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Explaining the symptoms of schizophrenia: Abnormalities in the awareness of action

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Abstract

We propose that the primary cognitive deficit associated with delusions of control is a lack of awareness of certain aspects of motor control. This problem arises because of a failure in the mechanism by which the predicted consequences of an action are derived from a forward model based on the intended sequence of motor commands. This problem leads to a number of behavioural consequences, such as a lack of central error correction, many of which have been observed in patients with delusions of control and related symptoms. At the physiological level, delusions of control are associated with over-activity in parietal cortex. We suggest that this over-activity results from a failure to attenuate responses to sensations of limb movements even though these sensations can be anticipated on the basis of the movements intended. The lack of attenuation may arise from long range cortico-cortical disconnections which prevent inhibitory signals arising in the frontal areas which generate motor commands from reaching the appropriate sensory areas.

Section snippets

Contrasting delusions of control and the anarchic hand sign

Rather than attempting to elucidate a biological basis for schizophrenia, our aim in this essay is to try and explain one symptom or class of symptoms. We shall concentrate on delusions of control. This is an example of a passivity experience in which a patient feels that his own actions are being created, not by himself, but by some outside force. The actions in question can be very trivial, such as picking up a cup or combing one's hair. Other examples of passivity include thoughts or

Explaining symptoms in cognitive, physiological and experiential terms

In order to understand symptoms like delusions of control we require an explanation at least three levels. First, at the cognitive level, we must understand how the symptom arises in terms of a model of motor control that can be applied to normal and abnormal cases and which makes a distinction between those aspects of motor control which reach awareness and those which do not. Second, at the physiological level we need to consider how the cognitive components of the model relate to underlying

Control of action and awareness of action

The motor system can be considered a control system in which the input is the motor command that produces a movement and the output is the sensory consequence of that movement (see Fig. 1). In order to produce a goal-directed movement the system must be able to estimate its current state (e.g. the current position of a limb) and must also represent its goal (e.g. the desired position of the limb). On the basis of these two representations the system can compute a sequence of motor commands that

The cognitive basis of the anarchic hand sign

In a patient with the anarchic hand sign the movements of the hand are no longer determined by the goals of the patient, but solely by the current context. The appearance of a door knob in the patient's line of vision is sufficient to elicit a reaching and grasping movement. Such movements are normally inhibited because they are incompatible with current goals. These inhibitory signals are no longer transmitted to the cortical regions controlling the movement of the hand because of damage to

The cognitive basis of delusions of control

In the patient with delusions of control something is wrong with that part of the motor system concerned with the generation of a forward model and the representation of the predicted state of the system. Since the rest of the system remains intact, the patient can represent the desired state, can calculate and carry out the motor commands required to achieve the desired state, and can check that the desired state has been reached (see Fig. 2).

However, in the absence of an awareness of the

Behavioural evidence

The anarchic hand sign is directly observable. The behaviour of the anarchic hand can be studied, as can the strategies adopted by the patient to cope with this aberrant behaviour. This is not the case with delusions of control. There is nothing obviously abnormal about the patient's actions. It is only from the patient's report of his anomalous experiences that we know that there is something wrong with the motor system. A major advantage of specifying the disorder in cognitive terms is that

The physiological under pinnings of motor control

At present we have only a very crude idea of how the motor control system illustrated in Fig. 1 can be mapped onto the central nervous system. Most of this knowledge comes from the study of neurological patients with circumscribed lesions. From such studies we know that prefrontal cortex has a major role in the formulation of goals and plans, see e.g. 20, 30, and that medial premotor cortex (supplementary motor cortex, SMA) has a role in developing appropriate sequences of motor commands and

Physiological abnormalities associated with delusions of control

If patients with delusions of control fail to predict the sensory consequences of their actions, then, at the physiological level, we would expect to see over-activity in regions concerned with analysis of the relevant sensations. Spence et al. [31]scanned patients with delusions of control while they performed a simple motor task in which they were required to move a joy stick in one of four directions, chosen at random, in time with a pacing tone. In comparison to a control task involving

Understanding delusions of control

At the cognitive level we suggest that delusions of control arise because of a failure to form a representation of the predicted consequences of an action. In addition to an abnormal experience of the control of movements this leads to measurable behavioural consequences in tasks involving mental practice, error correction and memory for actions.

At the physiological level we suggest that delusions of control arise because of a disconnection between frontal brain regions where actions are

Acknowledgements

This work was supported by the Wellcome Trust. S.-J. Blakemore is supported by a Wellcome Trust four-year PhD programme in neuroscience at University College London.

References (40)

  • J Decety et al.

    Mapping motor representations with PET

    Nature

    (1994)
  • R.J Dolan et al.

    Dopaminergic modulation of impaired cognitive activation in the anterior cingulate cortex in schizophrenia

    Nature

    (1995)
  • K.P. Ebmeier, Brain imaging and schizophrenia, in: J.A. Den Boer, H.G.M. Westenberg, H.M. van Praag (Eds.), Advances in...
  • D.L Feltz et al.

    The effects of mental practice on motor skill learning and performance. A meta-analysis

    J. Sport Psychol.

    (1983)
  • C.D Frith et al.

    Experiences of alien control in schizophrenia reflect a disorder in the central monitoring of action

    Psychol. Med.

    (1989)
  • C.D Frith et al.

    Regional brain activity in chronic schizophrenic patients during the performance of a verbal fluency task

    Br. J. Psychiatry

    (1995)
  • A.M Gordan et al.

    Memory representations underlying motor commands used during manipulation of common and novel objects

    J. Neurophysiol.

    (1993)
  • P. Haggard, M. Eimer, On the relation between brain potentials and awareness of voluntary movements, Exp. Brain Res.,...
  • M Jeannerod

    The Representing Brain — Neural correlates of motor intention and imagery

    Behav. Brain Sci.

    (1994)
  • M.I. Jordan, Computational aspects of motor control and motor learning, in: E.H. Heuer, E.S. Keele (Eds.), Handbook of...
  • Cited by (0)

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