On the Evolution of the Frontal Eye Field: Comparisons of Monkeys, Apes, and Humans

Schall, Jeffrey D.; Zinke, Wolf; Cosman, Josh; Schall, Michelle S; Paré, Martin; Pouget, Pierre

doi:10.1016/b978-0-12-804042-3.00130-5

Cited by 17 publications

(15 citation statements)

References 242 publications

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“…In macaques, the FEF is a cortical structure located at the bank of the arcuate sulcus, with large pyramidal neurons in layer 5, characteristic of cortical motor structures (Stanton, Deng, Goldberg, & McMullen, 1989; reviewed by Schall et al, 2017), whereas the SC is a multilayered subcortical structure located on the roof of midbrain (Mohler & Wurtz, 1976; reviewed by May, 2006). These two structures are intimately connected (Figure 1a): the FEF sends projections to the SC directly (Künzle, Akert, & Wurtz, 1976; Stanton, Goldberg, & Bruce, 1988a), and via the basal ganglia (Astruc, 1971; Hikosaka & Wurtz, 1983; Stanton, Goldberg, & Bruce, 1988b).…”

Section: Overview Of Sc and Fef Anatomy And Roles In Gaze Controlmentioning

confidence: 99%

Spatiotemporal transformations for gaze control

2020

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Sensorimotor transformations require spatiotemporal coordination of signals, that is, through both time and space. For example, the gaze control system employs signals that are time‐locked to various sensorimotor events, but the spatial content of these signals is difficult to assess during ordinary gaze shifts. In this review, we describe the various models and methods that have been devised to test this question, and their limitations. We then describe a new method that can (a) simultaneously test between all of these models during natural, head‐unrestrained conditions, and (b) track the evolving spatial continuum from target (T) to future gaze coding (G, including errors) through time. We then summarize some applications of this technique, comparing spatiotemporal coding in the primate frontal eye field (FEF) and superior colliculus (SC). The results confirm that these areas preferentially encode eye‐centered, effector‐independent parameters, and show—for the first time in ordinary gaze shifts—a spatial transformation between visual and motor responses from T to G coding. We introduce a new set of spatial models (T‐G continuum) that revealed task‐dependent timing of this transformation: progressive during a memory delay between vision and action, and almost immediate without such a delay. We synthesize the results from our studies and supplement it with previous knowledge of anatomy and physiology to propose a conceptual model where cumulative transformation noise is realized as inaccuracies in gaze behavior. We conclude that the spatiotemporal transformation for gaze is both local (observed within and across neurons in a given area) and distributed (with common signals shared across remote but interconnected structures).

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Section: Overview Of Sc and Fef Anatomy And Roles In Gaze Controlmentioning

confidence: 99%

Spatiotemporal transformations for gaze control

2020

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“…Finally, this review (but see also (Paus, 1996;Tehovnik et al, 2000;Amiez and Petrides, 2009;Vernet et al, 2014;Percheron et al, 2015;Schall et al, 2017) is proposing a new discussion for using fibers co-localizations between structures to study their evolution and function.…”

Section: Introductionmentioning

confidence: 99%

The comparative anatomy of frontal eye fields in primates

Petit

Pouget

2019

Cortex

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The frontal eye filed (FEF) is a relatively small frontal region that has been intensely studied. It received multiple definitions that help to locate it with some discrepancies between non-human primates and humans. The goal of this review is to provide an inter-species comparison of the location, extent, and boundaries of the FEF through the multiple anatomical and functional methodologies that has been used for its description as an oculomotor-associated area. We therefore propose a new orientation for using white matter fibers co-localizations between frontal structures to study their evolution and clarify the FEF homologies in primates.

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“…In most studied primates (e.g., macaques), FEF is granular, and is located in the arcuate sulcus where the most effective oculomotor effects of cortical stimulation are on its anterior wall. However, in the primates that do not have consistent or obvious arcuate sulcus because of their lisencephalic brains (e.g., squirrel monkeys), or do not have sulcus resembling arcuate (e.g., apes), the location of oculomotor area has mainly been determined by electrical stimulation (Huerta et al, ; Schall et al, ). In humans, the FEF location is based on functional imaging studies that placed it in agranular area 6 of Brodman (), or even in the primary motor area (Blanke et al, ; Luna et al, ; Paus, Marrett, Worsley, & Evans, ; Tehovnik, Sommer, Chou, Slocum, & Schiller, ), but not in granular area 8.…”

Section: Discussionmentioning

confidence: 99%

“…Recent anatomical studies reexamined the architecture of this region (comprising inferior and posterior precentral sulcus) using modern chemoarchitectonic methods in postmortem tissue (Rosano, Sweeney, Melchitzky, & Lewis, ; see also Schmitt et al, ), and described its histological features as resembling the macaque FEF more than agranular area 6. There is also suggestion that the FEF in the inferior precentral sulcus is homologous with the macaque FEF in the arcuate sulcus, while the FEF in the superior precentral sulcus is homologous with the premotor eye movement region caudal to the arcuate sulcus of macaques (Schall et al, ). Thus, defining the FEF (or brain areas in general) across species can be a difficult task and comparative studies may help identify those consistent features across phylogeny that can be used to identify homologous areas (see Percheron et al, ; Schall et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…There is also suggestion that the FEF in the inferior precentral sulcus is homologous with the macaque FEF in the arcuate sulcus, while the FEF in the superior precentral sulcus is homologous with the premotor eye movement region caudal to the arcuate sulcus of macaques (Schall et al, ). Thus, defining the FEF (or brain areas in general) across species can be a difficult task and comparative studies may help identify those consistent features across phylogeny that can be used to identify homologous areas (see Percheron et al, ; Schall et al, ). Truth comparison however, cannot be made until common methods are applied across all species.…”

Section: Discussionmentioning

confidence: 99%

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Frontal eye field in prosimian galagos: Intracortical microstimulation and tracing studies

Stepniewska

Pouget

Kaas

2017

J of Comparative Neurology

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The frontal eye field (FEF) in prosimian primates was identified as a small cortical region, above and anterior to the anterior frontal sulcus, from which saccadic eye movements were evoked with electrical stimulation. Tracer injections revealed FEF connections with cortical and subcortical structures participating in higher order visual processing. Ipsilateral cortical connections were the densest with adjoining parts of the dorsal premotor and prefrontal cortex (PFC). Label in a region corresponding to supplementary eye field (SEF) of other primates, suggests the existence of SEF in galagos. Other connections were with ventral premotor cortex (PMV), the caudal half of posterior parietal cortex, cingulate cortex, visual areas within the superior temporal sulcus, and inferotemporal cortex. Callosal connections were mostly with the region of the FEF of another hemisphere, SEF, PFC, and PMV. Most subcortical connections were ipsilateral, but some were bilateral. Dense bilateral connections were to caudate nuclei. Densest reciprocal ipsilateral connections were with the paralamellar portion of mediodorsal nucleus, intralaminar nuclei and magnocellular portion of ventral anterior nucleus. Other FEF connections were with the claustrum, reticular nucleus, zona incerta, lateral posterior and medial pulvinar nuclei, nucleus limitans, pretectal area, nucleus of Darkschewitsch, mesencephalic and pontine reticular formation and pontine nuclei. Surprisingly, the superior colliculus (SC) contained only sparse anterograde label. Although most FEF connections in galagos are similar to those in monkeys, the FEF-SC connections appear to be much less. This suggests that a major contribution of the FEF to visuomotor functions of SC emerged with the evolution of anthropoid primates.

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On the Evolution of the Frontal Eye Field: Comparisons of Monkeys, Apes, and Humans

Cited by 17 publications

References 242 publications

Spatiotemporal transformations for gaze control

Spatiotemporal transformations for gaze control

The comparative anatomy of frontal eye fields in primates

Frontal eye field in prosimian galagos: Intracortical microstimulation and tracing studies

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