Localization of human intraparietal areas AIP, CIP, and LIP using surface orientation and saccadic eye movement tasks

Abstract

In monkeys, areas in the intraparietal sulcus (IPS) play a crucial role in visuospatial information processing. Despite many human neuroimaging studies, the location of the human functional homologs of some IPS areas is still a matter of debate. The aim of the present functional magnetic resonance imaging (fMRI) study was to identify the distinct locations of specific human IPS areas based on their functional properties using stimuli adapted from nonhuman primate experiments, in particular, surface orientation discrimination and memory guided saccadic eye movements (SEM). Intersubject anatomical variability likely accounts for much of the debate. By applying subject by subject analysis, we can demonstrate that sufficient intersubject anatomical and functional commonalities exist. Both the lateral bank of the anterior part of IPS, the putative human homolog of the area AIP, and the caudal part of the IPS (putative CIP) showed activation related to spatial discrimination of surface orientation. Eye tracking conducted during fMRI data acquisition allowed us to show that both areas were separated by an area related to SEM. This area was located in the middle region of the IPS (most probably including LIP), i.e., similar to the location observed in nonhuman primates. In 10 of 11 subjects our putative CIP activation was located in a medial side branch of the posterior part of the IPS, on the opposite side as described in nonhuman primates, making this landmark a useful anatomical marker for the location of CIP.

Figure 1

Paradigm as employed in the study. Experiment 1 (a) employed a surface orientation discrimination task in a delayed matching to sample paradigm. Stimuli were presented at the centre of the screen. The cue was followed by a sample stimulus. After the sample stimulus, a single matching stimulus was presented. Subjects were instructed to press the left button with their right index finger when the stimulus showed the same orientation (task O) or the same color (task C) as the sample and the right button with the middle finger when the matching stimulus was different. Subjects responses were recorded by index or forefinger button press. Stimuli were presented for 1,000 ms with a stimulus onset asynchrony randomised between 2,500 and 4,500 ms. Experiment 2 (b) was an event‐related ‘go – no go’ memory guided saccadic eye movement task. The event condition was cued to the subject by a red or green cue at trial onset, event structure was then identical. The inset shows the six possible target points at the points of a virtual hexagon. Distance from central fixation to target were 5.8 degree in diagonal and 6.8 degree in horizontal plane. (c) Saccadic eye movement data from one subject. Top panel shows two ‘go’ trials from the block designed ‘go – no go memory guided saccade’ experiment. In the middle row, eye movement recordings of the two trials are shown (red: horizontal eye movement, dark blue: vertical eye movement, light blue: time of ‘target onset’, green: onset of ‘move’ cue). The bottom panel shows all data for each eye movement to the upper left target (4 events) for one subject in one session. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 2

Peak point activation loci for each individual's analysis in Experiments 1 and 2. The cross shows the mean position of each data set. The colored part of the cross indicates standard error of mean and the white continuation of the cross indicates one standard deviation from the mean. All data is provided in the tables given as supplementary data. Red: loci for individual's significant activations in AIP elicited by orientation discrimination vs. color discrimination (P < 0.05 small volume corrected (20‐mm radius sphere centered at left AIP, x = −40, y = −40, z = 40; and right AIP, x = 40, y = −40, z = 44; (Binkofski et al., 1999)). Green: loci for individual's significant activations in CIP elicited by orientation discrimination vs. color discrimination (P < 0.05 small volume corrected (20 mm radius sphere centered at left CIP, x = −16, y = −68, z = 57; and right CIP, x = 20, y = −67, z = 58; (Shikata et al., 2001)). Yellow: loci for individual's significant activations in the middle part of IPS elicited by saccadic eye movements vs. fixation (P < 0.05 FDR small volume corrected using the functionally derived region of interest, (see Methods: Definition of Regions of Interest section)). Enlarged images are taken from MNI brain z = 58 (left) and z = 45 (right).

Figure 3

Activated regions in four individual subjects, (top to bottom). Significant activations for surface orientation vs. color discrimination (red) (P < 0.001 uncorrected), for the motor response of the left index and middle finger (blue) (P < 0.05 corrected) and for delayed period for saccadic eye movements (green) (P < 0.05 corrected within fROI). Orange color indicates overlap between the areas of surface orientation discrimination and delay period prior to saccadic eye movements (Sub 9). First column, rendered brain viewed from left. Central column, an enlarged view of the areas around the IPS viewed from the right and from above. Right column, rendered brain viewed from above. In the enlarged view, activations during orientation discrimination (a, AIP; c, CIP) are located in anterior and posterior part of IPS. Activations related to the delay period prior to saccadic eye movement (b, middle part of IPS) are located between AIP and CIP. Arrows in enlarged view indicate border of parietal and occipital lobe in IPS.]