Ontogeny of memory: An update on 40 years of work on infantile amnesia

Highlights

• Infantile amnesia is the phenomenon of accelerated forgetting in young animals.

• We review progress made over the last 40 years in understanding infantile amnesia.

• The neurobiological causes of infantile amnesia appear to be multifaceted.

• Late development of the hippocampus, amygdala and prefrontal cortex all contribute.

• Developmental changes in neurotransmitter systems also appear to be involved.

Abstract

Given the profound influence that early life experiences can have upon psychosocial functioning later in life, it is intriguing that most adults fail to recall autobiographical events from their early childhood years. Infantile amnesia is the term used to describe this phenomenon of accelerated forgetting during infancy, and it is not unique to humans. Over the years, information garnered from animal studies has provided clues as to the neurobiological basis of infantile amnesia. The purpose of this review is to provide a neurobiological update on what we now know about infantile amnesia since the publication of Campbell and Spear’s seminal review on the topic more than 40 years ago. We present evidence that infantile amnesia is unlikely to be explained by a unitary theory, with the protracted development of multiple brain regions and neurotransmitter systems important for learning and memory likely to be involved. The recent discovery that exposure to early life stress can alleviate infantile amnesia offers a potential explanation as to how early adversity can so profoundly affect mental health in adulthood, and understanding the neurobiological basis for this early transition may lead to the development of effective therapeutic interventions.

Introduction

Early life experiences play a pivotal role in shaping personality and psychosocial functioning into adulthood. For example, early life adversity in humans is associated with increased risk of developing mental illnesses such as depression and anxiety [1], [2], [3], [4], [5], [6], and maternal separation in non-human primates imposes long-term detrimental effects upon behaviour [7], [8], [9].

Given the importance of these first few years of life, it is intriguing that most adults fail to maintain autobiographical memories from this critical period. In general, when adults are asked to remember their earliest memories, they rarely recall events that occurred before the age of 3 and have spotty recollection of experiences that occurred between 3 and 7 years of age [10], [11], [12], [13], [14], [15], [16]. This apparent childhood memory deficit is not caused by an inability at this age to form episodic memories [17]. In a study where children aged between 5 and 10 were asked to recall their earliest memories, they frequently recalled events that occurred when they were younger than 1 year old—and some as young as 1 month [18], [19]. In contrast, children aged between 12 and 13 failed to recall any events that occurred prior to the age of 1, suggesting that a child’s earliest episodic memory recollection is influenced by that child’s current age [18], [20]. Mere passage of time is insufficient to explain the transience of these memories formed in early childhood. For example, a 40 year old adult can readily remember events that occurred when they were 21, however, a 20 year old would be hard-pressed to recall an event that occurred when they were 1 year old. This indicates that our remembering ability increases with development and maturation. In other words, the rate of spontaneous forgetting is more rapid the younger our age. This phenomenon was first described in the literature over a century ago [21], but Freud was the first to refer to this accelerated forgetting as ‘infantile amnesia’ [22].

Compared to the extraordinary amount of progress made in understanding the mechanisms of learning and memory [23], we still have a poor understanding of spontaneous forgetting. Dementias such as Alzheimer’s disease are characterised by pathological forgetting, and anxiety disorders such as post-traumatic stress disorder involve an inability to forget a traumatic experience. Therefore, uncovering the secrets underlying forgetting is crucial. Most of what we understand about the mechanisms of forgetting has been derived from studies of infantile amnesia, as this form of spontaneous forgetting is relatively easy to observe and manipulate in a laboratory setting. The purpose of this review is to provide an update of what we have learned over the 40+ years since the publication of Campbell and Spear’s seminal review on the ontogeny of memory written largely based on infantile amnesia studies [24]. We aim to uncover how memory develops across the lifespan and what factors can influence this developmental trajectory, the mechanisms by which early memories are formed and rapidly forgotten, and address the paradox of how childhood experiences, though seldom remembered, are capable of dramatically influencing later development.