Segregated anatomical input to sub-regions of the rodent superior colliculus associated with approach and defense

Abstract

The superior colliculus (SC) is responsible for sensorimotor transformations required to direct gaze toward or away from unexpected, biologically salient events. Significant changes in the external world are signaled to SC through primary multisensory afferents, spatially organized according to a retinotopic topography. For animals, where an unexpected event could indicate the presence of either predator or prey, early decisions to approach or avoid are particularly important. Rodents' ecology dictates predators are most often detected initially as movements in upper visual field (mapped in medial SC), while appetitive stimuli are normally found in lower visual field (mapped in lateral SC). Our purpose was to exploit this functional segregation to reveal neural sites that can bias or modulate initial approach or avoidance responses. Small injections of Fluoro-Gold were made into medial or lateral sub-regions of intermediate and deep layers of SC (SCm/SCl). A remarkable segregation of input to these two functionally defined areas was found. (i) There were structures that projected only to SCm (e.g., specific cortical areas, lateral geniculate and suprageniculate thalamic nuclei, ventromedial and premammillary hypothalamic nuclei, and several brainstem areas) or SCl (e.g., primary somatosensory cortex representing upper body parts and vibrissae and parvicellular reticular nucleus in the brainstem). (ii) Other structures projected to both SCm and SCl but from topographically segregated populations of neurons (e.g., zona incerta and substantia nigra pars reticulata). (iii) There were a few brainstem areas in which retrogradely labeled neurons were spatially overlapping (e.g., pedunculopontine nucleus and locus coeruleus). These results indicate significantly more structures across the rat neuraxis are in a position to modulate defense responses evoked from SCm, and that neural mechanisms modulating SC-mediated defense or appetitive behavior are almost entirely segregated.

Keywords: approach; defense; segregated anatomical inputs; superior colliculus.

Figure 1

SC’s spacial maps. Illustration shows that predator movements in the upper visual field are detected in the medial sub-region of the rodent SC’s retinotopically organized map, which promotes defense-like responses. Whisker-related somatosensory stimuli associated with prey are detected in the lateral sub-region of the SC which evokes approach and appetitive behavior.

Figure 2

Sub-regions of the SC. On the left a photomicrograph of the SC’s cytoarchitecture (Nissl stained). Layers are identified in a reflected schematic (right). The medial/lateral sub-regions approximates the horizontal meridian in the collicular map of visual space.

Figure 3

Schematic representation of the FG injection sites into the medial and lateral sub-regions of SC. Lines indicate each injection site. Light gray represents the areas included in the population of all medial and lateral injection sites and dark gray shows the injection sites chosen as representative of the medial and lateral injection populations. Abbreviations: see list.

Figure 4

Photomicrographs of transverse sections of the rat brain showing representative cases with FG injection into the SCm (A) and SCl (B). Respective adjacent sections show the SC cytoarchitecture stained with Nissl stain (C,D). Abbreviations: see list.

Figure 5

Distribution of retrogradely labeled cells after a FG injection into SCm (left side-red dots) and SCl (right side-green dots). Open squares indicate which levels the pictures in Figures 6–8 were taken from. A photomicrograph of the injection sites is illustrated in Figure 4. Abbreviations: see list.

Figure 5

Distribution of retrogradely labeled cells after a FG injection into SCm (left side-red dots) and SCl (right side-green dots). Open squares indicate which levels the pictures in Figures 6–8 were taken from. A photomicrograph of the injection sites is illustrated in Figure 4. Abbreviations: see list.

Figure 5

Distribution of retrogradely labeled cells after a FG injection into SCm (left side-red dots) and SCl (right side-green dots). Open squares indicate which levels the pictures in Figures 6–8 were taken from. A photomicrograph of the injection sites is illustrated in Figure 4. Abbreviations: see list.

Figure 6

Photomicrographs of transverse sections of the rat brain showing some of the areas with exclusive FG-stained cells from a rat injected into the SCm (A–F) or into the SCl (G,H). Abbreviations: see list.

Figure 7

Photomicrographs of transverse sections of the rat brain showing some of the areas with differential topography of FG-stained cells from a rat injected into the SCm (A,C,E,G,I) or into the SCl (B,D,F,H,J). Abbreviations: see list.

Figure 8

Photomicrographs of transverse sections of the rat brain showing some of the areas with similar topography of FG-stained cells from a rat injected into the SCm (A,C) or into the SCl (B,D). Abbreviations: see list.

Figure 9

Summary of the functional inputs to sub-regions of the rat SC associated with approach and defense responses.