Actions, Reasons, Neurons and CausesJeffrey D. Schall

Narcisse Bichot, Leanne Boucher, Josh Brown, Corrie Camalier, Jeremiah Cohen, Erik Emeric, Doug Hanes, Richard Heitz, Shigehiko Ito,

Chi-Hung Juan, Min-Suk Kang, Aditya Murthy, Matthew Nelson, Pierre Pouget, Chenchal Rao, Supriya Ray, Takashi Sato, Stephanie Shorter-Jacobi,

Veit Stuphorn, Tracy Taylor, Kirk Thompson & Geoff Woodman

with Jean Bullier, Jon Kaas, Audie Leventhal,

Gordon Logan, Anne Morel, Tom Palmeri, Andrew Rossi

Workshop 7: Systems Biology of Decision MakingMathematical Biosciences Institute

June 2008

We are spending time on details, but I want to adopt broader perspective.

Consider:(1) The bee decided to fly North.(2) Bush decided to invade Iraq.

Does (2) include something more than (1)?

If not, what will become of law & human relations? If so, what?

The answer, it seems to me, depends on understanding what we mean by “decide”.

• 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

"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 described mathematically, e.g., signal detection theory, drift diffusion, 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

Rees et al. Nature Neuroscience 3, 716 - 723 (2000)

An empirical basis for distinguishing between choosing and deciding

It is deciding when medial frontal cortex is engaged.

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• The properties of neurons do not reveal function

• Formal (computational) theories of performance explain function

• But distinct models cannot be distinguished from behavior testing, e.g., diffusion or race

• Properties of neurons might provide constraints to distinguish between models …

• … if and only if the neural activity measured is the instantiation of the cognitive process in question, which constitutes a linking proposition

Necessity of formal linking propositions

Teller DY. 1984. Vision Research 24:1233-1246Schall JD. 2004. Ann Rev Psychol 55:23-50

Linking propositions for decision making

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Hanes & Schall (1996) described neural activity that looked like an accumulator.

They identified this activity with form of sequential sampling models.

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Linking propositions for decision makingRT = Decision time + Residual timeResidual time = Encoding time + Preparation time

Stimulus encoding Sequential sampling Response preparation

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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

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Munoz DP, Schall JD (2003) Concurrent distributed control of saccade initiation in the frontal eye field and superior colliculus. In The Oculomotor System: New Approaches for Studying Sensorimotor Integration. Edited by WC Hall, AK Moschovakis. CRC Press, Boca Raton, FL. Pages 55-82.

Saccade target selection and preparation are accomplished by a distributed network in the brain

This area (as part of a network) monitors conse-quences and adapts behavior

This area (as part of a network) specifies where, whether and when to move the eyes

How the brain chooses where to look

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How the brain chooses where to look

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Choosing target and choosing saccade

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

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Control of responses investigated with stop signal task

Countermanding performance

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Countermanding paradigm: Race model

Logan, G.D. & Cowan, W.B. (1984) On the ability to inhibit thought and action: A theory of an act of control. Psychological Review 91:295-327. Hanes DP and Schall JD (1995) Countermanding saccades in macaque.Visual Neuroscience 12:929-937

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Munoz DP, Schall JD (2003) Concurrent distributed control of saccade initiation in the frontal eye field and superior colliculus. In The Oculomotor System: New Approaches for Studying Sensorimotor Integration. Edited by WC Hall, AK Moschovakis. CRC Press, Boca Raton, FL. Pages 55-82.

Saccades are produced by a distributed network

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Hanes, D.P. and J.D. Schall (1996) Neural control of voluntary movement initiation. Science 274:427-430.

Countermanding physiology

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Hanes, D.P., W.F. Patterson, J.D. Schall (1998) The role of frontal eye field in countermanding saccades: Visual, movement and fixation activity. Journal of Neurophysiology 79:817-834.Pare M, Hanes DP (2003) Controlled movement processing: superior colliculus activity associated with countermanded saccades. Journal of Neuroscience 23:6480-6489.

Non-canceled saccades occur when movement-related activity reaches the threshold before SSRT

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Saccades are canceled if and only if movement-related activity is inhibited before SSRT

“Cancel” time

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Fixation cells in FEF & SC contribute to stopping saccades

Hanes, D.P., W.F. Patterson, J.D. Schall (1998) The role of frontal eye field in countermanding saccades: Visual, movement and fixation activity. Journal of Neurophysiology 79:817-834.

Paré M, Hanes DP (2003) Controlled movement processing: superior colliculus activity associated with countermanded saccades. Journal of Neuroscience 23:6480-6489.

Tempting to believe that movement cells are inhibited by fixation cells.

1 - The race model of countermanding performance assumes that the GO and the STOP processes have independent finish times.

Mapping the race model onto neural processes – two facts expose a paradox

2 – Saccades are produced by a network of interacting neurons.

How can a network of interacting neurons produce behavior that looks like the outcome of a race between independent processes?

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The STOP unit must inhibit the GO unit. But, if the inhibition is uniform and instantaneous, then the non-canceled movement will have longer than observed initiation times.Therefore, the inhibition of the STOP unit on the GO unit must be late and potent.

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dBoucher L, Logan GD, Palmeri TJ, Schall JD (2007) Inhibitory control in mind and brain: An interactive race model of countermanding saccades. Psychological Review 114:376-397

Delayed potent STOPReproduces countermanding behavior…

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Boucher L, Logan GD, Palmeri TJ, Schall JD (2007) Inhibitory control in mind and brain: An interactive race model of countermanding saccades. Psychological Review 114:376-397

Delayed potent STOP… and reproduces neural activation …

The GO unit is not modulated in non-canceled trials

The GO unit is modulated within SSRTin canceled trials

Boucher L, Logan GD, Palmeri TJ, Schall JD (2007) Inhibitory control in mind and brain: An interactive race model of countermanding saccades. Psychological Review 114:376-397

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from Gehring and Fencsik, Journal of Neuroscience 21(23):9430-9437

Error-related negativity

But what about errors?

The medial frontal lobe monitors consequences and conflict.

From Brown and Braver, Science, 307:1118-112118 February 2005

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Error-related neuron activity

Stuphorn V, Taylor TL, Schall JD (2000) Performance monitoring by supplementary eye field. Nature 408:857-860.

Error signals from single neurons correspond to scalp potentials… and are observed in ACC of monkeys.

Non-canceled error trials

Correct no stop signal trials

Emeric EE, Brown JW, Leslie M, Pouget P, Stuphorn V, Schall JD (2008) Error-related local field potentials in the medial frontal cortex of primates. Journal of Neurophysiology 99:759-772.

A framework for understanding guidance & control of action.

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.

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

(What about bees and ants and fish individually and as hives, colonies and schools?)

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

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• or by simultaneous stimulation of two different sites

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…

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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”