Organization of long-range inputs and outputs of frontal cortex for top-down control

Abstract

Long-range projections from the frontal cortex are known to modulate sensory processing in multiple modalities. Although the mouse has become an increasingly important animal model for studying the circuit basis of behavior, the functional organization of its frontal cortical long-range connectivity remains poorly characterized. Here we used virus-assisted circuit mapping to identify the brain networks for top-down modulation of visual, somatosensory, and auditory processing. The visual cortex is reciprocally connected to the anterior cingulate area, whereas the somatosensory and auditory cortices are connected to the primary and secondary motor cortices. Anterograde and retrograde tracing identified the cortical and subcortical structures belonging to each network. Furthermore, using novel viral techniques to target subpopulations of frontal neurons projecting to the visual cortex versus the superior colliculus, we identified two distinct subnetworks within the visual network. These findings provide an anatomical foundation for understanding the brain mechanisms underlying top-down control of behavior.

Secondary Motor Cortex: Where ‘Sensory’ Meets ‘Motor’ in the Rodent Frontal Cortex

“…It has been suggested that rostral M2 receives more somatic sensorimotor inputs, whereas caudal M2 receives more sensory inputs [10,13]. There may also be regional differences: unlike Cg1 which primarily receives afferents from visual areas, M2 has auditory inputs in addition to visual afferents and may therefore be multi-modal [14]. …”

“…Regions targeted by prelimbic and infralimbic cortices, but not M2, include ventral striatum, periaqueductal grey, septum, ventral tegmental area, and a few others [18]. Depending on the efferent target, projection neurons in mPFC reside in different cortical layers [18], and can have distinct long-range axonal collaterals [14]. …”

Visual experience sculpts whole-cortex spontaneous infraslow activity patterns through an Arc-dependent mechanism

“…Previous work has demonstrated that rodent cingulate cortex has reciprocal connections with the visual area and projects to motor areas (64,65). In addition, visual stimulation can elicit evoked responses in the cingulate cortex (66), and direct electrical stimulation of cingulate cortex can elicit movement (67)(68)(69).…”

Anterior Cingulate Cortex Input to the Claustrum Is Required for Top-Down Action Control

“…Identified candidate top-down circuits arising from frontal cortices include direct inputs to posterior sensory cortices, thalamus, and claustrum (Miller and Buschman, 2013; Zhang et al, 2014; Mathur, 2014). Given that prefrontal cortex neurons can encode task performance differentially based on projection target (Otis et al, 2017), it is critical to determine which signals are being propagated to claustrum, for instance, and how these signals (Zhang et al, 2016). …”

“…However, it is unknown whether claustrum mediates top-down or bottom-up information flow (Mathur, 2014), sits atop the information processing hierarchy to bind sensory information for conscious perception (Crick and Koch, 2005), or exists solely as a satellite processer for cortices (Olson and Graybiel, 1980). Based on recent work showing that the rat claustrum receives a dense innervation from the anterior cingulate cortex (ACC; White et al, 2017), an area implicated in top-down attention (Zhang et al, 2014, 2016), we hypothesize that the claustrum is positioned to receive top-down input for cognitive control (Mathur, 2014). Testing this, we found that ACC input to the mouse claustrum encodes an anticipatory top-down signal that is proportional to task load and required for optimal performance accuracy.…”