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The Journal of Neuroscience, April 18, 2007, 27(16):4374-4384; doi:10.1523/JNEUROSCI.5519-06.2007

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Behavioral/Systems/Cognitive
Novel and Distinct Operational Principles of Intralaminar Thalamic Neurons and Their Striatal Projections

Carolyn J. Lacey, J. Paul Bolam, and Peter J. Magill

Medical Research Council Anatomical Neuropharmacology Unit, University of Oxford, Oxford OX1 3TH, United Kingdom

Correspondence should be addressed to Dr. Peter J. Magill, Medical Reseach Council Anatomical Neuropharmacology Unit, University of Oxford, Mansfield Road, Oxford OX1 3TH, UK. Email: peter.magill{at}pharm.ox.ac.uk

Neurons of the intralaminar thalamus, including central lateral (CL) and parafascicular (Pf) nuclei, innervate the cortex and striatum and are important for cognitive, sensory, and motor processes. We tested the hypothesis that CL and Pf neurons provide functionally distinct inputs to the striatum. We performed recordings of single CL and Pf neurons in anesthetized rats and, after juxtacellularly labeling the neurons, their somatodendritic features and synaptic connections were characterized.

All CL neurons (n = 31) discharged classic low-threshold Ca²⁺ spike bursts during cortical slow-wave activity in vivo. In contrast, Pf neurons (n = 52) rarely fired such bursts, but instead discharged groups of spikes at relatively low frequencies. The activity of CL and Pf neurons was often temporally coupled to cortical slow oscillations. Identified CL neurons possessed archetypal "bushy" dendrites and preferentially established synapses with dendritic spines (91% of synapses) of striatal projection neurons. Pf neurons possessed "reticular-like" dendrites, and, on average, preferentially established synapses with dendritic shafts (63%) in striatum, although connectivity was markedly heterogeneous across neurons. Two of the six Pf neurons studied exclusively targeted dendritic shafts, whereas another neuron almost exclusively (97%) targeted spines. The remaining three neurons preferentially targeted dendritic shafts (53–70%).

Thus, the fundamental properties of CL and Pf neurons differ (the latter do not express the typical operational principles of thalamic relay neurons), and they provide different temporally patterned inputs to distinct striatal targets. This mechanistic diversity likely underpins the transmission of specific and discrete information from intralaminar thalamic nuclei to striatal and cortical targets.

Key words: basal ganglia; intralaminar thalamus; striatum; thalamostriatal; parafascicular; central lateral

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Received Dec. 20, 2006; revised March 13, 2007; accepted March 14, 2007.

Correspondence should be addressed to Dr. Peter J. Magill, Medical Reseach Council Anatomical Neuropharmacology Unit, University of Oxford, Mansfield Road, Oxford OX1 3TH, UK. Email: peter.magill{at}pharm.ox.ac.uk

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