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A simpler primate brain: the visual system of the marmoset monkey.

Solomon SG, Rosa MG - Front Neural Circuits (2014)

Bottom Line: Therefore, in order to understand some aspects of human visual function, we need to study non-human primate brains.Which species is the most appropriate model?Here we review the visual pathways of the marmoset, highlighting recent work that brings these advantages into focus, and identify where additional work needs to be done to link marmoset brain organization to that of macaques and humans.

View Article: PubMed Central - PubMed

Affiliation: Department of Experimental Psychology, University College London London, UK.

ABSTRACT
Humans are diurnal primates with high visual acuity at the center of gaze. Although primates share many similarities in the organization of their visual centers with other mammals, and even other species of vertebrates, their visual pathways also show unique features, particularly with respect to the organization of the cerebral cortex. Therefore, in order to understand some aspects of human visual function, we need to study non-human primate brains. Which species is the most appropriate model? Macaque monkeys, the most widely used non-human primates, are not an optimal choice in many practical respects. For example, much of the macaque cerebral cortex is buried within sulci, and is therefore inaccessible to many imaging techniques, and the postnatal development and lifespan of macaques are prohibitively long for many studies of brain maturation, plasticity, and aging. In these and several other respects the marmoset, a small New World monkey, represents a more appropriate choice. Here we review the visual pathways of the marmoset, highlighting recent work that brings these advantages into focus, and identify where additional work needs to be done to link marmoset brain organization to that of macaques and humans. We will argue that the marmoset monkey provides a good subject for studies of a complex visual system, which will likely allow an important bridge linking experiments in animal models to humans.

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The two major retino-thalamic pathways in marmoset. (A) Camera lucida drawings of representative midget (parvocellular-pathway) and parasol (magnocellular-pathway) ganglion cells in marmoset retina, each located about 1 mm from the fovea (reproduced from Ghosh et al., 1996). (B) Photomicrograph of the LGN, showing the pairs of parvocellular (P) and magnocellular (M) layers; the dorsal most P layer and ventral most M layer get input from the contralateral eye; the internal layers get input from the ipsilateral eye. These layers are embedded in a matrix of koniocellular cells that lie between the principal layers, including two prominently segregated zones (K1, K3). Scale bar = 0.5 mm. (C) peristimulus time histograms of the responses of representative OFF P- and M-cells to brief (0.2 s) decrements in light from a gray background. The P-cell shows sustained response, the M-cell shows transient response (reproduced from Cheong and Pietersen, 2014). Y-axis scale bars 50 impulses/s. Thick black bar shows the time and duration of the stimulus. (D) Spatial-frequency tuning of representative P- and M-cells for drifting achromatic gratings, modulated at 4 Hz (adapted from White et al., 2001). Y-axis scale bars 20 impulses/s. (E) Contrast response of representative P- and M-cells for drifting gratings of optimal spatial frequency (adapted from Cheong and Pietersen, 2014).
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Figure 2: The two major retino-thalamic pathways in marmoset. (A) Camera lucida drawings of representative midget (parvocellular-pathway) and parasol (magnocellular-pathway) ganglion cells in marmoset retina, each located about 1 mm from the fovea (reproduced from Ghosh et al., 1996). (B) Photomicrograph of the LGN, showing the pairs of parvocellular (P) and magnocellular (M) layers; the dorsal most P layer and ventral most M layer get input from the contralateral eye; the internal layers get input from the ipsilateral eye. These layers are embedded in a matrix of koniocellular cells that lie between the principal layers, including two prominently segregated zones (K1, K3). Scale bar = 0.5 mm. (C) peristimulus time histograms of the responses of representative OFF P- and M-cells to brief (0.2 s) decrements in light from a gray background. The P-cell shows sustained response, the M-cell shows transient response (reproduced from Cheong and Pietersen, 2014). Y-axis scale bars 50 impulses/s. Thick black bar shows the time and duration of the stimulus. (D) Spatial-frequency tuning of representative P- and M-cells for drifting achromatic gratings, modulated at 4 Hz (adapted from White et al., 2001). Y-axis scale bars 20 impulses/s. (E) Contrast response of representative P- and M-cells for drifting gratings of optimal spatial frequency (adapted from Cheong and Pietersen, 2014).

Mentions: Around 90% of the ganglion cells project to the lateral geniculate nucleus (LGN) of the thalamus (Jusuf et al., 2006b; Szmajda et al., 2008). The LGN of the marmoset has a basic laminar organization, which emerges before birth (Garey and de Courten, 1983). The size of the LGN increases rapidly after birth, without an increase in the number of neurons, and stabilizes at about 6 months of age (Fritschy and Garey, 1986b, 1988). Retinal input arrives mainly at two dorsal parvocellular layers and two ventral magnocellular layers, each receiving dominant input from either the contralateral or the ipsilateral eye. These layers are embedded in a matrix of smaller koniocellular neurons (Figure 2; Le Gros Clark, 1941; Kaas et al., 1978; Spatz, 1978; Solomon, 2002). In the marmoset koniocellular neurons are well segregated from the principal layers in two particular zones, one ventral to the magnocellular layers (K1), and one between the internal parvocellular and magnocellular layers (K3). This segregation has allowed targeting of koniocellular zones for electrophysiological recordings (see below) and anatomical tracing, so much of what we know about the koniocellular visual pathways in simian primates stems from work in marmoset.


A simpler primate brain: the visual system of the marmoset monkey.

Solomon SG, Rosa MG - Front Neural Circuits (2014)

The two major retino-thalamic pathways in marmoset. (A) Camera lucida drawings of representative midget (parvocellular-pathway) and parasol (magnocellular-pathway) ganglion cells in marmoset retina, each located about 1 mm from the fovea (reproduced from Ghosh et al., 1996). (B) Photomicrograph of the LGN, showing the pairs of parvocellular (P) and magnocellular (M) layers; the dorsal most P layer and ventral most M layer get input from the contralateral eye; the internal layers get input from the ipsilateral eye. These layers are embedded in a matrix of koniocellular cells that lie between the principal layers, including two prominently segregated zones (K1, K3). Scale bar = 0.5 mm. (C) peristimulus time histograms of the responses of representative OFF P- and M-cells to brief (0.2 s) decrements in light from a gray background. The P-cell shows sustained response, the M-cell shows transient response (reproduced from Cheong and Pietersen, 2014). Y-axis scale bars 50 impulses/s. Thick black bar shows the time and duration of the stimulus. (D) Spatial-frequency tuning of representative P- and M-cells for drifting achromatic gratings, modulated at 4 Hz (adapted from White et al., 2001). Y-axis scale bars 20 impulses/s. (E) Contrast response of representative P- and M-cells for drifting gratings of optimal spatial frequency (adapted from Cheong and Pietersen, 2014).
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Related In: Results  -  Collection

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Figure 2: The two major retino-thalamic pathways in marmoset. (A) Camera lucida drawings of representative midget (parvocellular-pathway) and parasol (magnocellular-pathway) ganglion cells in marmoset retina, each located about 1 mm from the fovea (reproduced from Ghosh et al., 1996). (B) Photomicrograph of the LGN, showing the pairs of parvocellular (P) and magnocellular (M) layers; the dorsal most P layer and ventral most M layer get input from the contralateral eye; the internal layers get input from the ipsilateral eye. These layers are embedded in a matrix of koniocellular cells that lie between the principal layers, including two prominently segregated zones (K1, K3). Scale bar = 0.5 mm. (C) peristimulus time histograms of the responses of representative OFF P- and M-cells to brief (0.2 s) decrements in light from a gray background. The P-cell shows sustained response, the M-cell shows transient response (reproduced from Cheong and Pietersen, 2014). Y-axis scale bars 50 impulses/s. Thick black bar shows the time and duration of the stimulus. (D) Spatial-frequency tuning of representative P- and M-cells for drifting achromatic gratings, modulated at 4 Hz (adapted from White et al., 2001). Y-axis scale bars 20 impulses/s. (E) Contrast response of representative P- and M-cells for drifting gratings of optimal spatial frequency (adapted from Cheong and Pietersen, 2014).
Mentions: Around 90% of the ganglion cells project to the lateral geniculate nucleus (LGN) of the thalamus (Jusuf et al., 2006b; Szmajda et al., 2008). The LGN of the marmoset has a basic laminar organization, which emerges before birth (Garey and de Courten, 1983). The size of the LGN increases rapidly after birth, without an increase in the number of neurons, and stabilizes at about 6 months of age (Fritschy and Garey, 1986b, 1988). Retinal input arrives mainly at two dorsal parvocellular layers and two ventral magnocellular layers, each receiving dominant input from either the contralateral or the ipsilateral eye. These layers are embedded in a matrix of smaller koniocellular neurons (Figure 2; Le Gros Clark, 1941; Kaas et al., 1978; Spatz, 1978; Solomon, 2002). In the marmoset koniocellular neurons are well segregated from the principal layers in two particular zones, one ventral to the magnocellular layers (K1), and one between the internal parvocellular and magnocellular layers (K3). This segregation has allowed targeting of koniocellular zones for electrophysiological recordings (see below) and anatomical tracing, so much of what we know about the koniocellular visual pathways in simian primates stems from work in marmoset.

Bottom Line: Therefore, in order to understand some aspects of human visual function, we need to study non-human primate brains.Which species is the most appropriate model?Here we review the visual pathways of the marmoset, highlighting recent work that brings these advantages into focus, and identify where additional work needs to be done to link marmoset brain organization to that of macaques and humans.

View Article: PubMed Central - PubMed

Affiliation: Department of Experimental Psychology, University College London London, UK.

ABSTRACT
Humans are diurnal primates with high visual acuity at the center of gaze. Although primates share many similarities in the organization of their visual centers with other mammals, and even other species of vertebrates, their visual pathways also show unique features, particularly with respect to the organization of the cerebral cortex. Therefore, in order to understand some aspects of human visual function, we need to study non-human primate brains. Which species is the most appropriate model? Macaque monkeys, the most widely used non-human primates, are not an optimal choice in many practical respects. For example, much of the macaque cerebral cortex is buried within sulci, and is therefore inaccessible to many imaging techniques, and the postnatal development and lifespan of macaques are prohibitively long for many studies of brain maturation, plasticity, and aging. In these and several other respects the marmoset, a small New World monkey, represents a more appropriate choice. Here we review the visual pathways of the marmoset, highlighting recent work that brings these advantages into focus, and identify where additional work needs to be done to link marmoset brain organization to that of macaques and humans. We will argue that the marmoset monkey provides a good subject for studies of a complex visual system, which will likely allow an important bridge linking experiments in animal models to humans.

Show MeSH
Related in: MedlinePlus