For Psychology 216, Fall 2009 NEUROSCIENCE OF DECIDING, CHOOSING & ACTING

Freedom is not some extra feature or characteristic (see Smullyan, Is God a Taoist).

Freedom from determinism is not necessary for social and legal responsibility. Although, some are arguing that neuroscience should change the legal system. “Cognitive neuroscience, by identifying the specific mechanisms responsible for behaviour, will vividly illustrate what until now could only be appreciated through esoteric theorizing: that there is something fishy about our ordinary conceptions of human action and responsibility, and that, as a result, the legal principles we have devised to reflect these conceptions may be flawed.” – Greene & Cohen (2004) For the law, neuroscience changes nothing and everything. Philos Trans R Soc Lond B Biol Sci. 359: “Brains do not commit crimes; people commit crimes. This conclusion should be self- evident, but, infected and inflamed by stunning advances in our understanding of the brain, advocates all too often make moral and legal claims that the new neuroscience does not entail and cannot sustain.” – Morse (2006) Brain Overclaim Syndrome and Criminal Responsibility: A Diagnostic Note. Ohio State Journal of Criminal Law 3: Goal of this presentation is to consider whether a sufficiently enriched compatibilism can be achieved from the marriage of law, philosophy, psychology and neuroscience to provide useful leverage on questions of criminal responsibility. But this requires agreeing on what we mean by “decision”, “choice”, “intention” and “action”.

Action – anything we do Actions have reasons - “I did” Events just have causes - “It happened” Reasons for actions are explanations in terms of purposes, i.e., intentions A particular movement may be intentional under one description but not under another e.g., a wink or a blink Decision – deliberation when alternatives vague, payoffs unclear or habits reversed New Guinea Peaberry or Bella Vista F.W. Tres Rios Costa Rica? Definitions Choice – action in the context of alternatives to satisfy a goal, desire or preference coffee or tea? choices take time Coffee or tea? Coffee!

"I feel that way right now. Ask me in two or three months and I may change. I don't think I will. I'm pretty sure that's my decision." — Michael Jordan on his retirement from professional basketball. Associated Press, 17 July 1998 “I look forward to playing and hopefully I can get to that point where I can make that decision.” — Michael Jordan on his anticipated return to professional basketball. Associated Press, 19 July 2001 Characteristics of decision Unlike choices, decisions cannot be predicted. The source of decisions is inaccessible to introspection.

Distinguish two meanings (1) As quantitative rules describing behavior (Game theory, Economics) But average measures of outcome do not specify mechanism (2) As process producing behavior Mechanism with a particular architecture Plausible mechanisms can be modeled mathematically, e.g., biased choice theory, signal detection theory diffusion, random walk EBRW, ITAM, TVA Decision as process has two distinct meanings (1) Decide to Alternative actions Can be identified with choosing Good/bad but not true/false (2) Decide that Alternative categories True/false Refining definition of decision

Now that we have the philosophical issues sorted out, how does the brain work? For higher mammals the mapping of brain states to behavior (and mental states?) is many-to-one. This is how neural causes can coexist with intentional reasons. In particular, what is the link between neural causes and intentional reasons? For “lower” animals and reflexes the mapping of brain state to behavior is one-to-one

Systems Channels What are “brain states”? Cells Circuits

The goal of cognitive neuroscience is to understand how mental processes (like deciding what to do) come from events in the brain. No single neuron decides must because that is how many neurons are in your brain! 10 neurons don’t. Channels in the membrane don’t decide. Do 100? 1,000? 1,000,000?

How does the brain choose where to look? How does the brain correct errors? How does the brain control when to move? An experimental system

Are intentions “real”? “The state of a man’s mind is as much a fact as the state of his digestion” (Lord Justice Bowen in Edginton v. Fitzmaurice, 1885) To be real (physical), intentions must be supervenient on the brain. Specifying this relationship constitutes a linking proposition which entails the following: bridge locus levels & signals – spikes, LFP, ERP, fMRI, etc. what is a brain state? Channels, neurons (glia), local circuits, modules, areas, global circuits? necessity of mathematical or computational model to translate between neurons and function e.g., interactive race model of countermanding performance (impulse control) many : 1 and 1 : many mapping of brain & behavior provides room for intentional reasons to coexist with neural causes “…every action begins with intention in the sense that intentions must be the immediate cause of those bodily movements through which persons act for those movements to be actions at all” (p 2, M. Moore 2008). How does intention gain causal efficacy? Must trace path back from muscles to intention. “how” entails when + where when? >100 ms & <1,000-2,000 ms before movement where? anatomically before but connected with motor/premotor circuits, capable of accomplishing what intentions must do (not motor, not sensory, memory + planning + representing entails PFC) how? (a) When must explanation translate from neural to cognitive terms? (b) Scientific explanation must account for Prob(move) & response time (both correct & error) Teller DY Vision Research 24: Schall JD Ann Rev Psychol 55:23-50

How the brain chooses where to look Response time

Neural activity Time from array presentation (sec) Choices are made when neurons resolve alternatives Thompson, K.G., D.P. Hanes, N.P. Bichot and J.D. Schall (1996) Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. Journal of Neurophysiology 76:

What if the alternatives are hard to distinguish? Or the consequences are uncertain? Look at the brighter of the two visual stimuli. Correct earns $1,000. Incorrect costs $1,000.

Earn $1,000 Pay $1,000

A procedure to probe the timecourse of decision process Response time Correct Error

Choosing target versus choosing eye movement Murthy A, Thompson KG, Schall JD. (2001) Dynamic dissociation of visual selection from saccade program-ming in frontal eye field. J Neurophysiol. 86:2634

One-to-many mapping Different movements can occur based on a single representation of the world If the brain “knew” where the target was, why did it make an error? Why do you say things you don’t mean? The mouth moves faster than the mind…

Another network of neurons controls when gaze shifts Time from stimulus (sec) 0.0 Neural Activity Hanes, D.P. and J.D. Schall (1996) Neural control of voluntary movement initiation. Science 274:

Many-to-one mapping The same eye movement can originate from different brain states An eye movement of a given direction can be evoked by activation of a particular site in the superior colliculus or frontal eye field or by simultaneous stimulation of two different sites

Time from EMG onset (msec) 0 from Gehring and Fencsik, Journal of Neuroscience 21(23): Error-related negativity But what about errors? The medial frontal lobe monitors consequences and conflict. Error-related neuron activity Stuphorn V, Taylor TL, Schall JD (2000) Performance monitoring by supplementary eye field. Nature 408:

Reconciling intentional reasons with neural causes If a given body movement can arise from different brain states, then the dependence of behavior on intention can be explained in terms of the representational content of the intention (reasons) and not its neural realization as such (causes) A movement can be called an intentional action if and only if it originates from a cognitive state with meaningful content which is the reason for the action The representation of a single focus of activation in the brain leading to an eye movement of a particular direction can be distinguished from the representation of two foci of activation leading to the same saccade through averaging. But, the two mappings of neural representations onto saccades do not have equal status. “Averaging” eye movements are maladaptive because they direct gaze to neither stimulus; they are unintentional errors that must be corrected to achieve the goal of vision. In contrast, an accurate saccade to one of the two stimuli would achieve the goal of vision and more likely would be owned as intentional. Self-monitoring distinguishes “I did” from “it happened”

Where do we go from here?