Visuomotor processing as reflected in the directional discharge of premotor and primary motor cortex neurons

Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455, USA.
Journal of Neurophysiology (Impact Factor: 2.89). 03/1999; 81(2):875-94.
Source: PubMed


Premotor and primary motor cortical neuronal firing was studied in two monkeys during an instructed delay, pursuit tracking task. The task included a premovement "cue period," during which the target was presented at the periphery of the workspace and moved to the center of the workspace along one of eight directions at one of four constant speeds. The "track period" consisted of a visually guided, error-constrained arm movement during which the animal tracked the target as it moved from the central start box along a line to the opposite periphery of the workspace. Behaviorally, the animals tracked the required directions and speeds with highly constrained trajectories. The eye movements consisted of saccades to the target at the onset of the cue period, followed by smooth pursuit intermingled with saccades throughout the cue and track periods. Initially, an analysis of variance (ANOVA) was used to test for direction and period effects in the firing. Subsequently, a linear regression analysis was used to fit the average firing from the cue and track periods to a cosine model. Directional tuning as determined by a significant fit to the cosine model was a prominent feature of the discharge during both the cue and track periods. However, the directional tuning of the firing of a single cell was not always constant across the cue and track periods. Approximately one-half of the neurons had differences in their preferred directions (PDs) of >45 degrees between cue and track periods. The PD in the cue or track period was not dependent on the target speed. A second linear regression analysis based on calculation of the preferred direction in 20-ms bins (i.e., the PD trajectory) was used to examine on a finer time scale the temporal evolution of this change in directional tuning. The PD trajectories in the cue period were not straight but instead rotated over the workspace to align with the track period PD. Both clockwise and counterclockwise rotations occurred. The PD trajectories were relatively straight during most of the track period. The rotation and eventual convergence of the PD trajectories in the cue period to the preferred direction of the track period may reflect the transformation of visual information into motor commands. The widely dispersed PD trajectories in the cue period would allow targets to be detected over a wide spatial aperture. The convergence of the PD trajectories occurring at the cue-track transition may serve as a "Go" signal to move that was not explicitly supplied by the paradigm. Furthermore, the rotation and convergence of the PD trajectories may provide a mechanism for nonstandard mapping. Standard mapping refers to a sensorimotor transformation in which the stimulus is the object of the reach. Nonstandard mapping is the mapping of an arbitrary stimulus into an arbitrary movement. The shifts in the PD may allow relevant visual information from any direction to be transformed into an appropriate movement direction, providing a neural substrate for nonstandard stimulus-response mappings.

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    • "This activation may suggest a gender difference in decoding strategy, whereby men may have analyzed the motor states of the characters more than women. Reference frames centered on body parts, such as the hand, are thought to be present in the dorsal premotor cortex (Caminiti et al., 1991; Crammond and Kalaska, 1994; Shen and Alexander, 1997; Johnson et al., 1999). Men also showed greater activation in the left anterior insula and the right superior parietal lobule (RSPL) while judging the emotional state of the character. "
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    ABSTRACT: Accurately reading the body language of others may be vital for navigating the social world, and this ability may be influenced by factors, such as our gender, personality characteristics and neurocognitive processes. This fMRI study examined the brain activation of 26 healthy individuals (14 women and 12 men) while they judged the action performed or the emotion felt by stick figure characters appearing in different postures. In both tasks, participants activated areas associated with visual representation of the body, motion processing and emotion recognition. Behaviorally, participants demonstrated greater ease in judging the physical actions of the characters compared to judging their emotional states, and participants showed more activation in areas associated with emotion processing in the emotion detection task, whereas they showed more activation in visual, spatial and action-related areas in the physical action task. Gender differences emerged in brain responses, such that men showed greater activation than women in the left dorsal premotor cortex in both tasks. Finally, participants higher in self-reported empathy demonstrated greater activation in areas associated with self-referential processing and emotion interpretation. These results suggest that empathy levels and sex of the participant may affect neural responses to emotional body language.
    Full-text · Article · Apr 2011 · Social Cognitive and Affective Neuroscience
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    • "Although the authors demonstrate very elegantly a correlation between MI activity and single kinematic parameters, it still remains to be seen whether individual MI neurons invariantly specify a given parameter regardless of context, a hallmark of genuine encoding (Hatsopoulos et al., in press). Previous attempts to characterize the encoding properties of MI neurons have failed to show invariant specification across different portions of the workspace (Caminiti et al., 1990), different postural states (Scott and Kalaska, 1995), different task paradigms (isometric versus isotonic) (Sergio and Kalaska, 1998), and even across time (Sergio and Kalaska, 1998; Johnson et al., 1999; Sergio et al., 2005; Hatsopoulos et al., 2007). "

    Preview · Article · May 2009 · Cortex
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    • "The influence of instructed speed could of course be due to different activation patterns of the muscles, which are certainly distributed in space.) We also note that a prior study found that target speed influenced delay-period activity (Johnson et al. 1999). Our results suggest that the influence of target speed in that study may have been related in part (but probably only in part) to the different reach speeds necessary to strike targets moving at different speeds. "
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    ABSTRACT: Neurons in premotor and motor cortex show preparatory activity during an instructed-delay task. It has been suggested that such activity primarily reflects visuospatial aspects of the movement, such as target location or reach direction and extent. We asked whether a more dynamic feature, movement speed, is also reflected. Two monkeys were trained to reach at different speeds ("slow" or "fast," peak speed being approximately 50-100% higher for the latter) depending on target color. Targets were presented in seven directions and at two distances. Of 95 neurons with tuned delay-period activity, 95, 78, and 94% showed a significant influence of direction, distance, and instructed speed, respectively. Average peak modulations with respect to direction, distance and speed were 18, 10, and 11 spikes/s. Although robust, modulations of firing rate with target direction were not necessarily invariant: for 45% of neurons, the preferred direction depended significantly on target distance and/or instructed speed. We collected an additional dataset, examining in more detail the effect of target distance (5 distances from 3 to 12 cm in 2 directions). Of 41 neurons with tuned delay-period activity, 85, 83, and 98% showed a significant impact of direction, distance, and instructed speed. Statistical interactions between the effects of distance and instructed speed were common, but it was nevertheless clear that distance "tuning" was not in general a simple consequence of speed tuning. We conclude that delay-period preparatory activity robustly reflects a nonspatial aspect of the upcoming reach. However, it is unclear whether the recorded neural responses conform to any simple reference frame, intrinsic or extrinsic.
    Preview · Article · Jan 2007 · Journal of Neurophysiology
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