How The Basal Ganglia Learn to Selectively Respond to Unexpected Rewarding Cues

[Stephen Grossberg]

The following article can be read at http://cns-web/bu.edu/Profiles/Grossberg

HOW THE BASAL GANGLIA USE PARALLEL EXCITATORY AND INHIBITORY LEARNING
PATHWAYS TO SELECTIVELY RESPOND TO UNEXPECTED REWARDING CUES. Brown, J.,
Bullock, D., and Grossberg, S. (1999). Journal of Neuroscience, in press.

After classically conditioned learning, dopaminergic cells in the
substantia nigra pars compacta (SNc) respond immediately to unexpected
conditioned stimuli (CS) but omit formerly seen responses to expected
unconditioned stimuli, notably rewards. These cells play an important
role in reinforcement learning. A neural model explains the key
neurophysiological properties of these cells before, during, and after
conditioning, as well as related anatomical and neurophysiological
data about the pedunculo-pontine tegmental nucleus (PPTN), lateral
hypothalamus, ventral striatum, and striosomes. The model proposes how
two parallel learning pathways from limbic cortex to the SNc, one
devoted to excitatory conditioning (through the ventral striatum,
ventral pallidum, and PPTN) and the other to adaptively timed
inhibitory conditioning (through the striosomes), control SNc
responses. The excitatory pathway generates CS-induced excitatory SNc
dopamine bursts. The inhibitory pathway prevents dopamine bursts in
response to predictable reward-related signals. When expected rewards
are not received, striosomal inhibition of SNc that is unopposed by
excitation results in a phasic drop in dopamine cell activity. The
adaptively timed inhibitory learning uses an intracellular spectrum of
timed responses that is proposed to be similar to adaptively timed
cellular mechanisms in the hippocampus and the cerebellum.  These
mechanisms are proposed to include metabotropic glutamate
receptor-mediated Ca2+ spikes that occur with different delays in
striosomal cells. A dopaminergic burst in concert with a Ca2+ spike is
proposed to potentiate inhibitory learning. The model provides a
biologically predictive alternative to temporal difference (TD)
conditioning models and explains substantially more data than
alternative models.

Keywords: dopamine, substantia nigra, reward, basal ganglia,
conditioning, pedunculopontine tegmental nucleus, lateral
hypothalamus, striosomes, adaptive timing

Preliminary version appears as Boston University Technical Report,
CAS/CNS-TR-99-011.

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