Composition and Topographic Organization of Signals Sent From the Frontal Eye Field to the Superior Colliculus

Abstract

The frontal eye field (FEF) and superior colliculus (SC) contribute to saccadic eye movement generation, and much of the FEF's oculomotor influence may be mediated through the SC. The present study examined the composition and topographic organization of signals flowing from FEF to SC by recording from FEF neurons that were antidromically activated from rostral or caudal SC. The first and most general result was that, in a sample of 88 corticotectal neurons, the types of signals relayed from FEF to SC were highly diverse, reflecting the general population of signals within FEF rather than any specific subset of signals. Second, many neurons projecting from FEF to SC carried signals thought to reflect cognitive operations, namely tonic discharges during the delay period of a delayed-saccade task (delay signals), elevated discharges during the gap period of a gap task (gap increase signals), or both. Third, FEF neurons discharging during fixation were found to project to the SC, although they did not project preferentially to rostral SC, where similar fixation neurons are found. Neurons that did project preferentially to the rostral SC were those with foveal visual responses and those pausing during the gap period of the gap task. Many of the latter neurons also had foveal visual responses, presaccadic pauses in activity, and postsaccadic increases in activity. These two types of rostral-projecting neurons therefore may contribute to the activity of rostral SC fixation neurons. Fourth, conduction velocity was used as an indicator of cell size to correct for sampling bias. The outcome of this correction procedure suggested that among the most prevalent neurons in the FEF corticotectal population are those carrying putative cognitive-related signals, i.e., delay and gap increase signals, and among the least prevalent are those carrying presaccadic burst discharges but lacking peripheral visual responses. Fifth, corticotectal neurons carrying various signals were biased topographically across the FEF. Neurons with peripheral visual responses but lacking presaccadic burst discharges were biased laterally, neurons with presaccadic burst discharges but lacking peripheral visual responses were biased medially, and neurons carrying delay or gap increase signals were biased dorsally. Finally, corticotectal neurons were distributed within the FEF as a function of their visual or movement field eccentricity and projected to the SC such that eccentricity maps in both structures were closely aligned. We conclude that the FEF most likely influences the activity of SC neurons continuously from the start of fixation, through visual analysis and cognitive manipulations, until a saccade is generated and fixation begins anew. Furthermore, the projection from FEF to SC is highly topographically organized in terms of function at both its source and its termination.

How laminar frontal cortex and basal ganglia circuits interact to control planned and reactive saccades

“…The model thus predicts that a significant population of presaccadic cells will be found in layer V, as reported previously by Segraves and Goldberg ( 1987). More recently, Sommer and Wurtz (2000) examined cells in FEF (presumably layer V) that project to the SC. They found presaccadic cells as well as a variety of cell types whose responses were not restricted to presaccadic, movement-related activity.…”

“…Their results suggest that additional signals may be processed in layer V beyond those modeled here. We have not attempted to model the FEF layer V projections to brainstem oculomotor areas (Schnyder et al, 1985), although the present model would suggest a significant presaccadic activity component in this projection, which could be -32-investigated using the method of Sommer and Wurtz (2000).…”

The involvement of the fronto-parietal brain network in oculomotor sequence learning using fMRI

“…It is clear that this network is essential for spatial attention during unpredictable saccade generation (Campana, Cowey, Casco, Oudsen, & Walsh, 2007) and mediating search strategies (Lane, Smith, Schenk, & Ellison, 2012), however the role of PPC -FEF network in predictable tasks in pursuit is less clear. Further evidence shows modulation of activity during single predictable saccades in FEF during single-unit recordings in monkeys (Sommer & Wurtz, 2000). The present study has shown that an area related to medial FEF or lateral SEF is important in oculomotor learning (both pursuit and saccades) of sequences of movements, and importantly, we have found the pattern of activity within these regions hold the key to this learning mechanism.…”

Control of eye movements and spatial attention

“…Our effects could thus have resulted from direct antidromic stimulation of neurons forming connections with the FEF, rather than from activation of neurons within the FEF, and the subsequent activation of structures to which the FEF projects. Although antidromic activation typically requires current levels greater than that used here (median ϭ 10 A) (20,21), we cannot rule out the contribution such activation may have made to our results. Moreover, the FEF is heavily interconnected with other cortical and subcortical structures, such as the superior colliculus and the lateral intraparietal area (LTP) (22), both of which are known to be involved in oculomotor behavior and spatial attention (13, [23][24].…”