fMRI Adaptation between Action Observation and Action Execution Reveals Cortical Areas with Mirror Neuron Properties in Human BA 44/45

Abstract

Mirror neurons (MNs) are considered to be the supporting neural mechanism for action understanding. MNs have been identified in monkey’s area F5. The identification of MNs in the human homolog of monkeys’ area F5 Broadmann Area 44/45 (BA 44/45) has been proven methodologically difficult. Cross-modal functional MRI (fMRI) adaptation studies supporting the existence of MNs restricted their analysis to a priori candidate regions, whereas studies that failed to find evidence used non-object-directed (NDA) actions. We tackled these limitations by using object-directed actions (ODAs) differing only in terms of their object directedness in combination with a cross-modal adaptation paradigm and a whole-brain analysis. Additionally, we tested voxels’ blood oxygenation level-dependent (BOLD) response patterns for several properties previously reported as typical MN response properties. Our results revealed 52 voxels in left inferior frontal gyrus (IFG; particularly BA 44/45), which respond to both motor and visual stimulation and exhibit cross-modal adaptation between the execution and observation of the same action. These results demonstrate that part of human IFG, specifically BA 44/45, has BOLD response characteristics very similar to monkey’s area F5.

The topographical organization of motor processing: An ALE meta-analysis on six action domains and the relevance of Broca’s region

“…However, these left IFG clusters are not consistently reported in the literature and moreover they are reported also for non-object-directed actions or actions with unclear intentions, also when performed with different effectors (Agnew et al, 2012;Ge et al, 2018;Lui et al, 2008;Wheaton et al, 2004). In addition, studies reporting activity within Broca's area, with regards to action observation, localize neural activity in an anterior portion of BA44 or directly in BA45 (de la Rosa et al, 2016;Decety et al, 1997;Grafton et al, 1996;Rizzolatti et al, 1996). Thus, considering exclusively meaningful object-directed actions in our meta-analysis would have introduced an unreasoned bias in focusing on a specific type of action.…”

“…These representations are only needed in contexts in which the motor aspects of an action have to be directly retrieved, providing an explanation for the absence of involvement of the area in action observation. Furthermore, the recruitment of BA44 and BA45 in the motor domain has been often linked to processes related to object-directed actions, especially when observing these specific type of actions (de la Rosa et al, 2016;Johnson-Frey et al, 2003;Nishitani and Hari, 2000). However, these left IFG clusters are not consistently reported in the literature and moreover they are reported also for non-object-directed actions or actions with unclear intentions, also when performed with different effectors (Agnew et al, 2012;Ge et al, 2018;Lui et al, 2008;Wheaton et al, 2004).…”

Greater involvement of action simulation mechanisms in emotional vs cognitive empathy

“…In the case of emotional empathy, overlap with localized action simulation areas was observed in the left pSTS, right middle STS, right precuneus/cuneus, bilateral SMA, and the left IFG. Notably, the IFG represents a critical region for observation-execution matching, based on single-cell recording in anatomically corresponding areas in the macaque brain ( di Pellegrino et al , 1992 ; Gallese et al , 1996 ), and fMRI data in humans including action perception and execution studies ( Caspers et al , 2010 ; Molenberghs et al , 2012 ) and fMRI adaptation paradigms ( Kilner et al , 2009 ; de la Rosa et al , 2016 ). Further, impaired imitation has been observed following transient lesions of bilateral IFG ( Heiser et al , 2003 ), and acquired IFG lesions are associated with human action encoding deficits ( Fazio et al , 2009 ).…”

Two Ways to Facial Expression Recognition? Motor and Visual Information Have Different Effects on Facial Expression Recognition

“…Researchers in several functional MRI (fMRI) studies examined cross-talk between motor-visual areas in a methodological rigorous way using fMRI adaptation paradigms with inconclusive results. While some scholars using this paradigm were able to identify cortical areas sensitive to both motor and visual input (Chong, Cunnington, Williams, & Kanwisher, 2008; de la Rosa, Schillinger, Bülthoff, Schultz, & Uludag, 2016; Kilner, Neal, Weiskopf, Friston, & Frith, 2009), others were not (Dinstein, Hasson, Rubin, & Heeger, 2007; Lingnau, Gesierich, & Caramazza, 2009). A recent physiological study with macaque monkeys pinned the fMRI adaptation effect to the adaptation of local field potentials rather than a neuronal firing rate change (Caggiano et al, 2013).…”