Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport
Abstract
The purpose of these experiments was to study the subcortical input to the frontal eye field (FEF) and to determine which subcortical structures might project to the FEF via pathways that contain only a single intervening synapse. We used retrograde transneuronal transport of herpes simplex virus type 1 (HSV-1) to label second-order neurons that send information to the FEF of cebus monkeys. The saccade region of the FEF was identified physiologically using intracortical stimulation and then injected with a strain of HSV-1 known to be transported transneuronally in the retrograde direction. Retrograde transport of virus labeled neurons was observed in all the thalamic sites known to innervate the FEF. In addition, we found neurons labeled by transneuronal transport in three subcortical sites: the pars reticulata of the substantia nigra, the optic and intermediate gray layers of the superior colliculus, and a posterior portion of the dentate nucleus of the cerebellum. Each of these sites has been shown in prior studies to project to thalamic regions that innervate the FEF. Moreover, the neurons labeled through transneuronal transport were located in a subregion of each subcortical site that is known to be involved in oculomotor control. These observations demonstrate that signals from the substantia nigra, superior colliculus and dentate nucleus can have a significant influence on the output of the FEF.
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Electrophysiological recordings from a transiently inactivated circuit in the brain have shed light on how corollary discharge is used for saccadic sequencing in rhesus monkeys.
“Electrophysiological recordings from a transiently inactivated circuit in the brain have shed some light on how CD is used for saccadic sequencing in rhesus monkeys62,63,65 (FIG. 6Aa).”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [65]
When the midbrain-to-prefrontal pathway was inactivated by muscimol, behavioural deficits in the simplest saccadic sequencing task were observed.
“When this pathway was inactivated by muscimol, a GABAA (γ-aminobutyric acid receptor type A) agonist, behavioural deficits in the simplest saccadic sequencing task were observed.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [65]
Neurons that connect the midbrain to the prefrontal cortex transmit bursts of action potentials that encode saccadic parameters.
“Neurons that connect the midbrain to the prefrontal cortex transmit bursts of action potentials that encode saccadic parameters.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [65]
In this saccadic sequencing example, corollary discharge emerges from a lower-level motor structure and ascends the neuraxis to impinge on a higher-level executive centre.
“This is an example in which CD emerges from a lower-level motor structure and ascends the neuraxis to impinge on a higher-level executive centre (FIG. 6Ab).”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [65]
The results conformed to the prediction that impairing corollary discharge of the first eye movements would cause incorrect second saccades, revealing a loss of corollary discharge.
“The results conformed to this prediction, revealing a loss of CD.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [65]
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References 36 · Cited by 306
- Authors
- Lynch, J. C., Hoover, J. E., & Strick, P. L.
- Affiliations
- University of Mississippi Medical Center (US)
- Corresponding author
- Lynch, J.C.
- Venue
- Experimental Brain Research
- Published
- 1994-07
- Volume
- 100
- Issue
- 1
- Pages
- 181-6
- ISSN
- 0014-4819 (ISSN-L)
- 1432-1106
- OpenAlex
- W2051557753
- Cited by
- 306
- References
- 36
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 3 · 2023: 6 · 2022: 4 · 2021: 8 · 2020: 12 · 2019: 6 · 2018: 10 · 2017: 5 · 2016: 10 · 2015: 5 · 2014: 7 · 2013: 9 · 2012: 13
- FWCI
- 14.60
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Experimental Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ey004159-13)
- National Eye Institute (EY4159)
- National Institute of Neurological Disorders and Stroke (NS-24328, R01NS024328, NS2957)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- frontal eye field, substantia nigra pars reticulata, superior colliculus, dentate nucleus, cerebellum, thalamus, oculomotor control, subcortical projections, herpes simplex virus type 1, Cebus monkeys, second-order neurons
- MeSH terms
- Animals, Cebus, Electric Stimulation, Hippocampus, Histocytochemistry, Ocular Physiological Phenomena, Saccades, Substantia Nigra, Superior Colliculi, Thalamic Nuclei, Visual Fields, Visual Pathways, Herpesvirus 1, Human
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