Technical Comments

Comment on “Movement Intention After Parietal Cortex Stimulation in Humans”

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Science  05 Mar 2010:
Vol. 327, Issue 5970, pp. 1200
DOI: 10.1126/science.1183735

Abstract

Desmurget et al. (Reports, 8 May 2009, p. 811) applied direct electrical stimulation (DES) to the human cortex to study the origin of movement intention. Their interpretation assumed that DES causes cortical activation, whereas it is possible that it actually evokes deactivation. The lack of certain knowledge about the true effects of DES limits its use for validation of cognitive models.

Intraoperative direct electrical stimulation (DES) applies an electrical current to the cortex of awake patients. The technique aids surgery in individuals with tumors or with epilepsy, identifying brain areas critical for important functions (13). The ability to map critical locations for each individual has tremendous clinical value, as the location of brain function varies between patients due to normal individual variability of cortical organization as well as functional reorganization in response to the individual’s brain pathology.

In addition to its clinical utility, DES has recently experienced a renaissance among cognitive neuroscientists (47). Recently, Desmurget et al. (7) used this technique to study the origin of willed action. They found that DES applied to either the left or right inferior parietal lobule (IPL) triggered a strong intention and desire to move the lips or contralateral limbs. The authors interpreted this finding as demonstrating that motor intention and awareness are consequences of increased parietal activity. However, was it indeed an increase of parietal activity, or rather parietal deactivation that evoked the desire to move?

There is clear evidence that DES at the same cortical sites (i.e., IPL) and with an identical stimulation regime as in Desmurget et al. (7) interferes with language functions when applied to the human left hemisphere (3) and disturbs visual object processing when applied to the right hemisphere (4). Although these previous findings are often assumed to demonstrate that DES actually inhibits cortical activity, these inhibitory behavioral effects likewise do not allow firm conclusions on the status of local activity. The uncertainty about whether DES induces an increase or decrease of cortical activity cannot be resolved by post hoc reinterpretation of the behavioral data alone.

Considering the biophysical effects of extracellular stimulation, it becomes clear that DES evokes a complex sum effect in a relatively large stimulated volume (8). Depending on the distance from the electrodes, action potentials are elicited or blocked at individual cell bodies and axons. In addition to distance, polarity of the nearest electrode, the diameter of passing fibers, and fiber orientation determine the resulting net effect at an individual axon or cell body. According to this variability, DES even at primary projection cortices can evoke phosphenes (9, 10), involuntary movements (10, 11), or auditory sensations (10) consistent with the assumption of increased activity. However, it also can induce negative phenomena like deafness (10) or numbness (10, 11), suggesting disruption of activity at these sites.

Moreover, it is not clear whether behavioral effects always result from localized stimulation or also may represent remote effects due to direct stimulation of axons or transsynaptic spread of current. Using functional magnetic resonance imaging (fMRI) simultaneously with electrical microstimulation in monkeys’ primary visual cortex, Tolias et al. (12) found a larger spread of activity around the electrode’s tip than expected from calculations based on passive spread of current. Additionally, extrastriate projection sites were observed to be activated by local stimulation in V1 (12).

The uncertainty about local and distant effects of intraoperative DES allows for alternative interpretations of the behavioral results reported by Desmurget et al. (7). If we assume that DES at the IPL in their study did not activate, but rather inactivated, parietal cortex, the same empirical outcome would suggest that not the IPL but rather another (so far unknown) structure in the human brain generates movement intention and awareness. According to this account, inhibition of the IPL could have disinhibited this structure or this structure might have been directly activated through stimulation of axonal pathways. Also contrary to the functional interpretation of the effects of DES at the premotor cortex (PMC) (7), the application of DES at this site might have caused a lack of awareness by a direct inhibitory effect while overt movements were induced by distant activation of primary motor cortex. Alternatively, opposite changes in the activity of a structure receiving convergent projections from IPL and PMC due to DES at these input gates to the motor network might have caused the observed behavioral effects.

Although all these interpretations are as plausible as the one given by Desmurget et al. (7), the inference that can be drawn with absolute certainty from their interesting observations is that the IPL is part of a network used for generating movement intention. Whether or not these intentions are elicited by “increased parietal activity” as argued in (7), or by the inactivation of IPL, or by the activity or the disinhibition of another undescribed structure connected to the IPL, remains unclear. All of these models of human motor intention, including the one espoused by Desmurget et al. (7), thus should be kept under consideration until further experiments can decide among them.

Despite its eminent clinical value, the lack of certain knowledge about the true local and distant effects of DES thus limits its use for validation of cognitive models. Because other neuroscience techniques, such as fMRI in healthy subjects, lesion analyses in stroke patients, and transcranial magnetic stimulation, all have their own sets of strengths and weaknesses, the most promising approach to understanding human brain function seems to be the combination of their complementary contributions (13).

References and Notes

  1. This work was supported by the Deutsche Forschungsgemeinschaft (KA 1258/10-1), the Bundesministerium für Bildung und Forschung (BMBF-Verbund 01GW0641 “Räumliche Orientierung”), and the European Commission (ERC StG 211078). We are grateful to C. Rorden, Center for Advanced Brain Imaging Atlanta, as well as two anonymous referees for their insightful discussion and suggestions to improve the manuscript.
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