It was our hypothesis that the latter task would activate the hippocampal formation more than either of the single-item learning tasks. Visually presented pairs of semantically unrelated nouns had to be learned by one of three strategies inducing a ( i) deep or ( ii) shallow encoding of the words in isolation of each other or inducing ( iii) both the deep encoding of the words as separate entities and the creation/storage of semantic associations between the two words. We tested this hypothesis in the human, reducing the complexity of a natural scene to the sensorily restricted environment of a word-learning experiment in the positron-emission tomography (PET) scanner. The less complex a scene is, the fewer associations are required to memorize it, and, thus, the less hippocampal activation can be expected. The anatomy and physiology of the hippocampal formation (dentate gyrus, Ammon’s horn/hippocampus proper, presubiculum) lends itself to store such patterns of neuronal coactivations temporarily ( 3, 4, 14– 24). The composition of these coactivations needs to be stored in memory for the later recovery of some or all aspects of that episode. The experience of an episode typically involves the simultaneous processing of diverse sensory inputs, bodily sensations, thoughts, and emotions in distributed cortical regions, creating patterns of coactivations in the cortex. At the same time, learning experiments with rats ( 14– 17) indicated that the hippocampal formation is important for the establishment of associations between components of episodes in memory. The function of the human hippocampal formation was pinned down to declarative memory alone and became specified even further to declarative learning/consolidation ( 3, 4), episodic memory ( 5), novelty detection ( 6– 9), the retrieval of deeply encoded items ( 10), and spatial learning ( 11– 13). In the years following this discovery, research with amnesic patients led to the finding that memory is not a unitary system but is divided into subsystems, each supported by a different but partially overlapping neuronal network.
The discovery that the mediotemporal brain regions, particularly the hippocampal formations, are essential for human memory ( 1, 2) set the ground for neuroscientific theories and experimental practice during the past 40 years.
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