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Weighing in on decisions in the brain: neural representations of pre-awareness practical intention

Abstract

Neuroscientists have located brain activity that prepares or encodes action plans before agents are aware of intending to act. On the basis of these findings and broader agency research, activity in these regions has been proposed as the neural realizers of practical intention. My aim in this paper is to evaluate the case for taking these neural states to be neural representations of intention. I draw on work in philosophy of action on the role and nature of practical intentions to construct a framework of the functional profile of intentions fit for empirical investigation. With this framework, I turn to the broader empirical neuroscience literature on agency to assess these proposed neural representations of intention. I argue that while these neural states in some respects satisfy the functions of intention in planning agency prospective of action, their fit with the role of intention in action execution is not well supported. I close by offering a sketch of which experimental task features could aid in the search for the neural realizer of intention in action.

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Notes

  1. 1.

    Non-human animals engage in goal-directed behaviors in some sense, but here the focus is a subset of goal-directed behaviors, human intentional actions. For a good overview of the analysis of intentional action, see Mele (2009b).

  2. 2.

    Earlier studies show that frontal areas evidence positive activity during the timeframe prior to movement when negative potentials, and the readiness potential, is measurable in parietal and precentral areas (Deecke et al. 1976).

  3. 3.

    Libet et al. (1983) understood this reported mental item more broadly to be the participants’ urge, desire, or intention to move.

  4. 4.

    Extensions of the Libet findings include, for instance, an fMRI study (Soon et al. 2008) and a single-cell recording study (Fried et al. 2011).

  5. 5.

    For a wide-ranging review of the neuroscience of free will, see Waller (2019) and Waller and Brager (forthcoming). For a book anthology of empirical and philosophical work on the Libet paradigm, see Sinnott-Armstrong and Nadel (2011). For a book length treatment of science and free will, see Mele (2009b).

  6. 6.

    My use of the terms conscious and unconscious here and throughout should be taken thinly to mean intentions of which the agent is aware or unaware of, respectively. Conscious intentions are one species of personal-level mental states. Other proposed challenges to free will from neuroscience include the dualist threat and the epiphenomenal threat (e.g., Mele 2014; Nahmias 2010; Waller forthcoming).

  7. 7.

    Here a practical decision should not be confused with practical deliberation. One can be uncertain about what to do and so deliberate—consider options—for hours or days. This deliberation is sometimes termed ‘deciding what to do.’ Here I take an act of deciding, a decision, to be the terminal event of resolving uncertainty about what to do. In this way, I follow the terminology and account of decisions in Mele (1992, 2009b). See Furstenberg (2014) for an explicit endorsement of EEG as a method for locating intentions in the brain.

  8. 8.

    Pacherie and Haggard (2011) note this in their discussion of Libet (p. 71).

  9. 9.

    Perhaps the most explicit discussion of locating the representation of intention in the brain comes from the work of John-Dylan Haynes and colleagues, with striking titles such as “Reading Hidden Intentions in the Brain” (Haynes et al. 2007) and “The Neural Code for Intentions in the Human Brain” (Haynes 2014a, b). The neuroscientists mentioned previously investigate and discuss the neural realizers of intentions to act prior to agent’s awareness of intending to act for endogenously generated movement. And, like those researchers, Haynes investigates endogenously generated activity. However, in contrast, Haynes is concerned specifically with the neural correlates of conscious intentions, or intentions that the agent is aware of having. In other words, Haynes is looking for the neural realizer of our personal-level intentions. In this sense, he is engaged in an agency-specific version of the search for the neural correlates of consciousness (Haynes 2014a). The neural correlates of consciousness refers to mapping a set of neurons’ activity to the having of a conscious mental state of some stripe (e.g., sensory states). Haynes is explicitly committed to the use of neurotechnology, in particular multivariate pattern analysis of fMRI signals, as a means to infer the encoding or representation of individual mental states (Haynes et al. 2007; see especially Haynes 2014a, p. 157; Haynes 2014b, p. 173). For reasons of scope and space, unfortunately, I will not be addressing this proposal for the neural representation of intention in this present paper. Instead I focus on the candidate neural realizers of intention pre-awareness. Later in this article I return to his proposal of the prefrontal cortex (PFC) as the site of prospective conscious intentions.

  10. 10.

    In opposition, Desmurget and Sirigu (2012) support that the intention to move, or ‘want’ as they term it, is generated by activity in the inferior parietal cortex, whereas the SMA provides the ‘urge’ to move, which appears to be more indicative of timing of the movement.

  11. 11.

    For an empirically-based argument that intentions cannot be localized in the brain, see Schurger and Uithol (2015). Schurger and Uithol (2015) argue that given the neural and indeed broader physiological distribution of interdependent action-related states, “the origins of actions cannot be confined unambiguously in space and time” (p. 764). I will not take up a detailed response to that argument here, but note that the SMA and pre-SMA are among the sites that make up this distributed action-related activity.

  12. 12.

    As such, what I say about locating intentions is at odds with an eliminative materialist stance (e.g., Churchland 1981; Stich 1983), at least regarding some theoretical entities of folk psychology. Moreover, the attempt to locate intentions in the brain is a stronger realist position on intentions as intentional states than the intentional stance proposed by Dennett (1981, 1991): the real patterns underscoring ascriptions of intentions to systems or agents in the former approach are localized, however, complexly, in neural structures.

  13. 13.

    For eliminativist accounts, see Chemero (2011); Stich (1983). For a neural representation fictionalist view, see Sprevak (2013). See Ramsey (2007) for a discussion of representation in cognitive science.

  14. 14.

    For a proposal that synapses and not neurons are the functional units for carrying information in the brain, see Cao (2014).

  15. 15.

    That is, on my view, representational content is not merely an intentional gloss. I acknowledge, however, that the theoretical positing of neural representations is bound up with the activities of neuroscientists as a community of epistemic agents. Here I take a view in the ballpark of Bechtel’s view about the ability of neuroscientists to uncover the reality of the representational states and mechanisms of the brain. The cognitive labor of neuroscientists and their explanatory goals are inextricable aspects of the theoretical positing of neural representations and mechanisms. For instance, Bechtel (2008, 2016) argues that representational contents are attributed to neural states in the service of designing experiments and interpreting results aimed at uncovering mechanistic explanations of the cognitive phenomena. Nonetheless, on his view, those states, as representational vehicles, play a representational role, operated over in neural processes. These states are not representational in the mere useful fiction, or instrumentalist sense.

  16. 16.

    Hence, what I say here about the representation of intention in the brain remains open with regard to, for instance, the informational approach and teleosemantic accounts. For representative informational semantics about content determination, see Dretske (1981), Dretsky (1988) and Usher (2001), among others. For representative teleosemantic accounts, see Millikan (1984), Papineau (1987), and Nanay (2013). For recent proposals of content determination, especially those related to neural representation, see Cao (2012), Neander (2017), and Shea (2018).

  17. 17.

    See, for instance, Roskies (2008) on the distance between how epistemically direct neuroimages from fMRI are assumed to be and how epistemically direct those images as indicators of brain activity actually are.

  18. 18.

    Why look to the proposed functional roles of personal-level intentions as a partial determinant of content of their neural realizers? This is generally the approach taken in neuroscience in some sense. If we are to take seriously that the activation of certain brain regions serves as a neural vehicle of the representational content of intentions, we’ll need to know which role of intentions, psychologically speaking, is implicated at which stage of processing for any given task that falls under the domain of volitional agency. Then we’ll need to get some sense of how activation in certain neural populations is utilized and affected in the production of such tasks and how that localized activation is connected via networks to the activation of other neural populations in task performance. That is, I’ll assume that the functional role of the neural activation in task competence is indicative of the content of the neural representation. The neural realizer of practical intentions should, sensibly speaking, play the same role on a neural-level that practical intentions play on the psychological level of task description.

  19. 19.

    While there seems to be no rational constraint against an agent’s desiring to A and desiring to not A simultaneously, intentions are subject to such rational constraints (Bratman 1987; Mele 2009a).

  20. 20.

    See Mele (1992, 2009b). A similar distinction is also made by Bratman (1984; present-directed intentions versus future-directed intentions), and Pacherie (2006; P-intentions and F-intentions).

  21. 21.

    Mele (1992, 2009b) gives an account of intentions were some intentions can be non-actively acquired. He gives the example of opening one’s office door. Although Al’s proximal intention to open his office door plays a role in his so opening the door, he needn’t have decided to open the office door. For mundane actions like this, the agent typically isn’t unsettled about what to do. Hence, the agent need not form an intention though the act of deciding.

  22. 22.

    Gollwitzer (1999)’s work concerns distal intentions, intentions to do something later, whereas Brass and Haggard (2008)’s account primarily applies to proximal intentions.

  23. 23.

    See Gollwitzer (1999) for an overview of empirical work that supports that implementation intentions do in fact enhance the likeliness of successful execution of planned actions.

  24. 24.

    One notable exception is Fridland’s (2019) argument that while practical intentions do play a role in guiding action, other control mechanisms feature more prominently in the unfolding of planned action, at least for skilled actions.

  25. 25.

    I thank a reviewer for pushing me to be clearer about my characterization of personal level.

  26. 26.

    A large experimental literature exists on the SMA and pre-SMA. Here I provide only a snapshot of studies for each proposed function of intention.

  27. 27.

    Committed meditators, the experimental group in Jo et al. (2015), were those who had at least three years of experience practicing mindfulness meditation.

  28. 28.

    Recall that the impetus for looking at SMA and pre-SMA activity as a neural representation of intention came from earlier work on the RP and its role in the production of voluntary actions. Given the equivocal nature of the evidence for the RP as motoric in content or as tied to conscious and active states, what ought we to conclude about the RP as a proxy representation of prospective intention? That activity in the SMA and pre-SMA has been implicated in inhibiting competing action plans and that the RP has been found to reliably precede self-initiated tasks and self-reports of intention is still strongly suggestive of the RP measuring (at the least) a partial realizer of intention pre-action.

  29. 29.

    I thank the reviewer who drew my attention to this important view regarding the role of practical intention in action initiation.

  30. 30.

    I thank a reviewer for drawing my attention to these accounts of intention.

  31. 31.

    See Mylopoulos and Pacherie (2017) for a competing proposed response to the interface challenge; see Levy (2017) for motor representations in relation to know-how.

  32. 32.

    See Waller (2012) for a proposal that a skilled action paradigm would aid in uncovering initiator of action for broadly conceived Libet tasks.

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Acknowledgements

Aspects of this article were presented at the Locating Representations Using Neuroimaging Workshop at Stanford, the Cognitive Science Speaker series at CUNY, the Summer Seminars in Neuroscience and Philosophy at Duke, and the lab meeting of the Institute of Philosophy, University of London. I am grateful to the organizers and participants at those events for their comments and suggestions. I am especially grateful to Felipe De Brigard, Patrick Haggard, Al Mele, David Papineau, Elisabeth Parés-Pujolràs, Sarah Robins, David Rosenthal, Adina Roskies, Aaron Schurger, Nick Shea, Walter Sinnott-Armstrong, and Jessey Wright, with whom I have discussed, in person or virtually, seeds of these ideas. Thank you to two anonymous reviewers for helpful feedback and suggestions.

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Waller, R.R. Weighing in on decisions in the brain: neural representations of pre-awareness practical intention. Synthese 199, 5175–5203 (2021). https://doi.org/10.1007/s11229-020-03020-4

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Keywords

  • Intentions
  • Practical reasoning
  • Neuroscience
  • Representation
  • Intentional action