The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging.

Abstract

Considerable evidence exists to support the hypothesis that the hippocampus and related medial temporal lobe structures are crucial for the encoding and storage of information in long-term memory. Few human imaging studies, however, have successfully shown signal intensity changes in these areas during encoding or retrieval. Using functional magnetic resonance imaging (fMRI), we studied normal human subjects while they performed a novel picture encoding task High-speed echo-planar imaging techniques evaluated fMRI signal changes throughout the brain. During the encoding of novel pictures, statistically significant increases in fMRI signal were observed bilaterally in the posterior hippocampal formation and parahippocampal gyrus and in the lingual and fusiform gyri. To our knowledge, this experiment is the first fMRI study to show robust signal changes in the human hippocampal region. It also provides evidence that the encoding of novel, complex pictures depends upon an interaction between ventral cortical regions, specialized for object vision, and the hippocampal formation and parahippocampal gyrus, specialized for long-term memory.The structures that are important for encoding and storage of novel information have been the focus of extensive research since the pioneering work of Scoville, Milner, and Penfield (1-4). A convergence of research in animals and humans has led to the hypothesis that the hippocampus and related medial temporal lobe structures are critical for the encoding of novel information for subsequent storage in the neocortex (2, 5-7). In humans, anterograde amnesia-the inability to learn new information-is associated with bilateral lesions of medial temporal lobe structures (2,8). In nonhuman primates, singleunit recordings have identified neurons that respond preferentially to novel or familiar stimuli. These neurons are found in structures that receive output from the hippocampus [such as the anterior thalamus (9) and nucleus accumbens (10)] and in structures that provide afferent input to the hippocampus [such as the entorhinal cortex (11)]. Lesion studies in animals have provided extensive data on the role of medial temporal lobe structures in the performance of behavioral tasks requiring storage of novel information. For example, lesions of hippocampus and adjacent cortical structures, such as the perirhinal and entorhinal cortices, impair performance on delayed nonmatching to sample tasks in nonhuman primates (12) and rats (13). Controversies remain about the exact structures that are most important for the performance of explicit memory tasks (12-16).Functional brain imaging studies have attempted to demonstrate the role of the hippocampus and related medial temporal lobe structures in the encoding and retrieval of long-term memories in the intact human brain. Several studies using positron emission tomography have shown no evidence of a medial temporal lobe contribution to encoding and recognition (17-19); however, more recent reports have shown changes in the hippocampus in re...

Memory encoding and hippocampally-based novelty/familiarity discrimination networks

“…Regional cerebral blood flow (rCBF), measured during a yes/no recognition memory test, was higher for novel than for familiar items at a number of sites in the extended limbic system. Other research has corroborated the general thrust of these early findings [7,9,15,17,18], and has extended the novelty assessment networks to other cerebral regions beyond the limbic system, including a number of anterior and posterior neocortical sites [11,12,19]. We proposed a specific relation between novelty assessment and memory encoding in the form of a novelty encoding hypothesis.…”

“…As mentioned earlier, we selected the seed voxels for our analysis in the hippocampus because of considerable evidence in the literature about the involvement of the hippocampus in novelty detection [1,2,[5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20]47]. It is also generally accepted that novelty detection involves regions beyond the hippocampus [ 1,2,12,17,19,20].…”

“…Typically, this voxel is chosen based on previous analyses of the data, theoretical motivation, or both. In the present case, we targeted the hippocampus proper for the selection of the seed voxel because previous research has demonstrated the involvement of the hippocampus in novelty assessment [7,11,12,[17][18][19][20]. Because of the size of the hippocampal region and evidence for its functional heterogeneity [17,35,36], however, the selection of a single representative voxel (a single coordinate in Talairach space) can be difficult.…”

“…Novelty/familiarity discrimination (also known as novelty detection, or novelty assessment) is useful for the organism in a variety of situations, can take a number of specific forms, and can serve several functions (see reviews by [1][2][3][4]). The hippocampal system has been found to be critically involved in many tasks involving neural novelty/familiarity (henceforth just 'novelty') discrimination [1,2,[5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20]. In this report, we describe a positron emission tomography (PET) study whose purpose was to explore the idea that novelty discrimination does not depend on the hippocampal system alone but is subserved by large-scale neuronal networks which include but go beyond the hippocampal system.…”

Differences in EEG power in young and mature healthy adults during an incidental/spatial learning task are related to age and execution efficiency

“…It is well established that the participation of the temporal and frontal lobes in information encoding and retrieval processes account for episodic memory (Gabrieli et al 1997;Rombouts et al 1997;Stern et al 1996), although the left prefrontal cortex appears to be mainly involved in episodic information encoding processes, while the right prefrontal cortex is mainly involved in its retrieval (Tulving et al 1994). Because some episodic information is incidentally acquired, some researchers have questioned the participation of the same cerebral structures and similar neural processes in encoding both episodic and incidental information.…”