Local and afferent synaptic pathways in the striatal microcircuitry

doi:10.1016/j.conb.2015.05.002

Current Opinion in Neurobiology

Volume 33, August 2015, Pages 182-187

https://doi.org/10.1016/j.conb.2015.05.002 Get rights and content

Highlights

•
The striatum acts as a ‘hub’ that receives afferent inputs from multiple pathways.
•
Recent studies have characterized several new types of striatal interneurons.
•
Intrastriatal connectivity between interneurons is selective and target-dependent.
•
New GABAergic, cholinergic, and dopaminergic afferents have been discovered and characterized.

The striatum is the largest structure of the basal ganglia, receiving synaptic input from multiple regions including the neocortex, thalamus, external globus pallidus, and midbrain. Earlier schemes of striatal connectivity presented a relatively simple architecture which included primarily excitatory input from the neocortex, dopaminergic input from the midbrain, and intrastriatal connectivity between projection neurons and a small number of interneuron types. In recent years this picture has changed, largely due to the introduction of new experimental methods to reveal cell types and their connectivity. The striatal microcircuit is now considered to consist of several newly defined neuron types which are intricately and selectively interconnected. New afferent pathways have been discovered, as well as novel properties of previously known afferents such as the midbrain dopaminergic inputs. In this review we aim to provide a summary of these recent discoveries.

Section snippets

Striatal neuron types

The striatum consists of a majority of projection neurons, the medium spiny neurons (MSNs) and a small, yet diverse population of interneurons. Interneurons were initially divided into four subtypes, including three types of GABAergic interneurons, and the tonically active cholinergic interneurons [1, 2]. These electrophysiologically defined subtypes also fitted a molecular profile based on immunostaining for markers such as parvalbumin (PV), calretinin (CR), somatostatin (SOM), and

Striatal interneuron connectivity

Striatal interneurons of the different types are instrumental in sculpting striatal output via intrastriatal synaptic connections. Perhaps the most prominent of the intrastriatal synapses are the GABAergic synapses formed between FS interneurons and MSNs [16] (Figure 1). These synapses are characterized by a very high connection probability, with each FS interneuron contacting a majority of its neighboring (within ∼100 μm radius) MSNs [17]. A single FS-MSN IPSP is sufficient to alter the

Striatal afferents

The striatum acts as a hub upon which numerous streams of information converge from different brain regions, mediated by different types of neurotransmitter. In recent years several new pathways have been discovered and characterized that are likely to have profound effects on the flow of information through the striatum (Figure 2).

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Acknowledgements

We thank Sten Grillner, Andrew Sharott, and Natalie Doig for comments on early versions of the manuscript. This work was supported by the Medical Research Council UK, the European Research Council, the Knut & Alice Wallenberg Foundation, and the Karolinska Institutet Strategic research program in Neuroscience (StratNeuro).

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View full text

Local and afferent synaptic pathways in the striatal microcircuitry

Highlights

Section snippets

Striatal neuron types

Striatal interneuron connectivity

Striatal afferents

Conflict of interest statement

References and recommended reading

Acknowledgements

Trends Neurosci

Curr Opin Neurobiol

Neuron

Neuron

J Neurosci

Neuron

PLOS ONE

J Physiol

Eur J Neurosci

J Neurosci

J Neurosci

Electrophysiological and morphological characteristics and synaptic connectivity of tyrosine hydroxylase-expressing neurons in adult mouse striatum

J Neurosci

Anatomical and electrophysiological changes in striatal TH interneurons after loss of the nigrostriatal dopaminergic pathway

Brain Struct Funct

Are striatal tyrosine hydroxylase interneurons dopaminergic?

J Neurosci

A novel functionally distinct subtype of striatal neuropeptide Y interneuron

J Neurosci

Complex autonomous firing patterns of striatal low-threshold spike interneurons

J Neurophysiol

Spontaneous activity of neostriatal cholinergic interneurons in vitro

J Neurosci

Relationships between the firing of identified striatal interneurons and spontaneous and driven cortical activities in vivo

J Neurosci

The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors

J Neurosci

Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons

Dev Neurobiol

Novel striatal GABAergic interneuron populations labeled in the 5HT3aEGFP mouse

Cereb Cortex

Novel fast adapting interneurons mediate cholinergic-induced fast GABA IPSCs in striatal spiny neurons

Eur J Neurosci

Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq

Science

Inhibitory control of neostriatal projection neurons by GABAergic interneurons

Nat Neurosci

Dynamics of synaptic transmission between fast-spiking interneurons and striatal projection neurons of the direct and indirect pathways

J Neurosci

Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo

J Neurosci

Distinct roles of GABAergic interneurons in the regulation of striatal output pathways

J Neurosci

Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex

Nat Neurosci

Pyramidal cell communication within local networks in layer 2/3 of rat neocortex

J Physiol

Dense, unspecific connectivity of neocortical parvalbumin-positive interneurons: a canonical microcircuit for inhibition?

J Neurosci

Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity

Nat Neurosci