Episodic-like memory in infancy: Insights from the developing hippocampus

On visits to my mother’s house, it is inevitable that we look through baby pictures, a tradition that has grown increasingly common since I began my research into memory development. I know the stories behind many of these pictures, mostly through my mother. This past winter, fixing her VHS player offered a new opportunity for reminiscing. The first unlabeled tape we played was of the day my twin sister and I arrived home from the hospital—the beginning of our life stories, and yet a day we could not remember.

Why are we so fascinated by our earliest memories? Memories for specific events in our lives (episodic memories) form the basis of our personal identities, and shape how we see ourselves in the world¹. Despite the immense amount of learning in the first few years of life, most of us report our first specific memories from around 3 to 4 years of age^2,*. This lack of specific memories from infancy and toddlerhood (termed infantile amnesia by Freud³) has been the subject of both scientific debate^4,5 and public interest⁶. More than just a philosophical question, understanding whether and how infants form memories for specific events has important implications for understanding why some early experiences have profound impacts on later development⁷. Excitingly, recent advances in neuroimaging methods in infants and young children⁸ are allowing us to probe the emergence and contents of early life memories.

Pictures can transport our family members back in time to specific moments from our infancy, even though our memories for those experiences are lost. Neuroimaging, and awake infant fMRI in particular, may help reveal the mechanisms by which we learn, remember, and forget our earliest experiences.

Infantile amnesia and brain development

Many theories of infantile amnesia^9–11 highlight developing brain systems, particularly the hippocampus¹², to explain why specific early life memories do not persist into adulthood. The hippocampus is critical for the encoding and retrieval of episodic memories in adults^13,14 and undergoes dramatic structural development in early life¹⁵. However, structural immaturity does not preclude function; many brain regions develop well into adolescence¹⁶ and are nonetheless associated with cognitive functions in childhood¹⁷. This leads to the question of whether specific memories from infancy are ‘lost’ during storage or retrieval, or were never formed in the hippocampus in the first place¹⁸. Elegant research with rodents^19–22 has begun to address this question, showing that memories for specific experiences are formed in the hippocampus in infancy and can be recalled via reactivating neurons with optogenetics in adulthood^21,22. Recent innovations in awake infant functional magnetic resonance imaging (fMRI)^23,24 has allowed translation of these findings to human infants.

Hippocampal contributions to infant memory

In our recent study²⁵, we scanned 26 infants aged 4 months to 2 years while they were awake and performing a memory task. We designed a task to examine ‘episodic-like’ memory^† for specific experiences tested at a delay outside of the window of working memory. In brief, infants viewed pictures of previously-unseen faces, objects, and scenes on top of a green kaleidoscopic background, and then saw the same picture an average of a minute later alongside a new picture from the same category in a visual paired comparison test. Using the logic of the ‘subsequent memory’ paradigm^26,27, we sorted encoding trials (i.e., the first time that infants saw a picture) based on infants’ looking time between the old and new picture at test. Hippocampal activity, particularly in the posterior subregion, was higher when infants first saw a picture that they would later show a familiarity preference for at test; moreover, infants with higher average familiarity preferences showed stronger memory-related hippocampal activity. Interestingly, there was age-related change, such that memory-related hippocampal activity was reliable only in infants older than one year of age. Because visual activation was reliable and not different between younger and older infants, this age-related change was not solely due to inadequate power to detect effects in younger infants. These results suggest that the human infant hippocampus is capable of encoding memories for specific experiences by at least the end of the first year of life, constraining theories of infantile amnesia based on deficits of memory encoding.

An early capacity for episodic-like memory encoding

The idea that infants are capable of forming specific memories early in life fits with a vast literature showing sophisticated episodic-like memory behaviors in infancy²⁸. Infant memory has been observed in tasks such as the visual paired comparison test²⁹, the mobile conjugate reinforcement paradigm³⁰, the deferred imitation paradigm³¹, and the relational binding task³², each of which exhibit one or more elements of episodic-like memory (e.g., one-shot learning, long-term retention, flexible associations, spatial/temporal context binding). One recent review³³ proposed that episodic-like memory may be even more ubiquitous in infancy than previously thought, given that paradigms that are not designed to study memory (e.g., surprise-induced learning³⁴ and social cognition³⁵) nonetheless require rapid and flexible encoding of events over extended delays.

If episodic-like memories can be formed in infancy, even in the hippocampus, why then, do they not persist into adulthood? We hypothesize that mechanisms of infantile amnesia may be more related to post-encoding processes, such as how infant memories are stored and/or later retrieved. Here, the rodent literature is quite suggestive. Neurogenesis in the hippocampus, which is prominent in early life^10,19,36, can induce forgetting by destabilizing memory engrams or altering their connections, suggesting that long term storage of infant memories may be disrupted. At the same time, infant memories can be recovered in adulthood through reminders²⁰ and optogenetic techniques^21,22, suggesting that some infant memories still exist in the brain, even if normally inaccessible for retrieval. Of course, memory encoding may still be impoverished in infancy. Indeed, we only tested memory for individual items and not relations (which engage the hippocampus more in adults³⁷), and hippocampal activity in our study tracked with familiarity preferences, which have been traditionally associated with partial or incomplete encoding³⁸. Assessing infant memories over time and across different paradigms will help reveal how different stage(s) of memory contribute to infantile amnesia.

Balancing between learning systems in early life

Hippocampal involvement in memory encoding in our study emerged around 9 to 12 months of age, which has been highlighted as an important time for memory development^39,40. Interestingly, this is notably later than hippocampal involvement in statistical learning (the ability to extract regularities from the environment), which we previously showed in infants aged 3 to 24 months⁴¹. Different developmental trajectories for statistical learning and episodic-like memory function in the infant hippocampus are consistent with anatomical development of the monosynaptic (entorhinal cortex to CA1 subfield) and trisynaptic (entorhinal cortex to dentate gyrus, CA3, and CA1) hippocampal pathways¹⁵, which have been computationally linked to statistical learning and episodic memory, respectively⁴². Subregion analyses also mapped onto known anatomical differences in the monosynaptic and trisynaptic pathways⁴³, with statistical learning effects strongest in the anterior (vs. posterior) hippocampus and memory encoding effects strongest in the posterior (vs. anterior) hippocampus.

Why would the hippocampus exhibit different developmental trajectories for statistical learning versus memory encoding? An ecological account proposes that developing organisms are adapted to meet their current environmental niche⁴⁴. When one has little prior knowledge (as is the case for an infant), it may be advantageous to extract general patterns in the environment before then encoding specific information^45,46. In other words, statistical learning may supply a ‘baseline’ from which novel information can then be compared⁴⁷. Just like perception starts broad and then narrows over development⁴⁸, cognitive processes like attention and learning may operate over broad (or ‘general’) information^†† before narrow (or ‘specific’) information⁴⁹. This may be adaptive for making predictions and guiding future behavior in a dynamic environment. At present, this is mostly theoretical, and longitudinal research is necessary for linking the emergence of statistical learning and episodic memory in the infant hippocampus. Nonetheless, these initial findings from awake infant fMRI are contributing to our understanding of how the infant brain may balance between learning systems in early life.

Looking forward

As much as my mother wishes I could remember our extravagant first birthday party, my specific memories from early life are sparse. But I still extracted meaning from the patterns in my early experiences⁵⁰, such as the fun we had and the love that was ever present. Awake infant fMRI is helping to reveal how we represent early experiences, with recent findings suggesting that the infant hippocampus is capable of forming episodic-like memories, even if such memories are later lost. This may constrain theories of infantile amnesia and inform our understanding of learning systems in early life. More broadly, this work highlights the promise of awake infant fMRI for characterizing mechanisms underlying cognitive development⁵¹ and contributing to our understanding of what it is like to be a baby.

Footnotes

*If you would like to contribute to our study of people’s earliest memories, please consider taking this anonymous, 5 minute survey: https://yalesurvey.ca1.qualtrics.com/jfe/form/SV_0IJ7NSrA1oYYNeK

^†Traditional theories define episodic memory as a type of declarative memory requiring explicit, conscious access — something that cannot be assessed in preverbal infants

^††General representations can arise from insufficient encoding and forgetting of details (‘fuzzy’ representations), or the abstraction of commonalities over multiple distinct episodes, which may exhibit distinct developmental trajectories⁵²

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