Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory - PubMed (original) (raw)

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Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory

Morris Moscovitch et al. J Anat. 2005 Jul.

Abstract

We review lesion and neuroimaging evidence on the role of the hippocampus, and other structures, in retention and retrieval of recent and remote memories. We examine episodic, semantic and spatial memory, and show that important distinctions exist among different types of these memories and the structures that mediate them. We argue that retention and retrieval of detailed, vivid autobiographical memories depend on the hippocampal system no matter how long ago they were acquired. Semantic memories, on the other hand, benefit from hippocampal contribution for some time before they can be retrieved independently of the hippocampus. Even semantic memories, however, can have episodic elements associated with them that continue to depend on the hippocampus. Likewise, we distinguish between experientially detailed spatial memories (akin to episodic memory) and more schematic memories (akin to semantic memory) that are sufficient for navigation but not for re-experiencing the environment in which they were acquired. Like their episodic and semantic counterparts, the former type of spatial memory is dependent on the hippocampus no matter how long ago it was acquired, whereas the latter can survive independently of the hippocampus and is represented in extra-hippocampal structures. In short, the evidence reviewed suggests strongly that the function of the hippocampus (and possibly that of related limbic structures) is to help encode, retain, and retrieve experiences, no matter how long ago the events comprising the experience occurred, and no matter whether the memories are episodic or spatial. We conclude that the evidence favours a multiple trace theory (MTT) of memory over two other models: (1) traditional consolidation models which posit that the hippocampus is a time-limited memory structure for all forms of memory; and (2) versions of cognitive map theory which posit that the hippocampus is needed for representing all forms of allocentric space in memory.

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Figures

Fig. 1

Fig. 1

Left panel: Medial temporal lobe structures and their connections viewed from the side (saggital section). (Adapted from Blumenfeld, 2002.) Right panel: Medial temporal lobe structures viewed from the underside of the brain. A, amygdala; E, entorhinal cortex; H, hippocampus; PH, parahippocampal cortex; PR, perirhinal cortex.

Fig. 2

Fig. 2

The hippocampal-diencepahalic systems showing connections between medial temporal structures and diencepahlic (thalamic) nuclei and frontal lobes. Solid lines show the extended hippocampal system, presumed to mediate recollection, and dotted lines show the extended perirhinal system, presumed to mediate familiarity. (Modified from Aggleton & Brown, 1999.)

Fig. 3

Fig. 3

Left panel: Autobiographical episodic memory performance. Mean scores on episodic components of the Autobiographical memory interview (AMI; Kopelman et al. 1989) for control (n = 22) and patient (n = 25) groups. The maximal score is 9 per time period. Vertical lines depict standard errors of the means. Middle panel: Autobiographical episodic memory performance during earliest time periods. Mean scores on episodic components of AMI for control (n = 22), late seizure onset (n = 11) and early seizure onset (n = 8). Late seizure onset describes patients who reported first seizures after age 18; early seizure onset describes patients who reported first seizures before age 5. The maximum score is 3 per time period. Right panel: Personal semantic memory performance. Mean scores on semantic components of AMI for control (n = 22) and patient (n = 25) groups. The maximum score is 21 per time period. Vertical lines depict standard errors of the means. (From Viskontas et al. 2000).

Fig. 4

Fig. 4

Activation from vividly (red) vs nonvividly (blue) recalled events. The cross hairs on the images are centred at activations within the spherical search regions of the hippocampus which have the following Talairach & Tournoux (1988) co-ordinates: Reading from left to right, x = −27, y = −21, z = −16. Radiological coordinates are used so that left/right is reversed. (From Gilboa et al. 2004.)

Fig. 5

Fig. 5

Activity in the medial temporal lobes is parametrically modulated by the level of recollective qualities of autobiographical memories, independent of their recency. Regions included the left hippocampus, modulated by the level of detail (a) and personal signfiicance (b); and the right hippocampus, by the personal significance of the memories (c).

Fig. 6

Fig. 6

Schematic renderings of remote and recent activations. Each point corresponds to a statistically significant activation from within the left hippocampus in either remote (top; n = 18) or recent (bottom; n = 16) conditions. Red and black squares represent activations at a significance level of P < 0.001 and P < 0.01 uncorrected, respectively. Activations are shown on a single sagittal plane taken from the Talairach & Tournoux (1988) atlas (25 mm lateral to the midline). Overlapping activations were offset slightly in the recent condition. Differences in the lateral displacement of the activations from the midline (along the _x_-axis of the Talairach atlas) are not represented in the figure. The lateral and vertical dimensions did not show any obvious systematic variability and therefore are not considered as a part of the overall pattern of interest. (From Gilboa et al. 2004.)

Fig. 7

Fig. 7

Brain regions activated in the comparison of all remote spatial memory tasks with the perceptual baseline task. The functional maps are overlaid on the averaged anatomical scans from all participants in relevant sagittal and axial views. The right hemisphere is shown on the left side of the images. Images were thresholded at P < 0.001, corrected. Areas of activity common across tasks included right parahippocampal gyrus (top), left retrosplenial cortex (bottom left) and right superior occipital cortex (bottom right). The hippocampus (open circle) was not activated in any task.

Fig. 8

Fig. 8

Structural scan of K.C.'s brain showing small amount of remaining hippocampal tissue that was unactivated (left); for comparison see right parahippocampal activation in parahippocampal cortex during remote spatial memory tasks (right).

Fig. 9

Fig. 9

Graphic illustration of a hippocampal–neocortical framework of long-term context-free and context-dependent memory. The open arrows represent connections between the hippocampus and specialized neocortical regions that allow for the reconstruction in memory of newly formed traces and of event-specific details. The closed arrows represent an example of a subnetwork of structures supporting one class of schematic information (spatial) that has been abstracted over time and that can exist independently of the hippocampus.

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References

    1. Addis DR, Moscovitch M, Crawley AP, McAndrews MP. Recollective qualities modulate hippocampal activation during autobiographical memory retrieval. Hippocampus. 2004a;14:752–762. - PubMed
    1. Addis DR, McIntosh AR, Moscovitch M, Crawley AP, McAndrews MP. Characterising the spatial and temporal features of autobiographical memory retrieval networks: a partial least squares approach. NeuroImage. 2004b;23:1460–1471. - PubMed
    1. Aggleton JP, Brown MW. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav. Brain. Sci. 1999;22:425–489. - PubMed
    1. Aggleton JP, McMackin D, Carpenter K, Hornak J, Kapur N, Halpin S, et al. Differential cognitive effects of colloid cysts in the third ventricle that spare or compromise the fornix. Brain. 2000;123:800–815. - PubMed
    1. Aguirre GK, D’Esposito M. Topographical disorientation: a synthesis and taxonomy. Brain. 1999;122:1613–1628. - PubMed

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