Abstract
The mammalian superior colliculus (SC) is a sensorimotor midbrain structure responsible for orienting behaviors. Although many SC features are known, details of its intrinsic microcircuits are lacking. We used transgenic mice expressing reporter genes in parvalbumin-positive (PV+) and gamma aminobutyric acid-positive (GABA+) neurons to test the hypothesis that PV+ neurons co-localize GABA and form inhibitory circuits within the SC. We found more PV+ neurons in the superficial compared to the intermediate SC, although a larger percentage of PV+ neurons co-expressed GABA in the latter. Unlike PV+ neurons, PV+/GABA+ neurons showed predominantly rapidly inactivating spiking patterns. Optogenetic activation of PV+ neurons revealed direct and feedforward GABAergic inhibitory synaptic responses, as well as excitatory glutamatergic synapses. We propose that PV+ neurons in the SC may be specialized for a variety of circuit functions within the SC rather than forming a homogeneous, GABAergic neuronal subtype as they appear to in other regions of the brain.
Highlights
The mammalian superior colliculus (SC) is a midbrain structure specializing in translating sensory information into commands for orienting movements and redirecting attention
Most of the red PV+ neurons and neuropil in the structure. The superficial layers (sSC) lie in a band located in the lower portion of the stratum griseum superficiale (SGS)
The appearance of the PV labeling in the Ai9;PV-Cre mouse (Figure 1B, white arrows), is similar to that observed in rats using immunohistochemistry (Illing et al, 1990)
Summary
The mammalian superior colliculus (SC) is a midbrain structure specializing in translating sensory information into commands for orienting movements and redirecting attention (reviewed in, Basso and May, 2017). In all areas of the cerebral cortex studied far, as well as in hippocampus and striatum, PV appears almost exclusively in a subpopulation of GABAergic neurons (Gonchar et al, 2008; Klausberger and Somogyi, 2008; Tremblay et al, 2016) In cortex, these GABAergic neurons exhibit fast-spiking patterns and form direct inhibitory synapses with the somata, proximal dendrites, and initial segments of cortical pyramidal neurons (Kawaguchi et al, 1987; Kawaguchi, 1993; Kawaguchi and Kubota, 1993, 1997; Gupta, 2000; Markram et al, 2004; Taniguchi et al, 2011; Taniguchi, 2014; Tremblay et al, 2016). These GABAergic PV+ neurons play a key role in intrinsic inhibitory microcircuits in cortical and subcortical regions
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