Accepted Manuscript Steps to a "Properly Embodied" Cognitive Science Mog Stapleton PII: S1389-0417(12)00024-1 DOI: http://dx.doi.org/10.1016/j.cogsys.2012.05.001 Reference: COGSYS 397 To appear in: Cognitive Systems Research Received Date: 16 April 2011 Accepted Date: 11 May 2012 Please cite this article as: Stapleton, M., Steps to a "Properly Embodied" Cognitive Science, Cognitive Systems Research (2012), doi: http://dx.doi.org/10.1016/j.cogsys.2012.05.001 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Steps to a "Properly Embodied" Cognitive Science 1 2 3 Mog Stapleton , School of Philosophy, Psychology and Language Sciences, University of 4 Edinburgh, Dugald Stewart Building, 3 Charles Street, George Square, Edinburgh EH8 9AD, 5 UK 6 7 Abstract 8 Cognitive systems research has predominantly been guided by the historical distinction between 9 emotion and cognition, and has focused its efforts on modelling the "cognitive" aspects of 10 behaviour. While this initially meant modelling only the control system of cognitive creatures, 11 with the advent of "embodied" cognitive science this expanded to also modelling the interactions 12 between the control system and the external environment. What did not seem to change with this 13 embodiment revolution, however, was the attitude towards affect and emotion in cognitive 14 science. This paper argues that cognitive systems research is now beginning to integrate these 15 aspects of natural cognitive systems into cognitive science proper, not in virtue of traditional 16 "embodied cognitive science", which focuses predominantly on the body's gross morphology, 17 but rather in virtue of research into the interoceptive, organismic basis of natural cognitive 18 systems. 19 20 Keywords: Proper embodiment; Embodied cognition; Affective neuroscience; Interoception; 21 Internal robotics; Enactive cognitive science.22 Corresponding author. Email address: M.L.Stapleton@sms.ed.ac.uk (M. Stapleton). 2 1. Introduction 23 24 The cognitive science of the twentieth century, reflecting the focus of the individual cognitive 25 sciences, was predominantly interested in perception, memory, problem solving, planning, and 26 other "cognitive" activities. For the most part, researchers interested in cognition ignored those 27 aspects that, as a hangover from Cartesian dualism, were considered "subjective", such as 28 consciousness and affect. This was due to a variety of factors, including the inheritance of 29 behaviourist and cognitivist psychology. Although cognitivism was a reaction to the 30 behaviourism of the early to mid twentieth century and thus directly opposed to many of its 31 claims, they both shared the assumption that the emotional domain was separate from the 32 cognitive domain, and furthermore, that emotion was potentially dissociable from cognition. As 33 a result, cognitive scientists have tended to consider it unnecessary to understand affect in order 34 to understand the other aspects of cognition, and for the most part have left research in this area 35 to a handful of "affective" neuroscientists and psychologists. 36 37 My aim in this paper is twofold. Firstly, to give a brief overview of some of the current research 38 in the individual cognitive sciences that suggests that the relation between affect and cognition is 39 more complex, and more important, than has traditionally been held to be the case by 40 mainstream cognitive science. I focus on research from neuroscience and robotics, as I think that 41 these provide the clearest models of current understanding. My second aim in the paper is to 42 show that this work is pointing us in the direction of a new type of embodied cognitive science. 43 Traditional "embodied" cognitive science, whose main focus was on gross morphological 44 sensorimotor interaction ignored the interactions between the control system and the internal 45 body, and thus had no place for the role of affect. I argue that recent work in neuroscience and 46 3 robotics suggests that cognitive systems are not merely superficially embodied in the sense that 47 the sensorimotor interactions with the environment are the only interactions relevant to cognitive 48 behaviour, but that cognitive systems are "properly embodied"; the internal body matters to 49 cognition. 50 2. Beyond morphological embodiment 51 52 What started in the late twentieth century as an embodied cognitive science revolution, has 53 slowly been becoming mainstream cognitive science (see, for example, Gibbs 2005; Chemero 54 2009; Shapiro 2011; Barrett 2011). Given the focus on the body, however, it might seem 55 surprising that until recently there was little research involving the internal and affective body 56 beyond designing robots to detect and display emotional expressions so as to make them more 57 appealing to, and facilitate interaction with humans (see, for example, Kismet n.d.). The focus of 58 embodied cognitive science is on decentralizing cognition and modelling how the morphology of 59 the body and its activity often reduce the processing load of the brain (Clark 1997, 2008; Pfeiffer 60 2007). The paradigmatic examples of this approach to cognitive systems research are Rodney 61 Brooks's "animats" (Brooks 1991; see also Meyer & Wilson 1991) and Barbara Webb's robotic 62 crickets (1994, 1996). Brooks's animats are distinctive in having no central controller as such; 63 rather, their cognitive architecture is organized in layers, each relating to the control of parts of 64 the robot's body, and which feed back to one another. Similarly, Webb's robotic crickets model 65 the use of the bodily architecture in cricket phonotaxis, which allows direct response to mating 66 calls, avoiding the need for complex information processing. Good introductions to embodied 67 cognitive science can be found in Clark (1997, 2001, 2003, 2008) and Bermúdez (2010, sect. 4). 68 69 4 The principal way in which bodily morphology engenders and shapes cognitive activity and 70 processes is through sensorimotor interaction with the world. In this way Webb's robotic crickets 71 exploit their morphology to allow sensing to directly control motor processes. The basic idea is 72 that some of the computational work essential to cognition can be partially offloaded to, and 73 realized by, bodily processes and structures external to the central nervous system. (Physical 74 gestures are another oft-cited example: see Clark 2008; Goldin-Meadow 2005.) Cognition is thus 75 "extended" so that it encompasses parts of the body (and plausibly also those parts of the non-76 biological world) that support the appropriate offloading of computations. However, this means 77 that as far as standard embodied cognitive science is concerned, the body qua body does not play 78 a special role; only the body in virtue of its ability to be a vehicle of computations. The result is 79 that, although research in this paradigm is based on the role of the body in cognition, the body 80 really isn't the important factor. 81 82 Recently, sensorimotor cognitive science has begun to bring research from developmental 83 psychology together with robotics, and in the process has taken embodiment research towards 84 using not only exteroceptive sensory information (vision, hearing, touch, etc.) to guide action but 85 also proprioceptive and kinaesthetic information (the sense of the location of the body and the 86 movement of the body, respectively). The result is that these sources of internal sensory 87 information not only aid sensorimotor activity but can also be integrated into "higher" cognitive 88 activity. This can be seen specifically with research using the iCub in the European project 89 "Robotcub" and in the follow-up projects such as ITALK and AMARSi. The iCub is designed, 90 with the help of some learning algorithms, to develop roughly like a toddler: through active 91 engagement with its environment, including interaction with humans. An example of what the 92 5 iCub can do through ontogenetic learning and development can be seen in Morse et al.'s work 93 with the iCub (2010), wherein it has learnt to name objects by associating the name of the object 94 not only with the object of attention when the name is given, but also with the part of egocentric 95 space that the object is normally presented in (for a video of this in action see Barras 2010). 96 97 These steps towards a robotics which integrates research from developmental psychology as well 98 as neuroscience are being interwoven with a train of cognitive systems research whose roots lie 99 in the biological sciences and phenomenology rather than the computationalist/functionalist 100 tradition that was the main voice of twentieth century cognitive science. While sensorimotor 101 research in robotics and philosophy of cognitive science has often come to be labelled as 102 "enactive" (principally through Alva Noë's use of the term "enactivism" to describe his 103 sensorimotor theory of consciousness: see Noë 2004, 2009), there is more to enactivism than 104 sensorimotor skills, and as such, enactive cognitive science should not be conflated with 105 sensorimotor cognitive science (for extended arguments on this see Ziemke 2007, 2008; Morse et 106 al. 2011; Di Paolo 2009; Ward & Stapleton forthcoming). 107 108 The main distinguishing feature of enactive cognitive science is the focus, not only on the 109 interaction between cognitive systems and their environment (i.e. predominantly sensorimotor 110 interactions), but also on the constitution of cognitive systems and the relation between their 111 constitution and their interaction with the environment (this distinction is from Moreno et al. 112 2008, cited in Ziemke 2008). For example, Ziemke (2008), and Ziemke and Lowe (2009) have 113 argued that being physical systems which can interact with their environment through sensors 114 and actuators is not sufficient for cognitive embodiment. They propose looking to the bodies of 115 6 living organisms for the future direction of cognitive robotics: what Di Paolo (2003) refers to as 116 an "organismically inspired robotics". While enactivism originated in the work on autopoiesis 117 and the structural coupling between an autopoietic system and the environment (see Maturana & 118 Varela 1992; Varela, Thomson & Rosch 1991; Thompson 2007), the principal notions which 119 have come to be of central importance to current cognitive science research are autonomy and 120 adaptivity (Di Paolo 2005; Thompson 2007). Autonomy and adaptivity take the key insights 121 from cellular autopoiesis, such as operational closure, self-construction, and sense-making, and 122 abstract away from the biological implementation. Having said this, the abstraction is not so 123 great that key biological functions such as homeostasis are ignored; the internal is key to 124 enactivism (see Di Paolo 2010). 125 126 These baby steps towards an enactive cognitive science can be seen in Vernon's conceptual 127 framework for the iCub architecture (Vernon 2010), in which the role of cognition is taken to be 128 "to anticipate events and increase the space of actions in which a system can engage" (Vernon 129 2010, p. 91). More specifically, the position is that: 130 131 (a) cognition is the process by which an autonomous self-governing agent acts effectively in the world in 132 which it is embedded, that (b) the dual purpose of cognition is to increase the agent's repertoire of effective 133 actions and its power to anticipate the need for and outcome of future actions, and that (c) development 134 plays an essential role in the realization of these cognitive capabilities. (Vernon 2010, p. 90) 135 136 The explicit focus on anticipation in this framework is very much in line with the current 137 understanding of the role of prediction in neuroscience, and indeed Vernon claims that: 138 139 7 [...] cognition arises from an agent's need to compensate for latencies in neural processing by anticipating 140 what may be about to happen and by preparing its actions accordingly. So we can agree fairly easily what 141 cognition is - a process of anticipating events and acting appropriately and effectively - and why it is 142 necessary - to overcome the physical limitations of biological brains and the limitations of bodily 143 movements operating in a dynamic environment. (Vernon 2010, p. 90) 144 145 In Vernon's model the internal components work together to comprise different "cognitive" 146 systems, such that the perception system comprises exogenous salience, endogenous salience, 147 egosphere, and attention selection; the action system comprises gaze control, vergence, reach and 148 grasp, locomotion; anticipation and adaptation are underpinned by the episodic and procedural 149 memory components; motivations are underpinned by the affective state component, which 150 works with the action selection component and provides "a very simple homeostatic process 151 which regulates the autonomous behaviour of the iCub" (Vernon 2010, p. 95). While Vernon's 152 architecture may be more modular that many embodied and enactive cognitive scientists would 153 be happy with, we can see a progression from more standard architectures in that internal and 154 affective information have critical roles. We see affect as a part of dynamic feedback re-entrant 155 couplings (rather than a feed-forward network) such that "affective information" is feeding 156 directly into action selection and from there into procedural memory, and from there to both gaze 157 control and episodic memory. Even though it might look at first glance as though there is an 158 affect "module", in fact the cognitive behaviour is a result of the dynamic behaviour between the 159 components, and even the explicitly affective information (i.e. that which the affective 160 component processes and integrates) is feeding back and through many of the components whose 161 principal activity is underpinning perception, action, and anticipation. 162 8 3. Affective perception 163 164 What evidence do we have that affective information feeds into the kinds of processes Vernon 165 outlines in his cognitive architecture? One source of evidence is from a model of affective 166 predictions in object perception by Barrett and Bar (2009). Barrett and Bar put together research 167 on visual processing in light of the generalized predictive coding approach to neuroscience. At 168 the heart of the generalized predictive coding approach is the hypothesis that the brain is 169 essentially a prediction engine, and the information that we garner from the world is encoded in 170 the errors in these predictions. The brain continues to recalibrate and generate new predictions 171 until the incoming sensory states match those predictions (Bar 2009; Friston 2009; Friston & 172 Kiebel 2009). Prediction has recently become something of a unifying framework guiding 173 understanding at various levels in neuroscience, from the statistics of neural firing to the level of 174 us as agents interacting in the world; see Clark (forthcoming) for an accessible introduction to 175 these principles. 176 177 Barrett and Bar address prediction somewhere in between these levels. Their thesis is that object 178 perception is generated by - and through (I add this because the processing is importantly not 179 strictly sequential, but involves a lot of feeding back at various stages) - predictions about the 180 relevance of an object or class of object, that is, its value to the agent either generally or at this 181 particular moment in time. This means that rather than perception being a matter of "bottom-up" 182 processing where the details are put together stage by stage to make the whole, the overall 183 prediction, i.e. the gist of the situation, is processed early on, becoming more and more detailed 184 or accurate through the recurrences. Barrett and Bar use an illustrative analogy of the Dutch style 185 of painting in the sixteenth and seventeenth centuries: first the gist of a situation is sketched, then 186 9 over time, through the recursive application of ever smaller dabs of paint, a detailed picture 187 emerges. The recursive (and ever finer) dabs of paint in this example correspond to the recursive 188 predictions that are generated as a result of errors in the predictions of sensory states. Their thesis 189 is that object perception arises partly as a result of predictions about the value of that object to 190 the agent. 191 192 Drawing on research from Aude Oliva's computational visual cognition lab at MIT (see, for 193 example, Oliva & Torralba 2006), Barrett and Bar propose that the brain quickly makes an initial 194 prediction about an object using low spatial frequency visual information, and then the details 195 are filled in by memory guided by context. Direct projections between the visual cortex and areas 196 of the prefrontal cortex provide a pathway for this recursive (re-)creation of the visual experience 197 of the object. The previous knowledge which is used to flesh out the gist of the prediction is 198 encoded in sensorimotor patterns which are stored for future use. Importantly for us here, they 199 argue that sensorimotor patterns are sensory in the fullest sense of the term: they not only involve 200 external sensations and their relations to actions, but also internal sensations - from organs, 201 muscles and joints, and how external sensations have influenced these internal sensations 202 (Barrett & Bar 2009, p. 1325). They thus show that the connections between various brain areas 203 give us reason to believe that representations of internal bodily (autonomic and endocrine) 204 changes are part of visual processing right from the stage at which the gist of a situation is being 205 processed by the frontal systems, giving even perception at this paucity of specificity an affective 206 flavour which helps code the relevance/value of the object of perception. 207 208 10 Looking at their model of visual processing in a bit more detail we can see exactly how they 209 propose that affective information feeds into object perception. Visual information comes 210 through the lateral geniculate nucleus (part of the thalamus), at which point a very unspecific 211 "gist" of this information is sent through the fast magnocellular pathway through the dorsal 212 visual stream, which includes the lateral parietal cortex, and also through fast magnocellular 213 pathways to V1 and from there to the dorsal stream. The dorsal stream sends information on to 214 the medial orbitofrontal cortex (mOFC) which then sends information to (i) the autonomic and 215 endocrine systems to effect bodily changes including preparation for action, and (ii) information 216 about those changes that have been ordered to the lateral parietal cortex, feeding that information 217 back into the dorsal stream. This shows that the processing of gist information is affective as the 218 internal bodily changes are caused and the representations of these are fed back into the lateral 219 OFC helping to refine the gist each time with the information about affective value that these 220 carry. The idea is that each time round the processing loops, better and better predictions are 221 being made and the perception of the object is getting less and less gist-like - and at the same 222 time developing more and more meaning (in terms of biological relevance) for the agent in virtue 223 of the affective aspect of the perception. Highly specific visual information (as opposed to "gist" 224 information) gets sent on a different route towards the orbital frontal cortex. From the lateral 225 geniculate nucleus it gets sent through slower parvocellular pathways to both the ventral visual 226 stream and V1, and from there to the ventral stream. Information from the ventral stream gets 227 sent to the lateral OFC (rather than the medial OFC as was the case in the dorsal loop). Also 228 feeding into the lateral OFC is information from the external senses and from the internal bodily 229 changes that were effected as a result of processing in the medial OFC. The lateral OFC thus 230 serves as an association area of all of this information from various senses including 231 11 interoception. So even the more specific visual processing that builds upon the gist that is being 232 created as a result of the dorsal loops is laden with affective value. I suggest that Barrett and 233 Bar's model of visual processing looks something like this: 234 235 Fig 1: Pictorial representation of Barrett and Bar's model of affective predictions in object perception (2009) 236 237 As my diagram above suggests, upon Barrett and Bar's proposal all the processing described 238 here is very recurrent and not at all static or sequential in a strict sense. Even in the simplified 239 form that I have presented Barrett and Bar's proposal, it is clear that affective value is feeding in 240 at various levels (i.e. both dorsal and ventral) and becoming part of the very dorsal processing 241 that it is feeding into. They suggest that it is likely that the real picture is even more complex, 242 which would only further the argument that affective value is inherently a part of visual 243 processing: 244 245 Taken together, these findings indicate that it may be more appropriate to describe the affective predictions 246 generated by the medial and lateral OFC as phases in a single affective prediction evolving over time, 247 12 rather than as two separate 'types' of affective predictions (with one informing the other). This 248 interpretation is supported by the observation that the medial and lateral OFC are strongly connected by 249 intermediate areas; in addition, the lateral OFC receives some low spatial frequency visual information and 250 the medial OFC some high spatial frequency information; and, magnocellular and parvocellular projections 251 are not as strongly anatomically segregated as was first believed (for a review, see Laylock et al. (2007)). 252 Furthermore, there are strong connections throughout the dorsal 'where' and ventral 'what' streams at all 253 levels of processing (Merigan and Maunsell 1993; Chen et al. 2007). Finally, the OFC has widespread 254 connections to a variety of thalamic nuclei that receive highly processed visual input and therefore can not 255 be treated as solely bottom-up structures in visual processing. (Barrett & Bar 2009, p. 1331) 256 4. The value of the internal 257 258 At this point we should step back and consider what is meant by affective. Barrett and Bar use 259 the term to denote information pertaining to the viscera, information which is likely to be a guide 260 to how the system is faring in the world. It is this information which is inherently valenced and 261 value-laden. Typically we think of "valence" as indicating positive or negative experience, but 262 its connection to value can be seen even if we set aside questions of phenomenality. This is clear 263 when we consider the variety of terms for which "valence" is used to refer: hedonic tone; utility; 264 good/bad mood; pleasure/pain; approach/avoidance; rewarding/punishing; appetitive/aversive; 265 and positive/negative (Barrett 2006, p. 40). Valence is rooted in the concept of value (see 266 Colombetti 2005 for a detailed discussion of value and valence), and Barrett and Bliss-Moreau 267 (2009) gesture towards this when - appealing to research by Owren and Rendall (1997, 2001) 268 - they suggest that core affect represents a basic kind of psychological meaning: 269 270 The basic acoustical properties of animal calls (and human voices) directly act on the nervous system of the 271 perceiving animal to change its affective state and in so doing conveys the meaning of the sound. (Barrett 272 & Bliss-Moreau 2009, p. 172) 273 13 274 While I don't want to pursue the issue of whether meaning can be reduced to affective changes, 275 we could instead think of meaning here as being the appraisal of value to the organism. In 276 emotion theory "appraisal" has traditionally had cognitive connotations (see Scherer 1999 for a 277 comprehensive review of appraisal theory) but contemporary appraisal theory acknowledges 278 appraisals which are very low-level and not grounded in deliberation. Scherer writes in regard to 279 low-level appraisals, which make up one of the components of his component theory of emotion: 280 281 ... one can argue that we need a general, overarching term to cover the fundamental fact that it is not the 282 objective nature of a stimulus but the organism's "evaluation" of it that determines the nature of the 283 ensuing emotion. A completely automatic, reflexive defence reaction of the organism also constitutes an 284 intrinsic assessment, a valuation, of the noxiousness of the stimulus (although it may not necessarily 285 produce a fully fledged emotion [...]). Even if simple feature detection is involved the outcome of the 286 process constitutes an assessment of the significance of the detected stimulus to the organism, given that 287 feature detectors that have any behavioral consequences are automatically "significance detectors". 288 (Scherer 1999, p. 647) 289 290 In this context, therefore, appraising value to the system can be something as basic as a response 291 required for maintaining homeostasis (the internal balance that keeps a system viable). In this 292 minimal sense, homeostatic behaviours such as withdrawing from a painful stimulus or seeking 293 water when thirsty are results of an appraisal that the current situation is incompatible with 294 homeostatic viability. There is a temptation to think of the behaviour as being a result of the the 295 interoceptive information, and thus a result of some personal or subpersonal level "cognitive" 296 deliberation, however recent research by A. D. Craig on "homeostatic emotions" (Craig 2003a, 297 2003b) suggests that the action/behaviour is an integral part of interoception (the afferent 298 14 homeostatic pathway). For example, in the basic pain pathway common to primates and non-299 primates which rises through the brainstem, the limbic motor cortex (ACC) is directly involved 300 in the loop receiving projections from the medial dorsal nucleus of the thalamus and sending 301 projections on to the periaqueductal grey. And, in the primate specific pathway, the limbic motor 302 cortex is also activated in virtue of direct projections from lamina I, and subsequently projects on 303 to the right anterior insula, in addition to area 3a of the sensorimotor cortex (which projects 304 directly to the primary motor cortex) receiving corollary projections from one of the afferent 305 projections from the thalamus to the interoceptive cortex in the insula (for details, see Craig 306 2003a, 2003b). 307 308 It can be seen from this that the "motor areas" of the central nervous system are part of the very 309 homeostatic loop itself, rather than functioning - at this basic level - as a result of deliberation 310 conceived in either personal or subpersonal level terms. They are so entwined with the afferent 311 homeostatic signals which ground interoception that it looks as though interoception is not 312 merely the passive representation of the physiological changes in the body, but has the motor 313 aspects already factored in. In other words, interoception includes motor information. So if 314 interoception includes information about and preparation for homeostatic behaviour, then it is by 315 nature functioning as a basic appraisal machine adapting the system in response to perturbations 316 from the environment. The point to which I want to draw attention is that if this minimal model 317 of appraisal of value is correct then it is appropriate to understand valence as affective 318 motivation: affective because it is constituted by afferent homeostatic information, and 319 motivational because it is also constituted by the activation of motor areas. 320 15 5. Internal robotics 321 322 In a similar vein to Craig's work in neuroscience on homeostatic behaviours, Parisi, in his 2004 323 article "Internal Robotics", explains how his lab have evolved behaviours such as sleeping, 324 feeling pain. and feeling hungry and thirsty in their agents, in order for them to cope with 325 particular environmental problems. The effective evolution of these behaviours illustrates the co-326 evolution of the internal environment and the control system (a neural network in the robots, the 327 nervous system in organisms) and external interactions. 328 329 Parisi argues that the behaviour of organisms is a result of two types of interaction: (1) between 330 the nervous system and the external environment, and (2) between the nervous system and the 331 internal environment. The nervous system can be thought of as a physical system which realizes 332 the function of mapping inputs onto outputs "in ways that allow an organism to survive and 333 reproduce in its environment" (Parisi 2004, p. 326). Inputs are caused by either physical or 334 chemical events outside the nervous system, and likewise outputs cause physical or chemical 335 events outside the nervous system. But (and this is what "embodied cognitive science" tends to 336 overlook) "outside the nervous system" includes not only the external environment but also the 337 internal body. The internal body provides inputs to the nervous system physically through 338 somatosensory and proprioceptive receptors (relating information about movement and location 339 of body) and through chemical means with molecules from the endocrine system modulating the 340 nervous system and even molecules from the nervous system itself feeding back to it. Likewise, 341 the internal body receives outputs from the nervous system both by chemical means and by 342 neural connections to parts of the autonomic nervous system. Of course, internal interactions are 343 predominantly chemical (as opposed to the predominantly physical interactions between the 344 16 nervous system and the external environment), and chemical interactions have quite different 345 properties to physical interactions. Physical interactions are mediated by neuron-to-neuron 346 connections where the specific "weights" of the connections seem to be the predominant factor 347 in information transfer such that the neurotransmitters that are used in the interactions play a 348 qualitative (rather than quantitative) role. Interaction between the nervous system and the body 349 relies predominantly on molecular based information transfer and can be slower, diffuse and 350 reliant on quantitative effects to activate thresholds. Nevertheless, apart from during states such 351 as sleep (plausibly), the nervous system is constantly interacting with both the external 352 environment and the internal environment (i.e. the internal, autonomic and homeostatic body) as 353 depicted in Fig.2 below. 354 355 Fig 2: Internal and external interactions (adapted from Parisi 2004) 356 357 It might seem appropriate to think of internal interactions (i.e. between the nervous system and 358 the internal environment) as underpinning the emergence of affect, while the external 359 interactions (between the nervous system and the external environment) underpin cognition. 360 17 However, Parisi argues that one cannot truly separate the cognitive and affective components, 361 nor understand one without the other: 362 363 For example, an organism may be able to do many different things (cognitive component), but what the 364 organism actually does at any particular time depends on its motivational state (affective component). The 365 current motivational state of an organism is a result of the interactions of the organism's nervous system 366 with the inside of the body, and it controls aspects of behaviour that seem to be purely cognitive, such as 367 selective attention. (Parisi 2004, p. 332) 368 369 The moral of Parisi's paper is that the behaviour of organisms results from both internal 370 interactions and external interactions; organisms live in two worlds, the external and the internal. 371 The building of artificial cognitive systems, therefore, whether their purpose is to model natural 372 cognitive systems or whether they are being designed as artificial cognitive systems in their own 373 right, must also simulate both interactions. In his own words: 374 375 The behaviour of an organism results from both the interactions of the organism's nervous system with the 376 external environment and its interactions with the internal environment. Therefore, what is needed is not 377 only an external robotics but also an internal robotics. If we want to understand the behaviour of organisms 378 what we need to reproduce in artificial physical organisms, i.e. robots, is not only the external morphology 379 of an organism's body and the interactions of the organism's nervous system with the external 380 environment, but also the internal physical structure of the organism's body and the interactions of the 381 organism's nervous system with what lies inside the body. (Parisi 2004, p. 326) 382 6. Affective cognition 383 384 The work I have reviewed so far gestures towards a very different way of thinking about 385 enhancing cognitive systems with affectivity than by adding some sort of an emotion module. 386 18 Crudely put the argument is that internal bodily affect is crucial to cognitive systems and that an 387 "emotion chip" just won't suffice. This gives us reason to step away from the emotion–cognition 388 distinction as it has traditionally been elucidated in the cognitive sciences. Without denying that 389 there are behaviours and experiences that are usefully labelled using emotion terms and that 390 these episodes can have effects on functions traditionally labelled "cognitive" such as perception, 391 memory, and learning, we can observe that there is another, more fundamental, aspect of affect 392 which is integrated into basic cognitive activity. Recent work by prominent figures in 393 neuroscience, such as Luiz Pessoa, Antonio Damasio and Joseph LeDoux underpins this change 394 of focus. 395 6.1 Somatic markers don't suffice 396 397 Outwith the neuroscience community, Antonio Damasio is best known for his work on somatic 398 markers in which he argues that emotion plays an important role in some cognitive processes 399 (see, for example, Damasio 1994). The somatic marker hypothesis for example is the hypothesis 400 that thoughts that arise get tagged with affective information in the ventromedial prefrontal 401 cortex (vmPFC) which enables the healthy person to utilize information about previous 402 experience quickly and subconsciously during decision making. In the Iowa Gambling Task that 403 is the principal methodology in Damasio and his colleagues' studies, this means that healthy 404 participants learn quickly which decks of cards yield high punishments as well as high pay-offs, 405 and so they naturally gravitate towards the safe decks, which yield lower pay-offs but also lower 406 punishments, and are ultimately better in terms of awarding winnings. The somatic marker 407 hypothesis is based on Damasio and his colleagues' findings that in participants who have 408 damage to the ventromedial prefrontal cortex there is no gravitation towards the safe decks. 409 Measurements of the skin conductance response of both healthy and vmPFC participants showed 410 19 that vmPFC participants did not have the kind of skin response in anticipation of choosing the 411 risky decks that healthy participants exhibited. Damasio and his colleagues proposed that this 412 was due to the vmPFC being the site where "cognitive" information coming from other cortical 413 areas is "tagged" by "emotional" information coming from limbic areas, and so the disruption of 414 these links caused by vmPFC damage dissociates the affective information from the cognitive 415 information. The hypothesis fits with what we know about the behaviour of those with vmPFC 416 damage: people with this kind of damage often perform well on standard psychological tests, IQ 417 tests, and so forth, and yet appear to be ultimately impaired in normal life; they have difficulty 418 making simple decisions when there is no clear "right" answer such as when choosing what 419 clothes to wear or what restaurant to choose (Saver & Damasio 1991); they also tend to be 420 impulsive and engage in risky behaviours that would have been alien to their pre-damaged self 421 (ibid.). 422 423 This hypothesis gives emotion an important place in cognitive processing; however, it still takes 424 emotion to be separate from cognition. It is thoughts, cognitions, that are tagged with affect in 425 virtue of links to what has traditionally been considered the emotion system, i.e. the amygdala, 426 and the insula, which is the locus of representations of the body. In effect, it is not really that 427 emotion plays a part in cognitive processes, but rather that for Damasio these somatic markers 428 solve a kind of localized frame problem: if choosing from one deck of cards in the gambling task 429 has resulted in a negative bodily reaction, negative affect gets tagged to thoughts of that deck, 430 and so when thoughts of that deck arise again for whatever reason that affect is played back, 431 shutting off - or severely reducing - possibilities for action. But making some possibilities for 432 action less motivating (or more motivating, as the case may be) doesn't mean that emotion is 433 20 actually playing a part in any of the cognitive processes per se, but that it is playing a role in the 434 meta-cognitive process of using cognitive processes plus affective processes for action selection. 435 So while decision making might be thought of as a cognitive process because it encompasses 436 cognitive processes such as memory, planning, etc., it is not itself a cognitive process in the same 437 manner as those processes. Rather it is a conglomerate of processes, and therefore although it is 438 interesting that it might also require encompassing processes traditionally considered to be 439 affective, this does not need to be a radical claim about cognitive processes per se. 440 6.2 Integrating affective information 441 442 Whilst the somatic marker hypothesis may not support the strong claim that cognition must be 443 affectively embodied, Damasio's more recent work does, in precisely the interoceptive way 444 explicated in the previous sections. Damasio (2010) talks of "primordial feelings" being 445 grounded in brainstem structures, in particular the nucleus tractus solitarius and parabrachial 446 nucleus. These structures are richly connected and are the locus of visceral sensory maps which 447 are key to regulating homeostatic processes. In combination with their connections with the 448 periaqueductal gray and the superior colliculus, Damasio hypothesizes that these brainstem 449 structures instantiate a primordial feeling state in virtue of their being the locus of initial neural 450 representations of changes in the autonomic and endocrine systems. These primordial feelings 451 are constant and provide a background to all cognition such that exteroceptive and interoceptive 452 perception, while having different foci, are nevertheless consistently meshed and thus each feed 453 into both experience and connections to other cognitive processes. This suggests that it may be 454 fruitful for us to think of interoceptive perception as part and parcel of exteroception as well, at 455 least in so far as exteroceptive information is processed. We can see this in particular in 456 Damasio's explanation of the role that the superior colliculus plays in the perceptual pathway. 457 21 The superior colliculus (SC) is a primarily visual structure, receiving information directly from 458 both the retina and the visual cortex . However, in addition to these maps of the visual world, the 459 SC also contains "topographical maps of auditory and somatic information, the latter hailing 460 from the spinal cord as well as the hypothalamus" (Damasio 2010, p. 84). Of particular interest is 461 that these maps may all be integrated: 462 463 The three varieties of maps - visual, auditory, and somatic - are in a spatial register. This means that 464 they are stacked in such a precise way that the information available in one map for, say, vision, 465 corresponds to the information on another map that is related to hearing or body state. There is no other 466 place in the brain where information available from vision, hearing, and multiple aspects of body states is 467 so literally superposed, offering the prospect of efficient integration. The integration is made all the more 468 significant by the fact that its results can gain access to the motor system (via the nearby structures in the 469 periaqueductal gray as well as the cerebral cortex). (Damasio 2010, p. 84) 470 471 Thus, according to Damasio, even very early on in the neural pathways we find that affective, 472 perceptual and motor information are inseparably intertwined. Due to the non-linear and 473 recurrent nature of the brain's pathways, such integrated channels of information feed into what 474 we might have thought of as purely perceptual pathways, and this integrated information 475 constrains what is then available for perception. 476 6.3 The amygdala as supporting the interdependency of affect and cognition 477 478 Pessoa's review of emotion and cognition (2008) gives us good neuroscientific grounding for 479 what might seem to be a radical thesis: that affect and cognition are mechanistically 480 interdependent (and often integrated). He argues that paradigmatic "cognitive" processes such as 481 memory and attention involve information from "emotion", whether considered in terms of 482 22 structure, function, or connectivity. While cognitive processes have traditionally been located in 483 the cortex, and correlates of emotion in subcortical (limbic) and para-limbic areas (those areas 484 that used to be considered the old, "mammalian" brain)1, Pessoa argues that these distinctions are 485 ungrounded. Traditionally what were considered emotional processes such as motivation, drive, 486 appraisals, bodily changes and arousal were thought (i) not to be involved in cognitive processes 487 such as attention, (ii) to be independent of top-down factors, and (iii) to be context-independent. 488 However, Pessoa explains that even the most paradigmatic of the structures that have been 489 associated with emotion, the amygdala, contravenes all three of these motivations. 490 491 In respect of connectivity of the amygdala, it is important to note that the amygdala receives 492 from, and gives out information to, areas other than those traditionally regarded as 'emotional' or 493 action-provoking. The brain has a small world topology which means that all brain areas are 494 connected by one or two intermediate areas (Sporns et al. 2004; Sporns & Zwi 2004; Bullmore & 495 Sporns 2009). It might be thought that because the prefrontal areas are among the most distant 496 from sensory periphery they receive the most highly processed and integrated information. 497 Highly processed information is supposed to bring greater flexibility, and support the abstract 498 processing required for "cognition". However, the amygdala is connectively equally removed 499 from the sensory periphery, and so receives just as highly processed and integrated information 500 as the prefrontal areas. Moreover, the amygdala makes (and receives) widespread projections to 501 the rest of the brain. It is one of the most highly connected regions of the brain. So if viewed 502 from a perspective of connectivity, the amygdala is in the "geometric centre" of the topological 503 map (see Pessoa 2008, Fig. 1), and even though it is a core affective region, it is "at least as well 504 situated to integrate and distribute information as certain PFC territories" (Pessoa 2008, p. 151). 505 1 See Maclean & Kral 1973 for the origins of this triune brain theory. 23 506 There thus seems insufficient justification for asserting that one of the key "emotion" areas, the 507 amygdala, is an "affective" rather than a "cognitive" structure. Pessoa (2010) expands on this 508 and suggests that the amygdala should instead be considered a predictive structure involved in 509 situations where the organism must work out the answers to questions in the environment such as 510 "What is it?" and "What's to be done?" 511 512 Understanding the amygdala as a hub in the brain's networks we can begin to see that it does 513 indeed play an important role in emotional situations. But this role is not of the kind that we 514 imagine when we are entrenched in the conception of the brain as a one-area-one-function 515 machine. This framework resulted in interpreting data in such a way that the amygdala has 516 generally become thought of as a "rapid-response fear module" (for a detailed rejection of this 517 view, see Sander et al. 2003). Now that we have a different framework in theoretical 518 neuroscience in which to view data within, that of networks (Sporns 2010; Sporns & Zwi 2004) 519 and prediction (Bar 2009; Friston & Kiebel 2009), we can see that there is evidence that the 520 amygdala plays a far more important role then previously supposed. The role it plays is of coding 521 for biological relevance (Sander et al. 2003). This can be understood in terms of the amygdala's 522 function being to "direct the various sources of attention [...] towards a source of sensory 523 stimulation (such as an object) when the predictive value of that stimulation is unknown or 524 uncertain" (Barrett et al. 2007). 525 526 The literature which shows that the amygdala is involved in emotion processing does not 527 necessarily imply either that the amygdala is an emotion structure or that its activation pertains to 528 24 emotional rather than non-emotional stimuli. Rather, conceived of as coding for significance, 529 previous findings can be accounted for, while also accounting for the important role it plays in 530 non-emotional processing (that is, processing that would not traditionally be considered 531 "emotional"). Similarly, Pessoa and Adolphs (2010) argue that the amygdala is not an emotion 532 module, but a core brain circuit with "broad connectivity with the cortex and other subcortical 533 structures" enabling it to play a modulatory role in multiple networks: 534 535 The precise functional importance of the amygdala in these networks remains to be investigated, but it is 536 unlikely that it will map specifically onto emotion. Instead, we think that it corresponds to broader and 537 more abstract dimensions of information processing, including processing of salience, significance, 538 ambiguity, unpredictability and other aspects of 'biological value'. More broadly, we argue that the 539 amygdala has a key role in solving the following problem: how can a limited capacity information 540 processing system that receives a constant stream of diverse inputs selectively process those inputs that are 541 the most relevant to the goals of the animal? (Pessoa & Adolphs 2010, p. 780) 542 543 There is much more work that needs to be done here to show how this new conception of the 544 activity of the amygdala fits in with the emerging theoretical neuroscience frameworks. But for 545 our purposes the importance of this re-evaluation of the amygdala's role in processing should be 546 clear. If activity in the amygdala is part of a network which codes for biological significance, and 547 it is a hub projecting to, and receiving projections from, most areas in the brain, including those 548 previously deemed to be "cognitive", it is going to be very difficult to continue to hold the coarse 549 distinction between either affect or emotion and cognition in terms of neural processing. 550 7. Conclusions: Towards a properly embodied cognitive science 551 552 25 Current neuroscience strongly suggests that processing is neither "affective" nor "cognitive". 553 Clearly there is still going to be a distinction in that certain networks may predominantly 554 underpin certain activities, but these must be specified in each particular case, for example, the 555 neural processing underpinning perception, or fear, or surprise, and so on. If there is such a thing 556 as "affective" or "cognitive" processing this will only be discovered by understanding in full the 557 correlates of these categories of abilities, activities or behaviours. Once this has been done we 558 may compare the correlates of all those categories which we consider "affective" and compare 559 these with those we consider "cognitive". If the difference reveals a pattern of processing that is 560 particular to affective categories or cognitive categories, then we may have grounds for 561 considering there to be affective or cognitive domains. However, (i) given the evidence that we 562 have so far on the underpinnings of these categories - in particular, the amount (and importance 563 of) recurrency in the neural processing - this looks unlikely to be the case; and (ii) this will 564 depend on whether theses categories have been accurately distinguished as "cognitive" or 565 "affective". 566 567 Even LeDoux, whose work on the amygdala as a fear centre helped to propagate this coarse 568 distinction, has recently shifted his focus away from "emotion" circuits and towards "survival 569 circuits", information about which feeds into the cognitive workspace along with information 570 from explicit memory, language, environmental activity, body feedback, and central nervous 571 system arousal (LeDoux 2012). This approach is reminiscent of Brooks's layered robots 572 discussed in section 2, and yet we can see that survival circuits, body feedback, and CNS arousal 573 support a more adaptive picture of cognition; that which underpins flexible adaptive behaviour in 574 an environment. The recent work on affective perception and the integration of affect into 575 26 "cognitive" functions reviewed here gives a good indication of the importance of the role of 576 internal information in natural cognitive systems and suggest ways in which these aspects might 577 be implemented in artificial cognitive systems. This would extend the concept of embodiment in 578 cognitive science beyond the current sensorimotor embodiment paradigm towards the 579 organismic, enactive paradigm. Such a properly embodied cognitive science embraces the 580 affective not merely as critical for realistic cognitive systems but as integrated in cognition itself. 581 582 Damasio has long argued for the importance of homeostasis and interoceptive information for 583 emotion and cognition (Damasio 1994, 1999) and develops this in a highly accessible way in the 584 central chapters of his recent book Self Comes to Mind (2010), and this is beginning to be 585 integrated into research in cognitive modelling and robotics, together with research on the 586 physiology of pain and touch. (While touch is usually considered to be an exteroceptive sense 587 there is also an argument for it being categorized as interoceptive; see Craig 2003a, 2003b, 588 2008.) But while haptics is now a common facet of robotics, interoception has yet to become an 589 orthodox part of cognitive systems research. Work from research groups such as those led by 590 Tom Ziemke (in particular, the Integrating Cognition, Emotion, and Autonomy (ICEA) project) 591 and Ezequiel Di Paolo, who have been working on developing the insights from physiology and 592 neuroscience outlined in section 2 and modelling these in robotic agents, is changing this, 593 however, and robotic modelling is beginning to integrate processes beyond sensorimotor 594 interaction (see Morse et al. 2011). 595 596 Interoception is inherently entwined with affect. While there are disputes in the emotion 597 literature as to how much bodily feelings are involved in emotion (if at all) there is little doubt as 598 27 to their role in affect more generally; and it is quite plausible that the basis of valence and arousal 599 (what Barrett calls "core-affect") lie in interoception (Craig 2008; Barrett & Bliss-Moreau 2009). 600 The move towards more biologically plausible robotics, a robotics which is not only 601 sensorimotor and superficially autonomous but which is interoceptive and provides a way to be 602 deeply autonomous, is a step towards an affective robotics, and thus a step towards a cognitive 603 science which is not merely embodied in terms of its sensorimotor possibilities but "properly 604 embodied". 605 606 Acknowledgements: The author would like to thank the reviewers Tom Ziemke and Giovanna 607 Colombetti for their helpful comments, and David Harris for his help with proof reading. 608 609 References 610 611 Bar, M. (2009). 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