Recall in Infancy: A Neurodevelopmental Account

ABSTRACT— Relations between developments in neural structures and changes in memory in infancy are a relatively recent focus of research. Greater knowledge about brain development, as well as methodological advances such as combined use of behavioral and electrophysiological techniques, have led to the generation and testing of specific hypotheses regarding sources of age-related change. Theory and data converge to suggest that the early-stage processes of encoding and consolidation are a significant source of age-related variability in memory early in life. Additional research is needed to determine how these processes change and interact with myriad other determinants of recall.     

Developments in long-term explicit memory late in the first year of life: behavioral and electrophysiological indices

Coincident with developments in the temporal-cortical explicit memory network, long-term recall abilities are newly emergent late in the first year of human life. We recorded event-related potentials (ERPs) in 9-month-olds as an index of the integrity of the neural substrate underlying a task thought to reflect explicit memory, namely, deferred imitation. ERP measures of recognition memory 1 week after unique laboratory experiences predicted whether and how much infants recalled of the experiences 1 month later. The findings further imply that memory storage and consolidation processes are a major source of variability in long-term recall memory late in the first year of life.     

Constructing a past in infancy: a neuro-developmental account

The ability to recall the past is fundamental yet until relatively recently, infants were assumed to lack the capacity. Contrary to this perspective, non-verbal tests indicate that developments in recall are well underway by late in the first year of life; by the end of the second year, long-term recall is reliable and robust. New research combining electrophysiological and behavioral measures is identifying the loci of age-related changes: they are attributed to more effective and efficient encoding, consolidation and storage processes associated with developments in the temporal-cortical network that subserves recall. The emerging framework, which applies to episodic and autobiographical memory, highlights the essential developmental continuities in memory from infancy onwards and sheds new light on the phenomenon of childhood amnesia.     

Learning to remember: Social-communicative exchanges and the development of children’s memory skills

For more than three decades, the question “What is memory development the development of?” has guided research on children’s memory. As theories and methodologies have evolved, so too has our knowledge of the mnemonic competencies of young children, and of age-related differences in memory performance. Unfortunately, however, current understanding of the development of memory is seriously limited, largely because the bulk of the literature is based on cross-sectional experiments. From our perspective, in order to increase our understanding of the development of children’s skills for remembering, it is necessary to conduct longitudinal studies that illuminate mechanisms underlying developmental change. In addition, experimental methods must be used to explore further the operation of these potential mediators of change. In this article, we review our own recent longitudinal and experimental research to illustrate how we are addressing a new call—to study both memory development and the development of memory.     

The development of explicit memory for basic perceptual features

In three experiments with 164 individuals between 4 and 80 years old, we examined age-related changes in explicit memory for three perceptual features--item identity, color, and location. In Experiments 1-2, feature recognition was assessed in an incidental learning, gamelike task resembling the game Concentration. In Experiment 3, feature recognition was assessed using a pencil-and-paper task after intentional learning instructions. The form of the explicit memory function across the life span varied with the particular perceptual feature tested and the type of task. Item recognition was excellent at all ages but was significantly poorer for older adults than children, color recognition peaked in late childhood on the gamelike task, and location recognition peaked in early adulthood on the pencil-and-paper task. These findings indicate that performance on explicit memory tests is not a consistent inverted U-shaped function of age across various features. Explicit memory performance depends on what is measured and how. Because explicit memory typically reflects a composite of different features, age-related changes in explicit memory will not necessarily correspond to the function for any single one.     

Reliability, Distribution, and Validity of Age-Related Cognitive Deficits in the Morris Water Maze

In the present study, F-344 rats throughout 1.5 to 26 months of age were tested in the reference memory version, a moving-platform repeated acquisition version, and in a cued platform version of the Morris water maze. The results suggest that: (1) performance in the water maze declines continuously, beginning at the earliest age, and very closely fits a linear function; (2) there are robust, reliable differences between individuals in terms of their performance in the Morris water maze, but chronological age accounts for only a fraction of the variance between individuals; (3) there is no evidence of a bimodal distribution among aged rats—there is no distinct subgroup of individuals that performs so poorly that they are qualitatively different from the majority of the population, and distinctions between “impaired” and “unimpaired” subjects must be based on arbitrary criteria that may not be consistent from one study to the next; (4) age-related deficits in the Morris water maze may not be restricted to learning and memory, but may also include deficits in attention, the ability to process spatial information, and/or the ability to develop efficient spatial search strategies; and (5) swim distance is the most appropriate measure of cognitive function in the Morris water maze, but the relationship between this measure and other measures of noncognitive function make it clear that swim distance may not be a pure measure of cognitive function. Although the Morris water maze remains a valuable preclinical test with better validity and specificity than many other behavioral tests, measures of performance in the Morris water maze should not be considered synonymous with cognitive function.     

Motivationally neutral stimulation of the nucleus basalis induces specific behavioral memory

The cholinergic system has been implicated in learning and memory. The nucleus basalis (NB) provides acetylcholine (ACh) to the cerebral cortex. Pairing a tone with NB stimulation (NBstm) to alter cortical state induces both associative specific tuning plasticity in the primary auditory cortex (A1) and associative specific auditory behavioral memory. NB-induced memory has major features of natural memory that is induced by pairing a tone with motivational reinforcers, e.g., food or shock, suggesting that the cholinergic system may be a “final common pathway” whose activation promotes memory storage. Alternatively, NB stimulation might itself be motivationally significant, either rewarding or punishing. To investigate these alternatives, adult male rats (n = 7) first formed a specific NB-induced memory (CS = 8.0 kHz, 2.0 s paired with NBstm, ISI = 1.8 s, 200 trials), validated by post-training (24 h) frequency generalization gradients (1–15 kHz) of respiration interruption that were specific to the CS frequency. Thereafter, they received the same level of NBstm that had induced memory, while confined to one quadrant of an arena, and later tested for place-preference, i.e., avoidance or seeking of the quadrant of NBstm. This NBstm group exhibited neither preference for nor against the stimulated quadrant, compared to sham-operated subjects (n = 7). The findings indicate that specific associative memory can be induced by direct activation of the NB without detectable motivational effects of NB stimulation. These results are concordant with a memory-promoting role for the nucleus basalis that places it “downstream” of motivational systems, which activate it to initiate the storage of the current state of its cholinergic targets.     

The K-factor: Individual differences in life history strategy

Until recently, variations in life history strategy were studied exclusively at the species level. Although this domain of study has been extended to examine systematic differences in life history strategy among various human ethnic groupings, more recent evolutionary theories of human development and related behavioral genetic work imply substantial within-group individual variation in life history strategy. We constructed a latent variable model identifying a single common factor, denoted as K, which underlies a variety of otherwise disparate life history parameters. This “K-Factor” loaded 0.36 on childhood attachment to the biological father, −0.36 on childhood attachment to any non-biological father figure, 0.38 on adult romantic partner attachment, −0.51 on mating effort, −0.58 on Machiavellianism, and −0.41 on risk propensity. The bivariate correlations of the K-factor with higher-order personality factors were statistically significant, −0.24 with “Big Neuroticism” and −0.67 with “Big Psychoticism”, and approached significance, correlating 0.12, with “Big Extraversion”. The K-factor appears to be an underappreciated individual difference variable of major importance to human development.     

Electroencephalogram and heart rate measures of working memory at 5 and 10 months of age

We recorded electroencephalogram (EEG; 6-9 Hz) and heart rate (HR) from infants at 5 and 10 months of age during baseline and performance on the looking A-not-B task of infant working memory (WM). Longitudinal baseline-to-task comparisons revealed WM-related increases in EEG power (all electrodes) and EEG coherence (medial frontal-occipital electrode pairs) at both ages. WM-related decreases in HR were only present at 5 months, and WM-related increases in EEG coherence became more localized by 10 months. Regression analyses revealed that baseline-to-task changes in psychophysiology accounted for variability in WM performance at 10 but not 5 months. HR and EEG power (medial frontal and lateral frontal electrodes) were unique predictors of variability in 10-month WM performance. These findings are discussed in relation to frontal lobe development and represent the first comprehensive longitudinal analysis of age-related changes in the behavioral and psychophysiological correlates of WM.     

Faustlos: Evaluation of a curriculum to prevent violence in elementary schools

The “Faustlos”¹ curriculum, an adaptation of the American Second Step program, for the prevention of aggressive behaviors of elementary school children was evaluated in a 3-year control group study (30 classes served as an experimental group, 14 classes as a control group). The results show significant changes in the emotional competences and prosocial developments of children aged 6–9 years. Children who participated in the “Faustlos” lessons showed significantly reduced anxiety and internalizing behaviors compared with the control group. The parents’ ratings of their children's behavior (according to the Child Behavior Checklist) provided clear evidence of improved social behavior outside the school environment.     

Metaphoric comprehension: Studies in reminding and resembling

The theoretical problems posed by metaphoric comprehension are discussed in the context of experiments on prompted recall. Listeners heard sentences of the form “Topic is (like) Vehicle.” In most cases, a statement of the implicit resemblance (the “ground”) was very effective in prompting recall of its related metaphor. This result could not be attributed to the activation, transfer, or additive combination of pre-existing properties of the topic and vehicle terms or to pre-existing associations between grounds and sentence terms. It is argued that the vehicle domain guides a novel schematization of the topic domain, that the perceived resemblance is a higher-order relation among entities (both explicit and implicit) in each domain, and that this abstract relation constitutes the “functional memory unit.” Prompted recall may begin with recognition of this previously experienced relation.     

The Critical Role of Cholinergic Basal Forebrain Neurons in Morphological Change and Memory Encoding: A Hypothesis

It has been known for a long time that cholinergic basal forebrain neurons which project to the cerebral cortex play a role in learning and memory. Behavioral studies following lesions, for example, repeatedly have suggested multiple learning-related roles for these neurons. Apart from behavioral studies, cholinergic neurons have been shown to possess extraordinarily plastic axons. This plasticity has not been related comprehensively to mnemonic devises, even though morphological changes in the CNS are prime candidates for the neural engram. In this paper, I propose a hypothesis that relates these two characteristics of cholinergic neurons. This hypothesis is that plastic cholinergic axon terminals induce structural reorganization in their targets during memory storage. Possible intracellular mechanisms are examined, whereby acetylcholine release in the cerebral cortex could cause postsynaptic structural changes. Finally, the characteristics of the overall cholinergic–cholinoceptive cell “engram” are elaborated with particular attention paid to the encoding of the stimulus properties along with the context and meaning of the stimulus.     

A double dissociation of implicit and explicit memory in younger and older adults

This study examined whether age-related differences in cognition influence later memory for irrelevant, or distracting, information. In Experiments 1 and 2, older adults had greater implicit memory for irrelevant information than younger adults did. When explicit memory was assessed, however, the pattern of results reversed: Younger adults performed better than older adults on an explicit memory test for the previously irrelevant information, and older adults performed less well than they had on the implicit test. Experiment 3 investigated whether this differential pattern was attributable to an age-related decline in encoding resources, by reducing the encoding resources of younger adults with a secondary task; their performance perfectly simulated the pattern shown by the older adults in the first two experiments. Both older and younger adults may remember irrelevant information, but they remember it in different ways because of age-related changes in how information is processed at encoding and utilized at retrieval.     

Associations Between Infant Brain Activity and Recall Memory

Long‐term explicit memory is thought to involve a complex neural circuit including the medial temporal lobe, the medial diencephalon, the prefrontal cortex, and association cortices. When this memory system and associated neural circuitry develops is of great interest to developmental psychologists and developmental cognitive neuroscience researchers. In the present report, we provide evidence of a relation between behavioral and neurophysiological measures of long‐term explicit memory in 9‐month‐old infants. These measures provide converging evidence of the development of long‐term explicit memory at least by the end of the first year of life.     

Effects on Episodic Memory of Stimulus Richness, Intention to Learn, and Extra-Study Repetition: Similar Profiles Across the Adult Life Span

The ability to benefit from various kinds of cognitive support in episodic memory was studied in a population-based sample of healthy adults aged 35–80 years (N = 1,000). The participants studied pictures of faces and names of 10-year-old children with instructions to remember the faces and the surnames. After study, an implicit name stem-completion test was administered, followed by face- and name-recognition tests. There was a negative age effect across all task variables. Across age, recognition was higher for faces than for names. An age-invariant positive effect of intention to learn was observed. Also, name completion and recognition performance showed a positive relationship across the adult life span. Overall, the results are in agreement with the views that (a) age-related episodic memory deficits are highly generalizable and (b) effects of cognitive support on memory are typically of equal size across the adult life span.     

Which is the real intelligence? A reply to Robinson (1999)

Robinson's ([Robinson, D.L. (1999). The ‘IQ’ factor: implications for intelligence theory and measurement. Personality and Individual Differences, 27, 715–735]) arguments that crystallized intelligence represents the “one valid intelligence factor” are disputed. It is argued that Robinson seriously underestimated the relevance of fluid abilities to “intelligence”, by using an inappropriate criterion for assessing the intelligence-saturation of cognitive ability variables. The relevance of fluid and crystallized abilities to popular, psychometric, and biological conceptions of intelligence is discussed, and the issue of age-related changes in fluid and crystallized intelligence is also addressed.     

Through the looking glass: Sex differences in memory for self-facial poses

This study investigated recognition memory of photographs of the subject's own face. Male and female subjects were photographed as they projected sociable faces, trustworthy faces, and intelligent faces. After deciding which face of 10 best represented each characteristic, and judging which photograph best represented their “real self,” a recognition memory test of poses was given. Half of each sex were tested under intentional learning conditions and the remainder were tested under incidental learning conditions. Females demonstrated superior recognition memory of their own facial projections and, in particular, recalled photographs of their “real self” and “most sociable” self most easily. No differences were found between the two learning conditions. Subjects' recognition performance was not related to their confidence of judgments. The results were discussed in terms of sex differences and the role of self in memory.     

Interpersonal dominance and coronary prone behavior

Type A “coronary-prone behavior” is a risk factor for coronary artery and heart disease. Questionnaire research indicates that interpersonal dominance is one of the strongest behavioral correlates of the Type A behavior pattern, although little effort has been made to demonstrate a link between the behavioral manifestations of interpersonal dominance and Pattern A responding. This study was conducted to establish such a link. All possible combinations of extreme As (N = 42) and Bs (N = 42) were matched in dyads that negotiated extreme bipolar opposite positions on a “teacher dismissal” issue. Analysis of process and outcome behaviors suggested that type A individuals are unilaterally more dominant than their Type B counterparts. Possible physiological mechanisms mediating dominance and cardiovascular disease are discussed.     

When the mind wanders: Age-related differences between young and older adults

Interest in mind wandering (MW) has grown in recent years, but few studies have assessed this phenomenon in older adults. The aim of this study was to assess age-related differences between young, young–old and old–old adults in MW using two versions of the sustained attention to response task (SART), one perceptual and one semantic. Different indicators were examined (i.e., reported MW episodes and behavioral indices of MW such as response time latency and variability, incorrect response and omission errors). The relationship between MW, certain basic mechanisms of cognition (working memory, inhibition and processing speed), cognitive failures and intrusive thoughts in everyday life was also explored. Findings in both versions of the SART indicated that older adults reported a lower frequency of MW episodes than young adults, but some of the behavioral indices of MW (response time variability, incorrect response and omission errors) were higher in old–old adults. This seems to suggest that MW becomes less frequent with aging, but more pervasive and detrimental to performance. Our results also indicated that the role of age and cognitive mechanisms in explaining MW depends on the demands of the SART task considered.