It Wasn't Me, It Was Someone Else: Agency Error and Alien Hand

A sense of agency is the feeling that you're initiating and controlling your own movements. This can go awry in schizophrenia, when individuals can experience delusions of control (Lafargue & Franck, 2009). In this state, the patient feels as if external forces are performing actions against his will. Loss of agency also occurs in alien hand syndrome, a rare and unusual neurological disorder in which the affected patient loses volitional control of one hand, which develops "a mind of its own."

A recent fMRI study looked at the pattern of neural activation associated with a sense of agency in normal participants (Yomogida et al., 2009). To do this, they used a "violation-of-visual-feedback paradigm" as shown below in Fig. 1. Subjects played a video game in which they controlled the movement of a character using a joystick. In the control condition, audio feedback was provided when they hit one of the targets (tomato - "squish" or balloon - "pop"). In the agency violation condition, the computer program moved the character in a different direction than the subject intended. In the sensory-matching violation condition, either the wrong feedback sound was presented, or the correct feedback was presented at the wrong time. A separate "oddball" task did not involve a motor response but controlled for the infrequent occurrence of the violation conditions.


Fig. 1 (Yomogida et al., 2009). Task paradigm of the agency and SM error task. On each trial, a target (red object) was presented in one of four locations on a screen. Subjects were asked to hit the target by controlling the character using a joystick. Three conditions were possible: control (C), agency violation (AGv), and sensory-matching violation (SMv).

To determine the regions of activation related to agency violation, the AGv - SMv subtraction was performed. Significant activations were found in bilateral supplementary motor area (SMA), left lateral cerebellum, right posterior parietal cortex, and right lateral occipito-temporal cortex (in the vicinity of the extrastriate body area; see Downing et al., 2001).


Adapted from Fig. 3 (Yomogida et al., 2009). Left: Activation areas specific to agency error. Right: Representative examples of activation profiles for control (C), sensory-matching violation (SMv), and agency violation (AGv) conditions. SMA: supplementary motor area, Cbll: left lateral cerebellum, rt. IPL: right inferior parietal lobule.

A region of particular interest for alien hand syndrome is the SMA, which is involved in the planning, initiation, and inhibition of motor responses. An older paper by Feinberg et al. (1992) identified two alien hand syndromes. One of these is associated with damage to the anterior corpus callosum, as happens in the classic "split brain" operation to sever the white matter connections between the two cerebral hemispheres (undertaken for seizure control). The more "alien" (or anarchic) of the syndromes involves damage to dorsomedial frontal cortex, including the SMA and the anterior cingulate.

However, note in Fig. 3 above that the "activation" in SMA is actually manifest as a smaller reduction in activity for agency errors compared to sensory matching errors. What does this mean? The authors don't say.

Activation of the cerebellum was linked to cerebellar abnormalities in schizophrenic patients who experience delusions of control. In contrast, the authors discounted the importance of occipito-temporal and posterior parietal regions for a sense of agency, since there was some increased activity in these areas for oddball errors, as well as agency errors. But in a recent brain stimulation study, Desmurget and colleagues (2009) implicated posterior parietal cortex in the intention to move:

Stimulating the right inferior parietal regions triggered a strong intention and desire to move the contralateral hand, arm, or foot, whereas stimulating the left inferior parietal region provoked the intention to move the lips and to talk. When stimulation intensity was increased in parietal areas, participants believed they had really performed these movements, although no electromyographic activity was detected. Stimulation of the premotor region [which did not include SMA] triggered overt mouth and contralateral limb movements. Yet, patients firmly denied that they had moved. Conscious intention and motor awareness thus arise from increased parietal activity before movement execution.

From The Learning Channel - credits



Here's a documentary about alien hand syndrome and the brain, circa 1993 (or maybe 1996). You'll have to sit through the melodramatic narration, the overwrought music, and the cheesy reenactments to watch interviews with afflicted patients and with Todd E. Feinberg, Joe Bogen, and Eran Zaidel.

You can read more about alien hand and willed actions in these blog posts:

In search of the conscious will

Electrical stimulation produces feelings of free will

The alien hand syndrome - caught on video

References

Desmurget M, Reilly K, Richard N, Szathmari A, Mottolese C, Sirigu A. (2009). Movement intention after parietal cortex stimulation in humans. Science 324:811-813.

Downing PE, Jiang Y, Shuman M, Kanwisher N. (2001). A cortical area selective for visual processing of the human body. Science 293:2470-3.

Feinberg TE, Schindler RJ, Flanagan NG, Haber LD. (1992). Two alien hand syndromes. Neurology 42:19-24. [PDF]

Lafargue G, Franck N. (2009). Effort awareness and sense of volition in schizophrenia. Conscious Cogn. 18:277-89.



Yomogida, Y., Sugiura, M., Sassa, Y., Wakusawa, K., Sekiguchi, A., Fukushima, A., Takeuchi, H., Horie, K., Sato, S., & Kawashima, R. (2009). The neural basis of agency: An fMRI study. NeuroImage DOI: 10.1016/j.neuroimage.2009.12.054