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Encoding by Response Duration in the Basal Ganglia

¹The Interdisciplinary Center for Neural Computation; ²Department of Physiology, Hadassah Medical School; ³The School of Engineering and Computer Science; and ⁴Department of Neurobiology, Life Science Institute, Faculty of Sciences, The Hebrew University, Jerusalem, Israel

Submitted 25 March 2008; accepted in final form 6 October 2008

Several models have suggested that information transmission in the basal ganglia (BG) involves gating mechanisms, where neuronal activity modulates the extent of gate aperture and its duration. Here, we demonstrate that BG response duration is informative about a highly abstract stimulus feature and show that the duration of "gate opening" can indeed be used for information transmission through the BG. We analyzed recordings from three BG locations: the external part of the globus pallidus (GPe), the substantia nigra pars reticulata (SNr), and dopaminergic neurons from the substantia nigra pars compacta (SNc) during performance of a probabilistic visuomotor task. Most (>85%) of the neurons showed significant rate modulation following the appearance of cues predicting future reward. Trial-to-trial mutual information analysis revealed that response duration encoded reward prospects in many (42%) of the responsive SNr neurons, as well as in the SNc (26.9%), and the GPe (29.3%). Whereas the low-frequency discharge SNc neurons responded with only an increase in firing rate, SNr and GPe neurons with high-frequency tonic discharge responded with both increases and decreases. Conversely, many duration-informative neurons in SNr (68%) and GPe (50%) responded with a decreased rather than an increased rate. The response duration was more informative than the extreme (minimal or maximal) amplitude or spike count in responsive bins of duration-informative neurons. Thus response duration is not simply correlated with the discharge rate and can provide additional information to the target structures of the BG.