Neostriatal cell subtypes and their functional roles

doi:10.1016/S0168-0102(96)01134-0

Neuroscience Research

Volume 27, Issue 1, 1 January 1997, Pages 1-8

https://doi.org/10.1016/S0168-0102(96)01134-0 Get rights and content

Abstract

The neostriatum is considered to be involved in the induction of purposeful movements or in the suppression of other movements through the internal segment of the globus pallidus (GP; the entopeduncular nucleus in the rodents) and the substantia nigra (SN) to which the striatal spiny neurons project. To understand how the striatum fulfills these functions, it is necessary to know the physiological and morphological characteristics of its constituent neurons. Aspiny interneurons in the striatum are considered to receive various excitatory inputs and to contribute importantly to determining whether spiny projection neurons fire or not. Both spiny and aspiny striatal cells have been shown to be heterogeneous in their physiological, chemical and connection characteristics. In this article, how these cell subtypes are organized in the local circuitry of the striatum and their physiological roles in the basal ganglia are discussed.

Introduction

Striatal projection neurons are usually silent, but under some conditions, fire phasically in response to massive excitatory inputs from the neocortex (Wilson, 1995). The neurons in the output parts of the basal ganglia (the internal segment of the globus pallidus [GPi; the entopeduncular nucleus in rodents] and the substantia nigra pars reticulata [SNpr]) are inhibitory and fire continuously. Striatal projection neurons are also inhibitory and innervate the output parts of the basal ganglia (Fig. 1). Thus, phasic firing of striatal projection cells can phasically suppress firing of output cells of the basal ganglia (Hikosaka, 1991). As a result, the thalamic relay cells whose activity is normally being suppressed by the basal ganglia are released from their inhibition, resulting in enhancement of the activity of the frontal cortex. The regulation of firing of spiny projection cells in the neostriatum is likely to be critical for basal ganglia function. To facilitate understanding of the regulatory elements, the cellular organization of the striatum needs to be clarified (Bolam and Bennett, 1995) (Table 1).

Section snippets

GABAergic spiny projection cells (ramp depolarization cells)

Striatal projection cells are GABAergic spiny neurons with soma diameters of about 15 μm. Many collaterals branch from their axons before the axons exit the striatum. In addition to GABA, they synthesize neuropeptides, including substance P, dynorphin and enkephalin. In vivo, spiny cells fire not tonically, but rather transiently for up to several seconds (Wilson, 1993), and respond directly to stimulation from both the cortex and the thalamus. The resting potentials are hyperpolarized far from

GABAergic spiny cells are divided into subgroups based on their projecting sites and compartment location

Some of the spiny cells directly project to the SNpr (GABAergic cells) or substantia nigra pars compacta (SNpc) (dopaminergic cells) (Fig. 1) (Gerfen, 1992). Those cells projecting to the pars reticulata and the pars compacta are spatially segregated into different compartments, called the matrix (85% in area) and the patch or striosome (15%) respectively (Johnston et al., 1990). These two can be distinguished on the basis of several chemical markers. Immunohistochemically, the calcium-binding

Projection cell subtypes interact with each other through their axon collaterals and interneurons

As described above, spiny projection cells are divided into four classes: (1) substance P matrix cells innervating the GPe, the SNpr, and, in some cases, the GPi; (2) enkephalin matrix cells innervating only the GPe; (3) substance P patch cells innervating the SNpc; and (4) enkephalin patch cells innervating only the GPe. These four types are considered to be differentially involved in basal ganglia function, and may interact with each other within the striatum.

However, the dendrites and axons

Striatal interneurons inhibit or modulate the activity of projection cells in a feedforward manner from the cortex or the thalamus

There are strong afferent inputs to the striatum from the cortex (Kitai et al., 1976) with two types of cortical cells playing a role: (1) pyramidal cells projecting to the corpus callosum and innervating the contralateral cortex and striatum in addition to the ipsilateral striatum (crossed corticostriatal cells); and (2) pyramidal cells innervating the ipsilateral striatum and also projecting to the pyramidal tract (ipsilateral corticostriatal cells) (Fig. 1) (Cowan and Wilson, 1994; Lévesque

Concluding remarks

We do not know how corticostriatal excitatory inputs are processed within the striatum and coded to generate firing patterns for the four types of projection cells which modulate the activities of the SN and the GP. However, recent physiological and anatomical studies have allowed the following conclusions to be drawn for striatal circuits. (1) Striatal neurons are not uniform in cellular physiological properties and are heterogeneous in their firing patterns. The transformation from excitatory

Acknowledgements

I thank Drs Toshihiko Aosaki and Yoshiyuki Kubota for valuable discussions, and Drs Raymond Kado and Charles J. Wilson for comments on the manuscript.

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