Single-Neuron Responses in Humans during Execution and Observation of Actions

Abstract

Direct recordings in monkeys have demonstrated that neurons in frontal and parietal areas discharge during execution and perception of actions [1-8]. Because these discharges "reflect" the perceptual aspects of actions of others onto the motor repertoire of the perceiver, these cells have been called mirror neurons. Their overlapping sensory-motor representations have been implicated in observational learning and imitation, two important forms of learning [9]. In humans, indirect measures of neural activity support the existence of sensory-motor mirroring mechanisms in homolog frontal and parietal areas [10, 11], other motor regions [12-15], and also the existence of multisensory mirroring mechanisms in nonmotor regions [16-19]. We recorded extracellular activity from 1177 cells in human medial frontal and temporal cortices while patients executed or observed hand grasping actions and facial emotional expressions. A significant proportion of neurons in supplementary motor area, and hippocampus and environs, responded to both observation and execution of these actions. A subset of these neurons demonstrated excitation during action-execution and inhibition during action-observation. These findings suggest that multiple systems in humans may be endowed with neural mechanisms of mirroring for both the integration and differentiation of perceptual and motor aspects of actions performed by self and others.

Observing object lifting errors modulates cortico-spinal excitability and improves object lifting performance

“…The current findings also provide an interesting new take on theories regarding the 'action observation system', where motor skills activate the same neural circuitry in left premotor cortex as observing the same action (Malfait et al, 2010;Mukamel et al, 2010). This link is normally considered to be an automatic mirroring relationship, implicitly preparing the observer to mimic the observed act.…”

“…These studies tend to be interpreted within the broader context of the putative human mirror neuron system (Gallese et al, 2011;Mukamel et al, 2010). The overlapping neuronal populations and cortical regions in human and non-human primates has been taken by some as a mechanism for observational learning, by means of implicit neural simulation of the observed action (Calvo-Merino et al, 2005;Jeannerod, 2001).…”

Shared electrophysiology mechanisms of body ownership and motor imagery

“…Sensorimotor tasks (Pineda, 2005), motor action execution, inhibition, and observation (Gastaut, 1952;Howe and Sterman, 1972;Niedermeyer and Lopes da Silva, 1993) are reflected in such mu oscillations. Additionally, both intracranial electrophysiology (Gastaut and Bert, 1954;Mukamel et al, 2010;Tremblay et al, 2004) and surface EEG (Cochin et al, 1999(Cochin et al, , 1998 consistently show comparable mu rhythm suppression during both the execution and the observation of different movements. Mu oscillations have also been investigated with respect to motor imagery (review in Neuper et al, 2006) and have been linked to mu suppression in parietal cortex, premotor, and primary sensorimotor areas (Pfurtscheller and Neuper, 1997;Pfurtscheller et al, 1997a).…”

Power modulation of electroencephalogram mu and beta frequency depends on perceived level of observed actions

“…2008; Dushanova and Donoghue 2010; Mukamel et al. 2010; Kilner and Lemon 2013; Vigneswaran et al. 2013).…”