Visuo-tactile cross-modal associations in cortical somatosensory cells

Yong-Di Zhou* and Joaquín M. Fuster

Neuropsychiatric Institute and Brain Research Institute, School of Medicine, University of California, Los Angeles, CA 90024
Proc Natl Acad Sci U S A. 2000 August 15; 97(17): 9777–9782. PMCID: PMC16941

Three adult rhesus monkeys (Macaca mulatta) were the experimental subjects for this study. They had been used in studies of short-term memory (14, 15). Animal care and surgical procedures were approved by the Animal Research Committee at the University of California, Los Angeles. The animals were trained to perform a visuo-haptic memory task in a fully automated, computer-controlled apparatus. During the task, the animal was seated in a primate chair facing a panel with a rectangular screen at about eye level for visual display (30 × 50 mm) and a rectangular opening at about waist level for access to tactile test objects (Fig. 1). The distance between the eyes of the animal and the screen was about 20 cm. A pair of visual images (icons) was used. These were black and white patterns of parallel stripes (3.5 mm apart). The stripes were vertical in one icon and horizontal in the other. The opening for the tactile test objects was normally closed by a shutter. When the shutter was opened (downward sliding), the animal could reach out through the opening and manipulate the objects behind the panel (the objects were at all times out of sight). The test objects were two vertical cylindrical rods of identical dimensions (axis, 150 mm and diameter, 19 mm), but different direction of parallel ridges on their surface (ridges 6 mm apart). One rod had the ridges along the axis of the cylinder (vertical ridges) and the other around its circumference (horizontal ridges). When not in the act of reaching and grasping the objects, the performing hand of the animal rested on a rounded pedal (handrest) in the center of the lower edge of the opening. The other hand was at all times restricted from access to the test objects by a plate attached to the primate chair. A displacement-sensitive transducer was connected to the spring-suspended seat of the animal. Signals from this transducer were recorded and used for control of body movements.

A task trial consisted of the following sequence of events—all registered by electronic switches and sensors. The trial began with the 3-s presentation of one of the icons (vertical or horizontal). The direction of its stripes symbolized the direction of the ridges in the rod to be chosen haptically later, after a 20-s delay (14 s in some tests). At the end of that delay, an auditory signal marked the accessibility of the two rods side by side. One rod was 5.5 cm to the right of the center of the opening, and the other 5.5 cm to the left. As soon as they became accessible, the animal reached out and palpated the rods. A pull of either rod led to closure of the opening and to fluid reward (2 ml) if the choice was correct. The icon and the position of its corresponding rod changed at random between trials. This prevented the animal from using spatial clues for the choices. Early in the study, instead of the icon, the monkey was presented with the sight of the sample object through a window at eye level—later substituted by the projection display screen.

Before testing the animals on the visuo-haptic task described above, the animals had been trained on a unimodal (haptic-haptic) task. This allowed comparisons of unit discharge between the two tasks. In that unimodal tactile task, a trial started with a click, which served as an alerting signal about 1.5 s before the touch of the tactile sample. The sample object was identical to one of the objects used for visuo-haptic choice. Here, instead of the visual cue, the animal had to palpate that sample object for the tactile match after the delay. In every other respect, the task was identical to the cross-modal task.

After the monkey had undergone behavioral training (performance criterion above 75% correct), two cylindrical pedestals for microelectrode recording were implanted bilaterally on the parietal cortex, leaving the dura intact. The pedestals were intended to be placed over hand representation areas of anterior parietal cortex (Brodmann's areas 3a, 3b, 1, and 2). The implantation was guided by cranial landmarks, our own experience with previous implants, and a stereotaxic map (courtesy of T. P. Pons, Wake Forest University, Winston-Salem, NC). In one of the animals, a pair of EOG (electrooculogram) electrodes was implanted in the periorbital bone for monitoring horizontal eye movements.

For a recording session, the animal was placed in the testing apparatus with its head fixed. Single-unit activity was recorded extracellularly with Elgiloy microelectrodes (impedance 1–2 megaohms). Spike records were selected for analysis on the basis of stability, uniformity, and clear isolation from background noise and the spikes from other units.