Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons

Abstract

1. Neurons in the superior colliculus (SC) of anesthetized paralyzed squirrel monkeys were injected intracellularly with horseradish peroxidase (HRP) to establish a morphological classification of tectal efferent neurons in this species. These neurons were physiologically identified by their antidromic responses following stimulation of the contralateral predorsal bundle or SC. These cells also responded with postsynaptic potentials to stimulation of the ipsilateral substantia nigra and cerebral peduncle and the contralateral tectum. 2. Quantitative light microscopic analysis of the somatodendritic profiles and axonal trajectories of 27 recovered cells revealed the existence of three major groups of tectal efferent neurons: L (n = 7), X (n = 8), and T (n = 12). 3. L neurons are small or medium size cells with relatively elaborate dendritic trees and are located mainly in the superficial layers of the SC. They participate in the ipsilateral descending and dorsal ascending tectofugal bundles. Intrinsic collaterals of L axons deploy a large number of boutons both near the parent cell body and more ventrally within the deeper tectal layers. 4. X neurons are mostly large in size and multipolar in shape with relatively complex dendritic trees. Their cell bodies are situated mainly in the stratum griseum intermedium and occasionally in the stratum opticum. Axons of X neurons participate in the crossed descending and ipsilateral ventral ascending projections of the SC. In addition, the axonal system of about half of the X neurons includes recurrent collaterals. 5. T neurons are located mainly in the ventral stratum opticum and the dorsal stratum griseum intermedium. They have small or medium-sized, trapezoid or ovoid cell bodies and relatively simple radiating or vertical dendritic trees. Their axons usually participate in two of the major tectofugal bundles besides providing a commissural component and recurrent collaterals. 6. Morphological details revealed in the present study support the notion that distinct tectofugal axonal systems originate from efferent neurons of the primate SC that differ both as to their location in the tectum as well as the appearance of their somata and dendritic trees. The resulting morphological classification of tectal efferent cells provides a framework for the analysis of tectal function in terms of populations of identified neurons.

Nigral Inhibition of GABAergic Neurons in Mouse Superior Colliculus

“…We observed very long-latency IPSCs in some neurons compared with previous in vivo studies (Chevalier et al, 1981(Chevalier et al, , 1984Karabelas and Moschovakis, 1985;Moschovakis et al, 1988). Because we routinely bath applied antagonists for ionotropic glutamate receptors, these long-latency IPSCs were not attributed to disynaptic activation through glutamatergic axons inducing spikes in GABAergic neurons, which in turn innervate the SGI GABAergic neurons.…”

AnIn VitroStudy of Horizontal Connections in the Intermediate Layer of the Superior Colliculus

“…Second, the excitatory responses only were evoked within a region extending Ͻ500 m from soma. The spatial extent of this excitation approximates the combined radii of the terminal fields of the recurrent collaterals and the dendritic fields of cells in this layer Moschovakis et al, 1988;Hall and Lee, 1997). These excitatory connections could elevate activity locally toward the command threshold for a movement, but their spatial range is insufficient to mediate global inhibition by exciting remote inhibitory interneurons (Meredith and Ramoa, 1998).…”

Preparing to Move Increases the Sensitivity of Superior Colliculus Neurons

“…Thus, rather than considering the SC as the source of the modulation as recent stimulation results suggest, we explore here how selection and preparation signals influence SC sensory responses. Our second approach was to explore different neuronal types within the SC (Moschovakis et al, 1988(Moschovakis et al, , 1996Sparks and Hartwich-Young, 1989;Munoz and Wurtz, 1995;Horwitz and Newsome, 1999;McPeek and Keller, 2002;Rodgers et al, 2006). Because different neuron types in SC are differently involved in processing leading up to eye movements (Basso and Wurtz, 1998;McPeek and Keller, 2002), we reasoned that an understanding of how different neurons within the SC were modulated with cues to make saccades would shed light on mechanisms and circuits underlying selection for action.…”