6/26/20071 ACQ and the Basal Ganglia Jimmy Bonaiuto USC Brain Project 6/26/2007

2 Actor-Critic Learning Actor – learns action policy Critic – learns value functions Different actor-critic architectures have been proposed for learning different value functions: –V(s) = State values (most common) –V(a) = Action values –Q(s,a) = State, action pair values

6/26/20073 Actor-Critic Architecture Core Data – recording of midbrain dopaminergic neurons in appetitive learning tasks (Schultz, 1992; Schultz, 1998) (from Barto, 1995)

6/26/20074 Critic – V(s), V(a), or Q(s,a)? How do dopamine cells know about reward value? –Largest striatum input is from cortex (Haber and Gdowski, 2004) –V(s) and Q(s,a) learning may require the ventral striatum, SNc, and/or VTA to receive a copy of the same cortical projections that the dorsal striatum receives (state information) –V(a) may only require a projection from the dorsal striatum or globus pallidus (actor) to the ventral striatum, SNc and/or VTA (critic) –Largest forebrain input to dopamine neurons is striatum (Haber and Gdowski, 2004) -V(a) may be more biologically plausible in terms of connectivity

6/26/20075 Actor-Critic in the Basal Ganglia Dopamine targets (striatum) are site of value and policy learning (Suri & Schultz, 2001) The striatum split into dorsal and ventral divisions (some say dorsolateral and ventromedial) (Voorn et al., 2004) –Ventral striatum – inputs from limbic structures (critic?) –Dorsal striatum – connected with motor and associative cortices (actor?)

6/26/20076 Role of Dopamine (Joel & Weiner, 2000) Dopamine neurons in the ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) –VTA projects to ventral striatum – learning state values –SNc projects to dorsal striatum – policy learning Little difference in VTA and SNc firing (Schultz et al., 1993) –Predicted by TD learning equation since the policy and values are both updated using TD error

6/26/20077 ACQ Reinforcement learning should maximize total utility, not necessarily total reward. Motivations map outcomes to utilities (Niv et al., 2006) Multiple critics – one for each dimension of interoception (hunger, thirst, etc.) –Q(s,a), s =internal state, a=action Actor –Composite policy Desirability – based on internal state Executability – based on environmental state –Eligibility trace from mirror and canonical motor signals ii

6/26/20078 ACQ – Actor/Multiple Critics x=executed action x=recognized action ^

6/26/20079 ACQ - Eligibility Trace = executed action (from efference copy) = recognized action (from mirror system) Action Outcome xxε Not Attempted 0.0 Unsuccessful Unintended Successful ^ Idealized situations (perfect recognition) Realistic implementation would have confidence values between 0.0 and 1.0 for x and x, but the pattern of values for ε would be the same ^

6/26/ ACQ - Weight Modification Desirability and Executability updated using same eligibility and reinforcement signals Requires different weight change rules: Desirability Executability Tonic dopamine level, d, added to TD error – Makes sign of weight change depend on ε(t) Don’t update the value of the last action unless some action is currently recognized Step function of eligibility trace – Makes sign of weight change depend on r(t) ^

6/26/ Multiple Critics – Q(s,a) Is there evidence for multiple critics gated by interoceptive information? –The lateral hypothalamus does project to the SNc, VTA, and the ventral striatum (Saper et al., 1979; Fadel & Deutch, 2002; Brog et al., 1993) –The accumbens shell of the ventral striatum is reciprocally connected with the lateral hypothalamus and has been called a “sensory sentinel” or “visceral striatum” (Kelley, 1999, 2004) –Motivational state, such as food deprivation can influence the magnitude of dopamine release in the ventral striatum (Wilson et al., 1995; Ahn & Phillips, 1999) –Sexual satiety is signaled by serotonin from the lateral hypothalamus to the ventral striatum, which reduces dopamine levels (Lorrain et al., 1999) i

6/26/ Internal State-Dependent Policy Is there evidence for internal state- dependent policies? (Kelley et al., 2005) –Information from the lateral hypothalamus reaches the dorsal striatum through the paraventricular nucleus –Hypothalamic-midline thalamic-striatal projections carry internal state information to cholinergic interneurons of the dorsal striatum These are thought to modulate dorsal striatal output neurons

6/26/ Eligibility Trace from the Mirror System What is the evidence for an eligibility signal from mirror neurons? –People can implicitly learn sequences through action observation (Bird et al., 2005) –The striatum is consistently implicated in implicit sequence learning and the magnitude of activation is correlated with reaction time improvement (Rauch et al., 1997, 1998) –The basal ganglia is active during action observation (Frey & Gerry, 2006) –Projection from ventral premotor cortex (including the arcuate sulcus) to dorsal and ventral striatum in the macaque (McFarland & Haber, 2000)

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