Segregated fronto‐cortical and midbrain connections in the mouse and their relation to approach and avoidance orienting behaviors

Abstract

The orchestration of orienting behaviors requires the interaction of many cortical and subcortical areas, for example the superior colliculus (SC), as well as prefrontal areas responsible for top–down control. Orienting involves different behaviors, such as approach and avoidance. In the rat, these behaviors are at least partially mapped onto different SC subdomains, the lateral (SCl) and medial (SCm), respectively. To delineate the circuitry involved in the two types of orienting behavior in mice, we injected retrograde tracer into the intermediate and deep layers of the SCm and SCl, and thereby determined the main input structures to these subdomains. Overall the SCm receives larger numbers of afferents compared to the SCl. The prefrontal cingulate area (Cg), visual, oculomotor, and auditory areas provide strong input to the SCm, while prefrontal motor area 2 (M2), and somatosensory areas provide strong input to the SCl. The prefrontal areas Cg and M2 in turn connect to different cortical and subcortical areas, as determined by anterograde tract tracing. Even though connectivity pattern often overlap, our labeling approaches identified segregated neural circuits involving SCm, Cg, secondary visual cortices, auditory areas, and the dysgranular retrospenial cortex likely to be involved in avoidance behaviors. Conversely, SCl, M2, somatosensory cortex, and the granular retrospenial cortex comprise a network likely involved in approach/appetitive behaviors.

The mouse cortico-tectal projectome

“…These medial SC zones send outputs to the RE, CM, and IAM shown to be activated during arousal and the presence of visual threats 69,70 . Our results also reveal an interesting divergent ILA→SC.m/l projection pathway that is consistent with the role of ILA in mediating fear extinction, risk assessment and evaluation to threat situations, particularly to looming stimuli and predators 17,18,57,71 .…”

“…(Figure 6c). These findings are congruent with functional networks implicating the lateral SC in appetitive and approach behaviors 17,18 .…”

“…For each newly defined SC zone, we describe the complex alignment of sensory, somatic sensorimotor, and higher-order cortico-tectal projections that coincide with functional subnetworks for navigation, defense, decision-making, and action selection 1,17,18 .…”

Cross‐modal modulation of cell activity by sound in first‐order visual thalamic nucleus

“…A candidate of subcortical source of auditory influence on the DLG is the superior colliculus (SC), which, receiving excitatory and inhibitory auditory inputs (Kimura, Donishi, Okamoto, & Tamai, ; Mellott, Beebe, & Schofield, ), integrates auditory information into visual processing for orienting behaviors (Costa, Piché, Lepore, & Guillemot, ; Meredith & Stein, ; Savage, McQuade, & Thiele, ). Recently, the superficial layers of the SC, the source of tectal afferents to the DLG, have been shown to be subject to auditory influence (Ghose, Maier, Nidiffer, & Wallace, ).…”

Cortical projections to the superior colliculus in grey squirrels (Sciurus carolinensis)

“…Most of the terminal label described in Gould et al ., was located within the lateral superior colliculus, a region of the superior colliculus not injected in our present study. Differences between medial and lateral superior colliculus connections with both cortical and subcortical structures have been reported in rats, mice and tree shrews (Dean et al ., ; Sahibzada et al ., ; Chomsung et al ., ; Furigo et al ., ; Favaro et al ., ; Comoli et al ., ; Savage et al ., ).…”