Research reportDopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum
Section snippets
Overview
Dopamine (DA) neurons of the substantia nigra (SN) and ventral tegmental area (VTA) respond to unexpected reward events [102]. However these cells respond to a wide category of salient stimuli [57], [99]-unexpected rewards are one member of this category. While it has been suggested that reward stimuli may be unique in producing a phasic DA response and that other arousing stimuli may produce only gradual DA elevations [102], this assumption is not made here. Novel, intense, rewarding,
DA neurons respond to salient unexpected events
Among the attributes that may imbue an event with salience are 1) novelty, 2) primary and conditioned reward properties, 3) primary and conditioned aversive properties, and 4) physical characteristics such as high intensity and fast rise-time. VTA DA neurons, i.e. those that give rise to mesolimbocortical DA pathways, respond to each of these types of salient events [57]. Single-unit recordings have demonstrated that VTA DA neurons show phasic elevations in activity in response to novel events
DA selectively promotes the processing of strong glutamate inputs to the striatum
If DA is a gatekeeper for glutamate input to the striatum, it is a selective gatekeeper that, within dorsal and ventral striatal regions, enhances the impact of strong input signals while dampening the impact of weaker signals [26], [27], [67], [88]. Cells in the dorsal and ventral striatum undergo transitions from a state of hyperpolarization (ca. −80 mV), far below the cell's action potential threshold, to a less polarized state (ca. −60 mV), within close range of action potential threshold
DA activity gates the throughput of sensorimotor and incentive motivational inputs to the striatum
The dorsal striatum receives glutamate inputs [42], [77] from virtually all sensory and motor regions of the cerebral cortex [64], [68], [71], [78], [107]. Neurons in the dorsolateral striatum (putamen) fire in relation to the movement of particular body parts [5], [23], [30], [31], [81], [121], and in some cases particular joints [2], [5], [31]. Some putamen cells show activity during the preparation of a movement [2], [53]. In some of these neurons, the neuronal activity during movement
Striatal plasticity: stimulus-response learning, salience assignment to synaptic inputs, and/or stimulus-response-outcome chunking
The prior discussion suggested that DA neurons are activated by salient environmental change and that elevations in synaptic DA activity within the striatum increase signal-to-noise ratios, permitting strong corticostriatal inputs privileged access to striatal outputs, by amplifying strong inputs and dampening the impact of weak (task-irrelevant) inputs. Further, it was noted that glutamate inputs to the striatum represent not only sensory and motor events, but also events coded on the basis of
Acknowledgements
I gratefully acknowledge Wayne Wicklegren, Marcel Kinsbourne, Jennifer Mangels, Peter Balsam, Yaniv Eyny, Amy Hale, Won Yung Choi, Michael Drew and Johannes Schwaninger with whom I have had stimulating discussions of these issues.
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