A Layer-specific Corticofugal Input to the Mouse Superior Colliculus

Abstract

In the auditory cortex (AC), corticofugal projections arise from each level of the auditory system and are considered to provide feedback "loops" important to modulate the flow of ascending information. It is well established that the cortex can influence the response of neurons in the superior colliculus (SC) via descending corticofugal projections. However, little is known about the relative contribution of different pyramidal neurons to these projections in the SC. We addressed this question by taking advantage of anterograde and retrograde neuronal tracing to directly examine the laminar distribution, long-range projections, and electrophysiological properties of pyramidal neurons projecting from the AC to the SC of the mouse brain. Here we show that layer 5 cortico-superior-collicular pyramidal neurons act as bandpass filters, resonating with a broad peak at ∼3 Hz, whereas layer 6 neurons act as low-pass filters. The dissimilar subthreshold properties of layer 5 and layer 6 cortico-superior-collicular pyramidal neurons can be described by differences in the hyperpolarization-activated cyclic nucleotide-gated cation h-current (Ih). Ih also reduced the summation of short trains of artificial excitatory postsynaptic potentials injected at the soma of layer 5, but not layer 6, cortico-superior-collicular pyramidal neurons, indicating a differential dampening effect of Ih on these neurons.

Thalamocortical and Intracortical Inputs Differentiate Layer-Specific Mouse Auditory Corticocollicular Neurons

“…Layer 5 corticocollicular neurons are morphologically and physiologically distinct from layer 5 neurons which project intracortically (Games and Winer, 1988;Llano and Sherman, 2009;Rock and Apicella, 2015). Layer 6 corticocollicular neurons, in contrast, are nonpyramidal, regular-spiking neurons with elongated somata and thin, but densely branching dendrites (Slater et al, 2013;Zurita et al, 2018). Therefore, similar to the corticothalamic system where layer 5 and layer 6 neurons have distinct roles in modulating the thalamus (Ojima, 1994;Reichova and Sherman, 2004;Llano and Sherman, 2009;Theyel et al, 2010), there are two major types of neurons comprising the corticocollicular projection.…”

Specialized Subpopulations of Deep-Layer Pyramidal Neurons in the Neocortex: Bridging Cellular Properties to Functional Consequences

“…Another particularly diverse subset of ET neurons located in L6 are termed corticothalamic (CT) neurons because of their projections to thalamus (Bourassa and Deschênes, 1995;Zhang and Deschênes, 1997;Briggs and Usrey, 2008;Ueta et al, 2013;Zurita et al, 2017;Chevée et al, 2018;Hasse et al, 2018). L6 CT neurons are comprised of several distinct subpopulations with disparate sublaminar distributions (see below) that project to primary sensory thalamus, higher-order thalamic nuclei, or both (Lévesque et al, 1996;Zhang and Deschênes, 1997;Thomson, 2010;Shima et al, 2016;Chevée et al, 2018).…”

Cortical projections to the two retinotopic maps of primate pulvinar are distinct

“…For now, it is uncertain why layer 6 neurons or layer 5 neurons are sometimes labeled with pulvinar injections, and sometimes not. However, it is worth noting that both layer 6 and layer 5 neurons in auditory cortex of mice were labeled by superior colliculus injections in a recent study (Zurita, Rock, Perkins, & Apicella, ), while previous studies found labeled neurons mainly in layer 5. Thus, projections of layer 5 and layer 6 neurons labeled by subcortical injections vary across studies of auditory cortex.…”