Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons

Abstract

1. Microelectrodes filled with horseradish peroxidase (HRP) were inserted in the superior colliculus (SC) of alert squirrel monkeys. Spontaneous eye movements were monitored in the dark during recording and intraaxonal injection of fibers carrying presaccadic signals. 2. Analysis of the relationship between neuronal activity and saccadic parameters indicates that saccade-related neurons can be functionally classified into: 1) vectorial long-lead burst neurons (n = 31), and 2) directional long-lead burst neurons. 3. Vectorial long-lead burst neurons have little if any spontaneous activity and burst intensely before spontaneous saccades within their movement fields with a latency of approximately 20 ms. Their cell bodies were recovered mostly (4/5) in the stratum opticum of the SC. The mediolateral and anteroposterior location of these tectal long-lead burst neurons (TLLBs) together with their movement fields are consistent with existing descriptions of the motor map of the deeper tectal layers. Due to their somatodendritic morphology and pattern of axonal trajectories, TLLBs belong to the T group of tectal efferent neurons that was described in our companion report. Through its branched axonal system each TLLB can relay a signal coding intended eye displacement to reticular targets of the predorsal bundle (PDB), contralateral tectum, ipsilateral mesencephalic reticular formation (MRF), and rostrally located ipsilateral targets of the SC, besides participating in intratectal information processing. 4. Recovered tectal neurons (n = 4) with activity not related to spontaneous saccades participate in the predorsal and ventral ascending tectofugal bundles as well as the projection to the ipsilateral mesencephalic reticular formation. They do not participate in the commissural projection of the SC and need not have recurrent collaterals. Due to their somatodendritic morphology and pattern of axonal trajectories, these cells belong to the X group of tectal efferent neurons that was described in the preceding paper. 5. Recovered cells of origin of directional long-lead burst fibers recorded in the SC (n = 5) are located in the tectorecipient portion of the MRF and their axonal terminals are entirely contained within the SC. The high-frequency portion of the discharge of these reticulotectal long-lead burst neurons (RTLLBs) precedes most contraversive saccades by approximately 19 ms.(ABSTRACT TRUNCATED AT 400 WORDS)

The Brain Stem Saccadic Burst Generator Encodes Gaze in Three-Dimensional Space

“…Because the modulation of primate SC neurons was observed to be more robust for purely conjugate than disconjugate saccades, it has been suggested that the SC is not tuned in three dimensions (Walton and Mays 2003). However, given that 1) the SC has strong anatomical connections to saccadic neurons in the PPRF and cMRF (Moschovakis et al 1988) and 2) neurons in both of these regions have been found to dynamically encode the movement of an individual eye (present study, Waitzman et al 2007) it is suggested that neurons in the SC should be reexamined for evidence of an individual eye command.…”

Macaque Frontal Eye Field Input to Saccade-Related Neurons in the Superior Colliculus

“…Two morphologically distinct types of output neurons have been identified in the superior colliculus stratum opticum and intermediate gray layers of squirrel monkeys (Moschovakis et al 1988a). T neurons located slightly more dorsally within the superior colliculus exhibit saccade-related burst activity during spontaneous eye movements, whereas the X class of neurons located more ventrally within the superior colliculus do not fire in association with spontaneous saccades and are believed to be analogous to the tecto-reticulo-spinal neurons identified in cats and may be the equivalent of prelude/build-up cells identified in macaque monkeys (Grantyn and Berthoz 1985;Moschovakis et al 1988b;Guitton 1985, 1986;Munoz and Wurtz 1995a). Both T and X neurons contribute to the efferent projections of the superior colliculus.…”

Through the eye, slowly; Delays and localization errors in the visual system

“…However, we do not know exactly how the computation that involves an eye-position signal (EPS) is implemented. Two main hypotheses have been offered: vector subtraction (postsaccadic 28,29 or presaccadic 30 ) and neuronal network 31 . When, in the double-step, the second stimulus is flashed shortly before the saccade, its signal might reach the brain after the saccade.…”