Did you do that?

Limited only perhaps by my emotional fortitude and physical abilities, I am unquestionably in control of myself. This sense is perhaps drawn most into question first thing in the morning when I play both sides of an internal civil war: on one side, my bed, on the other, the cold cruel world. Both sides battle it out until my sense of duty eventually overwhelms my preference for comfort. This internal battle reveals, at least to me, that what gives rise to my actions and thoughts is not the fluid expression of a singular me, but a noisier emergence of multiple players. In these moments, I find myself wondering how my ownership over my actions arises.

A thought experiment was posed by the 20th century philosopher Ludwig Wittgenstein, who posed

…what is left over if I subtract the fact that my arm goes up from the fact that I raise my arm?

 

Another way of phrasing this might be, what distinguishes the mere occurrence of an event from the action of an individual? One possible answer, proposed by British Neuroscientist Patrick Haggard, is a sense of agency [1].

 

My sense of agency over my actions is something I hadn’t given much consideration to until I discovered that it is something that can be studied, quantified, and in certain cases, lost. Our sense of agency has important implications in law (one can not be guilty if the mind is innocent), medicine (individuals suffering from depression and schizophrenia often exhibit reduced senses of agency), and even our understanding of free will.

 

Measuring Will

Some pioneering work on what gives rise to a sense of agency came in the 80s from the work of American Neuroscientist Benjamin Libet. Libet’s famous experiment (which is described in more detail here) showed what brain activity looked like preceding an unprompted, free, movement (in this case a flex of the wrist) [2]. The study replicated a previous finding [3] whereby a voltage recorded over the primary motor cortex, termed the Readiness Potential, showed a consistent deflection preceding movement by over 500 ms. Intriguingly, the Readiness Potential also preceded the subjects self-reported conscious urge to move by over 300 ms. The implication here is that our will or urge to complete actions may arise from an unconscious process that is blind to our central consciousness.

 

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Schematic of Libet’s experiment. Participants press a button ‘when they feel like it’ and note where on the clock the first felt the urge to do so. Brain activity consistently precedes the time of first conscious urge [4].

Timing as a measure of agency

The timing of events and the perception of their timing are important pieces to the agency puzzle. This in part relates to the concept of causality. An event can only be caused by an event that occured before it. A simple thought experiment puts you in a dark room with many switches and only one light bulb. As you feel around for a switch the others in your group do the same. At last you find a panel, but just before you flip the switch, the light comes on. In this case, the action of you flipping the switch occurred after the light turned on, and so you should feel no sense of agency in turning on the light. If, on the contrary, the light comes on immediately after you flip a switch you will feel, rightfully, that it was your action that vanquished the darkness. Extending the analogy, if the light flickers on a second or so after you flip the switch you might feel an intermediate sense of agency as it’s not clear if there was a delay in the circuit or if someone else found the correct switch just after you.

The importance of timing in ascribing agency was first catalogued Haggard and colleagues and was termed Intentional Binding [5]. Haggard found that when a subject felt their action (pushing a button) caused a reaction (a tone) that they reported the two events as occurring closer together in time then if the two events were independent (randomly timed tone). Importantly, it was shown that this effect vanished when the action was triggered by exogenous stimulation of the motor cortex, meaning Intentional Binding was driven by an individual’s intentions and not just their physical actions. This temporal binding is consistent with our conception of the timing of causal events. Perhaps our brains somehow encode causality into our perception of events by binding them closer together in time.  In a follow up study, Haggard et al. also demonstrated that when the effect of a causal process was further delayed, the binding effect was reduced, implying the subjects were ascribing less ownership or agency to the pairing [7].

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More delayed effects trigger less intentional binding and therefore less sense of agency (Figure from [7]).

Prospective vs. Retrospective Agency

So my sense of agency may the product of subconscious processes that may be inextricably linked to our perception of the timing of events. I still don’t have a great sense of what gives rise to my sense of agency from a mechanistic level though. There are two competing theories here, one of prospective agency, attributing ownership based on our plan of an action, and another of retrospective agency, attributing ownership only upon observing an effect of our action. In the prospective case, we make a plan and then execute it, like walking up and kicking a ball. In the retrospective case, we complete an action and then explain it, like starting a sentence without an end in mind but having it come together anyways.

Support for the prospective attribution of agency comes from the childhood quandary of “why can’t I tickle myself?” One popular theory is that since you are completing the action, your brain should be able to predict the sensation on say, your armpit, and suppresses the redundant sensorimotor signal. Indeed, it has been shown that brain activity correlated with sensory perception is reduced when an individual tickles themselves vs. when a robot arm applies the same stimulation  [8]. Further, when subjects were given control of a robot arm, their level of ticklishness increased as the latency between their control and the robots movement increased [12].  Our brains are constantly predicting the outcomes of our thoughts and actions, and the closer the prediction aligns with the outcome, the greater our sense of agency.

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Robotic tickling machine utilized in [12]. The greater the latency or variability from the subjects control and the robots movement, the greater the ticklishness.

Some individuals with schizophrenia report that someone else is controlling their thoughts and actions and that they feel a limited sense of agency. These same individuals also demonstrate the ability to tickle themselves [9]. If my inability to tickle myself is linked to my innate ability to predict the outcome of my actions, than it would follow that schizophrenia might somehow impair these predictions. Work out of Haggard’s lab in 2010 showed just this, with schizophrenic patients exhibiting no intentional binding for a predicted response that didn’t come, unlike healthy controls  [10]. This would provide support for the prospective model of agency where it is our execution of a planned action that gives rise to action ownership

 

Did you do that?

Retrospective agency is by construction a little backwards. It is your brain’s equivalent of political grandstanding, taking credit for anything good that happens after the fact. To put this method into perspective, think of any non-skilled action you complete throughout the day, be it spreading some peanut butter, tying your shoes, or peddling your bike. I personally can’t recall an instance where I intended to do something but my body just up and did something different. I may make a mistake, getting peanut butter on the counter for instance, but my hands moved in good faith to complete the action I set out to do. Assuming the prospective model, that my actions are dictated by my inner self, shouldn’t I expect the occasional miscommunication? Since I observe a perfect correlation between my intention and my actions, a much easier interpretation arises whereby my inner self is actually observing my actions (my perception of them) and imposing ownership over them after the fact (even if only a few milliseconds).

Some compelling work that suggested this came from Libet in a experiment exploring subjective experience [11]. Patients undergoing neurosurgical procedures were stimulated in a regions of the cortex that triggered sensations in various body parts. Once a region was located that elicited a sensation in one hand, external stimulation was applied to the other. It was found that the subjects felt the two stimulations were simultaneous when stimulation was applied to the hand 500 ms after stimulation directly to the cortex. This would imply that the brain is experiencing the stimulation ~500 ms before it occurs. While at first this seems backwards, one should consider that there is a transmission delay between our senses receiving inputs and them being effectively communicated to our relevant higher brain areas. Adding on the fact that many of our sensory pathways process inputs at vastly different speeds, it actually becomes intuitive that our brain might be purposely manipulating our perception of when things happen [7].

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Schematic for Libet’s cortical stimulation experiment [7]. Stimulating the hand 500 ms after stimulating a related somatosensory cortical region resulted in simultaneous experience. [image: http://www.blutner.de/philom/consc/consc.html%5D

So the question remains, which one is it? Are we predictive beings ascribing ownership over the actions which we planned or pragmatic individuals laying claim to the events that seem most probable. A clever variation of the original Intentional Binding experiment set out to distinguish the two possibilities [6]. Individuals were again instructed to push a button “when they felt like it” under the condition that their button press would possibly lead to a tone. In one set of experiments, a tone followed the button press 75% of the time while in another experiment a tone followed only 50% of presses.

To explore the role prospective agency, Haggard et al. looked at trials without a subsequent tone and found that when subjects were most expecting a tone (75%) there was greater Intentional Binding, suggesting that the prediction of the tone was important (green line). With the same set of subjects to explore the role of retrospective agency, they looked at trials with and without a subsequent tone when they had equal probability and found that the presence of the tone alone increased Intentional Binding as well (blue line). Together, these results suggest that in healthy individuals a sense of agency might arise as a combination of prospective and retrospective mechanisms.

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The level of intentional binding on trials without a tone (action only) is much greater when the tone is more probable (green line), supporting the prospective model of agency. The level of intentional binding is greater when the tone does occur then when it doesn’t (blue line), supporting the retrospective model of agency. (Figure adapted from [6])

All together, it feels like we don’t have a super cohesive explanation for how our sense of agency arises. This may be a product of how noisy a process it actually is. It seems to arise from a partially unconscious process and may be driven by factors both before and after we complete a given action. Some open questions remain, most pertinent is what, if anything, can I do to increase my sense of agency. Is it like a muscle that can fatigue but also be strengthened with repeated use? For the time being, my morning battle will likely continue with my sense of agency becoming apparent only after I extract myself from bed.

 

Citations

[1] Haggard, P.  Sense of agency in the human brain. Nature Reviews Neuroscience 18, 197-208 (2017).

[2] Libet, B., Gleason, C. A., Wright, E. W. & Pearl, D. K. Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. Brain 106, 623–642 (1983).

[3] Deecke, L., Grozinger, B., Kornhuber, H. H. Voluntary Finger Movement in Man: Cerebral Potentials and Theory. Biological Cybernetics 23, 99-119 (1976).

[4] Haggard, P. Human volition:towards a neuroscience of will. Nature Reviews Neuroscience 9 934-946 (2008)

[5] Haggard, P., Clark S., Kalogeras, J. Voluntary action and conscious awareness. Nature Neuroscience 5/4 382-385 (2002).

[6] Moore, J. & Haggard, P. Awareness of action: Inference and prediction. Consciousness and Cognition 17, 136–144 (2008).

[7] Eagleman, David M., Holcombe, Alex O. Causality and the perception of time. Trends in Cognitive Sciences 6/8, 323-324 (2002).

[8] Blakemore, S. Wolpert, D. Frith, C. Why can’t you tickle yourself? Neuroreport Review 11/11, R11-15 (2000).

[9] Blakemore, S. et al. The perception of self-produced sensory stimuli in patients with auditory hallucinations and passivity experiences: evidence for a breakdown in self-monitoring. Psychological Medicine 30, 1131–1139 (2000).

[10] Voss, M. et al. Altered awareness of action in schizophrenia: a specific deficit in predicting action consequences. Brain 133, 3104–3112 (2010).

[11]  Libet B. Brain stimulation in the study of neuronal functions for conscious sensory experiences. Human Neurobiology 1, 235–242 (1982).

[12] Blakemore, S., Frith, C., Wolpert, M. Spatio-Temporal Prediction Modulates the Perception of Self-Produced Stimuli. Journal of Cognitive Science 11/5 551-559

 

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