hippocampal man
• Perceptual, motor, and cognitive functioning
– IQ above average; language function intact,
speech fluency slightly impaired; spelling poor
– Appreciation of puns and linguistic ambiguities
– Difficulty with some spatial tasks (e.g., could not
use spatial floor plan to navigate through a novel
building, but could reproduce a floor plan of
family home)
Neuropsychology of Memory
• HM, Hippocampal man
• Memory
– Almost no capacity for new learning regardless of
materials (short stories, word lists, pictures, etc.)
– But there are certain tasks requiring memory that
are intact in H.M.
– Mirror drawing (covered?)
Neuropsychology of Memory
•
Multiple memory systems perspective
• HM also has a retrograde amnesia; that is, he
forgets events that occurred prior to surgery
• His retrograde amnesia is temporally graded:
The closer the event to surgery the less likely
he is able to recall it
• This finding suggests that the medial temporal
lobes are not always required to retrieve
memories (One possibility is that some process
occurs that makes it possible to retrieve
information that does not rely on medial
temporal lobes)
Neuropsychology of Memory
•
Multiple memory systems perspective
• In 1962 Milner and colleagues showed that HM
improved on tasks requiring skilled movements
• HM’s improvement was comparable to controls
• Skill was called ‘mirror tracing’ because it
requires participants to draw the outline of a
star while looking at the reflection of his hand
and the star on the mirror
• HM from had no conscious recollection of
having done this task in the past
• This is now viewed as a form of non-declarative
or implicit memory tasks
H.M.’s skilled learning performance
Encoding and Retrieval from longterm memory (LTM)
•
Multiple memory systems perspective
• Other forms of implicit memory include priming
effects that were reported by Warrington &
Weiskrantz (1968)
• In this study amnesics shown list of words (e.g.,
absent); at test participants were given word
stem completion task (e.g., abs_____), and
instructed to complete with first word that
comes to mind
• Results showed that amnesics (and controls)
were more likely to complete word stems with
previously studied words
Neuropsychology of Memory
• HM, Hippocampal man
• Gollins partial picture task
– Task involves recognition of fragmented line
drawings of 20 objects
– 5 cards for each object with each card showing
more and more fragments of the completed
drawings
– Participants are shown the 20 most difficult
cards, then the next-most-difficult cards etc.
Neuropsychology of Memory
• HM, Hippocampal man
• Gollins partial picture task
– Task involves recognition of fragmented line
drawings of 20 objects
– 5 cards for each object with each card showing
more and more fragments of the completed
drawings as shown in Figure
– Participants are shown the 20 most difficult
cards, then the next-most-difficult cards etc.
Neuropsychology of Memory
• HM, Hippocampal man
• Gollins partial picture task (Warrington &
Weiskrantz, 1968 Nature, 217, 972-974
– HM and normal controls performed this task, and then
after an hour of intervening activity performed the task
again
– Results shown in next figure show that H.M. and controls
made fewer errors on immediate tests as figures became
more complete and when tested after a 1 hour delay
there was memory retention
– Conclusion. Perceptual memory is intact in H.M.;
perceptual memory does not appear to be mediated by
medial temporal structures
Neuropsychology of Memory
• HM, Hippocampal man
• Dot pattern study (Gabrieli, 1990,
Neuropsychologia, 28, 417-427)
– H.M. and controls were shown a series of 5 dots arranged
in a unique pattern
– Baseline draw. Participants (Ps) were instructed to draw
any pattern they wanted (to control for pre-existing
biases)
– Experiment. Ps were shown a target pattern & copied that
pattern on dots
– After 6 hour delay, Ps were shown dots and were
instructed to draw on dots any pattern they wanted
Neuropsychology of Memory
• HM, Hippocampal man
• Dot pattern study (Gabrieli, 1990,
Neuropsychologia, 28, 417-427)
– H.M. and controls were shown a series of 5 dots arranged
in a unique pattern
– Baseline draw. Participants (Ps) were instructed to draw
any pattern they wanted (to control for pre-existing
biases)
– Experiment. Ps were shown a target pattern & copied that
pattern on dots
– After 6 hour delay, Ps were shown dots and were
instructed to draw on dots any pattern they wanted
Neuropsychology of Memory
• HM, Hippocampal man
• Dot pattern study (Gabrieli, 1990,
Neuropsychologia, 28, 417-427)
– Implicit memory – percentage of target figures drawn that
were identical to the copied target pattern (dots drawn in
the baseline condition were not scored)
– Explicit memory – Recognition memory – Ps were shown
4 dot patterns that drawn on the dots and selected the dot
pattern that had been copied
Dot pattern
• Top figure shows dot
pattern and target
stimuli
• Left panel of bottom
figure shows explicit
performance and right
panel shows implicit
performance of H.M.
and Controls
Neuropsychology of Memory
• HM, Hippocampal man
• Dot pattern study (Gabrieli, 1990,
Neuropsychologia, 28, 417-427)
– Implicit memory – dot pattern priming equivalent
for H.M. and controls
– Explicit memory – H.M. impaired on recognition
memory test compared to controls
Neuropsychology of Memory
• HM, Hippocampal man
• Dot pattern study (Gabrieli, 1990,
Neuropsychologia, 28, 417-427)
– Gabrieli and colleagues argued that this finding
cannot be attributable to activation of a preexisting memory (e.g., a semantic
representation)
– Proposed that it is attributable to a type of
perceptual priming, perhaps of a non-semantic
structural description of a pattern
Artificial grammar learning
• Amnesics can have intact capacity for
learning certain cognitive skills
• E.g., artificial grammar such as shown in
Figure
• Participants were shown novel letter strings
one at a time and were asked to classify the
strings as grammatical or nongrammatical
Artificial grammar learning
• Participants were then tested to determine
whether they could distinguish between
grammatical and nongrammatical letter
strings
• Results showed that amnesics and normal
controls could classify correctly about twothirds of the letter strings
•
Artificial Grammar
• Top panel shows an
example of an artificial
grammar
• Bottom panel shows
examples of
grammatical and
nongrammatical strings
• Knowlton et al. (1992).
Psychological Science,
3, 172-179
Artificial grammar learning
• Conclusions
– Declarative memory and MTL not required to
encode in memory those processes associated
with the encoding into memory artificial
grammars
Recognition memory: dualprocess models
• Several lines of evidence support the idea that two
distinct processes (recollection, familiarity)
mediated by different brain regions underlie
recognition memory
– Example. See face of a person – you recognize the
person as familiar but are unable to recollect anything
about the person, when or where you met that person
– Recollection – you recognize that person and can
recollect details about that person
–
Recognition memory: dualprocess models
• Evidence for dual process models (behavioral)
– Speeded recognition tests have shown that item
recognition tests (was this item studied) are made more
quickly than associative recognition tests (when or where
was this item studied)
– Analysis of confidence intervals has shown that when hit
rate is plotted against false alarm rate, curves are
different for associative recognition (linear) versus item
recognition (curvilinear)
– also two different parameters are required to account for
shape of curve suggesting that two distinctly different
cognitive processes are operating
Recognition memory: dualprocess models
• Evidence for dual process models (behavioral)
– Yonelinas has proposed that familiarity reflects the
strength of the memory trace (an is quantitative)
– Recollection reflects retrieval of qualitative, contextual
information
Recognition memory: dualprocess models
• Evidence for dual process models (lesion)
– Amnesics are much more impaired on associative
recognition tests than on item recognition tests
– Analysis of confidence intervals has shown that only 1
type of process (curvilinear) is required to account for
recognition performance
– See Yonelinas (2002) for further details
Neuropsychology of Memory
• Functional characteristics of amnesia
– working memory is intact
– semantic memory is spared (controversial)
– episodic memory is impaired
– procedural memory is intact
Neuropsychology of Memory
• Theoretical implications of amnesia
– provides evidence for STM versus LTM
distinction
– supports the notion that there are different
systems mediating explicit (episodic) and implicit
(procedural memory)
– may indicate that semantic and episodic memory
can be fractionated
– may provide insight into nature of consciousness
Neuropsychology of Memory
• Memory and Consciousness
– Tulving has proposed that different memory
systems have associated with them different
levels of consciousness
noetic -- awareness
episodic memory -- autonoetic, self awareness
semantic memory -- noetic, aware of the
information, but not aware of event
procedural memory -- anoetic no conscious
awareness
Neuropsychology of Memory
Episodic
Autonoetic
Semantic
Noetic
Procedural
Anoetic
Neuropsychology of Declarative
Memory
Brain regions mediating declarative memory
– what is common appears to be the circuit linking
regions in the temporal lobes, the hippocampus,
the mammiliary bodies and regions of the
thalamus (note: review Korsakoff’s)
– Next slides will review this in more detail
– See Eichenbaum (2002). The cognitive
neuroscience of memory and Moscovitch et al.
(2005). 207, 35-66. Journal of Anatomy
Neuropsychology of Declarative
Memory
• Medial temporal lobe
structures viewed
from the side
(saggital section)
• Moscovitch et al.
(2005)
Recollective and familiarity
memory systems
Neuropsychology of Declarative
Memory
Brain regions mediating declarative memory
– 3 major component brain regions involved in
declarative memory
– Cerebral cortex, parahippocampal region
– Hippocampus
– Parahippocampal region consists of perirhinal
cortex, parahippocampal cortex, and entorhinal
cortex
Neuropsychology of Declarative
Memory
Brain regions mediating declarative memory: flow
of information
– Bidirectional connections between cortex and
parahippocampal region
– Bidirectional connections between
parahippocampal region and hippocampus
– Highly processed information comes from
association areas of the cortex
– Info further processed by the parahippocampal
region and hippocampus before being projected
back to regions that provided the information
Neuropsychology of Declarative
Memory
Brain regions mediating declarative memory: flow
of information
– Aside: Background info about how sensory and
motor processing makes its way to association
areas
– Sensory info ->primary cortical areas (e.g., visual
cortex) -> secondary and tertiary unimodal
sensory regions -> multimodal association areas
located in temporal, parietal, and frontal lobes as
well as in cingulate area
Neuropsychology of Declarative
Memory
Brain regions mediating declarative memory: flow
of information
– Aside: Background info about how sensory and
motor processing makes its way to association
areas
– Motor ->primary cortical area (e.g., motor cortex)
ultimately projects to prefrontal and cingulate
areas
Neuropsychology of Declarative
Memory
Brain regions mediating declarative memory: flow
of information
– Association areas of the temporal -- object identification
using info from multiple sensory modalities
– Association areas parietal lobes – process spatial info
about visual and other sensory inputs
– Prefrontal and cingulate areas – process info about the
significance of stimuli, rules of tasks, and plans for tasks
– Each of these association areas provides input to the
parahippocampal region
Neuropsychology of Declarative
Memory
Parahippocampal region
– Consists of 3 distinct areas
 Perirhinal cortex
 Parahippocampal cortex
 Entorhinal cortex
– Inputs to parahippocampal region come from virtually
every higher-order association area
– Perirhinal and parahippocampal cortices project to the
parts of the entorhinal cortex
Neuropsychology of Declarative
Memory
Parahippocampal region
– Anterior cortical inputs from prefrontal cortex and anterior
cingulate project to the perirhinal cortex and entorhinal
cortex
– Posterior cortical inputs (temporal and parietal regions)
project to the perirhinal and parahippocampal cortices
Neuropsychology of Declarative
Memory
Hippocampus
– Consists of several subfields including the
CA1, CA3
Dentate gyrus
Subiculum
– Connected bidirectionally to the fornix, the
prefrontal cortex and the parahippocampal region
– Also connected to regions of the thalamus
(anterior)
Neuropsychology of Declarative
Memory
Linking brain and memory
– Distinct memory systems reviewed in this lecture include
– Recollective memory – conscious recollection of
experiences (autonoetic)
– Familiarity memory – memory for stimuli rather than for
events; stimuli are recognized as familiar wthout being
placed in spatial/temporal context (noetic)
– Semantic memory – memory for noncontextual content of
experience or knowledge about the world (facts,
concepts, word meanings, objects, tools etc.)
– It includes knowledge about ourselves (DOB, where we
lived, our jobs, facts about family etc.
Neuropsychology of Declarative
Memory
Linking brain and memory
– Recollective memory
Relies on hippocampus, mamiliary bodies, and
anterior thalamic nuclei via the fornix (see solid lines in
Figure)
– Familiarity memory
Relies on circuit involving perirhinal cortex and medial
dorsal thalamus
Damage to this circuit will impair recognition of even
single items (see dotted lines in Figure)
– Parahippocampal cortex may mediate place
memory
Recollective and familiarity
memory systems
Neuropsychology of Declarative
Memory
Linking brain and memory
– Semantic memory
Does not depend on medial temporal lobe and
diencephalic structures
Semantic memory relies on a network of anterior and
posterior neocortical structures
Precise structures depend upon attributes of memory
(see next slide—different colors represent site of
different memory attributes – (e.g., form, motion)
Brain regions include lateral and anterior temporal
lobe regions and the lateral inferior prefrontal cortex
particularly in the left hemisphere (see next slide)
Martin & Chao (2001). Current Opinion in Neurobiology
(a)
Ventral brain regions from occipital to temporal lobes—represent color and shape
properties (fusiform gyrus)
(b) Left lateral areas– motor areas in prefrontal cortex and parietal areas represent
manipulation of objects; posterior temporal lobes represent motion properties of objects
Semantic Memory