Distribution of Tyrosine Hydroxylase-Expressing Interneurons with Respect to Anatomical Organization of the Neostriatum

Bengi Ünal,Elizabeth D. Abercrombie,Fulva Shah,James M. Tepper,Osvaldo Ibáñez-Sandoval

doi:10.3389/fnsys.2011.00041

Abstract

We have recently shown in vitro that striatal tyrosine hydroxylase-expressing interneurons identified in transgenic mice by expression of enhanced green fluorescent protein (TH-eGFP) display electrophysiological profiles that are distinct from those of other striatal interneurons. Furthermore, striatal TH-eGFP interneurons show marked diversity in their electrophysiological properties and have been divided into four distinct subtypes. One question that arises from these observations is whether striatal TH-eGFP interneurons are distributed randomly, or obey some sort of organizational plan as has been shown to be the case with other striatal interneurons. An understanding of the striatal TH-eGFP interneuronal patterning is a vital step in understanding the role of these neurons in striatal functioning. Therefore, in the present set of studies the location of electrophysiologically identified striatal TH-eGFP interneurons was mapped. In addition, the distribution of TH-eGFP interneurons with respect to the striatal striosome–matrix compartmental organization was determined using μ-opioid receptor (MOR) immunofluorescence or intrinsic TH-eGFP fluorescence to delineate striosome and matrix compartments. Overall, the distribution of the different TH-eGFP interneuronal subtypes did not differ in dorsal versus ventral striatum. However, striatal TH-eGFP interneurons were found to be mostly in the matrix in the dorsal striatum whereas a significantly higher proportion of these neurons was located in MOR-enriched domains of the ventral striatum. Further, the majority of striatal TH-eGFP interneurons was found to be located within 100 μm of a striosome–matrix boundary. Taken together, the current results suggest that TH-eGFP interneurons obey different organizational principles in dorsal versus ventral striatum, and may play a role in communication between striatal striosome and matrix compartments.

Highlights

Acquisition of motor learning and volitional initiation of behavior critically depend on faithful transfer of information among the components of the basal ganglia
In the cumulative distribution for the coronal orientation, a 45° horizontal line was drawn dorsal to the anterior commissure extending from the ventral most point of the lateral ventricle to the ventral-most point of the external capsule (Voorn et al, 2004) in order to mark the division between dorsal and ventral striatum
On the basis of this division, it was estimated that 81% (51/63) of the recorded and filled neurons were in the dorsal striatum with the remaining 19% (12/63) within the territory of the ventral striatum

Summary

Introduction

Acquisition of motor learning and volitional initiation of behavior critically depend on faithful transfer of information among the components of the basal ganglia. The striatum plays a pivotal role in the shaping of the ongoing activity of the tonically active basal ganglia nuclei, the substantia nigra pars reticulata and globus pallidus external segment, via different dopamine receptor expressing spiny projection neurons (SPNs) that give rise to the direct and indirect striatofugal pathways, respectively (Albin et al, 1989; Gerfen et al, 1990; Kawaguchi et al, 1990; Kita, 2001; Kita et al, 2006). The remaining neurons are all local interneurons. The latter display a remarkable degree of neurochemical and electrophysiological diversity (Kawaguchi et al, 1995; Rymar et al, 2004; Oorschot, 2010). The GABAergic interneurons are comprised of parvalbumin (PV)-expressing fast-spiking, neuropeptide Y (NPY)–somatostatin (SOM)–nitric oxide synthase (NOS) co-expressing, calretinin (CR)-expressing (Kawaguchi, 1993; Kawaguchi et al, 1995; Wu and Parent, 2000; Tepper, 2010), and tyrosine hydroxylase (TH)-expressing (Dubach et al, 1987; Tashiro et al, 1989a; Meredith et al, 1999; Mazloom and Smith, 2006; Tande et al, 2006; Huot et al, 2007) cells

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Conclusion