Trends in Neurosciences
INMED/TINS special issueHuman memory development and its dysfunction after early hippocampal injury
Introduction
Memory is among the most fundamental aspects of cognitive development, enabling individuals to amass knowledge about the world and recall everyday events. Most neuroscientists believe that there are two types of long-term memory: non-cognitive and cognitive. Non-cognitive memories are typically described as unconscious or automatic, and include motor skills, conditioned responses and priming. By contrast, cognitive memories are those that can be consciously brought to mind and include knowledge of facts and of specific events. Cognitive memory can be further subdivided into episodic memory for personal experiences and semantic memory for general knowledge and facts [1]. Recall of items from episodic memory is by definition associated with retrieval of contextual details related to the encoding (e.g. I went to Paris with my family last summer), whereas recall of items from semantic memory is not (e.g. Paris is the capital of France). A similar distinction applies to recognition, whereby it can occur with retrieval of contextual details related to encoding (‘recollection-based recognition’) or without these additional details (‘familiarity-based recognition’ 2, 3). There are different views about the relationship between the episodic and semantic components of cognitive memory. One view is that semantic memories reflect the context-free ‘residue’ of many episodes, and thus depend on episodic memory for their formation [4]. By contrast, another view is that information enters cognitive memory in a serial fashion, and must first be encoded semantically before it can be encoded episodically [1].
The different types of long-term memory appear to rely on different brain circuits. Cognitive memories are mediated by a medial temporal lobe (MTL) circuit, involving the hippocampus and the perirhinal, entorhinal and posterior parahippocampal cortices, whereas non-cognitive memories are mediated by other brain regions. The neural basis of the semantic and episodic components of cognitive memory is more controversial. According to one view 5, 6, 7 (Figure 1), the structures involved in cognitive memory function in a hierarchy, wherein perceptual information first enters the parahippocampal regions mediating semantic memory (and familiarity-based recognition) and only then passes to hippocampal regions necessary for episodic memory (and recollection-based recognition). Others acknowledge the possibility of a division of labour within the MTL memory system, but contend that the hippocampus itself is involved in both semantic and episodic memory 8, 9 (Figure 1).
Developmental studies are an important tool for understanding the organization of the cognitive and neural mechanisms underlying memory. One fundamental question is when the organization of the components of cognitive memory that are present in adults becomes observable. If different types of memory and their neuroanatomical substrates become functional at different rates, they can be studied in isolation or when interacting in ways that are not easily observed in the mature system. Studies of the effects of early injury to the neural substrates of cognitive memory can also provide important information. For example if, as proposed by the hierarchical model, the hippocampus is crucial for formation of episodic memories but not for formation of semantic memories, children with early injury to this structure should be able to acquire a normal knowledge base despite impairments in episodic memory. This review aims to examine both normal development of cognitive memory and its dysfunction following early hippocampal injury in humans, with a view to providing an account of the developmental emergence of the different features of cognitive memory.
Section snippets
Development of recognition memory
Recognition is the first form of memory to emerge, appearing within the first days of postnatal life. This has been shown using the visual paired-comparison task, in which participants are first familiarized with one visual stimulus and then their memories tested by presenting the familiar stimulus alongside a novel one. Adult humans 10, 11, 12 and monkeys 13, 14 with bilateral MTL lesions, including those restricted to the hippocampus 15, 16, show the normal pattern of looking for longer at
Development of recall
Recall involves retrieving a representation, established on the basis of past experience, in the absence of ongoing perceptual support for that experience [29]. In adults, verbal report is commonly used as a measure of recall. However, this measure is not ideal for studying memory development in infants, who might be able to recall information from memory before they can verbally express the contents of their memories. For this reason, development of early recall has been studied most often
Flexible memory
Basic aspects of recognition and recall are functional within the first postnatal year and might be mediated by the MTL (see Box 2 for discussion of why these early memories are not accessible during adulthood). However, early memory remains different from later memory because infant memories are closely tied to the original learning context.
With age, infants become increasingly able to tolerate changes in context. For example, studies using the deferred imitation task document that 6-month-old
Early damage to the medial temporal lobes
Investigating memory following selective, bilateral hippocampal damage early in life provides a unique opportunity for understanding the role of the hippocampus in memory development. At a basic level, it is important to know whether cognitive memory can develop at all in the face of injury to a key component of the MTL circuit. If memory does develop, it becomes interesting to determine whether it can develop normally, perhaps reflecting the plasticity of the developing system, or whether
Concluding remarks
MTL-dependent memory might emerge from the earliest months of life, with certain aspects of recognition and recall showing a protracted course of development through middle childhood that might depend, at least in part, on the progressive development of the hippocampus. Development of memory abilities appears to unfold in a sequence beginning with novelty preferences and/or familiarity-based recognition, followed by recall, then by flexible memory, and ultimately by source memory. This sequence
References (110)
The hippocampus supports both the recollection and the familiarity components of recognition memory
Neuron
(2006)Visual paired comparison performance is impaired in a patient with selective hippocampal lesions and relatively intact item recognition
Neuropsychologia
(2004)- et al.
The primate hippocampus: ontogeny, early insult and memory
Curr. Opin. Neurobiol.
(2005) Dissociating intentional learning from relative novelty responses in the medial temporal lobe
NeuroImage
(2005)- et al.
Response to novelty: continuity versus discontinuity in the developmental course of intelligence
Adv. Child Dev. Behav.
(1985) On beyond mirror neurons: Internal representations subserving imitation and recognition of skilled object-related actions in humans
Cogn. Brain Res.
(2005)- et al.
Imitation, memory and the representation of persons
Infant Behav. Dev.
(1994) Generalization of deferred imitation during the first year of life
J. Exp. Child Psychol.
(2004)Hippocampus: cognitive processes and neural representations that underlie declarative memory
Neuron
(2004)Dissociable correlates of recollection and familiarity within the medial temporal lobes
Neuropsychologia
(2004)