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Specifying the Self for Cognitive Neuroscience

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Specifying the Self for Cognitive Neuroscience Opinion Specifying the self for cognitive neuroscience Kalina Christoff1, Diego Cosmelli2, Dorothe´ e Legrand3 and Evan Thompson4 1 Department of Psychology, University of British Columbia, 2136 West Mall, Vancouver, BC, V6T 1Z4 Canada 2 Escuela de Psicologı´a, Pontificia Universidad Cato´ lica de Chile, Av. Vicun˜ a Mackenna 4860, Macul, Santiago, Chile 3 Centre de Recherche en Episte´ mologie Applique´ (CREA), ENSTA-32, boulevard Victor, 75015 Paris, cedex 15, France 4 Department of Philosophy, University of Toronto, 170 St George Street, Toronto, ON, M5R 2M8 Canada Cognitive neuroscience investigations of self-experience processing [4,7–10], might not be self-specific, because they have mainly focused on the mental attribution of fea- are also recruited for a wide range of other cognitive tures to the self (self-related processing). In this paper, processes – recall of information from memory, inferential we highlight another fundamental, yet neglected, aspect reasoning, and representing others’ mental states [3,5,6]. of self-experience, that of being an agent. We propose In addition, the PCC appears to be engaged in attentional that this aspect of self-experience depends on self-spec- processes and might be a hub for attention and motivation ifying processes, ones that implicitly specify the self by [11,12], whereas the TPJ is important for attentional implementing a functional self/non-self distinction in reorienting [13]. Hence, describing these regions (singly perception, action, cognition and emotion. We describe or collectively) as self-specific could be unwarranted [3,5,6]. two paradigmatic cases – sensorimotor integration and Second, studies employing self-related processing ap- homeostatic regulation – and use the principles from proach self-experience through the self-attribution of men- these cases to show how cognitive control, including tal and physical features, and thereby focus on the self as emotion regulation, is also self-specifying. We argue that an object of attribution and not the self as the knowing externally directed, attention-demanding tasks, rather subject and agent. To invoke James’ [14] classic distinction, than suppressing self-experience, give rise to the self- this paradigm targets the ‘Me’ – the self as known through experience of being a cognitive–affective agent. We con- its physical and mental attributes – and not the ‘I’ – the self clude with directions for experimental work based on as subjective knower and agent. Thus, relying exclusively our framework. on this paradigm would limit the cognitive neuroscience of self-experience to self-related processing (the ‘Me’), to the neglect of the self-experience of being a knower and agent Investigating self-experience in cognitive neuroscience (the ‘I’) [6,15]. How does the embodied brain give rise to self-experience? In this paper, we focus on the ‘I’ – experiencing oneself as This question, long addressed by neurology [1] and neuro- the agent of perception, action, cognition and emotion – and physiology [2], now attracts strong interest from cognitive neuroscience and the neuroimaging community [3–6]. Glossary Recent neuroimaging studies have investigated self- Cognitive control: the process by which one focuses and sustains attention on experience mainly by employing paradigms that contrast task-relevant information and selects task-relevant behavior. self-related with non-self-related stimuli and tasks. Such Emotion regulation: the process by which one influences one’s experience and expression of emotion. paradigms aim to reveal the cerebral correlates of ‘self- Homeostatic regulation: the process of keeping vital organismic parameters related processing’ (see Glossary). Recent reviews identify within a given dynamical range despite external or internal perturbations. several brain regions that appear most consistently acti- ‘I’ versus ‘Me’: experiencing oneself as subjective knower and agent versus experiencing oneself as an object of perception or self-attribution. vated in self-related paradigms such as assessing one’s Self-related processing: processing requiring one to evaluate or judge some personality, physical appearance or feelings; recognizing feature in relation to one’s perceptual image or mental concept of oneself. Self-specific: a component or feature that is exclusive (characterizes oneself one’s face; or detecting one’s first name (see [4,6] for and no one else) and noncontingent (changing or losing it entails changing or extensive reviews). The medial prefrontal cortex (mPFC) losing the distinction between self and non-self). and the precuneus/posterior cingulate cortex (Precuneus/ Self-specifying: any process that specifies the self as subject and agent by implementing a functional self/non-self distinction. PCC) are the most frequently discussed [4–10], but two Sensorimotor integration: the mechanisms by which sensory information is additional regions, the temporoparietal junction (TPJ) and processed to guide motor acts, and by which motor acts are guided to facilitate temporal pole, are also consistently activated [6]. sensory processing. Task-negative/default-network brain regions: regions exhibiting sustained Although these studies have contributed valuable infor- functional activity during rest but showing consistent deactivations during mation about the neural correlates of self-related proces- externally directed, attention-demanding tasks. Such regions include the sing, two issues have recently arisen [3,6]. First, precuneus/posterior cingulate cortex, medial prefrontal cortex and bilateral temporoparietal junction. the identified regions, especially the midline regions Task-positive brain regions: regions consistently activated during externally (mPFC, Precuneus/PCC) often associated with self-related directed, attention-demanding tasks. Such regions include the intraparietal sulcus, frontal eye field, middle temporal area, lateral prefrontal cortex and dorsal anterior cingulate. Corresponding author: Thompson, E. ([email protected]). 104 1364-6613/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tics.2011.01.001 Trends in Cognitive Sciences, March 2011, Vol. 15, No. 3 Opinion Trends in Cognitive Sciences March 2011, Vol. 15, No. 3 we propose a theoretical framework that links this type of ception and action [1,20,21] (Figure 1b). These investiga- self-experience to a wide range of neuroscientific findings tions have focused on bodily awareness in sensorimotor at different levels of neural functioning. integration [20,21] and homeostatic regulation [1,22,23]. According to our proposal, experiencing oneself as an Central to this approach is the notion that the organism agent depends on the existence of specific types of dynamic constantly integrates efferent and afferent signals in a way interactive processes between the organism and its envi- that distinguishes fundamentally between reafference – ronment. We call these processes ‘self-specifying’ because afferent signals arising as a result of the organism’s own they implement a functional self/non-self distinction that efferent processes (self) – and exafference – afferent signals implicitly specifies the self as subject and agent [6,16].To arising as a result of environmental events (non-self). By illustrate the basic principles of self-specifying processes, implementing this functional self/non-self distinction, ef- we describe two paradigmatic examples – sensorimotor ferent–afferent integration implicitly specifies the self as a integration and homeostatic regulation – that underlie bodily agent [6,16,21]. the self-experience of being a bodily agent. We then argue that although externally directed attention-demanding Sensorimotor integration tasks can compromise self-related processing [7–10,17– The notion of self-specifying processes is easiest to illus- 19], such tasks can be expected to enhance another funda- trate through the systematic linkage of sensory and motor mental type of self-experience, namely that of being a processes in the perception–action cycle (Box 1). An organ- cognitive–affective agent [6,15,16]. In support of this point, ism needs to be able to distinguish between sensory and to show how cognitive neuroscience can begin to model changes arising from its own motor actions (self) and this type of self-experience, we apply the concept of self- sensory changes arising from the environment (non-self). specifying processes to cognitive control, including emotion The central nervous system (CNS) distinguishes the two by regulation. We conclude with suggestions for future exper- systematically relating the efferent signals (motor com- imental work based on our framework. mands) for the production of an action (e.g. eye, head or hand movements) to the afferent (sensory) signals arising Self-experience as arising from self-specifying from the execution of that action (e.g. the flow of visual or processes haptic sensory feedback). According to various models Many neuroimaging studies have focused on the type of going back to Von Holst [24], the basic mechanism of this self-experience that occurs when a person directs his or her integration is a comparator that compares a copy of the attention away from the external world (e.g. when task motor command (information about the action executed) demands are low, when performing a self-reflective task or with the sensory reafference (information about the senso- during rest) [7–10,17] (Figure 1a). At the same time, other ry modifications owing to the action) [25]. Through
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