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Visual and motor connectivity and the distribution of calcium-binding proteins in macaque frontal eye field: implications for saccade target selection.

Pouget P, Stepniewska I, Crowder EA, Leslie MW, Emeric EE, Nelson MJ, Schall JD - Front Neuroanat (2009)

Bottom Line: We found that the neurons in FEF that project to V4 + TEO are located predominantly in the supragranular layers, colocalized with the highest density of calbindin- and calretinin-immunoreactive inhibitory interneurons.In contrast, the cell bodies of neurons that project to SC are found only in layer 5 of FEF, colocalized primarily with parvalbumin inhibitory interneurons.These results provide useful constraints for cognitive models of visual attention and saccade production by indicating that different populations of neurons project to extrastriate visual cortical areas and to SC.

View Article: PubMed Central - PubMed

Affiliation: Center for Integrative and Cognitive Neuroscience, Vanderbilt Vision Research Center, Department of Psychology, Vanderbilt University Nashville, TN, USA.

ABSTRACT
The frontal eye field (FEF) contributes to directing visual attention and saccadic eye movement through intrinsic processing, interactions with extrastriate visual cortical areas (e.g., V4), and projections to subcortical structures (e.g., superior colliculus, SC). Several models have been proposed to describe the relationship between the allocation of visual attention and the production of saccades. We obtained anatomical information that might provide useful constraints on these models by evaluating two characteristics of FEF. First, we investigated the laminar distribution of efferent connections from FEF to visual areas V4 + TEO and to SC. Second, we examined the laminar distribution of different populations of GABAergic neurons in FEF. We found that the neurons in FEF that project to V4 + TEO are located predominantly in the supragranular layers, colocalized with the highest density of calbindin- and calretinin-immunoreactive inhibitory interneurons. In contrast, the cell bodies of neurons that project to SC are found only in layer 5 of FEF, colocalized primarily with parvalbumin inhibitory interneurons. None of the neurons in layer 5 that project to V4 + TEO also project to SC. These results provide useful constraints for cognitive models of visual attention and saccade production by indicating that different populations of neurons project to extrastriate visual cortical areas and to SC. This finding also suggests that FEF neurons projecting to visual cortex and SC are embedded in different patterns of intracortical circuitry.

No MeSH data available.


Related in: MedlinePlus

Locations of tracer injection sites in the superior colliculus (SC) and extrastriate visual areas V4 and TEO. Injection sites in monkeys N and R are shown on the dorsal view of SC reconstructed from the series of (A) coronal or (C) sagittal sections. In both monkeys, injections in SC (orange) cover the central part of SC. Injections in visual cortex (injection zone – black, diffusion zone – dark gray) are shown on the surface view of flattened cortex (B,E) and on the series of sagittal sections (D). Borders of areas V1, V2, MT, and MST/STP (blue dashed lines) were determined from adjacent sections stained for cytochrome oxidase and myelinated fibers. In flattened cortex opened sulci are shaded light gray and outlined in green. Abbreviations used are as follows:ArcS – arcuate sulcus, CS – central sulcus, CalS – calcarine sulcus, IOS – inferior occipital sulcus, IPS – intraparietal sulcus, LuS – lunate sulcus, MST – middle superior temporal visual area, MT – middle temporal area, OTS – occipito-temporal sulcus, PMTS – posterior medial temporal sulcus, PrCS – precentral sulcus, PS – principal sulcus, PsCs – postcentral sulcus, STS – superior temporal sulcus, Visual areas: MST – middle superior temporal visual area, MT – middle temporal area, STP – superior temporal polysensory area, TEO – caudal inferotemporal area, V1 – primary visual area, V2 – second visual area, V4 – fourth visual area.
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Figure 1: Locations of tracer injection sites in the superior colliculus (SC) and extrastriate visual areas V4 and TEO. Injection sites in monkeys N and R are shown on the dorsal view of SC reconstructed from the series of (A) coronal or (C) sagittal sections. In both monkeys, injections in SC (orange) cover the central part of SC. Injections in visual cortex (injection zone – black, diffusion zone – dark gray) are shown on the surface view of flattened cortex (B,E) and on the series of sagittal sections (D). Borders of areas V1, V2, MT, and MST/STP (blue dashed lines) were determined from adjacent sections stained for cytochrome oxidase and myelinated fibers. In flattened cortex opened sulci are shaded light gray and outlined in green. Abbreviations used are as follows:ArcS – arcuate sulcus, CS – central sulcus, CalS – calcarine sulcus, IOS – inferior occipital sulcus, IPS – intraparietal sulcus, LuS – lunate sulcus, MST – middle superior temporal visual area, MT – middle temporal area, OTS – occipito-temporal sulcus, PMTS – posterior medial temporal sulcus, PrCS – precentral sulcus, PS – principal sulcus, PsCs – postcentral sulcus, STS – superior temporal sulcus, Visual areas: MST – middle superior temporal visual area, MT – middle temporal area, STP – superior temporal polysensory area, TEO – caudal inferotemporal area, V1 – primary visual area, V2 – second visual area, V4 – fourth visual area.

Mentions: We determined the laminar distribution of FEF neurons labeled by simultaneous injections of different retrograde tracers in the SC and extrastriate visual areas V4 and TEO in three macaque monkeys. For two of these monkeys the tracers injected in both SC and V4 successfully transported to the FEF. Unfortunately, in the third monkey (T) the tracer injected into SC was not transported (Table 1), so partial data for this case will be described. The uptake regions for injected tracers are shown in Figure 1. The dorsal view of the SC injection site was reconstructed from 23 coronal sections in the first case (N) and from 19 sagittal sections in the second case (R). In both monkeys N and R injections covered an area in the central portion of the SC, spanning the superficial and intermediate layers. Cortical injections resulting in FEF labeling were made in the dorsolateral visual cortex (Figures 1B,D,E), just anterior to the lunate sulcus and posterior to the superior temporal sulcus in the vicinity of area V4 and caudal TEO (Desimone and Ungerleider, 1986; Gattass et al., 1988; Stepniewska et al., 2005). In none of the cases did the injection site penetrate white matter.


Visual and motor connectivity and the distribution of calcium-binding proteins in macaque frontal eye field: implications for saccade target selection.

Pouget P, Stepniewska I, Crowder EA, Leslie MW, Emeric EE, Nelson MJ, Schall JD - Front Neuroanat (2009)

Locations of tracer injection sites in the superior colliculus (SC) and extrastriate visual areas V4 and TEO. Injection sites in monkeys N and R are shown on the dorsal view of SC reconstructed from the series of (A) coronal or (C) sagittal sections. In both monkeys, injections in SC (orange) cover the central part of SC. Injections in visual cortex (injection zone – black, diffusion zone – dark gray) are shown on the surface view of flattened cortex (B,E) and on the series of sagittal sections (D). Borders of areas V1, V2, MT, and MST/STP (blue dashed lines) were determined from adjacent sections stained for cytochrome oxidase and myelinated fibers. In flattened cortex opened sulci are shaded light gray and outlined in green. Abbreviations used are as follows:ArcS – arcuate sulcus, CS – central sulcus, CalS – calcarine sulcus, IOS – inferior occipital sulcus, IPS – intraparietal sulcus, LuS – lunate sulcus, MST – middle superior temporal visual area, MT – middle temporal area, OTS – occipito-temporal sulcus, PMTS – posterior medial temporal sulcus, PrCS – precentral sulcus, PS – principal sulcus, PsCs – postcentral sulcus, STS – superior temporal sulcus, Visual areas: MST – middle superior temporal visual area, MT – middle temporal area, STP – superior temporal polysensory area, TEO – caudal inferotemporal area, V1 – primary visual area, V2 – second visual area, V4 – fourth visual area.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC2691655&req=5

Figure 1: Locations of tracer injection sites in the superior colliculus (SC) and extrastriate visual areas V4 and TEO. Injection sites in monkeys N and R are shown on the dorsal view of SC reconstructed from the series of (A) coronal or (C) sagittal sections. In both monkeys, injections in SC (orange) cover the central part of SC. Injections in visual cortex (injection zone – black, diffusion zone – dark gray) are shown on the surface view of flattened cortex (B,E) and on the series of sagittal sections (D). Borders of areas V1, V2, MT, and MST/STP (blue dashed lines) were determined from adjacent sections stained for cytochrome oxidase and myelinated fibers. In flattened cortex opened sulci are shaded light gray and outlined in green. Abbreviations used are as follows:ArcS – arcuate sulcus, CS – central sulcus, CalS – calcarine sulcus, IOS – inferior occipital sulcus, IPS – intraparietal sulcus, LuS – lunate sulcus, MST – middle superior temporal visual area, MT – middle temporal area, OTS – occipito-temporal sulcus, PMTS – posterior medial temporal sulcus, PrCS – precentral sulcus, PS – principal sulcus, PsCs – postcentral sulcus, STS – superior temporal sulcus, Visual areas: MST – middle superior temporal visual area, MT – middle temporal area, STP – superior temporal polysensory area, TEO – caudal inferotemporal area, V1 – primary visual area, V2 – second visual area, V4 – fourth visual area.
Mentions: We determined the laminar distribution of FEF neurons labeled by simultaneous injections of different retrograde tracers in the SC and extrastriate visual areas V4 and TEO in three macaque monkeys. For two of these monkeys the tracers injected in both SC and V4 successfully transported to the FEF. Unfortunately, in the third monkey (T) the tracer injected into SC was not transported (Table 1), so partial data for this case will be described. The uptake regions for injected tracers are shown in Figure 1. The dorsal view of the SC injection site was reconstructed from 23 coronal sections in the first case (N) and from 19 sagittal sections in the second case (R). In both monkeys N and R injections covered an area in the central portion of the SC, spanning the superficial and intermediate layers. Cortical injections resulting in FEF labeling were made in the dorsolateral visual cortex (Figures 1B,D,E), just anterior to the lunate sulcus and posterior to the superior temporal sulcus in the vicinity of area V4 and caudal TEO (Desimone and Ungerleider, 1986; Gattass et al., 1988; Stepniewska et al., 2005). In none of the cases did the injection site penetrate white matter.

Bottom Line: We found that the neurons in FEF that project to V4 + TEO are located predominantly in the supragranular layers, colocalized with the highest density of calbindin- and calretinin-immunoreactive inhibitory interneurons.In contrast, the cell bodies of neurons that project to SC are found only in layer 5 of FEF, colocalized primarily with parvalbumin inhibitory interneurons.These results provide useful constraints for cognitive models of visual attention and saccade production by indicating that different populations of neurons project to extrastriate visual cortical areas and to SC.

View Article: PubMed Central - PubMed

Affiliation: Center for Integrative and Cognitive Neuroscience, Vanderbilt Vision Research Center, Department of Psychology, Vanderbilt University Nashville, TN, USA.

ABSTRACT
The frontal eye field (FEF) contributes to directing visual attention and saccadic eye movement through intrinsic processing, interactions with extrastriate visual cortical areas (e.g., V4), and projections to subcortical structures (e.g., superior colliculus, SC). Several models have been proposed to describe the relationship between the allocation of visual attention and the production of saccades. We obtained anatomical information that might provide useful constraints on these models by evaluating two characteristics of FEF. First, we investigated the laminar distribution of efferent connections from FEF to visual areas V4 + TEO and to SC. Second, we examined the laminar distribution of different populations of GABAergic neurons in FEF. We found that the neurons in FEF that project to V4 + TEO are located predominantly in the supragranular layers, colocalized with the highest density of calbindin- and calretinin-immunoreactive inhibitory interneurons. In contrast, the cell bodies of neurons that project to SC are found only in layer 5 of FEF, colocalized primarily with parvalbumin inhibitory interneurons. None of the neurons in layer 5 that project to V4 + TEO also project to SC. These results provide useful constraints for cognitive models of visual attention and saccade production by indicating that different populations of neurons project to extrastriate visual cortical areas and to SC. This finding also suggests that FEF neurons projecting to visual cortex and SC are embedded in different patterns of intracortical circuitry.

No MeSH data available.


Related in: MedlinePlus