Figure. Organization, Extrinsic Connections, and Internal Circuits in the Superior Colliculus.

The superior colliculus (SC) has a laminar structure consisting of superficial, middle, and deep layers. The superficial (visuosensory) layer receives afferents from the retina, lateral geniculate nucleus (LGN), primary visual cortex (V1), and medial temporal visual area (MT/V5). The intermediate and deep layers receive inputs from the frontal eye field (FEF), intraparietal sulcus (IPS, parietal eye field), substantia nigra pars reticulata (SNr), inferior colliculus, and contralateral spinal cord. Brainstem modulatory inputs to the SC originate from the parabigeminal nucleus (PBG), pedunculopontine nucleus (PPN), laterodorsal tegmental nucleus (LTD), locus ceruleus (LC), and dorsal raphe (not shown). Superficial layer neurons project to the medial subnucleus of the inferior pulvinar, which in turn targets area MT/V5, and to the dorsal LGN, which targets V1. Neurons in the intermediate and deep layers provide a crossed descending projection (dotted lines) to innervate the saccadic control circuit, which includes excitatory burst neurons (EBNs) and inhibitory burst neurons (IBNs) targeted by the caudal pole of the SC and omnipause neurons (OPN) targeted by the rostral pole. The crossed descending axons from the SC descend areas of the reticular formation containing reticulospinal neurons and then reach the cervical spinal cord targeting primarily interneurons. Ascending projections from the middle and deep layers include collateral projections from saccadic neurons to the mediodorsal (MD) nucleus of the thalamus, which in turn projects to the FEF; projections to the centromedian/parafascicular (CMn/Pf) nuclei, which target the caudate nucleus (Cd); and projections to the medial pulvinar, which projects to the amygdala. The SC also sends inputs to the substantia nigra pars compacta, ventral tegmental area, subthalamic nucleus, PPN/LDT, and periaqueductal gray (not shown). Local circuits in the SC are critical for multisensory integration for orienting responses, visuospatial attention, and perceptual decision-making. Neurons in the intermediate and deep layers receive inputs from the visuosensory neurons of the superficial layer, are organized into a motor map in register with the visual map, and integrate visual with auditory inputs from the inferior colliculus and somatosensory inputs from the cervical spinal cord and dorsal column nuclei. Recurrent collaterals from the intermediate to the superficial layer may either excite superficial layer neurons projecting to the deep layers or, through GABAergic interneurons, suppress the activity of superficial layer neurons projecting to the pulvinar and dLGN. The SC receives input from the FEF and IPS, which are components of the dorsal attention network involved in goal-oriented visuospatial attention. These inputs trigger voluntary and reflex saccades. The FEF also projects to the Cd, which inhibits GABAergic neurons of the SNr projecting to the SC. Reciprocally, saccadic neurons of the SC send signals to the FEF through the MD. A signal from the deep layers of the SC modulates the sensory responsiveness of neurons in the superficial layers. Cholinergic input from the PBG and PPN/LDT may create focal excitation and global surround inhibition mediated by local GABAergic neurons within the SC. Dopaminergic projections from the LC modulate visual threat processing through GABAergic neurons at the intermediate layers of the SC.