Reward Prediction Error Signals are Metarepresentational

It is often thought that metarepresentation is a particularly sophisticated cognitive achievement. There is substantial evidence that dolphins and some primates can represent some of their own psychological states, but the existence of ‘metacognition’ in any other species remains highly controversial (Carruthers 2009; Hampton 2009; Smith 2009). Research on the extent to which humans metacognize their own psychological states is expanding in parallel (Fleming et al., 2012). Representing the mental states of others is believed to be even rarer or non-existent in non-human animals (Hare et al. 2001; Heyes 1998). That capacity, under the label ‘theory of mind’, was long thought to be a crucial and relatively late developmental transition even in humans (Leslie 1987; Perner et al. 1989; Wimmer and Perner 1983). Recent looking-time experiments suggesting infants have an ability to track others’ perceptions and beliefs at a very young age raise the possibility that infants have some lower-level capacity for mentalizing (Kovacs et al. 2010; Onishi and Baillargeon 2005; Surian et al. 2007), in which case they may be able to metarepresent before they have a fully-fledged concept of belief, desire, or any other psychological state (Apperly and Butterfill 2009). However, macaques do not show the same behaviour (Marticorena et al. 2011) and there has been no suggestion that the capacity for non-conceptual metarepresentation extends more widely than that. This paper argues that non-conceptual metarepresentation does extend much more widely, but based on a different set of considerations, located in a field where the issue of metarepresentation has been entirely overlooked: the literature on reinforcement learning in reward-guided decision-making tasks. Research on humans and other animals has produced an impressive body of converging evidence that midbrain dopamine neurons produce a reward prediction error signal (RPE) that is causally involved in choice behaviour (Rushworth et al. 2009; Schultz et al. 1997; Schultz 1998). RPEs are found in humans, primates, rodents and perhaps even insects (Claridge-Chang et al. 2009). This paper argues that RPEs carry metarepresentational contents. A metarepresentation is a representation whose content concerns the content of another representation. For the purposes of this paper, a non-conceptual representation is a representation without semantically-significant constituent structure. It follows that the use of a non-conceptual representation does not require the possession of any concepts. RPEs are non-conceptual representations. So there is no suggestion that deploying RPEs involves having a theory of mind or having concepts of mental states. RPEs are a more low-level form of representation, probably non-conscious,1 and quite different from the kind of thinking about the mental states of ourselves and others that is familiar from everyday experience. It is clear that the brain does implement many forms of low-level information processing, beyond the personal level representations that occur in the familiar stream of conscious thought. For example, low-level non-conceptual information processing has been found in some systems for perception and motor control. Could a non-conceptual representation ever represent another representation as a representation? In one sense, no. It is natural to understand ‘representation-as’ so as to require deployment of a concept. A thought represents Jane as a professor only if the thought includes the concept professor and predicates it of Jane. For a putative metarepresentation M to represent another representation R as a representation (in this sense), M must have a constituent that refers to the property of being a representation (or some other representational property of R, like being a belief, having a certain content or truth condition, referring to some particular, etc.). That is clearly ruled out since non-conceptual representations lack semantically-significant constituent structure. However, there is nothing in the idea of non-conceptual content that excludes representational properties from figuring in the correctness condition or satisfaction condition of a non-conceptual representation. Just as for all non-conceptual contents, such properties can figure in the correctness condition without there being a corresponding semantically-significant constituent of the representation.2 Nevertheless, we can still discern a sense in which a non-conceptual representation M might fail to represent another representation R as a representation: M might represent only vehicle properties of R. For example, the correctness condition of M might be: such-and-such neural network is firing more strongly than normal; or the variance of the firing rate of such-and-such neural assembly is high. If the neural assembly figuring in the content is a representation R, then M is indeed about another representation; but M does not represent R as a representation, since no representational property of R figures in the content of M. On the other hand, the correctness condition of M could concern the content of R, for example: the current visual representation of the location of the light is likely to be false. Then M would indeed represent R as a representation—in the sense in which non-conceptual content admits of the distinction. Accordingly, M’s having a correctness condition or satisfaction condition that concerns the content of another representation is taken to be a sufficient condition for M to be a metarepresentation. That is a reasonably stringent test. It is not enough that M concerns another representation. A representational property must figure in M’s correctness condition or satisfaction condition. This paper argues that non-conceptual information processing is responsible for the reward-guided decision-making that is elicited in certain simple experimental paradigms; and that one element of this information processing, the RPE signal, happens to have meta-level non-conceptual content. Since the mechanism which deploys a phasic dopaminergic signal for reinforcement learning of reward-driven behaviour is widespread, it follows that a form of non-conceptual metarepresentation is relatively common in the animal kingdom. But the argument does not suggest that metarepresentation is ubiquitous. It is only because of particular features of the way RPEs are generated and processed that an argument for metarepresentation can be sustained. The argument is that the modelling and empirical findings combine to produce good evidence for metarepresentation—the considerations are evidential, not constitutive. No sufficient condition is proposed which entails that a system contains metarepresentations. Nevertheless, these evidential considerations may also apply to other systems in which the difference between a prediction and feedback is used to update the prediction for the future (Friston 2010; Wolpert et al. 2011). However, the point does not generalise to all comparator circuits, nor to all mechanisms for combining two sources of information (Ernst and Banks 2002). Nor is the model obviously applicable to the data on the seemingly metarepresentational looking behaviour in infants mentioned above. Section 2 below summarises the evidence that RPEs are involved in reward-guided decision making. Section 3 shows that widely-accepted models of the information processing responsible for subjects’ choice behaviour in these settings presuppose that RPEs carry metarepresentational contents. That furnishes a prima facie reason to think that RPEs are metarepresentational. Although the question of metarepresentation has not been canvassed in the RPE literature, it has been much discussed in the literature on ‘metacognition’ in non-human animals. Section 4 examines strategies deployed in the metacognition literature to displace a metarepresentational reading. Those strategies can be used to test the claim that RPEs are metarepresentational. Section 5 argues that the prima facie case that RPEs are metarepresentational is not undermined by the arguments found in the metacognition literature. Instead, the kinds of considerations advanced there, together with a plausible framework for content attribution, add up to a positive argument that RPEs have metarepresentational contents. They have both indicative and imperative contents (they are so-called pushmi-pullyus). The indicative content is that the content of another representation—the agent’s (first-order) representation of the reward that will be delivered on average for performing a given action—differs from the current feedback, and by how much. The imperative content instructs that it be revised upwards or downwards proportionately.