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The Journal of Neuroscience, May 21, 2008, 28(21):5504-5512; doi:10.1523/JNEUROSCI.5493-07.2008

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Neurobiology of Disease
Recurrent Collateral Connections of Striatal Medium Spiny Neurons Are Disrupted in Models of Parkinson's Disease

Stefano Taverna, Ema Ilijic, and D. James Surmeier

Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois 60611

Correspondence should be addressed to Dr. D. James Surmeier, Department of Physiology, Feinberg School of Medicine, Northwestern University, 303 East Chicago Avenue, Chicago, IL 60611. Email: j-surmeier{at}northwestern.edu

The principal neurons of the striatum, GABAergic medium spiny neurons (MSNs), are interconnected by local recurrent axon collateral synapses. Although critical to many striatal models, it is not clear whether these connections are random or whether they preferentially link functionally related groups of MSNs. To address this issue, dual whole patch-clamp recordings were made from striatal MSNs in brain slices taken from transgenic mice in which D₁ or D₂ dopamine receptor expression was reported with EGFP (enhanced green fluorescent protein). These studies revealed that unidirectional connections were common between both D₁ receptor-expressing MSN (D₁ MSN) pairs (26%) and D₂ receptor-expressing MSN (D₂ MSN) pairs (36%). D₂ MSNs also commonly formed synapses on D₁ MSNs (27% of pairs). Conversely, only 6% of the D₁ MSNs formed detectable connections with D₂ MSNs. Furthermore, synaptic connections formed by D₁ MSNs were weaker than those formed by D₂ MSNs, a difference that was attributable to fewer GABA_A receptors at D₁ MSN synapses. The strength of detectable recurrent connections was dramatically reduced in Parkinson's disease models. The studies demonstrate that recurrent collateral connections between MSNs are not random but rather differentially couple D₁ and D₂ MSNs. Moreover, this recurrent collateral network appears to be disrupted in Parkinson's disease models, potentially contributing to pathological alterations in MSN activity patterns and psychomotor symptoms.

Key words: striatum; GABA; medium spiny neurons; lateral inhibition; patch clamp; Parkinson's disease

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Received Dec. 12, 2007; revised April 16, 2008; accepted April 17, 2008.

Correspondence should be addressed to Dr. D. James Surmeier, Department of Physiology, Feinberg School of Medicine, Northwestern University, 303 East Chicago Avenue, Chicago, IL 60611. Email: j-surmeier{at}northwestern.edu

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