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The Journal of Neuroscience, March 16, 2005, 25(11):2965-2976; doi:10.1523/JNEUROSCI.4036-04.2005

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Behavioral/Systems/Cognitive
Context-Dependent Modulation of Movement-Related Discharge in the Primate Globus Pallidus

Robert S. Turner^1,3,4 and Marjorie E. Anderson^2,3,4

¹Department of Neurological Surgery, University of California San Francisco, San Francisco, California 94122, and Departments of ²Rehabilitation Medicine and ³Physiology and Biophysics and ⁴National Primate Research Center, University of Washington, Seattle, Washington 98195

A selective contribution of the basal ganglia (BG) to memory-contingent motor control has long been hypothesized. The importance of memory context remains an open question, however, for the BG skeletomotor circuit. To investigate this question, we studied the perimovement discharge of a carefully selected group of 74 "arm-related" pallidal cells in two rhesus monkeys. The animals performed three tasks designed to dissociate multiple independent aspects of memory-contingent reaching while controlling movement kinematics. The activity of most neurons (88%) was influenced strongly by the memory demands of a task (remembering "where" or "when" to move), but the population as a whole showed no systematic preference for memory- or sensory-contingent conditions. The effects of memory context were primarily additive with those of movement kinematics (particularly movement direction). Considered separately, decreases and increases in firing had very different context preferences: decreases were nearly always larger for sensory-triggered movements, whereas increases were enhanced most often under memory-contingent conditions (i.e., self-initiated or self-guided movements). A similar pattern of preferences was found for both pallidal segments. The distinct context-specific enhancements of decreases and increases could not be explained as simple sensory responses or as interactions with preparatory or anticipatory processes present before movement initiation. Rather, they appear related to movement execution under specific contexts. Our results lead to the conclusion that movement facilitatory decreases in internal pallidal (GPi) activity are primarily greater under sensory-triggered conditions. GPi increases and their suppressive effects, perhaps on competing activity in pallidal-recipient centers, have increased prevalence under memory-contingent conditions.

Key words: basal ganglia; macaque; reaching; memory contingent; motor control; sensory guidance

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Received Sep 29, 2004; revised January 31, 2005; accepted February 1, 2005.

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