Dorsal premotor cortex is involved in switching motor plans

Abstract

Previous studies have shown that neural activity in primate dorsal premotor cortex (PMd) can simultaneously represent multiple potential movement plans, and that activity related to these movement options is modulated by their relative subjective desirability. These findings support the hypothesis that decisions about actions are made through a competition within the same circuits that guide the actions themselves. This hypothesis further predicts that the very same cells that guide initial decisions will continue to update their activities if an animal changes its mind. For example, if a previously selected movement option suddenly becomes unavailable, the correction will be performed by the same cells that selected the initial movement, as opposed to some different group of cells responsible for online guidance. We tested this prediction by recording neural activity in the PMd of a monkey performing an instructed-delay reach selection task. In the task, two targets were simultaneously presented and their border styles indicated whether each would be worth 1, 2, or 3 juice drops. In a random subset of trials (FREE), the monkey was allowed a choice while in the remaining trials (FORCED) one of the targets disappeared at the time of the GO signal. In FORCED-LOW trials the monkey was forced to move to the less valuable target and started moving either toward the new target (Direct) or toward the target that vanished and then curved to reach the remaining one (Curved). Prior to the GO signal, PMd activity clearly reflected the monkey's subjective preference, predicting his choices in FREE trials even with equally valued options. In FORCED-LOW trials, PMd activity reflected the switch of the monkey's plan as early as 100 ms after the GO signal, well before movement onset (MO). This confirms that the activity is not related to feedback from the movement itself, and suggests that PMd continues to participate in action selection even when the animal changes its mind on-line. These findings were reproduced by a computational model suggesting that switches between action plans can be explained by the same competition process responsible for initial decisions.

Correction and suppression of reaching movements in the cerebral cortex: Physiological and neuropsychological aspects

“…Neural activity related to switching motor plans has been described by a recent study (Pastor-Bernier et al, 2012), which also suggests that in premotor cortex a unique biased competition model can account for both initial decisions and for changing motor intention. This account of substitution of motor plans in premotor cortex is related to the above-discussed versions of the race model.…”

Organization and evolution of parieto-frontal processing streams in macaque monkeys and humans

“…PMd neurons participate in the composition (Caminiti et al, 1991;Mattia et al, 2013), suppression (Mirabella et al, 2011) and online control (Archambault et al, 2011; for a review, see Battaglia-Mayer et al, 2014;Archambault et al, 2015) of reaches, by providing the higherorder signal to change or suppress an ongoing motor plan or action, or to brake the natural eye-hand coordination (Gail et al, 2009). In an action space rich of many potential choices, both premotor and parietal cortex can maintain simultaneous representations of the possible motor responses (Kalaska and Crammond, 1995); within these processes, premotor cortex can encode two potential reach targets Kalaska, 2002, 2010), the reaching decision (Cisek and Kalaska, 2005), as well as the decision to switch motor plan (Pastor-Bernier et al, 2012).…”

Timing and communication of parietal cortex for visuomotor control

“…Within this network, premotor cortex first provides the higher-order signal about the change of target location, thus calling for the specification of a new reach goal. This is in line with the consequences of its lesion in humans, which delays reach onset, but not impair reach accuracy [18 ], and with its role in tasks requiring switching of motor plans [19]. Thanks to the fine-grain specification of hand kinematics both before and during the hand movement toward first or second target location, SPL areas can provide both the early transformation necessary to specify the reach goal, as well as a continuous estimate of limb position, speed and movement direction.…”

“…J Neurosci 2014, 34:11948-11958. This study shows anti-synchrony in partial spike-LFP correlation in the beta band (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) between parietal and dorsal premotor reach-related areas in monkeys, and hypothesizes that anti-synchrony can decrease the probability that actions potentials originated in parietal cortex activate premotor cortex during attentive fixation and reach planning. The results are interpreted within the frame of the literature suggesting that betaband activity can reduce the interaction between brain structures and can have an inhibitory role on movement initiation.…”

“…As an example, the effective connection strength between areas can be increased, if the timing of firing of cortical projecting neurons with small axon diameter, therefore slow conduction velocity, leads the activation of neurons with large axon diameter and faster conduction velocity. Studies of the temporal dynamics of parieto-frontal interactions indicates that while parietal and premotor cortex oscillate in-phase in the beta band (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30), partial spike-field coherence in parietal cortex is asynchronous with oscillations in premotor cortex during periods of attentive fixation and motor planning [8 ], probably down-modulating parieto-frontal communication. Using a population partial spike-field coherence approach to study temporal interactions between parietal areas 2/5 and motor cortex (MI), only a weak parietal influence was found on MI during reach planning, but a strong one during reach movement [9 ], with parietal cortex influencing encoding of movement direction in primary motor cortex.…”