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Schmolck Et Al 2002 Evaluation Essay

SCOVILLE & MILNER (1957)
A CASE STUDY: THE MEMORY OF H.M.

In Unit 1, the Cognitive Approach requires that you understand case studies and the case of H.M. in particular. H.M. was studied for his entire adult life after his operation. The 1957 case study cited above was simply the first of many carried out by Brenda Milner and her former-student, Suzanne Corkin.
This casestudy was carried out by William Scoville (left) and Brenda Milner (below left) in the 1950s. It was a key piece of research that established that memory is linked to the hippocampus and composed of different functions.

This research is significant for students in other ways:
  • It shows how scientific research proceeds, because before this case study, psychologists assumed memory was a single function that occurred throughout the brain. This study demonstrated that memory consists of different functions linked to different parts of the brain.
  • It illustrates the use of an instrumental case studyto study something that cannot be manipulated in a lab experiment
  • However, it illustrates the generalisability problems in case studies, because H.M. was a one-off case

WHO WAS H.M.?

Henry Gustav Molaison has been called the most important patient in the history of brain science. Henry suffered from epilepsy caused by a head injury when he was seven. As he grew up, his seizures got worse, until surgery was his only hope for relief.

The pioneering brain surgeon William Beecher Scoville proposed to remove the part of the brain that was causing the seizures. Henry agreed to the operation. In 1953, when Henry was 27, Scoville performed bilateral medial temporal lobe resection. This involved removing part of Henry’s temporal lobe, including parts of the hippocampus and amygdala.
Resection is still used today to treat epilepsy, but with the aid of lasers and detailed brain scans. Scoville didn't have these tools and wasn't even aware what the hippocampus did. Modern patients don't suffer the side-effects that H.M. did.
When Henry recovered from the surgery, he suffered from severe amnesia. He could remember his childhood: he knew his name and family and could remember the stock market crash of 1929. However, he struggled to remember the years leading up to the surgery and had gaps in his memory of the 11 years before.

Even more importantly, Henry had severe anterograde amnesia. He lost the ability to form new memories and forgot everything that happened to him in a matter of seconds.

This is how he described his condition:
like waking from a dream… every day is alone in itself - Henry Molaison
When it became clear how severe the side-effects of the surgery were, a young researcher named Brenda Milner conducted a case study on Henry Molaison and compared her findings with Dr Scoville's medical procedures and published the findings in 1957. She protected Henry's identity by referring to him as "H.M."

The case study caused a sensation and is one of the most widely-cited psychological studies ever. It changed our understanding of memory and the brain.

Milner carried on testing H.M. and published the results between 1962 and 1972, demonstrating the existence of procedural memory. Meanwhile, H.M. had become a full-time research participant, under the supervision of Suzanne Corkin at MIT, who carried on publishing studies (and, in 2013, a book about H.M. called Permanent Present Tense).

H.M. died in 2008, at the age of 82. His much-studied brain was removed and scanned using MRI. It was then sliced into 2401 pieces, each just 70 micrometres (millionths of a metre) thick, and turned into slides that would help researchers to map the brain.

After his death, H.M.'s identity was revealed to the world. He always supported the research he took part in (when it was explained to him). On one occasion he joked with Prof. Corkin:
It's a funny thing – you just live and learn. I'm living and you're learning - Henry Molaison
Fantastic animated summary of H.M.'s condition and Brenda Milner's research

THE H.M. CASE STUDIES
APRC

Aim

To investigate the extent and nature of H.M.'s memory deficits and how they relate to his brain damage. In particular, Milner (and later, Corkin) investigated the structure of memory as revealed in H.M.'s behaviour and the function of brain structures like the hippocampus.

Sample

One adult male, H.M., aged 27 at the start of the first case study. H.M. suffered from both retrograde amnesia (loss of memories from before his brain operation) and anterograde amnesia (loss of memories after his brain operation).
In fact, in Scoville & Milner's original study, 9 of Scoville's patients were described. However, since they suffered from disorders like schizophrenia, the resection didn't remove their symptoms. H.M. was the only one with "clean" amnesia - memory loss but no other mental problems.
Procedure

Brenda Milner's early tests were simple recall tasks, testing H.M.'s ability to recall events from his childhood, from his adult life before the operation and from his experiences after the operation. She also tested his short and long term memory recall. Finally, she tested his other cognitive faculties, like IQ, perception and general knowledge.
Other tests were carried out on H.M.. For example, the effect of reinforcement and punishment was investigated, to see if mild electric shocks would help H.M. to remember correct answers. Later, under the direction of Suzanne Corkin, brain scanning technology was used to improve our understanding of H.M.'s condition.
Results

H.M. forgot all new experiences after about 30 seconds; however he remembered a lot of information from before his sixteenth birthday. His personality was consistent, he had good language skills and an above-average IQ. His perception was normal, except for his ability to identify smell, which was very poor.

H.M.loved to describe clear memories of his childhood, over and over, though he lacked a context for them (like how long ago they happened). The face he saw in the mirror surprised himself. Every time H.M. met Milner (and later, Corkin), he introduced himself as if they had never met before, and told his stories again.

H.M. had a knowledge of past events (the Wall Street Crash, World War II). H.M. could not explain where he lived, who cared for him, what he ate for his last meal, what year it was, who the president was, or even how old he was.  In 1982, he failed to recognize a picture
of himself that had been taken on his 40th birthday in 1966.

However, he did acquire some knowledge from after his operation: he knew what
an astronaut was, that someone named Kennedy was assassinated and he learned what rock
music was. He learned how to play tennis, although he could not remember being taught the skills and denied that he knew how when asked.
Attempts to test punishment with electric shocks had to be abandoned. H.M. possessed huge tolerance for electric shocks, barely noticing shocks that normal people found quite painful. He also seemed to have difficulty noticing feelings of tiredness and hunger.

Conclusions

Milner's qualitative data shows a clear difference between short term and long term memory. They suggest that the hippocampus plays a vital role in transforming short term memories into long term memories, because this was something H.M. (whose hippocampus had been removed in the operation) couldn't do.
H.M.'s poor ability to identify smell may be linked to the fact that the olfactory bulb - which processes smell - is located close to the hippocampus. H.M.'s poor response to pain and confusion over hunger and tiredness probably links to the damage to his amygdala, which also explains his calm response to the situation he found himself in.
Milner's quantitative data and the later qualitative data suggests a more complex structure for memory.

H.M. did not improve at the maze task because, when he figured out the correct route through the maze, he immediately forgot it. However, he got better at the star task, despite forgetting his previous attempts. Later in life, he learned to play tennis.  This suggests H.M. remembered skills even if he forgot events.

H.M. also remembered some items of general knowledge (the moon landings, the Kennedy assassination), even though he couldn't remember the events taking place.

Milner termed this sort of memory "unconscious memory", but Eron Tulving later termed it procedural memory (skills) and semantic memory (general knowledge).
Milner also tested H.M. with maze tasks. H.M. attempted to trace the correct route through the maze with his finger. Milner then tested him over and over with the same maze to see if H.M. would remember the route, even if he didn't remember having attempted the task before.
In the 1962 case study, Milner asked H.M. to copy a five-pointed star by drawing between the lines of a template. However, H.M. could only see the reflection of the star and his hand in a memory. This made the task difficult. As with the maze task, Milner asked H.M. to re-attempt the task many times, to see if he grew more skilled at the procedure even though he didn't remember doing it before.
Over 252 attempts, H.M. never showed any improvement in the maze task.

However, H.M.did show improvement in the star-tracing task, making fewer mistakes on each attempt. He started with 30 errors, dropping to 20 on his second attempt and 10 by his seventh. Moreover, he kept these skills from one day to the next, getting better and better at it: on Day 2 he started making only 25 mistakes, immediately dropping to fewer than 10; by Day 3, he was making fewer than 5 mistakes each time.

EVALUATING THE H.M. CASE STUDIES AO3
GRAVE

Generalisability

Scoville & Milner reviewed 9 patients who had undergone resection surgery, but the others were sufferers of schizophrenia and depression whose symptoms interfered with memory testing. H.M. was unusual in that he suffered from "clean" amnesia - his memory loss was his only problem. This makes him much more representative of ordinary people.

On the other hand, H.M. was a "one-off" - a unique case. Scoville never performed this surgery again and modern resection surgery is accurate enough to avoid the sort of brain damage H.M. suffered. This means we can never be sure just how "normal" H.M. really was. Because no one expected the resection to cause memory loss, no one tested H.M.'s memory before the operation.
Reliability

Milner used tried-and-tested memory tests and puzzles. Most of these had been designed by other memory researchers and many of them were replicated on H.M. by later researchers like Suzanne Corkin. They all showed consistent results with H.M. - a great example of standardised procedures and test-retest reliability.
In fact, H.M.'s condition made him a great test subject. Since he never remembered having done the tests before, he never got bored of them and tackled them enthusiastically every time.
On the other hand, the case study itself is hard to replicate. Now that H.M. is dead, there may well never be a patient like him again.
Application

The application of H.M.'s case studies for psychology has been huge. Before H.M., psychologists thought that memory was a single function that took place all across the brain. After H.M., it became clear there are different memory functions that take place in different parts of the brain.
By revealing the importance of brain structures like the hippocampus, H.M.'s case studies led to safer and more successful brain surgery techniques.

However, some critics claim that H.M.'s case, being so famous, has led to too much attention being paid to the hippocampus and not enough to other regions of the brain linked to memory. Vann & Aggleton (2004) report the case of B.J. who had a snooker cue forced up his nose, damaging the base of his brain and causing amnesia, although his hippocampus was undamaged.
Validity

Brenda Milner visited H.M. at his family home and tested him there. Although her memory tests were quite artificial, she also made observations about H.M.'s behaviour and habits - such as his watching old movies on TV without remembering having seen them before - which backed up the test results.

Later, H.M. went to be cared for by Suzannne Corkin's team at Massachusetts Institute of Technology (MIT). This might have been a less natural environment for H.M., but, given his condition, he never noticed. In effect, all environments became strange for H.M., who couldn't even recognise himself in the mirror, let alone realise he was living in a strange place.

The strength of H.M. as a case study is the validity of his condition: H.M. suffered from "pure" or "clean" amnesia with few other symptoms and was willing to work with researchers to understand the brain.
Ethics

H.M. consented to his surgery in 1953. No one warned him about the memory side-effects because no one understood the function of the hippocampus at that time.

H.M. continued to consent to taking part in research for the rest of his life - every time it was explained to him, which was many times, daily, for over 50 years!

Critics point out that H.M. was in no position to withhold his consent - he was entirely dependent on the researchers for his care and did not understand his situation. It could be argued that H.M. was a "human guinea pig" whose sad condition was exploited by researchers.

However, the research followed the principle of Respect. Up until his death, H.M.'s real identity was kept secret to protect his privacy. Only 100 researchers were ever granted access to H.M., out of respect for his dignity. What's more, the research could be justified in terms of Social Responsibility.

Suzanne Corkin reflects on H.M.'s life in this way:
[H.M. was] an engaging, docile man, with a keen sense of humour, who knew he had a poor memory and accepted his fate … and hoped that research into his condition would help others live better lives - Suzanne Corkin
H.M. himself reflected on his brain damage and the research on him like this:
What [Dr Scoville] learned about me helped others, and I’m glad about that - Henry Molaison

EXEMPLAR ESSAY
AN 8-MARK ESSAY ON H.M.'S CASE STUDIES

Assess how case studies of H.M. have contributed to our understanding of memory. (8 marks)
  • A 8-mark “evaluate” question awards 4 marks for AO1 (Describe) and 4 marks for AO3 (Evaluate). You need a conclusion for top band (7-8) marks.

Description
H.M. suffered from life-threatening epilepsy and in 1953 Dr Scoville cured this by removing H.M.'s hippocampus.
As a result, H.M. suffered from retrograde amnesia (remembering only his life before age 16 with clarity) and anterograde amnesia (forgetting all his new experiences within 30 seconds).
H.M. was visited by Brenda Milner who conducted tests on him like the star-drawing test and published several case studies on his condition in the '50s and '60s.
Milner showed that, without a hippocampus, H.M. could not create new episodic memories but he could still learn semantic memories (like the moon landings) and procedural memories (like the star test or playing tennis).

Evaluation
Before H.M., psychologists did not appreciate that memory was made up of different functions that took place in different parts of the brain, particularly the hippocampus.
Milner's research on H.M. led to the development of the Multi Store Model and to Tulving's concepts of procedural and semantic memory as well as episodic memory.
Some researchers argue H.M.'s fame has led to too much focus on the hippocampus: the case of B.J. whose amnesia was brought on by a snooker cue up the nose suggests other areas of the brain are important too.
Now that H.M. is dead, his brain has been scanned and sliced into slides only 70 microns thick in order to help researchers understand the structure of the brain in more detail.

Conclusion
H.M.'s value to researchers comes from his being a "clean" or "pure" amnesia sufferer who had very specific brain damage and no mental disorders other than memory loss. This has made him very valuable as a research subject.

  • Notice that for a 8-mark answer you don’t have to include everything on H.M.. I haven’t mentioned the maze tests or details on how the star-drawing test worked. I haven't evaluated the studies in terms of ethics. But I have tried to make the two halves – Description and Evaluation – evenly balanced.

Introduction

The logic of concealed information tests (CIT) is that stimuli that are known or familiar to people should elicit a different response relative to comparable stimuli that are new (Lykken, 1959). Such tests could have various forensic applications, for example, to determine whether a person who denies having information about certain crime details or certain sensitive information actually possesses such information. CITs have been studied for many decades using several dependent variables, including long-standing, peripheral psychophysiological measures (Ben-Shakhar and Elaad, 2003) and, more recently, electrophysiological (event-related potential, ERP) (Rosenfeld et al., 1988, 1991, 2008; Farwell and Donchin, 1991; Allen et al., 1992) and hemodynamic ones (functional magnetic resonance imaging, fMRI) (Langleben et al., 2002; Phan et al., 2005; Christ et al., 2009; Nose et al., 2009; Ganis et al., 2011).

ERP-based CITs have garnered increased attention lately due to several advantages (e.g., Rosenfeld et al., 2008). (1) They have shown high accuracy rates reliably in detecting concealed information in mock crime scenario paradigms, at least in the laboratory conditions tested. (2) They are relatively inexpensive to implement. (3) The data can be acquired relatively quickly by using a few recording sites on the head. However, the underlying neural mechanisms are largely undetermined. A critical, understudied issue in the field is that people can learn and remember information about an event in many ways.

For example, memory theories distinguish between semantic and episodic memory (Tulving, 1972), and different brain systems have been implicated in each. Episodic memory depends on mediotemporal lobe structures, especially the hippocampus, whereas semantic memory does so much less, if at all, and depends on association cortex, such as anterior temporal cortex (Vargha-Khadem et al., 1997; Schmolck et al., 2002; Eichenbaum et al., 2007; Patterson et al., 2007; Bayley et al., 2008). That different brain systems support episodic and semantic memory raises the important issue that the brain signatures should differ when concealed information revealed on a CIT relies to different degrees on episodic vs. semantic memory. For example, evidence from developmental amnesia patients, who have hippocampal damage and impaired episodic but spared semantic memory, suggests that even residual hippocampal function (despite 50% volume loss or more) is necessary and sufficient to support relative sparing of the ability to imagine false events (Maguire et al., 2010), which is a necessary episodic memory ability for effective deception; neural signatures of such hippocampal activity would thus be expected to be greater for a CIT based on episodic memory relative to one based on semantic memory.

Indeed, the episodic-semantic distinction extends also to the kind of autobiographical memory typically tested in CITs (e.g., Martinelli et al., 2012), the focus of this paper. There are episodic and semantic forms of autobiographical memory. An episodic memory encompasses concrete and unique details associated with distinct events that were experienced by a person in a specific spatiotemporal context and, critically, becomes an episodic autobiographical memory (EAM) when this memory also refers to the self in relation to that context (Tulving, 2002). For example, details about a specific experience that happened at a certain time and place that caught one by surprise. In contrast, semantic autobiographical memory (SAM) encompasses personal information, including general knowledge of personal facts not associated with a specific time and place of acquisition (e.g., “my name is Pat” or “my birthday is December 5th”) and non-specific events, including both repeated and extended events (e.g., schema and script knowledge about “birthdays” not associated with any specific time and place, such as that birthdays are fun and involve friends and family) (Schank and Abelson, 1977). Studies in neurological patients confirm this distinction. For example, amnesic patient K.C. (Tulving, 1993) could report semantic knowledge, such as his own date of birth, but not any autobiographical episodic information (e.g., autobiographical details about any specific birthday). An important question is whether autobiographical probes associated with high semantic vs. episodic memory are associated with different neural processes in the context of a CIT, as would be predicted by neurocognitive studies of these two types of memories (e.g., Tulving et al., 1988; Martinelli et al., 2012). This question also has applied relevance because it could provide information about the brain signatures of these different types of memories that can inform how to maximize detecting concealed information in specific cases. It is important to note that, although there may be distinct neural systems supporting EAM and SAM (e.g., Martinelli et al., 2012), most information in real life is often associated with both EAM and SAM, though with different relative strengths. Note that, for simplicity, in the rest of the paper we will often omit the attribute “autobiographical” and refer simply to semantic and episodic memory.

The main previous ERP study that addressed a related question with an explicitly applied focus is one by Rosenfeld et al. (2006). “High-impact” and “low-impact” probes were compared that differed in semantic and episodic memory content. The high-impact probe was the participant's name, whereas the low-impact probe was the experimenter's name (i.e., “JULIE”). The ERP differences between high-impact probes and a set of random control names (referred to as “irrelevants” in the CIT literature) were much larger than those between the low-impact probes and the irrelevants (i.e., the CIT effect was larger for high than low-impact probes). However, important issues about this finding need to be resolved. First, the same low-impact probe was used for all participants (i.e., the experimenter's name was always “JULIE”). This raises the concern that there could be something intrinsically special, and consistently so across participants, about this name (e.g., frequency, length, associations). This confound was not present for the high-impact probes, as they varied across participants. Furthermore, it is unclear whether the female name used for everybody in the low-impact condition might have been processed differently by male and female participants (i.e., Julie is a female name), as well as individuals (i.e., different people named Julie that each one knows), increasing variability in the results. The ERPs were also recorded from only three sites, limiting assessment of spatial distribution differences between conditions. Finally, the study examined only the P3, leaving it open what effects other ERPs might show, such as the centroparietal N400 marker of semantic memory (Kutas and Federmeier, 2011) or the parietal late positive complex (LPC) associated with episodic recollection (Rugg and Curran, 2007). We would argue that the better way to describe the high- and low-impact probes is in terms of how they activate different kinds of memory. For example, both probes activate semantic and episodic memory, but in different ways for the participant's name (“high-impact”) and the experimenter's name (“low-impact”). Specifically, the participant's name could activate semantic memory more automatically than episodic memory, on average, because people are overlearned experts at responding to their own name, whereas most episodic memories associated with their name would be remote and many would be highly similar and so not distinctly memorable, such as people calling their name, potentially resulting in a lot of interference for recalling associated episodic memories and making them effortful to activate (Soderlund et al., 2012). Thus, semantic memory would be exceptionally automatic for the participant's name, consistent with evidence for a large auditory N400 for one's own name relative to other proper names and no evidence for a posterior LPC effect, suggesting little difference in episodic memory for one's own name and other proper names (Muller and Kutas, 1996). However, by telling subjects that the experimenter's name is “Julie,” subjects acquire a recent episodic memory, which is less effortful to activate than the more remote memories associated with one's own name (Soderlund et al., 2012), predicting a larger LPC for the experimenter's than participant's name, but this has not yet been examined to date. In summary, we would suggest that in the study by Rosenfeld et al. (2006), the participant's name would predominantly activate SAM, whereas the experimenter's name would predominantly activate recent EAM, but such ideas have not yet been systematically addressed.

Thus, the first goal of the current study was to address the question of concealed information based on different types of memory more directly while getting around the limitations in the previous work. First, comparable stimuli without a gender component were used for the semantic (the participant's date of birth) and episodic (a “secret” date given to the participant just before the study) autobiographical memory conditions. Second, all probes and irrelevants varied by person, eliminating any systematic biases in the group average. Third, 32 recording sites were used, enabling potential scalp distribution differences in the ERPs elicited by the two conditions to be determined. Fourth, and related to the previous point, not only the P3 but also other ERPs were evaluated, including the frontal N2, the N400, and the LPC.

A second important issue that has not been addressed systematically in the ERP literature is the effect of stimulus repetition. Because of the relatively low signal-to-noise ratio achievable with all behavioral and psychophysiological measures employed, the typical CIT paradigm averages several tens of trials in which probes and irrelevants repeat many times. Differences between probes and irrelevants using psychophysiological measures, such as skin conductance, decrease rapidly with stimulus repetition because of habituation (e.g., Ben-Shakhar et al., 1975; Ben-Shakhar and Elaad, 2002). However, the same effect may not be present with ERP measures because they may tap into different mechanisms. Furthermore, potential differences between semantic and episodic probes may change over the course of the experimental session. For example, repeated presentation will reactivate semantic and/or episodic memories associated with a probe but do less so if at all for irrelevants, since no distinct semantic or episodic information is available about them. This could result in a difference between probes and irrelevants that becomes larger over time, as ERP repetition effects can be greater for meaningful than meaningless items (Schendan and Maher, 2009; Voss et al., 2010). Another possibility is that repetition of the probes might alter the activation of the semantic and/or episodic memory underlying each. For example, the episodic probe might develop increasing associations with the experimental context, resulting in development of semantic memory (Gratton et al., 2009). This might reduce the N400 (which is smaller when semantic memory activates more successfully) (Voss et al., 2010; Voss and Federmeier, 2011), thereby reducing differences between semantic and episodic probes. On the other hand, all stimuli, including the semantic probe, might develop additional episodic memories with each exposure in the experiment, resulting in additional episodic memories that might increase the LPC (which is larger for more episodic memory), thereby also reducing differences between semantic and episodic probes and associated CIT effects.

The key idea in classical CIT theories is that probes will generate an orienting response associated with, for example, increased skin conductance (e.g., Sokolov, 1963; Gati and Ben-Shakhar, 1990). Although these theories may be adequate to explain autonomic nervous system findings, they cover only a subset of the central nervous system processes engaged by a probe during the CIT (relative to irrelevants) and implicitly assume that probes activate only one kind of memory. However, in the framework described here, semantic and episodic probes may be associated with different neural processes.

Current theories of memory predict that semantic probes would primarily activate semantic memories stored in the neocortex and indexed by ERPs such as the N400 and P3b, whereas episodic probes would primarily activate episodic memory stored in mediotemporal and linked cortical structures, indexed by late parietal potentials, such as the LPC (Paller and Kutas, 1992; Rugg et al., 1998; Dien et al., 2004; Voss and Paller, 2006). In practice, most stimuli are associated with both semantic and episodic memories, and so they would elicit some combination of these effects. For the stimuli in this study, one's date of birth is associated with strong SAM, activating meaning-related processes about oneself in semantic memory but also activating episodic memories incidentally (e.g., events during a specific birthday party, although this may be reduced by providing only the day and month of each date). Prior to the experiment, the birth date is also associated with relatively remote episodic memories of birthday events and other experiences involving one's birth date, such as filling out applications (e.g., for jobs, insurance, taxes). In addition, as the birth date is repeatedly experienced over the course of the experiment, each of these experiences may be encoded as a new (1) episodic memory (Paller and Wagner, 2002) and/or (2) constructed memory that combines new and old (i.e., due to incidental recollection of various birth date memories) episodic elements as well as semantic memory (Hassabis and Maguire, 2009).

New, recent episodic memory encoding can also occur for a different date with no semantic or episodic memory associated with it before the experiment, such as the secret date. Importantly, while multiple trace theory proposes that the hippocampus supports all episodic memories, regardless of how long ago they were encoded (Nadel et al., 2000), some evidence suggests that different parts of the hippocampus support more recent vs. remote episodic memory (Kesner and Hunsaker, 2010; Mankin et al., 2012). Further, between 3 days and 3 months after the learning episode, episodic memories may become semantic by increasing connectivity between cortical areas while decreasing connectivity with the hippocampus (Harand et al., 2012), and a study comparing episodic memories for events ranging in time from very recent (3–14 days old) to very remote (10 years old) found evidence that the hippocampus and the EAM cortical network are integrated more strongly for recent than remote memories (Soderlund et al., 2012). Consequently, more remote memories require more strategic top-down processes in prefrontal cortex for them to be retrieved than do more recent memories. This predicts that ERP effects related to EAM will be greater for the secret date, which involves very recent episodic memory, than the birth date, which involves mostly much more remote episodic memory.

On the other hand, the secret date is minimally meaningful (i.e., low in semantic memory) relative to the birth date. Repeated experiences with any date could potentially begin to construct new semantic memory about that date (Curran et al., 2002; Gratton et al., 2009), but the ability to do so would be minimal because little meaningful information is provided about any dates within the experiment. Notably, the information that the probe is a secret date to be kept concealed during the experiment is meaningful and could lead to learning this as new semantic memory due to repeated experiences with it; knowledge and semantic memory typically require multiple experiences to acquire (Glisky and Schacter, 1987; Verfaellie and Cermak, 1994). Another important way that all these semantic and episodic memory processes could affect the CIT is by inducing standard oddball effects thought to be related to ongoing contextual updating processes in working memory (Kutas et al., 1977; Donchin and Coles, 1988; Dien et al., 2004; Polich, 2007). This could result in a larger P3b to the probes than irrelevants. Further, the P3b to probe conditions could differ as a function of the relative combination of associated semantic and episodic memory. In sum, the birth date potentially activates a combination of high semantic memory and remote episodic memory for multiple birthdays related events, whereas the secret date potentially activates a combination of low semantic memory and recent episodic memory for a single event. Despite reflecting a combination of memory influences, the birthdate and secret date provide an interesting and important starting point for assessing the role of semantic and episodic memory in CITs.

The focus of this paper is on the frontal N2, N400, P3, and LPC components. The frontal N2 is important because recent studies suggest that concealed information in CITs modulate this component with visual (Gamer and Berti, 2010) and auditory stimuli (Matsuda et al., 2009), with probes eliciting a larger frontal N2 than irrelevants. This would be predicted by orienting reflex theory (Ben-Shakhar and Elaad, 2003), as the probe is more meaningful than the irrelevants and occurs infrequently (it is “novel” within the local stimulus sequence). If the frontal N2 reflects primarily an orienting reflex to meaningful information, the N2 should be larger for (1) probes and targets than irrelevants, and (2) semantic autobiographical information, such as one's date of birth, relative to recently acquired episodic information, such as a random (secret) date seen just before the study. However, the frontal N2 is known to be modulated by other variables as well, including the extent to which a stimulus matches to memory (e.g., Folstein and Van Petten, 2008; Folstein et al., 2008): the less a stimulus matches memory, the larger the N2. The precise type of memory involved is usually not specified, but knowledge (e.g., of an object category) and working memory have been mainly studied so far. Thus, an alternative prediction can be made based on the idea that match to knowledge is relevant for N2 modulation. The numbers and month abbreviations used as stimuli will activate knowledge about numbers and months, respectively. This predicts that the N2 will be larger to the irrelevants (minimal memory: people have minimal knowledge about the numbers in random dates that have no task relevance) than a meaningful item (e.g., birth date with rich semantic and remote episodic memories). In addition, depending upon how much new memory is encoded for the episodic item (e.g., a “secret” probe date will be associated with new episodic memory and possibly new knowledge induced by repetition within the experimental context), the N2 to this item may be in-between that to irrelevants and the semantic item.

The centroparietal N400 is larger when an item activates semantic memory less relative to more successfully (Kutas and Federmeier, 2011). Although people know the numbers and month abbreviations used to denote dates, an arbitrary date is not very rich in meaning. In contrast, one's birth date is personally meaningful because it is rich in SAM. This predicts that the N400 will be larger for irrelevant dates than the semantic item (birthdate). In addition, as with the frontal N2, depending upon the extent to which new semantic memory is encoded for the episodic item, its N400 may be in-between that to irrelevants and the semantic item. However, the N2, which merely requires new knowledge to be acquired, may be more sensitive to the memory manipulations in this experiment than the N400, which requires the more demanding encoding of a meaningful representation. After all, the episodic manipulation can induce new knowledge to be learned, but this new information is minimal in meaning, and meaningful representations would typically require a stronger induction event than that used in this experiment (Gratton et al., 2009). For example, acquisition of category knowledge with minimal associated meaning modulates a frontocentral N2 but not necessarily the N400 (Folstein et al., 2008). The N400 may thus show little or no difference between irrelevants and episodic items, instead differing primarily between irrelevants and semantic items.

The effect of concealed information on the P3 has been investigated in numerous ERP studies (e.g., Rosenfeld et al., 1988; Allen et al., 1992; Rosenfeld et al., 2004), but almost all used fewer than five recording sites and so differences between the spatial distribution of the P3 in the different conditions may have been missed. Indeed, the P3 is a family of components, and what has usually been referred to as P3 in previous studies is most likely an instance of the P3b, which has been dissociated from the P3a (Dien et al., 2004; Polich, 2007; Verleger, 2008). The P3b is known to be modulated by many factors, including the subjective probability of items in a perceived category, the complexity of the task and stimuli, and stimulus value (e.g., Johnson, 1986, 1993). We predicted that the P3b to probes would be larger than to irrelevants, replicating previous findings (e.g., Rosenfeld et al., 2004). Further, the semantic probes might elicit a larger P3b than the episodic probes in part because they were the only items associated with strong semantic memory and so they may stand out more in the stream of irrelevants, which are associated only with episodic information acquired during the study.

Finally, the LPC is typically larger during tasks that entail the reactivation of episodic memories (Rugg and Curran, 2007) and so we expected the LPC to be larger to probes, for which episodic memories have been clearly associated, than to irrelevants, for which episodic memory is minimal, and larger to probes in the episodic than semantic condition.

Materials and Methods

Subjects

Twenty-five naïve healthy volunteers (18 females, between 18 and 35 years of age, mean = 21, SD = 3.5 average age: z years), recruited from the University of Plymouth (UoP), took part in for course credit. Data from eight participants were excluded due to excessive artifacts (7) or failure to carry out the task as instructed (1). Participants had normal or corrected vision, and no history of neurological or psychiatric disease. All procedures were approved by the UoP Ethics Board.

Stimuli

The stimuli were dates in the format “day month” (e.g., 15 Apr, Figure 1) commonly used by our European participants, subtending about 3 × 2° of visual angle. Three types of dates were used in each condition: irrelevants, probe, and target. During the week preceding the study, at the same time detailed and demographics and health questionnaires were administered, participants were asked over the phone to provide their own date of birth (only the day and month were required) and a list of other important dates (dates of birth of close relatives and friends, anniversaries and so on), so that a set of irrelevant dates could be generated for each participant that excludes these personally important dates. For the semantic autobiographical condition, the probe was the birth date of each participant. For the episodic autobiographical condition, the probe was a date that differed from all other dates used in the study and was not on the participant's list of important dates. The irrelevant dates used for the episodic and semantic conditions were always different. Irrelevant dates never shared the day or the month of the probe or target dates, and they were never famous dates. Furthermore, the target never shared the day or month of the probe.

Figure 1. Schematic of the experimental paradigm. Participants were tested in two memory conditions in separate blocks: semantic autobiographical and episodic autobiographical. In both conditions, they saw four irrelevant dates, randomly intermixed with a target date and a probe date. In the semantic autobiographical condition, the probe was the participant's date of birth. In the episodic autobiographical condition, it was a secret date in an envelope each participant opened just before the study. Participants reported whether they possessed associated memories for any of the dates, responding honestly to both the irrelevant dates (by pressing the “no” key) and the target date (by pressing the “yes” key), but lying about their birth date or secret date (by pressing the “no” key). Note: Item type labels in the figure shown for illustration only and did not appear on the stimuli.

Procedure

Before beginning the EEG setup, participants were shown a target date and then were unexpectedly taken into an adjacent fire refuge area by an assistant and the experimenter and they were given an envelope containing their “secret” date. Next, the experimenter left the room, and participants were told by the assistant to open the envelope and to memorize the secret date contained in it, ensuring not to do anything that could reveal they knew this date to the experimenter. Participants were also told that this was their own secret date, different from everyone else's, and that they should keep the note it was written on in their pocket or purse. After setting up the EEG cap and electrodes, participants were seated on a comfortable chair in front of a computer screen (about 114 cm away) in a dark room. Two conditions were administered in separate blocks, the semantic and episodic conditions, with order counterbalanced across participants. In the semantic condition, the probe date was the individual's birth date whereas, in the episodic condition, it was the “secret date.” This secret date varied by participant to match the between-participant variability of the date of birth. In both semantic and episodic conditions, participants were instructed to deny possessing any memory for the probe date (birth date or secret date, respectively) throughout the session by giving a deceptive “no” response. They were also instructed to give an honest “yes” response about knowing the target date. Thus, participants had to report honestly whether they knew each date, but they had to lie about the probe date. In sum, participants responded honestly to both the target (pressing “yes”) and the irrelevants (pressing “no”) but deceptively to the probe (pressing “no”). Participants responded by pressing one of two buttons with the index and middle finger of their dominant hand. They were instructed to respond as fast as possible without sacrificing accuracy. Each item was presented for 800 ms with an inter-trial interval of 3000 ms. In each condition, each item (four irrelevants, one probe, and one target) was presented 35 times in a pseudo-random order for a total of 210 trials. The constraints on the pseudo-random sequence were that a probe and a target could never appear in temporally adjacent trials, and any individual irrelevant could only repeat for a maximum of three times in the sequence. The same abstract sequence (i.e., the sequence of irrelevant, probe and target types of items) was used for the two conditions to eliminate potential differences due to sequence statistics. Each condition was split into two blocks of ~7 min each, to test the effect of stimulus repetition. There was a short practice session (10 trials) before the experimental trials. Finally, at the end of the study, participants were asked to recall the target and the secret dates and indicate if they had any pre-experiment memory associated with any of the other dates. Since there was 100% recall accuracy in all cases, the recall data were not further analyzed.

Electrophysiological Data Acquisition

The electroencephalogram (EEG) was sampled at 250 Hz from Ag/AgCl electrodes (gain = 20,000, bandpass filtering = 0.01–100 Hz). EEG data were collected from 32 electrodes arranged in a geodesic array (Figure 3) and additional electrodes placed below the right eye referenced to left mastoid to monitor eye blinks, on the tip of the nose, and the right mastoid, all of which were referenced to the left mastoid. Note that in this configuration, Fz is just posterior to site 27, Cz coincides with site 28, and Pz is just posterior to site 29. Horizontal eye movements were monitored using two electrodes placed on the outer canthi of the right and left eyes, referenced to each other. Electrode impedance was below 5 kΩ for all channels.

Analyses

Performance measures were submitted to ANOVAs with three factors: item type (average of irrelevants; probe; target), memory condition (semantic and episodic), and repetition (first and second half). To ensure participants carried out the task, follow-up ANOVAs also contrasted targets with irrelevants and targets with probes. However, the main comparison of interest for each memory condition was between probes and irrelevants because the same response (“no”) was associated with both. As this comparison was the main focus of this experiment, and targets received a different response (“yes”) from all other items, confounding their comparison with other items, ERP analyses focus only on an item factor that include probes and irrelevants; note, preliminary analyses that included ERPs to the targets confirms expected target P3b effects. In the following, significant differences between probes and irrelevants (in the behavioral or ERP data) will be referred to as the CIT effect.

Response times

Response times (RTs) and accuracy rates were analyzed in the omnibus ANOVA and planned comparisons.

ERPs

ERPs were averaged off-line for an epoch of 1000 ms, including a 100 ms baseline. Trials affected by blinks, eye movements, muscle activity or amplifier blocking were rejected off-line. An average of 31 artifact-free trials per item type per participant went into the analyses (MIN = 16, SD = 4.2). A One-Way ANOVA showed no differences in the number of trials across conditions (including both repetitions), F(5, 85) = 1.05, p > 0.1, η2 = 0.06. Data were analyzed unfiltered but shown filtered at low-pass 30 Hz in the figures. Repeated measures ANOVAs on the mean amplitude of the average ERPs assessed the effects of item type and condition on the N2, N400, P3, and LPC components. The time windows used for the main analyses centered arounds the mean peak latency of the N2 (250–350 ms), the N400 (350–500 ms), the P3 (400–600 ms), and the LPC (750–900 ms). To assess the overall pattern of results, a “lateral” ANOVA assessed lateral sites (13 pairs, see electrode montage in Figure 3) using factors of Item Type (probes vs. irrelevants), Site, and Hemisphere. A second, “midline” ANOVA assessed the midline sites (six electrodes) using factors of Item Type and Site.

Planned focal analyses were also conducted at frontal sites 1 and 2 for the N2, central site 28 (Cz) for the N400, and parietal site 30 for the P3b and LPC, where these components were maximal. These analyses compared (1) probes and irrelevants (i.e., the CIT effect) in both memory conditions, since we predicted differences between probes and irrelevants in both cases, and (2) probes between the two conditions, since we predicted differences between the semantic and episodic probes. Note that we did not carry out amplitude-latency analyses on the P3b because the overlapping N400 made it difficult to determine P3b peak latency in single participants. The focal analysis was carried out on the mean amplitude data within the time windows used in the main analyses. At focal sites, onset of the CIT effect (i.e., probes vs. irrelevants) and the difference between semantic and episodic probes was determined. For the N2 and N400, 25 ms time windows were used, between 100 ms and 350 ms, and 300 and 550 ms, respectively. A paired t-test between the conditions of interest was carried out on each time window until a significant difference was found in three successive time windows. The time window preceding the first significant time window was used as an estimate of the onset time of the effect. For the P3, the same logic was used with 25 ms time windows between 200 and 600 ms.

Results

Behavior

Figure 2 shows the behavioral results. RTs varied by item type, F(1, 16) = 54.09, p < 0.001, η2 = 0.77. Furthermore, RTs were faster in the second than first half of each memory condition block, F(1, 16) = 21.49, p < 0.001, η2 = 0.57, and this repetition effect was modulated by item type, F(2, 32) = 4.73, p < 0.05, η2 = 0.23. Follow-up analyses to parse this effect compared each item type with the other two. RTs were slower to probes than irrelevants, F(1, 16) = 73.90, p < 0.001, η2 = 0.82, and both RTs were faster in the second than first half, F(1, 16) = 25.32, p < 0.001, η2 = 0.61, but the repetition effect tended to be marginally larger in the episodic than semantic condition, F(1, 16) = 3.68, p = 0.07, η2 = 0.19. Similarly, RTs were also slower to targets than irrelevants, F(1, 16) = 85.84, p < 0.001, η2 = 0.84, and both RTs were faster in the second than first half, F(1, 16) = 12.35, p < 0.005, η2 = 0.44, but the repetition effect tended to be marginally larger in the episodic than semantic condition, F(1, 16) = 3.22, p = 0.09, η2 = 0.17. In contrast, RTs to targets and probes were similar, and both RTs were faster in the second than first half, F(1, 16) = 24.11, p < 0.001, η2 = 0.60, but probes were slower than targets in the first half, whereas the opposite held in the second half, F(1, 16) = 8.30, p < 0.05, η2 = 0.34. Accuracy showed only a main effect of item type, F(1, 16) = 15.36, p < 0.001, η2 = 0.49. Follow-up analyses revealed that accuracy was lower for targets than both irrelevants, F(1, 16) = 17.11, p < 0.001, η2 = 0.52, and probes, F(1, 16) = 13.36, p < 0.005, η2 = 0.46. Accuracy was also lower for probes than irrelevants, F(1, 16) = 11.67, p < 0.005, η2 = 0.42. Notably, there were no significant main effects of memory on RTs and accuracy and no significant repetition effects on accuracy.

Figure 2. Behavioral results. Top, average response times (RTs) to irrelevants, probes, and targets in the semantic (red bars) and episodic (gray bars) autobiographical conditions during the first (light bars) and second (dark bars) repetition. Bottom, accuracy for the same conditions. Error bars depict 1 SEM.

Event-Related Potentials (ERPs)

Qualitatively, the ERP waveform showed an occipitotemporal P1 and a corresponding anterior N1, followed by a frontocentral P2 and N2, and a centroparietal N400, P3b, and LPC (Figures 3–7). Four main differences between items and memory conditions are evident in the ERPs. The first difference is on the N2, maximal at frontal sites between 250 and 350 ms (Figures 3, 4 and 5A). Second, a clear N400 component overlapping the first part of the P3b is present in the episodic condition, maximal at central sites, and to a lesser extent in the semantic condition (Figures 3 and 5B). The third difference is on the P3b, maximal at centroparietal sites between 400 and 600 ms (Figures 4 and 5C). Fourth, LPC differences appear later at the same sites, lasting until the end of the epoch (Figures 4 and 5C). Omnibus statistics are shown in Tables 1–3 and described below.

Figure 3. Grand average ERPs elicited by irrelevants (thin solid lines) and probes (thick solid lines) in the semantic (black lines) and episodic (red lines) autobiographical conditions. ERPs are plotted between-100 and 900 ms (at all scalp recording sites). ERPs are shown negative up and referenced to the average of the left and right mastoids. A diagram with the location of the recording sites is shown on the bottom right.

Figure 4. Topographic maps of the ERP difference between probes and irrelevants for (top) the N2 (250–350 ms), (middle) P3b (400–600 ms), and (bottom) LPC (750–900 ms) in the semantic (left column) and episodic (right column) autobiographical conditions. An N400 map is not shown because there was no CIT effect in the episodic condition, and the P3b map for the semantic condition captures the N400 as a positive difference at Cz (28); thus, the centroparietal distribution in the P3b time period of the semantic condition reflects the combination of the overlapping central maximum of the N400 CIT effect and the parietal maximum of the P3b CIT effect. Note, the voltage scale is not the same for all topographic maps.

Figure 5. The left side of each panel shows the ERP time course for episodic probes (thin orange line), semantic probes (thin black line), and difference between episodic and semantic probes (thick blue line). The right side of each panel shows a topographic map for the difference wave shown on the left: (A) N2; (B) N400; (C) P3b and LPC.

Table 1. Results of the omnibus lateral (Lat) and midline (Mid) ANOVAs for the N2 (probe vs. irrelevants, 250–350 ms).

N2 (250–350 ms) and N400 (350–500 ms)

N2. Omnibus results at lateral and midline sites (Table 1) showed a larger N2 for irrelevants than probes at frontal and frontocentral sites (I × S), and ERPs were more positive during the second than the first half (R, lateral sites, 3.81 vs. 3.31 μV, respectively; midline sites, 5.55 vs. 4.79 μV, respectively, Figures 6 and 7). At lateral sites, repetition effects were maximal at centroparietal sites and larger over the right hemisphere at frontocentral sites, but symmetric or larger over the left hemisphere at more posterior sites (R × S × H).

Figure 6. Grand average ERPs elicited by irrelevants (thin solid lines), probes (thick solid lines) in the semantic (black lines) and episodic (red lines) autobiographical conditions in the first half of trials. ERPs are plotted between 100 and 900 ms (at all scalp recording sites). ERPs are shown negative up and referenced to the average of the left and right mastoids. A diagram with the location of the recording sites is shown on the bottom right.

Figure 7. Grand average ERPs elicited by irrelevants (thin solid lines), probes (thick solid lines) in the semantic (black lines) and episodic (red lines) autobiographical conditions in the second half of trials. ERPs are plotted between 100 and 900 ms (at all scalp recording sites). ERPs are shown negative up and referenced to the average of the left and right mastoids. A diagram with the location of the recording sites is shown on the bottom right.

Planned focal analyses on frontal pair 1 and 2 showed that probes were more positive than irrelevants (4.35 vs. 2.10 μV, respectively), F(1, 16) = 40.01, p < 0.001, η2 = 0.71, and this CIT effect tended to be larger on the right than the left (3.46 vs. 2.99 μV, respectively), F(1, 16) = 4.01, p = 0.063, η2 = 0.20. Importantly, this CIT effect was larger in the semantic than episodic condition, F(1, 16) = 5.53, p < 0.05, η2 = 0.26, due to the probes in the semantic condition being more positive than those in the episodic condition (4.87 vs. 3.83 μV, respectively), F(1, 16) = 4.50, p < 0.05, η2 = 0.22. This result is the opposite of the hypothesis that the N2 CIT effects reflect orienting to novelty but consistent with the alternative hypothesis that the N2 is sensitive to match to knowledge. No repetition effects were significant.

The onset of the CIT effect in the two memory conditions was determined at right frontal site 2, where the differences were largest. Results showed that the CIT effect onset between 200 and 225 ms in the semantic probe condition, and slightly later, between 225 and 250 ms, in the episodic probe condition. A second onset analysis showed that the onset of the difference between probes in the two memory conditions was also between 225 and 250 ms.

N400. The N400 is the only ERP component to show a CIT effect only in the semantic condition. The N400 is smallest for the semantic probe, relative to the episodic probe and all irrelevants, which are indistinguishable from each other (Figure 3). Figure 4 (middle) shows an overall centroparietal scalp distribution between 400 and 600 ms due to the combination of the central CIT effect on the earlier N400 and the parietal CIT effect on the later P3b. Figure 5B shows the memory effect around central sites where the N400 overlaps least with the frontal N2 and parietal P3b, illustrating that the N400 is more negative to episodic than semantic probes and has a central maximum and overall centroparietal scalp distribution, which is characteristic of the N400 index of semantic memory (Kutas and Federmeier, 2011). The omnibus analyses on the N2 and P3b capture the early and late part of the N400, so the focus was on planned focal analyses.

A focal analysis on Cz (site 28) showed that probes were less negative than irrelevants (7.29 vs. 5.16 μV, respectively), F(1, 16) = 7.05, p < 0.05, η2 = 0.31, and this effect was larger in the semantic than episodic condition (3.27 vs. 0.96 μV, respectively), F(1, 16) = 6.16, p < 0.05, η2 = 0.28. A follow-up analysis showed that the difference between probes and irrelevants was only significant in the semantic condition, t(16) > 2.35, p < 0.05, for both repetitions. ERPs were more positive during the second than first repetition, F(1, 16) = 4.58, p < 0.05, η2 = 0.22, but this effect did not interact with any other factors. Finally, ERPs were more positive during the semantic than episodic conditions, F(1, 16) = 8.73, p < 0.01, η2 = 0.35.

Finally, an onset analysis of the CIT effect in both memory conditions was carried out at Cz. Results showed that the CIT effect onset between 400 and 425 ms in the semantic conditions, whereas it onset between 475 and 500 ms in the episodic condition. A second onset analysis showed that the onset of the difference between probes in the two memory conditions was between 400 and 425 ms.

P3b (400–600 ms)

Omnibus results (Table 2) showed a larger P3b for probes than irrelevants at lateral (I, 6.84 vs. 4.30 μV, respectively) and midline sites. This CIT effect was maximal at lateral and midline centroparietal sites (I × S), and lateral results showed that this effect was larger on the right at frontocentral sites but on the left at more posterior sites (I × S × H). Importantly, the difference between probes and irrelevants was larger in the semantic than episodic condition at lateral and midline sites (M × I), and this interaction was largest at centroparietal sites (lateral, M × I × S). ERPs at this time tended to be more positive during the second than the first half (R). At lateral sites, this repetition effect was larger on the right at frontal and posterior sites, but symmetrical at central sites, and maximal at right centroparietal sites (R × S × H). The lateral repetition effect was also modulated by item type, as it was larger for probes than irrelevants (I × R × S × H), and by memory type, as it was larger at centroparietal sites in the semantic condition, but at fronto-central sites in the episodic condition (M × R × S).

Table 2. Results of the omnibus lateral (Lat) and midline (Mid) ANOVAs for the P3b (probe vs. irrelevants, 400–600 ms).

Planned focal analyses were conducted at parietal site 30 where the P3b was maximal. Consistent with the omnibus analysis, the P3b was larger for probes than irrelevants, F(1, 16) = 38.35, p < 0.001, η2 = 0.71 (10.77 vs. 7.15 μV, respectively). Importantly, this CIT effect was larger in the semantic than episodic condition, F(1, 16) = 5.26, p < 0.05, η2 = 0.25 (4.80 vs. 2.45 μV, respectively) because the P3b was more positive for the semantic than episodic probes, F(1, 16) = 4.53, p < 0.05, η2 = 0.22 (11.84 vs. 9.7 μV, respectively). There was a non-significant trend for the P3b to be larger during the second than the first half, F(1, 16) = 3.56, p = 0.08, η2 = 0.18, and the CIT effect was numerically larger during the second than the first half, but this interaction of item and repetition was also not significant, F(1, 16) = 2.47, p = 0.14, η2 = 0.13 (4.11 vs. 3.14 μV, respectively). Thus, the CIT effect did not change significantly as a function of repetition (if anything, it became slightly larger).

The onset of the CIT effect in the two memory conditions was determined at parietal site 30 where the differences were largest. Results showed that the CIT effect onset between 375 and 400 ms in the semantic probe condition, and, later, between 450 and 475 ms in the episodic probe condition. The onset of the difference between the probes in the two memory conditions was also analyzed, revealing an onset between 375 and 400 ms.

LPC (750–900 ms)

Omnibus analyses (Table 3

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