Roles of Monkey Premotor Neuron Classes in Movement Preparation and Execution

Neurosciences Program, Stanford University, Stanford, California 94305-4075, USA.
Journal of Neurophysiology (Impact Factor: 2.89). 08/2010; 104(2):799-810. DOI: 10.1152/jn.00231.2009
Source: PubMed


Dorsal premotor cortex (PMd) is known to be involved in the planning and execution of reaching movements. However, it is not understood how PMd plan activity-often present in the very same neurons that respond during movement-is prevented from itself producing movement. We investigated whether inhibitory interneurons might "gate" output from PMd, by maintaining high levels of inhibition during planning and reducing inhibition during execution. Recently developed methods permit distinguishing interneurons from pyramidal neurons using extracellular recordings. We extend these methods here for use with chronically implanted multi-electrode arrays. We then applied these methods to single- and multi-electrode recordings in PMd of two monkeys performing delayed-reach tasks. Responses of putative interneurons were not generally in agreement with the hypothesis that they act to gate output from the area: in particular it was not the case that interneurons tended to reduce their firing rates around the time of movement. In fact, interneurons increased their rates more than putative pyramidal neurons during both the planning and movement epochs. The two classes of neurons also differed in a number of other ways, including greater modulation across conditions for interneurons, and interneurons more frequently exhibiting increases in firing rate during movement planning and execution. These findings provide novel information about the greater responsiveness of putative PMd interneurons in motor planning and execution and suggest that we may need to consider new possibilities for how planning activity is structured such that it does not itself produce movement.

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Available from: Matthew T Kaufman, Dec 24, 2013
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    • "We recorded neural activity from motor and premotor cortex during a variety of reaching tasks (Churchland et al. 2006; Kaufman et al. 2010). Neurons showed a broad range of response patterns (Fig. 4) and rarely resembled the predictions of the traditional model (Churchland and Shenoy 2007; Churchland et al. 2010, 2012). "
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    ABSTRACT: The motor cortex was the one of the first cortical areas to be explored electrophysiologically, yet little agreement has emerged regarding its basic response properties. Often it is assumed that single-neuron responses reflect a preference for a particular movement or movement variable. It may be further assumed that movement is generated by (or at least accompanied by) a growing population-level preference for the relevant movement. This view has been attractive because it provides a canonical form for the single neuron, a link between preparatory and movement activity, a way of interpreting the population response, and a platform for designing analyses and couching hypotheses. However, this traditional view yields predictions that are at odds with basic features of the data. We discuss an alternative simplified model, in which outgoing commands are produced by dynamics that generate different output patterns as a function of the initial preparatory state. For reaching tasks, we hypothesized simple quasioscillatory dynamics because they provide a natural basis set for the empirical patterns of muscle activity. The predictions of the dynamical model match the data well at both the single-neuron and population levels, and the quasioscillatory patterns explain many of the otherwise odd features of the neural responses. Copyright © 2014 Cold Spring Harbor Laboratory Press; all rights reserved.
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    • "Sustained preparatory neural activities preceding voluntary movements have been reported in humans (Kornhuber and Deecke, 1965; Libet et al., 1983; Soon et al., 2008) and monkeys (Romo and Schultz, 1987; Kato et al., 1995; Kaufman et al., 2010). Here, however, we further demonstrate that the increased neural activity preceding self-initiated movement is also associated with a heightened sensory sampling (EODR) that precedes movement onset. "
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    • "More specifically, the waveforms of pyramidal neurons tend to be broader and slower than those seen in the most interneurons. Using this classification, several extracellular-recording studies have been able to elucidate roles of pyramidal neurons and interneurons for visual working memory in the prefrontal cortex (Wilson et al., 1994; Rao et al., 1999; Constantinidis and Goldman-Rakic, 2002; Diester and Nieder, 2008; Hussar and Pasternak, 2012), visual attention in V4 (Mitchell et al., 2007), visual perceptual decision-making in the frontal eye field (Ding and Gold, 2011), motor control in the motor and premotor cortices (Isomura et al., 2009; Kaufman et al., 2010), and auditory processing during the passive listening in the auditory cortex (Atencio and Schreiner, 2008; Sakata and Harris, 2009; Ogawa et al., 2011). Interestingly, most of these studies showed differential roles in pyramidal neurons and interneurons. "
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