Mirror Neuron Populations Represent Sequences of Behavioral Epochs During Both Execution and Observation

Abstract

Mirror neurons (MNs) have the distinguishing characteristic of modulating during both execution and observation of an action. Although most studies of MNs have focused on various features of the observed movement, MNs also may monitor the behavioral circumstances in which the movement is embedded, including time periods preceding and following the observed movement. Here, we recorded multiple MNs simultaneously from implanted electrode arrays as two male monkeys executed and observed a reach, grasp, and manipulate task involving different target objects. MNs were recorded from premotor cortex (PM-MNs) and primary motor cortex (M1-MNs). During execution trials, hidden Markov models (HMMs) applied to the activity of either PM-MN or M1-MN populations most often detected sequences of four hidden states, which we named according to the behavioral epoch during which each state began: initial, reaction, movement, and final. The hidden states of MN populations thus reflected not only the movement, but also three behavioral epochs during which no movement occurred. HMMs trained on execution trials could decode similar sequences of hidden states in observation trials, with complete hidden state sequences decoded more frequently from PM-MN populations than from M1-MN populations. Moreover, population trajectories projected in a 2D plane defined by execution trials were preserved in observation trials more for PM-MN than for M1-MN populations. These results suggest that MN populations represent entire behavioral sequences, including both movement and non-movement. PM-MN populations showed greater similarity than M1-MN populations in their representation of behavioral sequences during execution versus observation. Mirror neurons (MNs) are thought to provide a neural mechanism for understanding the actions of others. However, for an action to be understood, both the movement per se and the non-movement context before and after the movement need to be represented. We found that simultaneously recorded MN populations encoded sequential hidden neural states corresponding approximately to sequential behavioral epochs of a reach, grasp, and manipulate task. During observation trials, hidden state sequences were similar to those identified in execution trials. Hidden state similarity was stronger for MN populations in premotor cortex than for those in primary motor cortex. Execution/observation similarity of hidden state sequences may contribute to understanding the actions of others without actually performing the action oneself.

Movement initiation and grasp representation in premotor and primary motor cortex mirror neurons

“…However, an alternative method which seeks to circumvent this by constraining random subspaces to the covariance structure of the full dataset (Elsayed et al, 2016) is biased towards identifying orthogonality between two different subspaces, due to regression to the mean within the null distribution. The finding that execution and observation are more overlapping in F5 is consistent with recent work demonstrating MirN activity in ventral premotor cortex (PMv) and M1 during execution of reach and grasp to be associated with a series of hidden states, which were recapitulated during observation in PMv, but not M1 (Mazurek et al, 2018). Overall, although M1 neurons can be active during both execution and observation, the pattern of this activity at the population level was quite different between the two conditions.…”

“…While the roles of F5 and M1 during the execution of visually-guided grasp have been studied extensively (Umiltá et al, 2007; Davare et al, 2008; Schaffelhofer & Scherberger, 2016), a more systematic understanding of the differences between action execution and observation activity in these two key nodes in the grasping circuitry could provide important insights into dissociations between representation of potential actions at the cortical level, and recruitment of descending pathways and muscles for actual action execution (Schieber, 2011). Along these lines, recent work comparing MirNs in premotor and motor cortex found premotor MirNs, but not those in M1, showed similar state transitions in execution and observation (Mazurek et al, 2018). State-space analyses have also previously found that F5 and the upstream anterior intraparietal area (AIP) exhibit different dynamics during immediate and delayed grasping actions (Michaels et al, 2018).…”

“…At the spinal level, PTNs not only excite motoneurons via cortico-motoneuronal (CM) projections (Porter & Lemon, 1993; Rathelot & Strick, 2006), but also exert indirect effects via segmental interneuron pathways, which in turn display their own complex activity before and during movement (Prut & Fetz, 1999; Takei & Seki, 2013). A dynamical systems approach (Shenoy et al, 2013) has recently suggested that movement-related activity unfolds in largely orthogonal dimensions to activity during action preparation, such that movement is implicitly gated during movement preparation (Kaufman et al, 2014; Elsayed et al, 2016), and a similar mechanism has been hypothesised to operate during action observation (Mazurek et al, 2018). While the roles of F5 and M1 during the execution of visually-guided grasp have been studied extensively (Umiltá et al, 2007; Davare et al, 2008; Schaffelhofer & Scherberger, 2016), a more systematic understanding of the differences between action execution and observation activity in these two key nodes in the grasping circuitry could provide important insights into dissociations between representation of potential actions at the cortical level, and recruitment of descending pathways and muscles for actual action execution (Schieber, 2011).…”

Movement initiation and grasp representation in premotor and primary motor cortex mirror neurons

“…While the roles of F5 and M1 during the execution of visually-guided grasp have been studied extensively ( Umilta et al, 2007 ; Davare et al, 2008 ; Schaffelhofer and Scherberger, 2016 ), a more systematic understanding of the differences between action execution and observation activity in these two key nodes in the grasping circuitry could provide important insights into dissociations between representation of potential actions at the cortical level, and recruitment of descending pathways and muscles for actual action execution ( Schieber, 2011 ). Along these lines, recent work comparing MNs in premotor and motor cortex found premotor MNs, but not those in M1, showed similar state transitions in execution and observation ( Mazurek et al, 2018 ). State-space analyses have also previously found that F5 and the upstream anterior intraparietal area (AIP) exhibit different dynamics during immediate and delayed grasping actions ( Michaels et al, 2018 ).…”

“…At the spinal level, PTNs not only excite motoneurons via cortico-motoneuronal (CM) projections ( Porter and Lemon, 1993 ; Rathelot and Strick, 2006 ), but also exert indirect effects via segmental interneuron pathways, which in turn display their own complex activity before and during movement ( Prut and Fetz, 1999 ; Takei and Seki, 2013 ). A dynamical systems approach ( Shenoy et al, 2013 ) has recently suggested that movement-related activity unfolds in largely orthogonal dimensions to activity during action preparation, such that movement is implicitly gated during movement preparation ( Kaufman et al, 2014 ; Elsayed et al, 2016 ), and a similar mechanism has been hypothesised to operate during action observation ( Mazurek et al, 2018 ) and action suppression ( Pani et al, 2019 ). While the roles of F5 and M1 during the execution of visually-guided grasp have been studied extensively ( Umilta et al, 2007 ; Davare et al, 2008 ; Schaffelhofer and Scherberger, 2016 ), a more systematic understanding of the differences between action execution and observation activity in these two key nodes in the grasping circuitry could provide important insights into dissociations between representation of potential actions at the cortical level, and recruitment of descending pathways and muscles for actual action execution ( Schieber, 2011 ).…”