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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 primary visual cortex (V1) of marmoset. (A) Photomicrographs of neighboring coronal sections through V1, showing the laminar structure as revealed by staining for cytochrome oxidase (left) and Nissl substance (right). Scale bar = 0.5 mm. Reproduced from Solomon (2002). The terminology of layers follows that defined by Brodmann. (B) Tuning for grating orientation and direction in two representative V1 neurons. Left: orientation selective neuron, responding equally well to gratings of appropriate orientation, in both directions of drift (adapted from Cheong et al., 2013). Right: direction selective neuron (adapted from Tinsley et al., 2003). (C) Spatial frequency tuning of representative parafoveal V1 neuron (adapted from Yu and Rosa, 2014); the response to low spatial frequencies is negligible. (D) Tuning for the size of a patch of drifting grating, of optimal spatial frequency (adapted from Yu and Rosa, 2014): response is suppressed in large sizes, showing presence of extraclassical receptive field modulation, or suppressive surround. Scale bars in (B–D) show 20 impulses/s. (E) Distribution of orientation selectivity amongst V1 neurons in marmoset. The abscissa shows an orientation selectivity index based on the circular variance (higher numbers indicate poorer tuning); the ordinate shows half-width at halfheight of a von Mises function fit to the tuning curve. The inset at right shows orientation tuning of example neurons that are indicated in the plot. Adapted from Yu and Rosa (2014).
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Figure 4: The primary visual cortex (V1) of marmoset. (A) Photomicrographs of neighboring coronal sections through V1, showing the laminar structure as revealed by staining for cytochrome oxidase (left) and Nissl substance (right). Scale bar = 0.5 mm. Reproduced from Solomon (2002). The terminology of layers follows that defined by Brodmann. (B) Tuning for grating orientation and direction in two representative V1 neurons. Left: orientation selective neuron, responding equally well to gratings of appropriate orientation, in both directions of drift (adapted from Cheong et al., 2013). Right: direction selective neuron (adapted from Tinsley et al., 2003). (C) Spatial frequency tuning of representative parafoveal V1 neuron (adapted from Yu and Rosa, 2014); the response to low spatial frequencies is negligible. (D) Tuning for the size of a patch of drifting grating, of optimal spatial frequency (adapted from Yu and Rosa, 2014): response is suppressed in large sizes, showing presence of extraclassical receptive field modulation, or suppressive surround. Scale bars in (B–D) show 20 impulses/s. (E) Distribution of orientation selectivity amongst V1 neurons in marmoset. The abscissa shows an orientation selectivity index based on the circular variance (higher numbers indicate poorer tuning); the ordinate shows half-width at halfheight of a von Mises function fit to the tuning curve. The inset at right shows orientation tuning of example neurons that are indicated in the plot. Adapted from Yu and Rosa (2014).

Mentions: The laminar organization of marmoset V1 (Figure 4A) is similar to that seen in other diurnal primates, as revealed by the distribution of Nissl stain, and several neurochemical markers (Gebhard et al., 1993; Spatz et al., 1994; Goodchild and Martin, 1998; Solomon, 2002; Bourne et al., 2007). Although the layers of V1 are fully formed at birth, many important developmental events occur postnatally, with marked changes particularly within the first 3 months (Missler et al., 1993a,b; Spatz et al., 1994; Bourne et al., 2005; Fonta et al., 2005; Ribic et al., 2011). The reader should note that some studies (e.g., Spatz, 1975a; Vogt Weisenhorn et al., 1995; Elston et al., 1996, 1999; Solomon, 2002; Bourne and Rosa, 2003b) have employed a nomenclature of cortical layers in V1 that differs from the more commonly used Brodmann scheme (Hassler, 1966; see Casagrande and Kaas, 1994 for a discussion of the relative merits of the two schemes). The main difference to keep in mind is that in the Hassler scheme the layers IVa and IVb of the Brodmann nomenclature are considered subdivisions of layer III.


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

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

The primary visual cortex (V1) of marmoset. (A) Photomicrographs of neighboring coronal sections through V1, showing the laminar structure as revealed by staining for cytochrome oxidase (left) and Nissl substance (right). Scale bar = 0.5 mm. Reproduced from Solomon (2002). The terminology of layers follows that defined by Brodmann. (B) Tuning for grating orientation and direction in two representative V1 neurons. Left: orientation selective neuron, responding equally well to gratings of appropriate orientation, in both directions of drift (adapted from Cheong et al., 2013). Right: direction selective neuron (adapted from Tinsley et al., 2003). (C) Spatial frequency tuning of representative parafoveal V1 neuron (adapted from Yu and Rosa, 2014); the response to low spatial frequencies is negligible. (D) Tuning for the size of a patch of drifting grating, of optimal spatial frequency (adapted from Yu and Rosa, 2014): response is suppressed in large sizes, showing presence of extraclassical receptive field modulation, or suppressive surround. Scale bars in (B–D) show 20 impulses/s. (E) Distribution of orientation selectivity amongst V1 neurons in marmoset. The abscissa shows an orientation selectivity index based on the circular variance (higher numbers indicate poorer tuning); the ordinate shows half-width at halfheight of a von Mises function fit to the tuning curve. The inset at right shows orientation tuning of example neurons that are indicated in the plot. Adapted from Yu and Rosa (2014).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 4: The primary visual cortex (V1) of marmoset. (A) Photomicrographs of neighboring coronal sections through V1, showing the laminar structure as revealed by staining for cytochrome oxidase (left) and Nissl substance (right). Scale bar = 0.5 mm. Reproduced from Solomon (2002). The terminology of layers follows that defined by Brodmann. (B) Tuning for grating orientation and direction in two representative V1 neurons. Left: orientation selective neuron, responding equally well to gratings of appropriate orientation, in both directions of drift (adapted from Cheong et al., 2013). Right: direction selective neuron (adapted from Tinsley et al., 2003). (C) Spatial frequency tuning of representative parafoveal V1 neuron (adapted from Yu and Rosa, 2014); the response to low spatial frequencies is negligible. (D) Tuning for the size of a patch of drifting grating, of optimal spatial frequency (adapted from Yu and Rosa, 2014): response is suppressed in large sizes, showing presence of extraclassical receptive field modulation, or suppressive surround. Scale bars in (B–D) show 20 impulses/s. (E) Distribution of orientation selectivity amongst V1 neurons in marmoset. The abscissa shows an orientation selectivity index based on the circular variance (higher numbers indicate poorer tuning); the ordinate shows half-width at halfheight of a von Mises function fit to the tuning curve. The inset at right shows orientation tuning of example neurons that are indicated in the plot. Adapted from Yu and Rosa (2014).
Mentions: The laminar organization of marmoset V1 (Figure 4A) is similar to that seen in other diurnal primates, as revealed by the distribution of Nissl stain, and several neurochemical markers (Gebhard et al., 1993; Spatz et al., 1994; Goodchild and Martin, 1998; Solomon, 2002; Bourne et al., 2007). Although the layers of V1 are fully formed at birth, many important developmental events occur postnatally, with marked changes particularly within the first 3 months (Missler et al., 1993a,b; Spatz et al., 1994; Bourne et al., 2005; Fonta et al., 2005; Ribic et al., 2011). The reader should note that some studies (e.g., Spatz, 1975a; Vogt Weisenhorn et al., 1995; Elston et al., 1996, 1999; Solomon, 2002; Bourne and Rosa, 2003b) have employed a nomenclature of cortical layers in V1 that differs from the more commonly used Brodmann scheme (Hassler, 1966; see Casagrande and Kaas, 1994 for a discussion of the relative merits of the two schemes). The main difference to keep in mind is that in the Hassler scheme the layers IVa and IVb of the Brodmann nomenclature are considered subdivisions of layer III.

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