The Mirror Neuron System and the Strange Case of Broca's Area

Overview

Journal Hum Brain Mapp

Publisher Wiley

Specialty Neurology

Date 2014 Nov 5

PMID 25366580

Citations 13

Authors

Gabriella Cerri

Monia Cabinio

Valeria Blasi

Paola Borroni

Antonella Iadanza

Enrica Fava

Luca Fornia

Valentina Ferpozzi

Marco Riva

Alessandra Casarotti

Filippo Martinelli Boneschi

Andrea Falini

Lorenzo Bello

Affiliations

Soon will be listed here.

Abstract

Mirror neurons, originally described in the monkey premotor area F5, are embedded in a frontoparietal network for action execution and observation. A similar Mirror Neuron System (MNS) exists in humans, including precentral gyrus, inferior parietal lobule, and superior temporal sulcus. Controversial is the inclusion of Broca's area, as homologous to F5, a relevant issue in light of the mirror hypothesis of language evolution, which postulates a key role of Broca's area in action/speech perception/production. We assess "mirror" properties of this area by combining neuroimaging and intraoperative neurophysiological techniques. Our results show that Broca's area is minimally involved in action observation and has no motor output on hand or phonoarticulatory muscles, challenging its inclusion in the MNS. The presence of these functions in premotor BA6 makes this area the likely homologue of F5 suggesting that the MNS may be involved in the representation of articulatory rather than semantic components of speech.

Citing Articles

Connectivity Reveals the Relationships between Human Brain Areas Associated with High-Level Linguistic Processing and Macaque Brain Areas.

Wang F, Lu X, Chen X, Wang Q, Li Q, Li H Tomography. 2024; 10(7):1089-1098.

PMID: 39058054 PMC: 11280774. DOI: 10.3390/tomography10070082.

Object-oriented hand dexterity and grasping abilities, from the animal quarters to the neurosurgical OR: a systematic review of the underlying neural correlates in non-human, human primate and recent findings in awake brain surgery.

Tariciotti L, Mattioli L, Vigano L, Gallo M, Gambaretti M, Sciortino T Front Integr Neurosci. 2024; 18:1324581.

PMID: 38425673 PMC: 10902498. DOI: 10.3389/fnint.2024.1324581.

Occupation-modulated language networks and its lateralization: A resting-state fMRI study of seafarers.

Wu H, Peng D, Yan H, Yang Y, Xu M, Zeng W Front Hum Neurosci. 2023; 17:1095413.

PMID: 36992794 PMC: 10040660. DOI: 10.3389/fnhum.2023.1095413.

The widespread action observation/execution matching system for facial expression processing.

Sato W, Kochiyama T, Yoshikawa S Hum Brain Mapp. 2023; 44(8):3057-3071.

PMID: 36895114 PMC: 10171515. DOI: 10.1002/hbm.26262.

Spatio-Temporal Neural Dynamics of Observing Non-Tool Manipulable Objects and Interactions.

Li Z, Iramina K Sensors (Basel). 2022; 22(20).

PMID: 36298121 PMC: 9611388. DOI: 10.3390/s22207771.

References

Hickok G . Computational neuroanatomy of speech production. Nat Rev Neurosci. 2012; 13(2):135-45. PMC: 5367153. DOI: 10.1038/nrn3158. View

Buccino G, Vogt S, Ritzl A, Fink G, Zilles K, Freund H . Neural circuits underlying imitation learning of hand actions: an event-related fMRI study. Neuron. 2004; 42(2):323-34. DOI: 10.1016/s0896-6273(04)00181-3. View

Mantini D, Hasson U, Betti V, Perrucci M, Luca Romani G, Corbetta M . Interspecies activity correlations reveal functional correspondence between monkey and human brain areas. Nat Methods. 2012; 9(3):277-82. PMC: 3438906. DOI: 10.1038/nmeth.1868. View

Rizzolatti G, Craighero L . The mirror-neuron system. Annu Rev Neurosci. 2004; 27:169-92. DOI: 10.1146/annurev.neuro.27.070203.144230. View

Duncan J, Owen A . Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci. 2000; 23(10):475-83. DOI: 10.1016/s0166-2236(00)01633-7. View

Dinstein I, Thomas C, Behrmann M, Heeger D . A mirror up to nature. Curr Biol. 2008; 18(1):R13-8. PMC: 2517574. DOI: 10.1016/j.cub.2007.11.004. View

Binkofski F, Buccino G, Posse S, Seitz R, Rizzolatti G, Freund H . A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. Eur J Neurosci. 1999; 11(9):3276-86. DOI: 10.1046/j.1460-9568.1999.00753.x. View

Kraskov A, Prabhu G, Quallo M, Lemon R, Brochier T . Ventral premotor-motor cortex interactions in the macaque monkey during grasp: response of single neurons to intracortical microstimulation. J Neurosci. 2011; 31(24):8812-21. PMC: 3121557. DOI: 10.1523/JNEUROSCI.0525-11.2011. View

Nishitani N, Hari R . Viewing lip forms: cortical dynamics. Neuron. 2002; 36(6):1211-20. DOI: 10.1016/s0896-6273(02)01089-9. View

10.

Luders H, Dinner D, MORRIS H, Wyllie E, Comair Y . Cortical electrical stimulation in humans. The negative motor areas. Adv Neurol. 1995; 67:115-29. View

11.

Molenberghs P, Cunnington R, Mattingley J . Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neurosci Biobehav Rev. 2011; 36(1):341-9. DOI: 10.1016/j.neubiorev.2011.07.004. View

12.

Duffau H, Capelle L, Denvil D, Gatignol P, Sichez N, Lopes M . The role of dominant premotor cortex in language: a study using intraoperative functional mapping in awake patients. Neuroimage. 2003; 20(4):1903-14. DOI: 10.1016/s1053-8119(03)00203-9. View

13.

Grezes J, Armony J, Rowe J, Passingham R . Activations related to "mirror" and "canonical" neurones in the human brain: an fMRI study. Neuroimage. 2003; 18(4):928-37. DOI: 10.1016/s1053-8119(03)00042-9. View

14.

Sereno M, Tootell R . From monkeys to humans: what do we now know about brain homologies?. Curr Opin Neurobiol. 2005; 15(2):135-44. DOI: 10.1016/j.conb.2005.03.014. View

15.

Tandon N, Narayana S, Lancaster J, Brown S, Dodd S, Vollmer D . CNS Resident Award: role of the lateral premotor cortex in articulation. Clin Neurosurg. 2003; 50:341-9. View

16.

Espadaler J, Rogic M, Deletis V, Leon A, Quijada C, Conesa G . Representation of cricothyroid muscles at the primary motor cortex (M1) in healthy subjects, mapped by navigated transcranial magnetic stimulation (nTMS). Clin Neurophysiol. 2012; 123(11):2205-11. DOI: 10.1016/j.clinph.2012.04.008. View

17.

Juch H, Zimine I, L Seghier M, Lazeyras F, Fasel J . Anatomical variability of the lateral frontal lobe surface: implication for intersubject variability in language neuroimaging. Neuroimage. 2005; 24(2):504-14. DOI: 10.1016/j.neuroimage.2004.08.037. View

18.

Morin O, Grezes J . What is "mirror" in the premotor cortex? A review. Neurophysiol Clin. 2008; 38(3):189-95. DOI: 10.1016/j.neucli.2008.02.005. View

19.

Toni I, de Lange F, Noordzij M, Hagoort P . Language beyond action. J Physiol Paris. 2008; 102(1-3):71-9. DOI: 10.1016/j.jphysparis.2008.03.005. View

20.

Mengotti P, Corradi-DellAcqua C, Negri G, Ukmar M, Pesavento V, Rumiati R . Selective imitation impairments differentially interact with language processing. Brain. 2013; 136(Pt 8):2602-18. DOI: 10.1093/brain/awt194. View