Neural basis of action understanding: Evidence from sign language aphasia

Abstract

Background The neural basis of action understanding is a hotly debated issue. The mirror neuron account holds that motor simulation in fronto-parietal circuits is critical to action understanding including speech comprehension, while others emphasize the ventral stream in the temporal lobe. Evidence from speech strongly supports the ventral stream account, but on the other hand, evidence from manual gesture comprehension (e.g., in limb apraxia) has led to contradictory findings. Aims Here we present a lesion analysis of sign language comprehension. Sign language is an excellent model for studying mirror system function in that it bridges the gap between the visual-manual system in which mirror neurons are best characterized and language systems which have represented a theoretical target of mirror neuron research. Methods & Procedures Twenty-one life long deaf signers with focal cortical lesions performed two tasks: one involving the comprehension of individual signs and the other involving comprehension of signed sentences (commands). Participants' lesions, as indicated on MRI or CT scans, were mapped onto a template brain to explore the relationship between lesion location and sign comprehension measures. Outcomes & Results Single sign comprehension was not significantly affected by left hemisphere damage. Sentence sign comprehension impairments were associated with left temporal-parietal damage. We found that damage to mirror system related regions in the left frontal lobe were not associated with deficits on either of these comprehension tasks. Conclusions We conclude that the mirror system is not critically involved in action understanding.

The role of putative human anterior intraparietal sulcus area in observed manipulative action discrimination

“…The absence of PCS activation in experiment 1 cannot be attributed to a statistical lack of power as this study included five more subjects than experiment 2, where the PCS activation was present. The absence of a featural attention effect for manipulative actions in premotor cortex may suggest a more limited role for the premotor level for perceiving others actions, which is consistent with a number of studies (Buxbaum & Kalenine, 2010;Caramazza, Anzellotti, Strnad, & Lingnau, 2014;Negri et al, 2007;Rogalsky et al, 2013;Stasenko, Garcea, & Mahon, 2013).…”

An fMRI study of perception and action in deaf signers

“…We recently studied a group of deaf brain damaged signers and found that damage to the dorsal sensorimotor stream is not associated with sign comprehension deficits (Rogalsky et al, 2013), arguing that functional activation overlap found in the present experiment does not reflect sign or action understanding. Instead, sign comprehension deficits were associated with temporal lobe lesions, consistent with previous work (Hickok, Love-Geffen, & Klima, 2002).…”

Earlier and More Robust Sensorimotor Discrimination of ASL Signs in Deaf Signers During Imitation

“…We predicted that during sign observation, Deaf signers would show less sensorimotor system activity and less differentiation of sign types in the sensorimotor system, because of the possibility that for those individuals the task would involve language systems of the brain more robustly than sensorimotor systems. This hypothesis was based on prior work using a similar paradigm in a passive (non-imitative) task (Kubicek & Quandt, 2019), as well as other functional neuroimaging evidence (Corina & Knapp, 2006; Emmorey, Xu, Gannon, Goldin-Meadow, & Braun, 2010; Okada et al, 2016; Rogalsky et al, 2013). However, in opposition to our prediction, we found no significant differences in overall alpha/beta ERD between the two groups while participants were observing the signs.…”

“…Some researchers have asked whether deaf signers, due to their extensive use of the hands and body for language, may show increases in mirroring activity when perceiving sign language. However, some sign language researchers determine that these processes have little to no role in in the higher-level neural and cognitive processing of sign languages (Corina & Knapp, 2006; Emmorey, Xu, Gannon, Goldin-Meadow, & Braun, 2010; Okada et al, 2016; Rogalsky et al, 2013). Several reports found no evidence to support the involvement of mirroring during sign perception (Rogalsky et al, 2013), and in fact generally suggested that signers recruit less of the sensorimotor system during sign perception, possibly because they are relying more on linguistic processing (Möttönen, Farmer, & Watkins, 2016).…”

“…However, some sign language researchers determine that these processes have little to no role in in the higher-level neural and cognitive processing of sign languages (Corina & Knapp, 2006; Emmorey, Xu, Gannon, Goldin-Meadow, & Braun, 2010; Okada et al, 2016; Rogalsky et al, 2013). Several reports found no evidence to support the involvement of mirroring during sign perception (Rogalsky et al, 2013), and in fact generally suggested that signers recruit less of the sensorimotor system during sign perception, possibly because they are relying more on linguistic processing (Möttönen, Farmer, & Watkins, 2016). Some findings suggest that deaf signers’ neural representations of action processing differ from hearing non-signers’ (Corina et al, 2007; Emmorey, McCullough, Mehta, Ponto, & Grabowski, 2011; Emmorey et al, 2010; Mole & Turner, 2017).…”