Motor intention activity in the Macaque's lateral intraparietal area I. Dissociation of motor plan from sensory memory

Pietro Mazzoni, R. Martyn Bracewell, Shabtai Barash, Richard A. Andersen

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1. The lateral intraparietal area (area LIP) of the monkey's posterior parietal cortex (PPC) contains neurons that are active during saccadic eye movements. These neurons' activity includes visual and saccade-related components. These responses are spatially tuned and the location of a neuron's visual receptive field (RF) relative to the fovea generally overlaps its preferred saccade amplitude and direction (i.e., its motor field, MF). When a delay is imposed between the presentation of a visual stimulus and a saccade made to its location (memory saccade task), many LIP neurons maintain elevated activity during the delay (memory activity, M), which appears to encode the metrics of the next intended saccadic eye movement. Recent studies have alternatively suggested that LIP neurons encode the locations of visual stimuli regardless of where the animal intends to look. We examined whether the M activity of LIP neurons specifically encodes movement intention or the locations of recent visual stimuli, or a combination of both. In the accompanying study, we investigated whether the intended-movement activity reflects changes in motor plan. 2. We trained monkeys (Macaca mulatta) to memorize the locations of two visual stimuli and plan a sequence of two saccades, one to each remembered target, as we recorded the activity of single LIP neurons. Two targets were flashed briefly while the monkey maintained fixation; after a delay the fixation point was extinguished, and the monkey made two saccades in sequence to each target's remembered location, in the order in which the targets were presented. This 'delayed double saccade' (DDS) paradigm allowed us to dissociate the location of visual stimulation from the direction of the planned saccade and thus distinguish neuronal activity related to the target's location from activity related to the saccade plan. By imposing a delay, we eliminated the confounding effect of any phasic responses coincident with the appearance of the stimulus and with the saccade. 3. We arranged the two visual stimuli so that in one set of conditions at least the first one was in the neuron's visual RF, and thus the first saccade was in the neuron's motor field (MF). M activity should be high in these conditions according to both the sensory memory and motor plan hypotheses. In another set of conditions, the second stimulus appeared in the RF but the first one was presented outside the RF, instructing the monkey to plan the first saccade away from the neuron's MF. If the M activity encodes the motor plan, it should be low in these conditions, reflecting the plan for the first saccade (away from the MF). If it is a sensory trace of the stimulus' location, it should be high, reflecting stimulation of the RF by the second target. 4. We tested 49 LIP neurons (in 3 hemispheres of 2 monkeys) with M activity on the DDS task. Of these, 38 (77%) had M activity related to the next intended saccade. They were active in the delay period, as expected, if the first saccade was in their preferred direction. They were less active or silent if the next saccade was not in their preferred direction, even when the second stimulus appeared in their RF. 5. The M activity of 8 (16%) of the remaining neurons specifically encoded the location of the most recent visual stimulus. Their firing rate during the delay reflected stimulation of the RF independently of the saccade being planned. The remaining 3 neurons had M activity that did not consistently encode either the next saccade or the stimulus' location. 6. We also recorded the activity of a subset of neurons (n = 38) in a condition in which no stimulus appeared in a neuron's RF, but the second saccade was in the neuron's MF. In this case the majority of neurons tested (23/38, 60%) became active in the period between the first and second saccade, even if neither stimulus had appeared in their RF. Moreover, this activity appeared only after the first saccade had started in all but two of these neurons. In general, the neurons' responses thus did not anticipate the saccades in the DDS task. 7. The majority of LIP neurons have activity related to the next intended saccade. Cells in LIP also carry a signal coding the memory of the location of the sensory stimulus, although at the population level this signal is less prominent than the intended movement signal in the DDS task. The intended movement signal is not simply an attention signal for a spatial location because it was reduced or absent when a location required attention but not a saccade to it. The posterior parietal cortex is thus not only involved in sensory and attentional processing but also participates in the formulation of movement plans.

Original languageEnglish
Pages (from-to)1439-1456
Number of pages18
JournalJournal of neurophysiology
Issue number3
StatePublished - Sep 1996


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