Heterogeneous Attractor Cell Assemblies for Motor Planning in Premotor Cortex

Abstract

Cognitive functions like motor planning rely on the concerted activity of multiple neuronal assemblies underlying still elusive computational strategies. During reaching tasks, we observed stereotyped sudden transitions (STs) between low and high multiunit activity of monkey dorsal premotor cortex (PMd) predicting forthcoming actions on a single-trial basis. Occurrence of STs was observed even when movement was delayed or successfully canceled after a stop signal, excluding a mere substrate of the motor execution. An attractor model accounts for upward STs and high-frequency modulations of field potentials, indicative of local synaptic reverberation. We found in vivo compelling evidence that motor plans in PMd emerge from the coactivation of such attractor modules, heterogeneous in the strength of local synaptic self-excitation. Modules with strong coupling early reacted with variable times to weak inputs, priming a chain reaction of both upward and downward STs in other modules. Such web of "flip-flops" rapidly converged to a stereotyped distributed representation of the motor program, as prescribed by the long-standing theory of associative networks.

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

“…A more concrete proposal of Mattia et al (2013) is that the PMd control processes are mediated by attractor-based systems. Individual attractors could then represent both the motor plan and any spatially specified target, the former as a point attractor and the latter as a plane attractor.…”

“…Neural modulations during motor plan maturation in PMd, studied at the level of multiunit activity, display two stereotyped forms of transition toward either lower or higher states, when compared to the level of activity measured at the time of target presentation (Mattia et al, 2013). These transitions were also observed when the movement was successfully canceled suggesting that they participate causally in that process too, but with a dynamic complementary to that of completing the Go-process.…”

“…However, all attempts to demonstrate the existence of a motor plan at an advanced level prior to its realization, which could then be realized by sub-threshold activation-based control, have been inconclusive for reaching movements, although evidence exists for analogous neural modulations with respect to saccadic eye movement control (Schall, 2001;Shenoy et al, 2013). Recent neurophysiological evidence and complementary simulations suggest an alternative, namely that the cortical control of movement generation resides in the dynamic of motor neurons under attractor-based control (Mattia et al, 2013;Shenoy et al, 2013). In this last scenario, mature motor plans corresponds to rapid and hierarchically organized changes in the state of neural activity occurring after target presentation.…”

“…In this last scenario, mature motor plans corresponds to rapid and hierarchically organized changes in the state of neural activity occurring after target presentation. Different modules with preferred high-and lowfiring states, and with heterogeneity in excitability (Mattia et al, 2013), are gradually recruited and could evolve in the corresponding motor act when external control breaks are released. Thus, motor plans can be assumed to be primarily rooted in premotor cortex, but motor execution would also involve other frontal structures with a cognitive control function, including the pre-SMA/SMA complex or basal ganglia.…”

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).…”