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The Feeling of Thinking: Sense of Agency in Delusions of Thought Insertion

Philip Gerrans

University of Adelaide The predictive coding model of motor control explains delusions of alien control in

terms of loss of a “sense of agency” for intentional action. In this paper I argue that the same model can explain delusions of thought insertion in terms of loss of a sense of agency for inner speech. The essential idea is that inner speech is a form of imaginary action. I explain how imaginary actions in general, and imaginary speech in particular, acquire and lose a sense of agency, and apply the model to the neuroscientific evidence from schizophrenia. I consider problems for the account deriving from the indirect connection between thought and language.

Keywords: predictive coding, sense of agency, language of thought, schizophrenia, delusions of thought insertion, inferior parietal lobule

The Feeling of Thinking

Action has a distinctive phenomenology: A “sense of agency” typically accompanies the intentional control of bodily movement. This sense of agency is subtle, evanescent, and hard to isolate, because it tends to be submerged in the buzzing, blooming confusion of everyday experience. Consequently, clinicians and re- searchers typically infer the nature of the sense of agency from pathological cases and experi- ments that produce an often profound attenua- tion or loss of this elusive sensation. In some conditions, for example, people report the ex- perience of passively performing actions; that is, controlling movements without feeling as though they are in fact in control. An example is an experiment in which schizophrenic subjects were asked to move a joystick and did so, which indicates that they explicitly intended the move- ment. However, the patients reported a sense of passivity; that is, not being the agent of the action ( Mlakar, Jensterle, & Frith ; Frith, 1994 ;

Spence et al., 1997 ). It is important to note that the experience here is not the same as the ex- perience of involuntary action (such as occurs in alien hand syndrome), but of performing an action without a sense of agency. These subjects suffered from delusions of alien control, a par- adigmatic schizophrenic delusion in which peo- ple report that they are performing actions con- trolled by someone else. In this paper, I assume that delusions of alien control result from loss of the sense of agency. My target, however, is a question raised by theoretical explanations of the sense of agency and its loss in pathological cases: Can there be a sense of agency for thought?

One reason for thinking that thought can be accompanied by a sense of agency comes from the delusion of thought insertion that also oc- curs in schizophrenia. In these delusions pa- tients report that they are experiencing another person’s thoughts. An oft-quoted example is the following: “The thoughts of Eamonn Andrews come into my mind. There are no other thoughts there, only his . . . He treats my mind like a screen and flashes his thoughts onto it like you flash a picture” ( Mellor, 1970 , p. 17). Perhaps this patient has lost the sense of agency for her thoughts in the same way that patients with delusions of alien control lose the sense of agency for action?

In the remainder of this article, I develop an account of the sense of agency for thoughts

Philip Gerrans, Department of Philosophy, University of Adelaide, Australia. Correspondence concerning this article should be ad- dressed to Philip Gerrans, Department of Philosophy, School of Humanities, Faculty of Arts, Room 13, Level 7, Napier Building, Adelaide University SA 5005, Australia. E-mail: philip.gerrans@adelaide.edu.au

Psychology of Consciousness: Theory, Research, and Practice © 2015 American Psychological Association 2015, Vol. 2, No. 3, 000

2326-5523/15/$12.00 http://dx.doi.org/10.1037/cns0000060

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using a version of the predictive coding theory of motor control that researchers have proposed to explain the sense of agency for actions ( Wol- pert, 1997 ; Hohwy, 2013 ; Clark, 2013). The basic idea of forward models is that actual sen- sory feedback from movements is compared with predicted feedback to control movement (see below for a full account). To apply this framework to thoughts, we need to reconceptu- alize thinking “as a motor process,” as John Campbell suggested ( Campbell, 1999 ). To do so, we need to think of the thoughts in question as linguistic, that is, as “inner speech” ( Lang- land-Hassan, 2008 ; Shergill et al., 2003 ; Jardri et al., 2009 ). The rationale for this framework is that speech production is a motor process. In this article, I am only concerned with the argu- ment that inner speech can be experienced pas- sively in the same way as bodily action, by virtue of their sharing the same neurocomputa- tional principles. Before concluding, I consider whether such an approach faithfully captures the nature of thought itself.

I argue that the best way to conceptualize inner speech is as imaginary speech (according to an account of imagination I outline below). This approach sidesteps a problem for action- based accounts that stems from the fact that, according to the predictive coding account, the sense of agency arises in the process of using sensory feedback to control movements. In the case of inner speech, however, there is no such feedback. When we speak audibly we can use auditory and bodily reafference (sensory feed- back consequent on self-initiated movement) to monitor and refine our speech (think of trying to learn a foreign language), but when we pontif- icate in foro interno our tongues and lips do not

move 1 and our words echo only in the chambers of our minds. However, an essential but slightly neglected aspect of the predictive coding theory of action both predicts and explains the evi- dence that imaginary actions are associated with

a sense of agency, despite the absence of feed- back. The strategy I adopt is to show, first, that imaginary actions involve a sense of agency, which, notably, becomes compromised in schizophrenia. Second, I suggest that inner speech is a form of imaginary action. Finally, I will argue that the neurocomputational evidence suggests that hyperactivity in the right inferior parietal lobule, associated with passively expe-

rienced speech, is best understood as a malfunc- tion in a system that monitors imaginary speech.

The Phenomenology of Imaginary Action

To understand how imaginary actions can generate a sense of agency, we need to detour slightly into a discussion of predictive coding and examine the nature of the actual mecha- nisms that implement predictive coding archi- tecture in the human brain.

The particular version of predictive coding used to explain delusions of control is repre- sented below in Figure 1 . The predictive coding framework generates a model cognitive archi- tecture for motor control, which is also repre- sented in Figure 1 (the forward model, as it is known).

Based on a cognitive model, or representation of the world, the brain calculates actions re- quired to achieve a particular goal (the inverse model; Wolpert, 1997 ; Kawato & Wolpert, 1998; Shadmehr, Smith, & Krakauer, 2010 ). Such actions are translated into motor com- mands, which are then translated into bodily movements, while the brain simultaneously models the predicted result of the movements (called the corollary discharge or efferent copy in models like the one below). The movements produce sensory feedback, which is matched to the predictive model. If there is a match, then the action has been successful, no further action is required, and the accuracy of the model is reinforced. If a mismatch occurs, the error sig- nal provides the basis for a new set of motor commands to fine-tune the movement, and the process iterates until there are no error signals. For example, if the prediction was that the hand should move 5 cm to reach a target but it actually moves 7 cm, an error signal will be generated and a new instruction to move 2 cm back toward the target will be issued to correct the error, and so on. According to this view, the mind is a device whose main purpose is to mitigate or eliminate prediction errors. Of note, the predictive coding system is hierarchical. Er- rors generated at one level are signaled to higher levels, which supervise the level below. Error signals and corrections propagate up and down the hierarchy. My intention to park the car, for

1 Actually there is sometimes some very attenuated overt vocal activity.

2 GERRANS

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THE FEELING OF THINKING

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minute adjustments of pressure on the steering type of control arises when an error signal is wheel and accelerator ( Patherie, 2000 ).

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almost instantaneously matched to a prediction.

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This matching process and any adjustments oc- cur instantaneously, and the relevant signals are

2 None of these theorists explain the phenomena in quite

never referred to higher levels of control.

the same way as I do here. My account is very close in spirit

According to the account presented here, the to that of Patherie, 2000 and Danckert ( Danckert et al., 2002 , 2004 ) who emphasized not just the bottom-up gener- sense of agency arises in the interaction be- ation of the sense of agency via activity in the rIPL, but the tween this essentially proprioceptive feedback crucial role of prefrontal structures. In this sense my account loop and another feedback loop for higher level, directly reflects the essential idea of predictive coding that explicit, visually guided control ( Patherie, what we experience is the consequence of a dynamic pro- 2000 ; Jeannerod, 2006 ; Lafargue & Sirigu, cess of top-down cancelation of surprisal (the technical term used in predictive coding theory to refer to an error signal

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2006 ; Jardri et al., 2009 ). 2 In this case, explicit generated by discrepancy between predicted and actual visual information is used to control movement feedback).

match between prediction and action but of the matching process itself under deliberate forms of control. As we engage prefrontal systems for attentively guided multichannel resolution of prediction error, activity in the relevant frontal parietal circuitry generates the experience of controlling an action. It is not error signals per se which generate the sense of agency (other- wise tripping or spilling drinks would generate it), but their availability for top-down regula- tion. On this account, slightly paradoxically, it seems that the sense of agency is more likely to arise in situations where the control of action is not automatically successful. In fact the appear- ance of paradox is misleading. We are more aware of our agency when learning a musical instrument, walking through a minefield, or threading a needle, than when successfully per- forming a routine task automatically; the latter tasks, being automated, are regulated at lower levels in the predictive coding hierarchy.

So far I have argued that the sense of agency for action arises in the process of higher level control of movement required for multisensory integration. In this context, multisensory inte- gration refers, for example, to the use of visual attention to regulate movements which, when automatically performed, are managed proprio- ceptively. To illustrate this, one might think of playing scales on a musical instrument automat- ically versus learning some difficult new finger- ing. In the latter case, we might look at the score and monitor the movements of our fingers and the keyboard, with successful performance de- pendent on the integration of visual and propri- oceptive feedback to cancel error signals.

The Right Inferior Parietal Cortex Implements a Comparator

Before turning to the case of imaginary action and imaginary speech, we need to substantiate this account of the relationship between higher and lower levels of control by describing the mechanisms involved and the way they gener- ate the sense of agency. The essential mecha- nism is the modulation of levels of activation in the right inferior parietal lobule by prefrontal systems ( Macaluso & Driver, 2005 ). The pari- etal cortex is a multisensory integration area and, in the context of actions, it integrates sen- sory feedback, functioning as a matching mech- anism when its activity is modulated by signals

from the motor cortex and higher level prefron- tal systems ( Blakemore et al., 2002 ; Danckert et al., 2004 ; Hohwy, 2013 ).

The mechanism for prediction is inhibition or attenuation of activity in right inferior parietal areas, consequent on signals from the motor cortex that produce the movement. In effect the motor cortex “tells” the inferior parietal cortex what proprioceptive information is coming as a consequence of the movement (“A corollary of the motor signal involved in intended effort, in the SMA, could be sent to attenuate parietal activity”, Lafargue & Franck, 2009 , p. 284). As

a result, incoming reafferent signals do not pro- duce as much activation as they would if the right parietal regions had not been preattenu- ated. This attenuation of activation implements the prediction of sensory reafference. If, how- ever, reafference is unpredicted, such as when an object is much heavier than predicted, or if grasp is imprecise, levels of activation in the inferior parietal lobule (IPL) rise, effectively functioning as a signal that reafference was not predicted. This signal propagates up the hierar- chy until higher level cognition is engaged in the form of visually guided control. Under these conditions prefrontal areas are active, instruct- ing the motor cortex to command new move- ments to correct the error. As the error is cor- rected, activity in the rIPL subsides ( Lafargue & Sirigu, 2006 ; Jardri et al., 2013). Note that the process of prediction via attenuation, matching and signaling of prediction error, and cancel- ation exploit the same basic architecture for both automatic and controlled movements. Here automatic movements involve rapid online can- celation of error using proprioceptive informa- tion, whereas higher level control requires at- tentively guided, top-down regulation of movement.

Thus the sense of agency arises in this pro- cess of modulating activity in the rIPL. This account predicts that loss of the sense of agency would arise when activity in the rIPL cannot be modulated. In effect, the movement could be launched but the error correction system would not function properly. Frith (1992) made a very telling observation about these cases when he noted that people with schizophrenia, although able to control their movements, seem unable to become aware of their initiation and control of those movements in contexts of attentive top- down control. Accordingly, he described their

4 GERRANS

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Evidence from both neurotypical and patho- logical cases suggests that the same mecha- nisms produce a sense of agency (and its loss in pathological cases) for imaginary actions. In neurotypical subjects, Fitts’s Law—the time re- quired to rapidly move to a target area is a function of the distance to the target and the size of the target—applies to actual and imaginary movements ( Danckert, Rossetti, d’Amato, Dal- ery, & Saoud, 2002 ). This finding provides fur- ther evidence that the sense of agency is gener- ated in the process of controlling action from “above,” because an imaginary movement is entirely under voluntary control. However, for people with positive schizophrenia symptoms, imaginary movements do not obey Fitts’s Law, which suggests that people with schizophrenia are not actually in control of the imaginary

movement once it is “launched.” 3 For them, the

imaginary movement is experienced as passive because they do not produce the typical pattern of parietal activation that accompanies high- level control ( Danckert et al., 2002 ).

This latter statement might appear to be a slight puzzle because we have argued that sense of agency involves the integration of sensory reafference. But there is no reafference to inte- grate in the case of imaginary action! However on closer examination the puzzle resolves. In fact, the lack of reafference in the context of trying to monitor an action produces an error signal in the form of sustained activation in the rIPL. This state of affairs is exemplified by some studies of deafferented patients by Lafar- gue and collaborators who have conducted an elegant set of experiments with hemiparetic pa- tients, asking them to compare or estimate the efforts involved in making and attempting ac- tions with paralyzed and nonparalyzed limbs. In the absence of feedback from the deafferented limbs, patients seem to rely on the phenomenol- ogy generated by the attempt to control the action ( Lafargue, D’Amico, Thobois, Brous- solle, & Sirigu, 2008 ; Lafargue & Franck, 2009 ; Lafargue & Sirigu, 2006 ). Similarly, a patient with no proprioceptive feedback has the capac-

ity to become aware of her efforts to produce actions ( Lafargue, Paillard, Lamarre, & Sirigu, 2003 ). Together, these cases suggest that the sense of agency is a form of awareness of ac- tivity in predictive coding systems consequent on motor instructions, generated in the process of trying to modulate the error signaled by un- predicted activity in the rIPL. Imaging, lesion, and TMS studies implicate the rIPL in the sense of agency and its loss in cases of damage or dysfunction ( Ganesan, Hunter, & Spence, 2005 , 1984; MacDonald & Paus, 2003 ; Sirigu et al., 2003 ). Lafargue and Franck (2009 , p. 84) sum- marized evidence from lesion and imaging stud- ies of motor control and their relevance to the loss of sense of agency in schizophrenia as follows: “A corollary of the motor signal in- volved in intended effort, in the SMA, could be sent to attenuate parietal activity due to propri- oceptive feedback during active and so effortful movements. The balance between both phe- nomena might be abnormal in schizophrenia.”

One way to interpret these cases of deaffer- ented action is to say that what is happening is that the patients are actually imagining per- forming actions. As with imagined movements, all the neural activity prior to execution or trans- lation into overt action is occurring, but there is no feedback because the action is not performed ( Decety & Lindgren, 1991 ; Jeannerod & Frak, 1999 ). In imaginary cases, motor output is sup- pressed and there is no sensory reafference. As Jeannerod (2006) explains, the action is entirely covert . Yet there is a sense of agency because there is no feedback to modulate activity in the rIPL, which serves as the comparator.

To summarize: When we imagine performing an action there is no bodily feedback, yet there is a sense of agency, which waxes and wanes as we control the imaginary action, more or less successfully. This sense of agency for imagi- nary action can be explained in terms of the lack of cancelation of surprisal. When we imagine a movement we attenuate the rIPL in the same way as when we perform an actual movement. But in the imaginary case no reafference is produced because motor output is suppressed,

3 I realize that this is not decisive evidence for my ac- count. There may be other neurocognitive issues involved in

schizophrenia that could also explain this phenomenon. I mention it as evidence in favor.

THE FEELING OF THINKING 5

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as exemplified in hemiparetic patients who can- not produce or sense movement.

Jeannerod (2006) summarizes the idea as fol- lows.

If motor preparation, which normally lasts for a very brief period of time, could be prolonged, the intention to act would become progressively a motor image of the same action . If this were the case, then the non- conscious to conscious transition would be only deter- mined by the time allowed for the preparation process to access awareness and to become conscious. Actions which fail or which are canceled at the last moment may be situations where a nonconscious program is transformed into a conscious image ( Jeannerod, 2006 , p. 190).

The transition is not so much from conscious to nonconscious because action preparation and initiation is not intrinsically unconscious. Rather Jeannerod (2006) is describing the way in which a sense of agency is generated when feedback is either unpredicted or absent. This absence of predicted sensory feedback is com- mon to imaginary action and the attempts of deafferented patients ( Saoud et al., 2000 ; Danckert et al., 2002 ) and explains why a sense of agency arises in both cases.

To summarize: The account of the sense of agency for imaginary action proposed here in- volves the following elements. The relevant in- tention is translated into a motor instruction that activates all the covert components of the action control system. However, because actual overt movement is inhibited, there is no translation of these instructions into movement, and the action remains covert, not overt. An important feature of the covert system is the prediction of feed- back produced by attenuation of activity in the rIPL. However, because there is no propriocep- tive reafference to modulate activity in the rIPL, its level of activation increases, signaling an error. Attention is captured and higher level cognitive resources are recruited, which is ex- perienced as the sense of agency for imaginary action. This sense of agency is of course elu- sive, context-sensitive, and difficult to parse phenomenologically. In the normal course of things, action produces all sorts of sensory feed- back in which the fleeting sense of agency can

be quickly submerged, which is why patholog- ical cases are so important in helping to describe

a subtle and evanescent phenomenology. This account predicts that damage or dysfunction in the rIPL would impair a sense of agency for

imaginary action in the same way it impairs it for actual actions, which is, in fact, the case.

Inner Speech Is Imaginary Action

We now turn to the case of inner speech. In essence it is covert speech, as indicated by the common term subvocalization. In inner speech, the mechanisms of speech production are acti- vated, but output or translation into overt action is inhibited. The motor instruction to produce a phoneme should produce a corollary discharge that attenuates activity in areas that process feedback consequent to speech production ( Ford & Mathalon, 2004 ; Ford & Mathalon, 2005 ; Ford, Roach, Faustman, & Mathalon, 2007 ; Allen, Aleman, & McGuire, 2007 ; Jones & Fernyhough 2007a ). However, because the overt component of speech is inhibited, there is no sensory reafference. In such a case we would predict that inner speech, like imaginary action, should produce a sense of agency, as activity in predictive circuitry is not modulated by feed- back.

Just as people with schizophrenia are poor at monitoring imaginary actions, perhaps they are also poor monitors of inner speech, precisely because inner speech is a form of imaginary

action. 4 If this hypothesis is the correct expla- nation of delusions of thought insertion, then we would expect to see abnormal activity in brain areas that monitor covert speech.

A complicating factor, however, is the diffi- culty in distinguishing auditory verbal halluci- nation (AVH) or “hearing voices” from “in- serted thoughts.” The concept of auditory hallucination covers a range of cases (see Wilkinson, 2014 for a discussion). The intuitive concept of auditory hallucination refers to an experience of external auditory perception in the absence of an external auditory source. However, some AVHs are not experienced as external in origin, or even especially auditory. Such cases may resemble the phenomenology

4 Equating inner speech with imaginary action limits the type of imagination involved to that described by Jean-

nerod, 2006 : the covert rehearsal of an action without an overt component. Clearly, imagination is a more complex phenomenon than this description suggests. For a full dis- cussion of the nature of imagination, its different categories, and their relationship to the cases under discussion, see Gerrans and Mulligan (2013) and Chap. 7 of Gerrans (2014) .

6 GERRANS

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However, in an interesting imaging study, Jardri et al. (2009) made progress on differen- tiating AVH and delusions of thought insertion. Their subject was an 11-year-old boy (YP) with AVH, delusions of alien control and thought insertion. The researchers identified distinct brain regions involved in delusions of thought insertions and the generation of AVH, respec- tively. Their experiment contrasted the re- sponses of controls (four healthy adults) and the patient YP in two conditions. In one condition, the patient listened to a short passage of speech read either by himself (“self” condition) or someone else (“other” condition). When YP read the passage, he was asked to subvocalize the words. When read by another person, YP was instructed to listen passively. Controls showed an increase in activity in the right IPL for the “other” condition and a reduction in activity for the “self” condition. YP, in contrast, showed similarly high levels of activity in the right IPL in both conditions and no reduction for the “self” condition. It appears that the high baseline level of activity in the IPLs was not modulated by self-initiation of inner speech (subvocalization).

However, after the 10 sessions of low-frequency rTMS (transcranial magnetic stimulation, which inhibits ac- tivity in the target area) over the right IPL (t1), a significant positive activation of activity in right IPL (for the “other” condition) was observed in YP and this difference was similar to that observed in the control group ( Jardri et al., 2009 , p. 135).

In other words, when the baseline level of activity in the right IPL was attenuated, YP’s pattern of response more closely resembled that of the controls; that is, a spike in the “other” condition occurred.

Jardri and collaborators (2009) noted that this pattern is consistent with the findings of Jean- nerod (2006) , Blakemore et al., 2002 , and others discussed above—(a) that a loss of sense of agency is associated with high baseline levels of activity in rIPL, and (b) that these high baseline levels seem to prevent the rIPL from playing its

role of representing prediction error for in- tended actions. They also noted that although rTMS over the rIPL reduced the delusions of thought insertion, it did not reduce AVH. Hence, they cautiously concluded that (a) AVH and delusions of agency are dissociable phe- nomena with differentiable neural substrates (though, as they point out, there may be com- plex overlaps of neural substrates) and (b) faulty monitoring of inner speech is an instance of a problem with agency rather than audition.

Although the nature of inner speech and its relation to inserted thought remains controver- sial, some evidence supports the approach taken here. Namely, episodes of inner speech are “in- ner vocal actions” monitored by a circuit that includes the rIPL.

But Is Thought Speech?

If this account is accurate, then we can see how we might lose a sense of agency for our own thoughts. Still, a potential limitation of identifying inner speech with thoughts is that although this account explains loss of a sense of agency for inner speech, according to most views of thought, speech is not thought! The process of thinking is the process of moving from one thought to another, which involves association, deduction, induction, analogical reasoning, imagery, pattern completion, and so on. Although speaking might express the out- come of these processes, it represents the man- ifestation of a different cognitive process. Speech, including inner speech, expresses thoughts, but it is not thought itself.

Nevertheless, this may not be a decisive ob- jection to treating delusions of thought insertion as inner speech, as there is an intimate connec- tion between thought and language. In some views, natural language is a medium of thought ( Carruthers, 2002 ); in other views, language plays a coordinating and indexing role, keeping track of thoughts while they are manipulated. Inner speech might be an important thinking tool ( Vygotsky, 1978 ; Vygotsky, 1986 ; Jones & Fernyhough, 2007a ; Jones & Fernyhough, 2007b ). The view that thought itself is nonlin- guistic is consistent with the idea that we often experience the outcome of thought processes as episodes of inner speech. Not only that, but we often initiate thought via inner speech. Perhaps inputs and outputs to thinking are encoded lin-

THE FEELING OF THINKING 7

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8 GERRANS

guistically, even if thinking is not. Thus, tions.” In the case of inner speech, the loss of thoughts are intimately connected with inner the sense of agency for subvocalization is ex- speech, and many of the outputs of thought pressed as the delusion of thought insertion: processes are experienced as inner speech. It is “Someone else is thinking via my mind”. This this class (and I suspect only this class) of account does not explain why the experience is mental states that are candidates for explanation expressed in terms of externality rather than using the forward model.

passivity. That is to say, it only explains the loss of sense of agency, rather than the delusional

Conclusion

attribution of agency to an external source.

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Inner speech is a form of imaginary action.

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