Functional neuroimaging studies of encoding, priming, and explicit memory retrieval

Abstract

Human functional neuroimaging techniques provide a powerful means of linking neural level descriptions of brain function and cognition. The exploration of the functional anatomy underlying human memory comprises a prime example. Three highly reliable findings linking memory-related cognitive processes to brain activity are discussed. First, priming is accompanied by reductions in the amount of neural activation relative to naive or unprimed task performance. These reductions can be shown to be both anatomically and functionally specific and are found for both perceptual and conceptual task components. Second, verbal encoding, allowing subsequent conscious retrieval, is associated with activation of higher order brain regions including areas within the left inferior and dorsal prefrontal cortex. These areas also are activated by working memory and effortful word generation tasks, suggesting that these tasks, often discussed as separable, might rely on interdependent processes. Finally, explicit (intentional) retrieval shares much of the same functional anatomy as the encoding and word generation tasks but is associated with the recruitment of additional brain areas, including the anterior prefrontal cortex (right > left). These findings illustrate how neuroimaging techniques can be used to study memory processes and can both complement and extend data derived through other means. More recently developed methods, such as event-related functional MRI, will continue this progress and may provide additional new directions for research.

Figure 1

(A) Horizontal sections from two levels show fMRI activation maps for a “shallow encoding” task contrasted with fixation and for a “deep encoding” task contrasted with fixation (averaged data from 12 normal subjects; K-S statistical activation map threshold = P < 0.001; brighter colors indicate greater significance; functional data overlie averaged anatomic image; right shown on the right). Both tasks share certain brain areas in common such as posterior visual areas whereas only the deep encoding task shows increased activation of left inferior and dorsal prefrontal areas (indicated with yellow arrows). These robust activations (P < 10⁻⁸) are at peak coordinates [Talairach 1998 atlas (91) (x, y, z)] -40, 9, 34 and -46, 6, 28 for the more dorsal activations and -40, 19, 3 and -43, 19, 12 for the more ventral prefrontal activations. The direct contrast between the deep and shallow encoding tasks also indicated that these regions differed significantly. (B) A horizontal section showing left dorsal prefrontal cortex activation in an amnesic patient during a “deep encoding” task, collected in collaboration with Verfaellie, Schacter, and Gabrieli. Robust activation was detected at -46, 3, 31 similar to normal subjects. The time course of activation within this region is shown to the right. Repeating items across the deep encoding task revealed significantly reduced activation (priming) as indicated by the time course (+, fixation control condition). This latter finding suggests that priming-related changes are present at a functional–anatomic level in amnesia, consistent with preserved behavioral priming often observed in amnesia.

Figure 2

A horizontal section shows averaged (n = 4) fMRI data for an object–classification task in which items were either new or repeated (primed). These activation maps are based on the t statistic and are derived from continuous runs of intermixed trials (mean intertrial interval = 8 s). Event-related fMRI techniques were used to make activation maps (61) and to remove the overlapping contributions of adjacent trials (60). The time course for a region of right extrastriate cortex (peak coordinate = 32, -48, -16) is shown for the new and repeated trials separately. Repeated items show a reduced level of activation relative to new items, suggesting a neural correlate of priming.