Recognition Memory and Novelty Preference: What Model - LPNC

In H. Hayne & J. Fagen (Eds) Progress in Infancy Research (2003), Lawrence Erlbaum Associates, New Jersey, Vol3., pp 95-120.

Recognition Memory and Novelty Preference: What Model? Olivier Pascalis 1 & Michelle de Haan 2

1-The University of Sheffield, Department of Psychology, Western Bank, S10 2TP Sheffield, UK. e-mail: [email protected] 2- Cognitive Neuroscience Unit, Institute of Child Health, University College London, Mecklenburgh Square, Wolfson Centre, London WC1N 2AP. e-mail: [email protected]

Pascalis, O & de Haan, M (2003). Recognition Memory and Novelty Preference: What Model? In H. Hayne & J. Fagen (Eds) Progress in Infancy Research (2003), Lawrence Erlbaum Associates, New Jersey, Vol3., pp 95-120.

In H. Hayne & J. Fagen (Eds) Progress in Infancy Research (2003), 2 Lawrence Erlbaum Associates, New Jersey, Vol3., pp 95120.

Introduction Interest in the study of early memory development has increased over the past two decades. A key step in this progress has been the development of several non-verbal tasks that allow assessment of memory in human infants and in nonhuman primates who cannot express their memories through Ianguage. These tasks include delayed non-match to sample (DNMS; Diamond, 1995), mobile conjugate reinforcement (Rovee-Collier, 1997), deferred imitation (Bauer, 1996; Collie & Hayne, 1999; Meltzoff, 1990), visual paired comparison (Fantz, 1964; Fagan,

1973;

Pascalis,

de

Haan,

Nelson

&

de

Schonen,1998),

habituation/dishabituation (Martin, 1975), and recording of event-related potentials (ERPs; see Nelson, 1994 for a review). Of these tasks, visual paired comparisons and habituation/dishabituation were among the first used in the scientific study of infant memory and are perhaps still the most common. Both techniques infer memory for familiar stimuli based on longer looking at novel compared to familiar stimuli. There has been renewed interest in these tasks due to recent studies of the neurobiological bases of novelty preferences.

The

aim of this chapter is to review the data and recent theories on the meaning of novelty preferences and evaluate the merits and limitations of these models in light of recent ERP and other neuroscientific data (for comprehensive reviews of the development of infant memory more generally, see Diamond, 1990; Nelson, 1995; Rovee-Collier, 1997).


The Visual Paired Comparison Procedure The visual paired comparison (VPC) task developed by Fantz (1964) is a common way to measure visual recognition memory in preverbal and nonverbal individuals. The VPC task exploits individuals’ attraction to novelty in order to assess their recognition memory for previously seen stimuli.

The basic

procedure is relatively simple: The participant is first presented with a stimulus for a familiarization period (see below for a discussion of various types of familiarization). Thereafter, the participant is presented with the same stimulus paired simultaneously with a novel one (Figure 1 and 2). The key measure is the length of time spent fixating each of the two stimuli (Figure 3). Longer duration of looking to one stimulus, generally the novel one, indicates discrimination and recognition memory. Note that this interpretation rests on the assumption that infants do not have an a priori preference for one versus the other stimulus (i.e., that without familiarization there would be equal looking to both stimuli in the pair). The VPC task must be distinguished from another, similar task: the habituationdishabituation task. In that task, the individual is familiarized with a stimulus until his/her looking decreases to a predetermined criterion (see infant control procedure, below), and then a new stimulus is presented in isolation. Recognition is defined as

‘recovery’ of looking to the new stimulus i.e., an

increase in attention to it relative to looking to the familiar stimulus duration the last trials of habituation and/or on re-presentation following habituation. Thus, the main procedural difference between the two tasks is that in VPC the novel


stimulus is presented simultaneously with the familiar one and the infant ‘chooses’ which one to look at, while in habituation-dishabituation the novel stimulus is presented alone. Whether this procedural difference affects the type of memory processes that are assessed is not known. In this chapter, we focus on VPC because it is the only one used to study long term recognition memory in infants and the one for which we know something about the neural substrates.

The VPC task has been to assess a wide range of abilities in human infants. For example, perceptual abilities such as visual acuity, colour discrimination and categorization (see Slater, 1995; Atkinson, 2000) have been assessed by administering the paired comparison task immediately after the familiarization phase. In this way the memory demands are minimized and perceptual abilities primarily contribute to differential looking.

In order to increase the memory

demands, a delay (e.g. minutes, days, months) can be added between the end of familiarzation phase and the visual preference test. Using this procedure, infants as young as 3 days of age show evidence of recognition memory by novelty preference even when a 2 minute delay is imposed between familiarization and the VPC test

(Pascalis & de Schonen, 1994).

Retention over even longer

delays, from days to months, can be demonstrated by 3-6 months of age (Bahrick, & Pickens, 1995; Fagan, 1973; Pascalis et al., 1998).

At first glance, the VPC task may seem both easy to administer and easy to interpret. The most common interpretation of infants’ visual preferences is one


adapted from a neural model of the orienting reflex (Sokolov, 1963). In this model, during familiarization an internal representation or trace of the stimulus is established. Looking generally decreases over this time because, with continued exposure, the internal representation becomes increasingly similar to the actual external stimulus and orientation towards it is inhibited. When the test pair is presented, the infant then ‘compares’ both stimuli with the internal representation and is more attracted to the novel stimulus to the extent that it does not match the internal representation.

The infant then begins constructing an internal

representation of the novel stimulus. While this simple model provides a plausible account of why infants prefer to look at novel stimuli, it has difficulty accounting for the fact that infants sometimes show a preference for looking at familiar rather than novel stimuli.

Both

preferences for novel relative to familiar stimuli and preferences for familiar relative to novel stimuli provide evidence of recognition, in that in both instance infants show differential responsiveness to two stimuli based on prior exposure to one of them. Why do infants show one versus the other type of preference, and is there any functional significance to the different preferences? In the following sections, we will first review studies which used visual paired comparisons to assess memory and found novelty or familiarity preferences, and then present several models that have been proposed to account for the difference in results.


Studies showing a Novelty Preference Infants as young as a few days old show novelty preferences both when tested immediately following familiarisation (Slater, Morison & Rose, 1983) or 2 minutes after habituation (the longest delay used with such young infants; Pascalis et al., 1998). The results of several studies suggest that by 3-6 months of age infants can tolerate delays of days to weeks. Two studies found that 3- and 6-montholds showed novelty preferences after either a 2-minute (Cornell, 1974; Pascalis et al., 1998) or 24-hour delay (Pascalis et al., 1998), one study found 9-montholds showed novelty preferences after delays up to 10 minutes (Diamond, 1995), and one study found that 6-month-olds showed novelty preferences after a 2week delay (Fagan, 1973). In contrast the results of other studies suggest that infants’ memories may persist only seconds. Pancratz and Cohen (1970) found a novelty preference by 4-month-olds immediately after the familiarization period but not when he tested the infants after a 5-minute retention interval, Cornell (1974) found that infants younger than 6 months showed no evidence of delayed recognition, and Diamond (1995) observed that 4-month-old infants spent a greater proportion of time looking at novel stimuli following a 10-second.

Studies showing a Familiarity Preference Fewer studies have reported familiarity preferences. Slater (1995) reported the results of a pilot study conducted to determine the adequate familiarization period in the newborn. He found that ‘the babies whose accumulated looking time over the six trials exceeded 180 seconds gave a novelty preference and all of the


babies whose accumulated time was less than the 180 seconds gave a familiarity preference’.

Rose, Gottfried, Melloy-Carminar, and Bridger (1982) compared

recognition in infants aged 3.5, 4.5 and 6.5 months after variable familiarization periods (5 seconds to 30 seconds). They found a familiarity preference after limited exposure to the stimulus that shifted to a novelty preference after more extended exposure (see Richards, 1997 for similar results). Differences between the ages were also shown, with the youngest group requiring more familiarization time than the oldest group to show novelty preferences. These experiments demonstrate a shift from a familiarity preference to novelty preference that is dependent on the familiarization time.

More recently, a series of studies has been reported which describes the opposite pattern: a change from novelty to familiarity preference. Bahrick and colleagues (Bahrick et al., 1997; Bahrick & Pickens, 1995) familiarized 3-monthold infants with a moving stimulus for 4 40-second trials, with a minimum criterion of 120 seconds accumulated looking.

They then presented infants with a

recognition test consisting of two 60-second trials in which the familiar stimulus was presented in its original motion paired with the familiar stimulus presented in a new motion (with left-right reversal of position across the two trials). They found novelty preferences after a 1-minute delay, no preference after 1 day or 2 weeks, and familiarity preferences after longer delays of 1 and 3 months. They also found that during the intermediate period of no preference a ‘reminder’ (brief exposure to static picture of the stimulus) could reinstate the novelty preference.


Courage and Howe (1998) attempted to replicate Bahrick et al.s’ findings with the same age group and similar procedure. Infants were first habituated with a moving stimulus until they reached the familiarization criterion and then after a delay, were presented with a pair of stimuli consisting of the familiar object in the original motion and a new object in a different motion. Three-month-olds also showed a shift from novelty to familiarity preference, but over a different timescale: infants showed a novelty preference after a 1-minute or 1-day retention interval, no preference after 1 week, a familiarity preference after 1 month, and no preference after 3 months.

Models of Familiarity and Novelty Preference The results of the studies reviewed above suggest that infants sometimes express recognition through novelty preferences and sometimes through familiarity preferences. What can account for these changing patterns of visual attention? Is there a general model for recognition memory that can explain these results? Below we outline several explanations that have been put forth to account for infants’ looking behaviour.

Age.

Hunt (1963) hypothesized that as infants develop the ability to recognize

repeatedly presented stimuli, the act of recognizing is initially rewarding in and of itself, and thus infants will prefer to look at familiar compared to novel stimuli. With continued development, the act of recognition becomes commonplace and


the infant becomes more intrigued by novel stimuli, and thus will prefer to look at novel compared to familiar stimuli.

There was some initial support for this model. For example, in one study, infants were familiarized with a mobile in their homes beginning at 4 months of age (Weizmann, Cohen & Pratt, 1971).

When tested after a 6-week delay they

showed a significant preference for looking at the familiar mobile, but by 8 weeks this was beginning change to a preference for the novel one. Subsequent studies (reviewed above) have shown that even newborns will show novelty preferences following adequate familiarization (Pascalis & de Schonen, 1994; Slater et al., 1983) and that infants of the same age might sometimes show both novelty and familiarity preferences. Thus, age alone cannot account for shifting preferences in the VPC task.

Encoding. Whether infants express immediate memory as a novelty or a familiarity preference may depend on how well the stimulus has been encoded: if the stimulus is well encoded, the infant will show a novelty preference, but if it is incompletely encoded the infant will show a familiarity preference. Three factors are thought to contribute to the encoding of a stimulus:

1) the amount of

familiarization time, 2) the complexity of the stimulus, and 3) the age of the infant (Nelson, 1995; Sophian, 1980).

The younger the infant and the more complex

the stimulus, the more familiarization time that will be required to fully encode the


stimulus.

At some point between partial and full encoding, there is an

intermediate period during which no preference is observed. This is not because the familiar stimulus is not recognized, but because the familiar and novel stimuli are equally interesting to the infant at that level of encoding.

Bornstein (1985) has described 4 general types of procedure that can be used to familiarize a participant with a visual stimulus and that will affect how well it is encoded: 1- Fixed-trials procedure:

In this procedure, a stimulus is presented to the

participant for a predetermined number of trials of a fixed and relatively brief duration.

For example, a stimulus is presented 8 times with 15-second

duration of each presentation. 2- Familiarization: In this procedure, the stimulus is presented once for a more prolonged duration (Fagan, 1973). For example, a stimulus is presented one time for 100 seconds.

A disadvantage of both of these procedures is that they do not take into account whether or not the participant is actually looking at the stimulus during the time it is presented. Thus, in these procedures, different participants who are exposed to the stimulus for the same amount of time might vary substantially in how much time they actually looked at the stimulus (and by inference, how well they have encoded it). Two other procedures attempt to take this factor into account.


3- Fixed-level procedure: In this procedure, a stimulus is presented until the infant accumulates a predetermined amount of looking time. For example, the stimulus might be presented until the infant has looked at it for a total of 30 seconds. 4- Habituation to criterion with infant-controlled trials:

In this procedure

(Horowitz, Paden, Bhana & Self, 1972), trial length is defined by the participant’s looking: a trial begins when the participant first looks at the stimulus and ends when the participant first looks away. participant controls the length of the familiarization:

In addition,

Trials are repeatedly

presented in the same way until the length of the participant’s look decreases below a certain criterion defined by the length of his/her initial looking. For example, the procedure might continue until the participant’s duration of looking on any three consecutive trials totals 50% or less of their looking on the first three ‘criterion’ trials.

Both the fixed level procedure and the habituation to criterion procedure have the advantage over the fixed trial and the familiarization procedures in that they attempt to ensure that different infants have encoded the stimulus to similar extent and to ensure that the infants are ‘habituated’ to the stimulus at the end of the familiarzation period.

Thus, novelty preferences in immediate memory may

be more likely following the fixed level procedure or the habituation to criterion procedure than the other two procedures.


The results of several studies reviewed above support the view that infants’ looking shifts from a familiarity to a novelty preference as familiarization time increases (Richards, 1997; Rose et al., 1982; Slater, 1995). It is important to note that this model focuses on infants’ visual preference during memory tests administered immediately after familiarization. By itself, it cannot account for results showing shifting preferences related to the length of delay between familiarization and test (Bahrick & Pickens, 1995; Bahrick et al., 1997; Courage & Howe, 1998). Recall that these studies show that a novelty preference after short delay (which would suggest complete encoding) can shift to a null preference or a familiarity preference with increasing delay. Some additional mechanism, such as memory decay, must be added to the encoding model to account for these findings.

For example, the model could be modified so that

any internal representation that is discrepant from the external stimulus, either because the stimulus is not yet fully encode or because the representation has faded, is predicted to elicit a familiarity preference (see Bahrick & Pickens, 1995)

Affect. Infants’ affect may also influence whether they look longer at familiar or novel stimuli. In one study, for example, 7-month-old infants were exposed to a moving and speaking puppet in two conditions, one designed to elicit positive affect during familiarisation and the other designed to elicit neutral affect (Nachman, Stern, & Best, 1986). Both groups then received an identical test that consisted of static, silent presentations of the familiar puppet paired with a new one.


Infants who smiled more during familiarisation (even those in the neutral familiarisation group) showed a familiarity preference while those who displayed neutral affect during familiarisation showed a novelty preference. The authors concluded that positive affect itself causes a preference for novelty. The results of another study, however, have shown that in 5- to 9-month-olds, positive affect is associated with long look durations and slower learning while neutral affect is associated with shorter looks and faster learning (Rose, Futterweit & Jankowski, 1999). These findings ssuggests that affect effects infants’ learning rather than their preference for familiarity per se.

Thus, compared to infants who show

neutral affect, infants who show positive affect during familiarisation may form less complete internal representations of the stimulus and thus be more likely to show familiarity preferences.

Individual Differences in Encoding. Several studies suggest that there are individual differences in encoding style that may contribute to individual differences in novelty preference during a test. Infants who show shorter, more distributed looking to the visual stimulus during familiarisation are more likely to show novelty preferences than those who show longer, less distributed looking (Jankowski, Rose & Feldman, 2001; Rose, Feldman & Jankowski, 2001). Interestingly, a recent study showed that when infants were induced to adopt a short, distributed looking pattern during familiarization, they did show novelty preferences (Jankowski et al., 2001). This


finding demonstrates that the individual differences are due to the encoding style spontaneously adopted by the infants and that this style can be modified.

Delay. The length of delay may also influence the direction of infants’ looking. For example, Bahrick et al. (1997) interpreted the results of their studies on motion recognition with a four-phase model of infant recognition memory. In the following presentation of the model, the delays associated with each phase are taken from Bahrick and Pickens (1995); however, the model is not specific with respect to retention interval. The phases represent recent, transition, remote and inaccessible memory. Phase 1-- Recent memory (1-minute delay). Memory is maximally accessible and a novelty preference is shown. Phase 2-- Transition period (1 day-1 week delay). No preference is shown. Phase 3--Remote memory (1-3 month delay). Memory is less accessible, and a familiarity preference is shown. Phase 4--Inaccessible memory (>3 month delay): the memory is inaccessible (i.e., forgotten) and there is no preference. The idea of a multi-phase memory system is not new in the adult literature. McGaugh (1966) proposed a 3-trace system in which an immediate memory trace is distinguished from both a short-term trace (several seconds to several hours) and a slowly created, more permanent trace. Neuropsychological studies of amnesic patients provide partial support for this view as some patients exhibit


normal memory with short and intermediate delays but show memory impairments with long delays (see McCarthy & Warrington, 1992). There is now a consensus that the medial temporal lobes’ structures may initially store the information but transfer it to the neocortex for longer-term storage. Bahrick’s data would have been a developmental illustration of this model if the trace had been stored and accessible at long delays instead of being lost systematically.

The 4-phase model represents an interesting attempt to explain recognition memory during infancy; however, it raises several crucial questions. There are 4 points which call into question the use of this model as a general model of recognition memory.

1-Delays One problem with the 4-phase model is the time frame: results from several studies are not consistent with the initially proposed timetable. For example, the model states that delays of 1-7 days fall in the transition period when no preference between novel and familiar stimuli is shown. However, Pascalis et al. (1998) found that 3- and 6-month-olds show a novelty preference following a 1day delay and Fagan (1973) found a novelty preference in 6-month-old infants after a 2 week retention interval. Even Courage and Howe (1998), who conducted a study using a procedure very similar to Bahrick et al. (1997) reported a novelty preference after a 1-day delay which falls during Bahrick et al.’s null-preference transition period. Furthermore, infants are known to show a


familiarity preference for the mother’s face (Bushnell, Sai, Mullin, 1989; Pascalis, de Schonen, Morton, Deruelle & Fabre-Grenet, 1995). According to Bahrick’s model this would indicate that infants have only remote memory for the mother’s face, less accessible even than a habituated face, which seems unlikely. Thus, some further factors in addition to delay must be involved to generate the different results observed.

2-Motion/Static Another important factor to consider is that no previous study assessing infant memory for static stimuli after various delays has found a switch from novelty to null to familiarity preference with increasing delay. The only change noted in those studies was a switch from a novelty to a null preference. Thus, the dynamic pattern of infant attention over increasing delays described by Bahrick et al. may apply to memory for motion but not memory for static objects.

This interpretation is supported by evidence showing that there are 2 anatomically distinct visual streams, one for motion and one for form processing, that project to 2 different parts of primary visual cortex and continue within independent streams to higher processing (Atkinson, 2000). When presented with an object in motion, the visual system will process the form and color of the stimulus from the retina along a different pathway in a different way than the motion. The motion information will be processed in the posterior temporal lobe whereas the form and color information will be processed in the inferior temporal


lobe. Our knowledge of recognition memory is largely based on static pictures, and less is known about memory for motion. Thus it is possible that motion recognition differs from static object recognition, so that results from studies of motion recognition do not generalise to studies of static object recognition. This assumption is supported by the fact that Courage and Howe (1998) mixed form and motion recognition and their results differed from both static picture recognition and motion recognition. Whereas Fagan (1973) found a novelty preference for a static picture after 24 hours or 2 weeks delay, Courage and Howe showed a novelty preference after 24 hours but found no preference after a 1-week delay.

Do the discrepant results reflect the interference between a motion recognition system and an object recognition system? Without further evidence it is difficult to firmly decide if the 4-phase model is specific to motion or can be applied more generally to visual recognition of any object. There is one other study, however, showing a similar pattern of change in preference for auditory stimuli, suggesting that the pattern may occur in some other instances (Spence, 1996).

3-Length of familiarization and recognition test. Another unusual aspect of the paradigm used by Bahrick et al. (1997) and Courage and Howe (1998) is that both the familiarization and the recognition tests were quite lengthy. Typically, the test pair is shown for long enough to allow participants to inspect both pictures but not long enough to allow new


habituation. In Bahrick et al., each test pair was shown for two 1-minute trials. This raises the question of whether further visual habituation began during those periods and/or if reactivation was occurring. When looking at the new stimulus during a recognition test, infants start a new habituation process, turning the new stimulus into a familiar stimulus with time. Such a conclusion is supported by a study (Fagan, 1974) showing that a 5-second familiarization period is enough to induce a novelty preference. This problem can be illustrated in a study in which we examined how the length of the test trial (2-20-second trials) influenced babies’ looking. 3-month-old infants were habituated with an infant controlled procedure to the static picture of a face. The recognition test was carried out 24 hours later. Infants showed a novelty preference (60% of the time) but closer examination showed that this occurred only on the first test trial (68.7%) and not during the second one (51.3%). Our interpretation of this result is that the long looking to the “novel” stimulus in the first trial was enough to cause habituation, so that this stimulus was no longer considered novel by the second test trial (Pascalis, 1993, unpublished dissertation). None of the studies cited previously included analyse comparing the novelty preference observed during the first 1minute recognition test with the one obtained during the second 1-minute recognition test. 1 It is then impossible to evaluate the impact that an unusually

1

Courage and Howe looked at the first longest uninterrupted look in the first and

second retention test and found that it was toward the novel stimulus for both of these. This measure is, different, however, from the percentage of looking time.


long presentation had on the recognition test. Has habituation to the new stimulus occurred?

4-Null Preference Generally, a preference for either the novel or the familiar stimulus is interpreted as recognition of the familiar stimulus whereas a null preference is interpreted as a failure of recognition. In contrast, Sophian (1980) proposed that novelty preference follows a complete encoding of the stimulus, familiarity preference an incomplete encoding and a null preference a transition between both preference. Bahrick and Pickens (1995) also proposed that a null preference is only a temporary status (phase 2) between a novelty and familiarity preference that reflects the transition between short term, intermediate and long term memory. Both views are problematic because they do not provide an index of forgetting. A compromise would be to argue that it is not possible to make firm conclusions when a null preference is observed if the habituation used is documented as long enough to create a novelty preference.

Thus, while these data and Sophian’s model highlight the fact that the short term and long-term memory traces might be expressed differently, clearly other factors, such as the encoding experience, nature and emotional content of the stimuli, etc, will all contribute to whether the behavioral output is a familiarity preference, a novelty preference, or no preference at all.


Studies with Adults Humans McGaugh’s 3-phase model (1966) described earlier is not specific to infants and we need now to review the adult literature on human and nonhuman primates to find data supporting memory changes across retention interval.

It is relatively unusual to use the VPC task to study visual recognition in human adults, however, the few existing studies have successfully demonstrated novelty preferences in adults. Novelty preferences have been found in human and nonhuman adults after delays of 10 seconds (Pascalis & Bachevalier, 1998), as well as after delays of several hours (McKee & Squire, 1993; Manns, Stark & Squire, 2000). We recently conducted an experiment to determine if human adults’ long term recognition memory can also be assessed with the VPC task. The participants were told that they were participating in a study of vision and that they had only to watch a screen for several seconds. It was explained that they would have to come back on different days for further assessment of their vision. They were familiarized with 12 objects for 5 seconds each. They were then presented with 4 unique test pairs consisting of a novel and one of the familiar stimuli after delays of 24 hours, 1 week, and 1 month. The results displayed on Figure 4 show that a significant novelty preference is observed only after a 1-day delay, while no preference was observed after the 1-week and 1 month retention intervals (i.e., 50% of fixation time to the novel stimulus). These results demonstrate that long-term recognition memory can be measured in


human adults using the VPC task after a 24-hour period with only a 5–second familiarization period. Moreover, over the delays tested, there was no change from a novelty to a familiarity preference with increasing delay. We did observe a switch from a novelty preference to a null preference, a forgetting behavior predicted by any model. The short familiarization of 5 seconds might be the reason for the null preference observed after 1 week or 1 month. Non human primates The VPC task has also been used to study recognition memory in nonhuman primates. For adult monkeys, novelty preferences can be observed with delays ranging from 10 seconds (Bachevalier, Brickson & Hagger, 1993) up to 24 hours (Pascalis & Bachevalier, 1999). Gunderson and Swartz (1985) found that preference for novelty following a 24-hour delay is present as early as one month of age in monkeys. As for human infants, the familiarization period is the determining factor for infant monkeys’ recognition. With shorter delays of only 10 seconds, novelty preference is present in monkeys as young as 15 days of age, but not younger (5 days) (Bachevalier et al., 1993).

Thus, the results of studies with adult human and non-human primates do no support the 4-phase model, as none find evidence of a switch from novelty to familiarity preference with increasing delay. These studies lend weight to the arguments that the 4-phase model may not apply generally to recognition memory but more specifically to recognition measured using certain types of stimuli or testing procedures.


We are still left with the findings that infants sometimes show familiarity and sometimes novelty preferences. Is there a model to understand this? We aim now to tackle this problem with a different approach.

Event-related Potentials Even-related potentials (ERPs) may provide insight in to the puzzle of why infants sometimes show novelty and sometimes show familiarity preferences. The use of ERP measures to study infant recognition is of great interest to researchers because ERPs can provide information about the timing of neurocognitive processes that occur while an individual is processing a stimulus, rather than provide information only about the outcome of these processes (see Nelson & Monk, 2001 for a review of the use of ERPs to study cognitive development).

For example, while measures of looking time only indicate

whether the infant recognises the stimulus or not, ERPs could provide information about whether the neural processes related to familiarity and novel preferences are similar or different. This information would help disambiguate whether the function of novelty and familiarity preferences are similar or different.

Event-related potentials are transient changes in the brain’s electrical activity that occur response to a discrete event (e.g., brief presentation of a visual stimulus). These signals can be measured by recording electrodes placed on the scalp. Detecting the changes in electrical activity that occur in the brain following


presentation of the event requires the summation of the activity of large numbers of neurons that fire in synchrony in response to the event. Because time is required for the summation of activity across neurons, the current that is detected by ERPs is likely the slower post-synaptic potentials rather than the more rapid action potentials (Allison, Woods, & McCarthy, 1986). The ERP is thought to reflect primarily the activity of pyramidal cells in the cortex and hippocampus, because the position and orientation of these cells relative to the scalp surface make their activity most likely to be conducted up to the scalp (Allison, 1984).

ERPs are ideal for studying the neural correlates of infant memory because they are non-invasive and they can be recorded passively (without the need for the infant to make a behavioural response). Electrodes are simply secured to the scalp by one of various methods (see Johnson et al., in press; Nelson, 1994), and the infant is presented with a series of stimuli.

Typically, stimuli are

repeatedly for brief durations (e.g., durations less than 1 second), because the changes that occur in response to the stimulus can be relatively small compared to the background brain activity. In order to detect the change, it is necessary to average across of a number of presentations so that activity time-locked to the presentation of the stimulus is retained and background activity that is random with respect to the presentation of the stimulus averages to small values. The resulting average ERP waveform consists of a series of components and slow waves that are thought to reflect particular aspects of information processing. Components reflect processes that occur more discretely in time and are seen as


deflections in the ERP that have clearly-defined peaks, while slow waves reflect processes that occur over more prolonged periods and are seen as sustained deviations from baseline in the ERP. Figure 5 shows the pattern of components and slow waves typically observed in studies of visual recognition in infants.

Nelson and Collins (1991; 1992) used ERPs to examine infants’ visual recognition of faces. Four, 6-, and 8-month-old infants were familiarized with two faces for 10 500-ms trials each and then were immediately presented with one of the familiar faces frequently (60% probability), the other familiar face infrequently (20%) and a series of trial-unique novel faces infrequently (20%). They found that late slow wave activity differed among the test faces: positive slow wave activity was interpreted as representing the updating of a decaying/incomplete memory, return to baseline was interpreted as complete encoding, and a negative slow wave was interpreted as detection of novelty. Interestingly, they found an age progression in which only 8-month-olds were able to treat familiar stimuli the same regardless of frequency of occurrence. These results suggest that younger infants may have more rapid decay of memories than older infants.

In addition, the framework proposed by Nelson (1994) suggests that novelty preferences and familiarity preference may have different neural correlates. For example, longer looking to the familiar stimulus may be functionally related to the positive slow wave that is elicited by a familiar stimulus. Both are thought to be reactions to incomplete stimulus representations; in this instance the novel


stimulus might elicit a return to baseline/unencoded or a negative slow wave/novelty detection without further encoding. In contrast, longer looking to novelty may be functionally related to the positive slow wave elicited by the novel stimulus with the familiar stimulus eliciting return to baseline for a fully encoded stimulus.

ERP studies support the finding obtained from looking time studies that the nature of the encoding experience has an impact on later recognition. While Nelson and Collins (1992) found that 4-month-olds show no ERP evidence of recognition following a brief familiarisation, another study (Pascalis et al., 1998) found that even 3-month-olds were able to show recognition and complete encoding of the familiar stimulus if a habituation-to-criterion familiarization procedure was used prior to the ERP memory test (see also de Regnier, Georgieff & Nelson, 1997 for findings showing that 4-month-olds show evidence of recognition simpler paradigm than that used by Nelson & Collins [1992] is used) .

Few ERP studies have investigated the effects of delay. However, one such study demonstrates that following habituation-to-criterion, a short delay does not impact the nature of the waveforms (Nelson, Thomas, de Haan & Wewerka, 1998).

In that study, 8-month-olds showed the same ERP evidence of

recognition of the face after both a 1-minute and a 5-minute delay.


Thus, data from ERP experiments generally support the findings from VPC experiments: early in life infants are able to recognize a stimulus that they have encountered previously and processing of familiar and novel stimuli produces distinguishable waveforms. Nelson’s (1994) theory of the functional correlates of infants’ late slow-wave activity in recognition memory tasks suggests that novelty and familiarity preferences may have different neural correlates.

The ERP

studies also suggest that the nature of the encoding experience affects the expression of recognition in the ERP waveforms, as it affects the expression of recognition in looking times. The preliminary evidence with relatively short delays (5 minutes) suggests that the ERP correlates of recognition do not change with delay if the stimulus was initially well-encoded. However, longer delays will need to be tested to examine whether changes do occur with increasing delays.

Novelty Preference Model While numerous factors have been documented to affect infants’ recognition memory, there is not a fully satisfactory model of recognition memory in the human infant. Our understanding might be improved by analyzing the cerebral structures involved in recognition. In this section we will first review the studies of the neural bases of novelty preference in human adults and in nonhuman primates, and then relate these findings to human infants.

A neural model of recognition memory has been described in human and nonhuman adult primates that can assist our understanding of this system during


infancy (Murray & Miskin, 1984). This model describes in detail the neural pathways that are involved in recognition memory as measured by the VPC task. It has been developed on the basis of work with amnesic patients and with on animals with specific brain lesions. As proposed by Mishkin and Murray (1994), visual information is processed sequentially along an occipito-temporal pathway (Figure 6). This ventrally directed chain of cortical visual areas appears to extract stimulus-quality information, such size, colour, shape and texture, from the retinal input reaching the striate cortex, until the final stations of the inferior temporal cortex (area TE) synthesize a complete representation of the object. Storage of the object’s representation is achieved each time a perception formed in the final station of the visual cortical sensory system activates the pre- and entorhinal areas, which in turn, trigger the medial thalamic nuclei and the orbital prefrontal cortex. The medial temporal lobe and orbito-frontal cortex also sends projections to the basal forebrain, which has connections that feed back to the sensory areas.

This model is relevant for recognition as measured by VPC. Indeed, recognition memory loss on the VPC task is found in both infant and adult monkeys with damage to the medial temporal lobe, including the hippocampal formation, amygdala and surrounding tissue (Bachevalier et al., 1993). Similarly, using the VPC task, McKee and Squire (1993) demonstrated impaired recognition memory in amnesic patients with hippocampal damage. Recently, Pascalis and Bachevalier (1999) showed that, adult monkeys with neonatal hippocampal


lesions, exhibit a preference for novelty after short delays of 10 sec but not after longer delays of 30 sec to 24 hrs whereas normal monkey present novelty preference at any delay. In studies with more selective lesions within the medial temporal lobe, the novelty preference has been shown to depend on the integrity of the hippocampal formation (Zola et al., 2000) and the perirhinal cortex (Clark & al.,1996; 1997). These results are also consistent with neuroimaging work with human adults indicating that the hippocampus plays an important role in encoding and responding to stimulus novelty (Dolan & Fletcher, 1997; Elliottt & Dolan, 1998), even in tasks like VPC where there is no intention or objective requirement for memory retrieval (Schacter, Alpert, Savage, Rauch, & Albert, 1996; Rugg, Fletcher, Frith, Frackowiak & Dolan, 1997).

While these studies are informative with regards to the neural underpinnings of novelty preference in the VPC task, they do not provide information about familiarity preferences as none were seen in those studies. Understanding the neural bases of familiarity preferences is of interest in order to test the different models described above. For example, if familiarity preferences following incomplete encoding and delay are both due to further encoding of incomplete stimulus representations, then both may have similar neural correlates. However, if familiarity preferences after long delays reflect a different stage of memory storage, the neural correlates might be different from those observed following incomplete encoding.


The ‘mere exposure effect’ in human adults may relate to familiarity preferences observed in infants. This effect refers to the phenomenon that briefly preexposing adults to visual stimuli is sufficient to establish a subsequent verbally reported preference for those stimuli, even when this previous exposure is subliminal (i.e., so brief that explicit recognition is at chance). It is possible that infants’ familiarity preferences, particularly those seen after brief familiarization periods, represent a similar phenomenon. In one functional magnetic resonance imaging study using the mere exposure effect, adults were subliminally exposed to a set of visual stimuli and subsequently were asked to make memory judgements or preference judgements for pairs of stimuli consisting of either a familiar and novel stimulus or two novel stimuli (Elliott & Dolan, 1998). While their recognition performance was at chance, adults showed evidence of implicit memory for the stimuli in that in preference judgements they were more likely to choose the familiar stimulus. The results indicated that right hippocampal regions were activated by stimulus novelty regardless of context. Preference judgements were associated in addition by subcortical (caudate and pulvinar), medial occipital and left frontal activations while memory judgements were associated with by left parietal and frontal activations. Thus, familiarity preferences might be mediated by neural structures that are not identical to those mediating novelty preferences.

Is this system mature enough to support recognition memory during infancy? It has been thought for years that the hippocampal formation was not mature at


birth and that it developed slowly during infancy in primates. However, this assumption was based on the development of the hippocampus in rodents that are born at a more premature level than primates. Recently, Alvarado and Bachevalier (2000) wrote a review of the development of the medial temporal lobe system in monkeys and showed that at birth the vast majority of cells and connections are in place in the hippocampal formation. There is even evidence that some of the connections are functional before birth (Berger, Alvaraz and Goldman-Rakic., 1993)! Seress (2000) wrote an heuristic and fascinating review on the development of the hippocampal formation in humans. He concluded also that these structures are anatomically more mature than was thought, even if it can not firmly concluded that they are equally functionally mature.

Although the infant visual object processing pathway is still immature, visual recognition observed as novelty preferences in VPC seems to be depend on a neural network similar to the mature one as illustrated by lesions’ studies (Webster, Bachevalier & Ungerleider, 1995). With regards to familiarity preferences, it is possible that, at least for those seen following brief familiarizations, they might in part depend on a slightly different network involving contributions from subcortical and occipital areas.

Concluding Remarks The data reviewed in this chapter provide help for our understanding of the development of visual recognition memory. Visual paired comparisons involve


the incidental learning of a stimulus to be recognized after a delay, with recognition assessed by a longer looking toward the novel or the familiar stimulus. This paradigm is useful because it can be used across the lifespan if the familiarization times are carefully adapted for each age group. The fact that it is also observed in monkeys has facilitated the identification of its neural bases. The cerebral structures involved in novelty preferences appear to be relatively constant throughout ontogeny though there may be some developmental changes in the pathway and its connections. The observation that infants sometimes prefer to look at familiar stimuli has led to the development of several models of how the direction of infants’ looking relates to the status of their internal representations of stimuli.

The results of ERP

studies suggest that familiarity preferences may have different neural correlates than novelty preferences, although a more systematic investigation of ERP indices of memory at different ages following different delays is needed. This will help determine whether familiarity preferences in delayed recognition reflect decay (decreased accessibility of the stimulus representation) or whether they reflect a stage in information storage.


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Diamond, A. (1995). Evidence of robust recognition memory early in life even when assessed by reaching behavior. Journal of Experimental Child Psychology, 59, 419-456. Dolan, R. J., & Fletcher, P. C. (1997). Dissociating prefrontal and hippocampal function in episodic memory encoding. Nature, 388 , 582-585. Elliott, R., & Dolan, R. J. (1998). Neural response during preference and memory judgements for subliminally presented stimuli: A functional neuroimaging study. The Journal of Neuroscience, 18, 4697-4704. Fagan, J.F. (1973). Infants' delayed recognition memory and forgetting. Journal of Experimental Child Psychology, 16, 424-450. Fagan, J.F. (1974). Infant recognition memory: the effects of length of familiarization and type of discrimination task. Child Development, 45, 351356 Fantz, R.L. (1964). Visual experience in infants: Decreased attention to familiar patterns relative to novel ones. Science, 146, 668-670. Gunderson, V. M. & Swartz, K. B. (1985). Visual recognition in infant pigtailed macaques after a 24- hour delay. American Journal of Primatology, 8, 259264. Horowitz, F., Paden, L., Bhana, W. & Self, P. (1972). An "infant control" procedure for studying infant visual fixations. Developmental Psychology, 7, 90. Hunt, J.M. (1963). Piaget’s observations as a source of hypotheses concerning motivation. Merrill-Palmer Quarterly, 9, 263-275. Jankowski, J. J., Rose, S. A., & Feldman, J. F. (2001). Modifying the distribution of attention in infants. Child Development, 72, 339-351. Johnson, M. H. de Haan, M., Hatzakis, H., Oliver, A., Smith, W., Tucker, L. A. & Csibra, G. (2001). Recording and analyzing high density ERPs with infants using the geodesic sensor net. Accepted for publication in Developmental Neuropsychology.


Manns, J. R., Stark, C.E. L., & Squire, L. R. (2000). The visual-paired comparison task as a measure of declarative memory. Proceedings of the National Academy of Sciences USA, 97, 12375-1239. Martin, R.M. (1975). Effects of familiar and complex stimuli on infant attention. Developmental Psychology, 11, 178-185. McCarthy, R.A. & Warrington, E.K. (1992) Actors but not scripts - the dissociation of people and events in retrograde-amnesia. Neuropsychologia, 30, 633-644. McGaugh, J.L. (1966). Time dependent processes in memory storage. Science, 153, 1351-1358. McKee, R.D. & Squire, L.R. (1993) On the development of declarative memory. Journal of Experimental Psychology: Learning, Memory and Cognition, 19, 397-404. Mishkin M., Murray E.A. (1994). Stimulus recognition. Current Opinion in neurobiology. 4, 200-206. Meltzoff, A., N. (1990). Towards a developmental cognitive science. The implications of cross-modal matching and imitation for the development of representation and memory in infancy. In A. Diamond (Ed.), Development and neural bases of higher cognitive functions (pp.1-31). New York: New York Academy of Sciences Press. Nachman, P. A., Stern, D. N., & Best, C. (1986). Affective reactions to stimuli and infants’ preference for novelty and familiarity. Journal of the American Academy of Child Psychiatry, 25, 801-804. Nelson, C. A., & Collins, P. F. (1991). Event-related potential and looking-time analysis of infants’ responses to familiar and novel events: Implications for recognition memory. Developmental Psychology, 27, 50-58. Nelson, C. A., & Collins, P. F. (1992). Neural and behavioral correlates of recognition memory in 4- and 8-month-old infants. Brain & Cognition, 19, 105-121.


Nelson, C. A. (1994). Neural correlates of recognition memory in the first postnatal year of life. In G. Dawson & K. Fischer (Eds.), Human behavior and the developing brain (pp. 269-313). New York: Guilford Press. Nelson, C. A. (1995). The ontogeny of human memory: A cognitive neuroscience perspective. Developmental Psychology, 31, 723-738. Nelson, C. A., Thomas, K. M., de Haan, M. & Wewerka, S.S. (1998). Delayed recognition memory in infants and adults as revealed by event-related potentials. International Journal of Psychophysiology, 29, 145-165. Nelson, C. A. & Monk, C. (2001). The use of event-related potentials in the study of cognitive development. In C. A. Nelson & M. Luciana (Eds.), Handbook of Developmental Cognitive Neuroscience (pp. 125-136). Cambridge, MA: MIT Press. Pancratz, C.N. & Cohen, L.H. (1970). Recovery of habituation in infants. Journal of Experimental Child Psychology, 9, 208-216. Pascalis, O. & de Schonen, S. (1994). Recognition memory in 3-4-day-old human infants. NeuroReport, 5, 1721-1724. Pascalis, O., de Schonen, S., Morton, J., Deruelle, C., & Fabre-Grenet, M. (1995). Mother’s face recognition by neonates: a replication and an extension. Infant Behavior and Development, 18, 79-85. Pascalis, O., & Bachevalier, J. (1998). Face recognition in Primates: a cross species study. Behavioral Processes, 43, 87-96. Pascalis O., de Haan M., Nelson C.A., de Schonen S. (1998). Long-term recognition assessed by visual paired comparison in 3- and 6-month-old infants. . Journal of Experimental Psychology: Learning, Memory and Cognition, 24, 249-260. Pascalis, O., & Bachevalier, J. (1999). Neonatal aspiration lesions of the hippocampal formation impair visual recognition memory when assessed by paired-comparison task but not by delayed nonmatching-to-sample task. Hippocampus, 9, 609-616.


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Sophian, C. (1980). Habituation is not enough: Novelty preferences, search and memory in infancy. Merrill-Palmer Quarterly, 26 239-257. Spence, M. (1996). Young infants’ long-term auditory memory: Evidence for changes in preferences as a function of delay. Developmental Psychobiology, 29, 685-695 Webster, M.J.; Bachevalier, J. & Ungerleider, L. (1995). Developement and plasticity of visual memory circuits. In B.Julesz, G. Cowan and I. Kovacs (Eds), Maturational Windows and Cortical plasticity in Human Development. Addison-Wesley publishing company. Weizmann, F., Cohen, L. B., & Pratt, J. (1971). Novelty, familiarity, and the development of infant attention. Developmental Psychology, 4, 149-154. Zola, S. M., Squire, L. R., Teng, E., Stefanacci, L., Buffalo, E. A., & Clark, R. E. (2000). Impaired recognition memory in monkeys after damage limited to the hippocampal region. Journal of Neuroscience, 20, 451-463.


Figure 3: Videoframes (3/100 sec) of a infant’s eye movements during the retention tests of the VPC task. From top to bottom, the corneal reflections of the two stimuli (two white bars inside the monkey’s pupils) indicate that


the child looked at the stimulus on its left, then, at the center, and finally at the stimulus on the right.

Figure 6: Schematic representation of the postulated circuit for visual recognition memory in adult monkeys.


% of fixation to the novel

60

55

50

45

40 24 Hours

1 Week

1 month

Figure 4: Percent looking time at the novel object during each delay conditions of the VPC task.


Familiarization

Recognition test Figure 1: Visual Paired Comparison task (VPC): Infant is presented with the sample for a familiarization period. Thereafter, the participant is confronted with the familiar stimulus and a new stimulus. The time spent fixating each stimulus is recorded.


Figure 2: Example of the experimental setting. The infant is watching pictures, a camera located above the screen record her eye movments.


Figure 3: Videoframes (3/100 sec) of a infant’s eye movements during the retention tests of the VPC task. From top to bottom, the corneal reflections of the two stimuli (two white bars inside the monkey’s pupils) indicate that the child looked at the stimulus on its left, then, at the center, and finally at the stimulus on the right.


Figure 6: Schematic representation of the postulated circuit for visual recognition memory in adult monkeys.


% of fixation to the novel

60

55

50

45

40 24 Hours

1 Week

1 month

Figure 4: Percent looking time at the novel object during each delay conditions of the VPC task.


Familiarization

Recognition test Figure 1: Visual Paired Comparison task (VPC): Infant is presented with the sample for a familiarization period. Thereafter, the participant is confronted with the familiar stimulus and a new stimulus. The time spent fixating each stimulus is recorded.


Figure 2: Example of the experimental setting. The infant is watching pictures, a camera located above the screen record her eye movments.


The Infant Event-Related Potential During a Visual Recognition Task PSW 15

10

5

Nc Return to Baseline

0

-5

-10

-15

NSW -20 0

200

400

600

800

1000

1200

1400

-25 Latency (milliseconds)

* Nc (negative component) -middle latency response occurring 400 to 800 msec after stimulus onset -attentional response

* PSW (positive slow wave) - later latency response occuring 800 to 1700 msec after stimulus onset -memory updating

* NSW (negative slow wave) - later latency response occuring 800 to 1700 msec after stimulus onset -detection of novelty

* Return to baseline - later latency response occuring 800 to 1700 msec after stimulus onset -present for stimuli not requiring memory updating and not detected as novel

Figure gure 5: An example of different components observed in the infant event-related potential.

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Recognition Memory and Novelty Preference: What Model - LPNC

Recognition Memory and Novelty Preference: What Model - LPNC

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