Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice

Abstract

The human brain activity related to strategies for navigating in space and how it changes with practice was investigated with functional magnetic resonance imaging. Subjects used two different strategies to solve a place-learning task in a computer-generated virtual environment. One-half of the subjects used spatial landmarks to navigate in the early phase of training, and these subjects showed increased activation of the right hippocampus. The other half used a nonspatial strategy and showed, with practice, sustained increased activity within the caudate nucleus during navigation. Activation common to both groups was observed in the posterior parietal and frontal cortex. These results provide the first evidence for spontaneous variability and shift in neural mechanisms during navigation in humans.

Figure 1.

A view of the virtual environment. Note that the landscape and a tree can be viewed at a distance, whereas the objects down the stairs at the end of the arms are not visible from the center of the maze.

Figure 2.

The behavioral results. A, The total number of errors made in the training phase (sections II and III) averaged across subjects in the spatial memory, shift, and nonspatial strategy groups. B, The number of errors made while performing the probe trial in sections I (probe 1) and IV (probe 2) averaged across subjects in the spatial memory, shift, and nonspatial strategy groups. C, The average time that the spatial memory, shift, and nonspatial strategy groups required to perform one trial in sections (S) I to IV of the experiment. SEM are shown. Asterisks indicate that the spatial memory group is different from the nonspatial strategy group; p < 0.05.

Figure 3.

Brain activity common to both spatial memory and nonspatial strategy groups (experimental minus control task). The t maps are superimposed onto the anatomical average of all participants and displayed in the sagittal plane. A, Posterior parietal cortex. B, Middorsolateral prefrontal cortex. C, Motor–premotor cortical region. D, Supplementary motor cortex. E, Putamen. L, Left hemisphere; R, right hemisphere.

Figure 4.

Activity in the hippocampus and caudate nucleus found in the spatial memory group and nonspatial strategy group, respectively. The t maps are superimposed onto the anatomical average of all participants and displayed in the sagittal and coronal planes. A, Activity in the right hippocampus when contrasting the experimental and control conditions of the spatial memory group, minus those of the nonspatial strategy group in the first scan (x = 32; y = -14; z = -20; t = 4.41). B, Activity in the right caudate nucleus found in the nonspatial strategy group (scan 5) (x = 14; y =-8; z = 22; t = 4.04).