Coding of intention in the PPC

We define intention as a high-level plan for a movement that specifies the type and goal of the movement, such as the wish “I want to pick up my cup of tea.” Such a high-level movement plan would not necessarily contain all the details of the movement, such as the movement path, muscle activation patterns, and joint angles, but it would encode the end-point location of the movement and what kind of movement is to be made. Intentions are derived from the integration of sensory input and may occur at the beginning of a sequence of ever more specific movement plans along the sensorimotor pathway. In the example of picking up a cup of tea, necessary specifications include which arm to use, the movement trajectory and speed, and the details of the muscle force pattern. These movement specifications may be included in the movement plan closer to the motor output stage and may not be present at the earlier, or higher-level, stages of movement planning.

Evidence that the PPC is involved in high-level cognitive functions for sensorimotor transformation first came from the observation of neurological deficits after PPC lesions (Balint, 1909). Patients with PPC lesions do not have a primary sensory or motor deficit; however, they have difficulties in estimating the location of stimuli in space or may be unable to plan movements appropriately (Geshwind and Damasio, 1985). The observations suggest that a disconnection occurs between the sensory and motor systems in the sensorimotor pathway (Goodale and Milner, 1992). Human functional magnetic resonance imaging (fMRI) experiments and monkey electrophysiological recordings further supported the concept that the PPC is neither strictly sensory nor motor, but encodes high-level cognitive functions related to action (Andersen, 1987; Goodale and Milner, 1992; Mountcastle et al., 1975). The monkey is a particularly good model for the study of the PPC, since its sophisticated eye-hand coordination is similar to that of humans and the PPC in both species seems to perform similar functions (Connolly et al., 2000; DeSouza et al., 2000; Rushworth et al., 2001).

Planning Activity in the PPC

For separating sensory from motor components of behavior, the so-called memory task has been particularly useful (Hikosaka and Wurtz, 1983). In this task, a subject is first cued to the location of a movement by a briefly flashed stimulus, but must withhold the movement response until a go signal occurs (Fig. 89.1A). A typical PPC cell shows a burst of activity during the cue and at the movement period, indicating its relation to both sensory and motor components of the movement. During the memory period, cells in many parietal areas are also active, even in the dark (Gnadt and Andersen, 1988; Snyder et al., 1997). Figures 89.1B and 89.1C show the activity of a PPC neuron while the animal performed a delayed-reach task to targets in eight different directions (Fig. 89.1B). The histogram corresponding to each movement direction depicts the average firing rate of the neuron during the trial. The activity of the cell strongly increased during stimulus presentation, the waiting period, and the movement period of the task—in this example most strongly, in the right-down direction. The increased activity during sensory, planning, and movement periods of the trial indicates that the PPC is neither a purely sensory nor a purely motor area but is involved in the high-level planning of movements, consistent with a role of this area in sensorimotor transformations.

Figure 89.1..  

Spatial tuning of reach-related activity in PPC in a delayed reach task to separate sensory from motor components of behavior. a, Paradigm: animals memorized the location of a briefly flashed visual target, then waited in complete darkness for a go signal and made a reach to the remembered target location. b, Activity of a typical PPC cell with reach-related activity during stimulus presentation, waiting, and movement period of the task. Activity is maximal in the right-down direction for this cell. Each histogram depicts the cell's activity in one of eight tested reach directions (white arrows; left-down direction occluded). Each histogram shows a spike density histogram representing the average action potential firing rate of all trials in the particular reach direction, and the short horizontal bars indicate the time of the target flash and the reach. c, Spatial tuning of the average firing rate during the waiting period (same cell as in b). Mean firing rate is plotted as amplitude along the movement direction, illustrating the strongest responses for right-down. (Data from Batista et al., 1999.)

The neuron in Figure 89.1 shows strongest activity for stimuli and movements down and to the right while being essentially silent for movements in the opposite direction. This directional tuning of activity is illustrated in the polar plot in Figure 89.1C, with the mean firing rate during the waiting period plotted as amplitude along the movement direction. Directional tuning is very common for many PPC neurons, with different neurons coding for different preferred directions. Hence, the combined activity of many neurons can code the direction of movements quite precisely.

To demonstrate that the activity during the delay period does not simply represent the sensory memory of the target, we used a paradigm in which the animals planned movements to two stimuli. For example, it has been shown that the delay period activity of neurons in the lateral intraparietal area (LIP) represents only the next planned eye movement, even though the animal had to hold two cued locations in memory (Mazzoni et al., 1996a). More recently, a similar result was also found for reach movements in the parietal reach region (PRR) (Batista and Andersen, 2001). Figure 89.2 shows a typical PRR neuron during this experiment. In the delayed-reach task (Fig. 89.2A), the cell showed strong activity during the stimulus, delay, and movement periods when the movement was to a target inside of the response field of the cell (left panel) and no activity when the movement was to a target outside of the response field (right panel). On randomly chosen trials, an intervening reach task was used (Figs. 89.2B, C). In one task (B), a cue was first shown within the response field of the cell, and the animal began to plan, but not execute, a reach movement to that target. The activity of the cell was highly elevated. However, a second target was briefly shown outside the response field, and the animal had to change his plan to reach to the second target first. During this period, the cell was not active. After reaching to the second target, the animal had to reach to the remembered location of the first target that had been presented within the response field, and the cell became vigorously active again. The cell was active when a reach movement was planned to the target location within the response field of the cell, but was not active when the animal was remembering that location but planning a reach elsewhere. Corresponding results were found for the intervening reach task when the first cue was presented outside of the response field and the second in the response field of the cell (Fig. 89.2C). The delay period activity of PRR neurons therefore represents only the next planned reach movement, even though the animal had to remember two cued locations. The finding that nearly all PRR cells showed this behavior in these double movement task experiments rules out the coding of sensory memory in the delay period activity for most PRR neurons. This memory is most likely represented elsewhere or in a very small subpopulation of PRR cells.

Figure 89.2..  

Example of a PRR neuron during the intervening reach task. Each panel in a–c shows, from top to bottom: timing of the cue stimulus into (filled bar) or out of (open bar) the response field (RF); spike rasters of 10 trials; spike density function (using a triangular kernel); timing of the button presses (horizontal bars) in one representative trial; and the acquired target (filled: in RF; open: out of RF). Vertical bar: calibration of firing rate. a, Delayed reach task with strong activity of the cell during the stimulus, delay, and movement periods when movements are planned inside the RF (left panel) and no activity when planned out of the RF (right panel). b, Activity of the same cell during an intervening reach task, when the first cue was shown in the RF and a second cue was presented out of the RF. c, Same cell with an intervening reach task, with the first cue out of the RF and the second cue in the RF. The cell was active when a reach was planned to the target location in the RF, but not when the animal was remembering that location and planning a reach to a location out of the RF. (Modified from Batista and Andersen, 2001.)

Temporal Evolution of Planning Activity

Further evidence supporting the view that the PPC is involved in sensorimotor transformations comes from studies that elucidate the dynamic evolution of PPC activity during the task, changing in nature from sensory to cognitive to motor with the evolution of the task. For example, it was demonstrated in a delayed eye movement task (Platt and Glimcher, 1999) that the early activity of LIP neurons varied as a function of the reward probability or the probability that a stimulus location became a saccade target. However, during later task periods, the cells coded only the direction of the upcoming eye movement. In another study of LIP (Breznen et al., 1999; Sabes et a., 2002), monkeys were trained to make eye movements to specific locations cued on an object, and the object was rotated between the extinction of the cue and the saccade. At the beginning of the trial, LIP cells were found to carry information about the location of the cue and about the orientation of the object, both of which are important to perform the task. However, near the time of the eye movement, the same neurons encoded the direction of the intended movement. Finally, in a study investigating the neural activity of PRR neurons when monkeys reached to auditory versus visual targets in a memory reach task (Cohen and Andersen, 2000), it was found that, during the cue period, visually cued trials carried more information about target location than did auditory cued trials. However, the amount of spatial information increased during the auditory trials, and the activity in the visual and auditory trials was not significantly different when the reach occurred. These studies emphasize the temporal evolution of activity in the PPC to reflect sensory, cognitive, and motor signals at different stages during a task.

Decision Processes for Movement Planning

Recording experiments have found that the neural activity in LIP is related to the decision of a monkey to make an eye movement. Both the prior probability and the amount of reward associated with a particular movement influenced the neural representation of visual activity in LIP, which points to a role of this area in decision making (Platt and Glimcher, 1999). As monkeys accumulated sensory information for the planning of an eye movement, activity in LIP and the prefrontal cortex was found to increase, consistent with the idea that these areas are weighing decision variables for the purpose of eye movement planning (Coe et al., 2002; Gold and Shadlen, 2001; Shadlen and Newsome, 1996; Thompson et al., 1996).

Monkeys and humans have been shown to choose between two targets for a reach, depending on eye position and the stimulus locations in space, essentially favoring targets that tend to center the reach with respect to the head (Scherberger et al., 2003). We recently investigated the neural activity in PRR during this choice paradigm in the monkey and found that the neural activity of single PRR cells was only transiently related to the visual stimulus at the beginning of the trial, which was essentially identical for both choices. Later in the trail, the activity closely reflected the animal's choice of target for a reach (Scherberger and Andersen, 2001). This result suggests a role for PRR in decision processes for the generation of reach movements similar to that for LIP in decision processes for eye movements. Moreover, eye position gain effects have been shown in PRR and in LIP, and these gain effects may bias the decision of animals to choose targets based on the eye position. These and other findings suggest that decision making for movement planning is a distributed process that may involve many cortical areas including the PPC, and the particular areas involved may depend on the specific sensory input and motor actions considered.

Intention and Attention

Given the fact that the PPC sits at the interface between sensory and motor systems, it is perhaps not surprising that the issue of how to distinguish intention from attention in this area has been of considerate research interest. To separate sensory from movement processing, antisaccade and antireach paradigms have been used in which animals were trained to make movements in the opposite direction to a briefly flashed visual stimulus. Activity in the medial intraparietal area (MIP) has been shown to code mostly the direction of the movement plan, not the location of the stimulus (Eskandar and Assad, 1999; Kalaska, 1996). In LIP, the reverse has been reported for eye movements (Gottlieb and Goldberg, 1999); however, recently it has been reported that most LIP cells also code the direction of the planned eye movement after a brief transient response linked to the stimulus (Zhang and Barash, 2000). The antisaccade and antireach results suggest that the PPC contains both sensory- and movement-related responses and is involved in the intermediate stages of sensorimotor transformations.

In an experiment specifically designed to separate spatial attention from intention, monkeys were trained to attend to a flashed target and plan a movement to it during a delay period (Snyder et al., 1997). However, in one case the plan was for a saccadic eye movement, while in the other case the plan was for a reach. In other words, during the memory period, the only difference in the task was the type of movement the animal was planning. Figure 89.3 shows two intention-specific neurons from PPC, one from LIP (A) and one from PRR (B), while the animal planned an eye or arm movement to the same location in space. The activity of the LIP neuron showed a transient response due to the briefly flashed stimulus followed by activity during the delay period when the animal was planning an eye movement (left histogram) but not when the animal was planning an arm movement to the same location (right histogram). In contrast, the PRR neuron showed no elevated activity in the delay period when an eye movement was planned but a strong activity for the planning of an arm movement. Such results were typical in the PPC: LIP was much more active for the planning of eye movements, whereas PRR was more active during arm movement planning. PRR includes MIP, 7a, and the dorsal aspect of the parieto-occipital area (PO); however, MIP contains the highest concentration of reach-related neurons. These results from LIP and PRR strongly argue for a role of the PPC in movement planning.

Figure 89.3..  

LIP and PRR neuron activity during a delayed saccade and delayed reach movement task. a, LIP cell showing elevated activity during the delay period (150 to 600 msec after the cue) before a saccade (left) but not before a reach movement (right). b, PRR cell showing no saccade activity (left) but showing reach activity (right) during the delay period with both movements planned to the same location in space. The neural activity in the delay period depended specifically on the movement intention. In all panels, short horizontal bars indicate the timing of the target flash (filled: saccade cue; open: reach cue), and long horizontal bars indicate the timing of the motor response (saccade or reach). Each panel shows a spike raster (eight trials aligned on cue presentation, every third action potential shown) and the corresponding spike density function (computed as in Fig. 89.2). Thin horizontal lines indicate the animal's vertical eye position during each trial. Vertical bars indicate calibration of firing rate and eye position. (Modified from Snyder et al., 1997.)

Intentional Maps

The experiments mentioned above indicate a topographical separation of intentions within the PPC (Fig. 89.4). While area LIP seems to be specialized for the planning of saccades (Gnadt and Andersen, 1988), MIP and area 5 are more dedicated to the planning of reach movements (Buneo et al., 2002; Kalaska, 1996; Snyder et al., 1997). Other groups have identified areas PO, 7m, 7a, and PEc as additional reaching-related areas within the PPC (Battaglia-Mayer et al., 2000; Ferraina et al., 1997, 2001; MacKay, 1992). Furthermore, the anterior intraparietal area (AIP) seems to play a specialized role for grasping, as demonstrated by Sakata and colleagues (1995). Cells in AIP respond to the shape of objects and the formation of the hand during grasping. Recent results of fMRI studies in humans were found to be consistent with the electrophysiological findings in the monkey. Rushworth et al. (2001) found that a peripheral attention task activated the lateral bank of the intraparietal sulcus, while the planning of manual movements involved activity in the medial bank. Connolly et al. (2000) reported a similar result using event-related fMRI. A specialized area for grasping has also been identified in the anterior aspect of the intraparietal sulcus in humans, which may be homologous to the monkey area AIP (Binkofski et al., 1998). Simon et al. (2002) also found a systematic anterior-posterior organization of activations associated with grasping, pointing, and eye movements. All this suggests that the parietal cortex is composed of distinguishable subregions both in monkeys and in humans.

Figure 89.4..  

Anatomical map of intentions in the PPC. AIP, anterior intraparietal area; LIP, lateral intraparietal area; MIP, medial intraparietal area.