Comparative features of calretinin, calbindin, and parvalbumin expressing interneurons in mouse and monkey primary visual and frontal cortices

Medalla, Maria; Mo, Bingxin; Nasar, Rakin; Zhou, Yuxin; Park, Jun‐Woo; Luebke, Jennifer I.

doi:10.1002/cne.25514

Cited by 13 publications

(13 citation statements)

References 126 publications

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“…Specifically, GABA+ and PV+ expression peaks in L2/3 and 4C in marmoset V1, but in L4 and 5 in mouse V1. Similar differences between mouse and primate V1 in the laminar distribution of PV cells were reported previously (Kooijmans et al, 2020; Medalla et al, 2023). Our results on the laminar distribution of PV and GABA immunoreactivity is consistent with previous qualitative and quantitative studies in macaque V1 (Hendry et al, 1989; Blumcke et al, 1990; DeFelipe et al, 1999; Disney and Aoki, 2008; Kelly et al, 2019; Kooijmans et al, 2020; Medalla et al, 2023), and with a quantitative study in marmoset V1(Goodchild and Martin, 1998).…”

Section: Discussionsupporting

confidence: 88%

Laminar specificity and coverage of viral-mediated gene expression restricted to GABAergic interneurons and their parvalbumin subclass in marmoset primary visual cortex

Federer,

Balsor,

Ingold

et al. 2024

Preprint

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In the mammalian neocortex, inhibition is important for dynamically balancing excitation and shaping the response properties of cells and circuits. The various functions of inhibition are thought to be mediated by different inhibitory neuron types of which a large diversity exists in several species. Current understanding of the function and connectivity of distinct inhibitory neuron types has mainly derived from studies in transgenic mice. However, it is unknown whether knowledge gained from mouse studies applies to the primate, the model system closest to humans. The lack of viral tools to selectively access inhibitory neuron types has been a major impediment to studying their function in the primate. Here, we have thoroughly validated and characterized several recently-developed viral vectors designed to restrict transgene expression to GABAergic cells or their parvalbumin (PV) subtype, and identified two types that show high specificity and efficiency in marmoset V1. We show that in marmoset V1 AAV-h56D induces transgene expression in GABAergic cells with up to 91-94% specificity and 80% efficiency, depending on viral serotype and cortical layer. AAV-PHP.eB-S5E2 induces transgene expression in PV cells across all cortical layers with up to 98% specificity and 86-90% efficiency. Thus, these viral vectors represent promising tools for studying GABA and PV cell function and connectivity in the primate cortex.

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Section: Discussionsupporting

confidence: 88%

Laminar specificity and coverage of viral-mediated gene expression restricted to GABAergic interneurons and their parvalbumin subclass in marmoset primary visual cortex

Federer,

Balsor,

Ingold

et al. 2024

Preprint

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“…To provide a potential neural mechanism explaining these observations, we built a simple computational model that incorporated different types of interneurons, VIP and SST, which are both modulated by an arousal signal. In the case of humans and other primates, similar action may be expected from interneurons expressing calbindin (CB) and calretinin (CR), which are thought to be analogous to SST and VIP in rodents (Medalla et al, 2023) and similarities between both circuits have been well documented (Kooijmans, Sierhuis, et al, 2020). When we simulated different arousal strengths, this architecture produced two dynamical regimes that depend strongly on the firing rate of the interneurons.…”

Section: Discussionmentioning

confidence: 97%

A disinhibitory circuit mechanism explains a general principle of peak performance during mid-level arousal

Beerendonk,

Mejías,

Nuiten

et al. 2023

Preprint

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Perceptual decision-making is highly dependent on the momentary arousal state of the brain, which fluctuates over time on a scale of hours, minutes, and even seconds. The textbook relationship between momentary arousal and task performance is captured by an inverted U-shape, as put forward in the Yerkes-Dodson law (Yerkes and Dodson, 1908). This law suggests optimal performance at moderate levels of arousal, and impaired performance at low or high arousal levels. However, despite its popularity, the evidence for this relationship in humans is mixed at best. Here, we use pupil-indexed arousal and performance data from various perceptual decision-making tasks to provide converging evidence for the inverted U-shaped relationship between arousal and performance across different task types (discrimination, detection) and modalities (visual, auditory). To further understand this relationship, we built a neurobiologically plausible mechanistic model and show that it is possible to reproduce our findings by incorporating two types of interneurons that are both modulated by an arousal signal. The model architecture produces two dynamical regimes under the influence of arousal: one regime in which performance increases with arousal, and another regime in which performance decreases with arousal, together forming an inverted U-shaped arousal-performance relationship. We conclude that the inverted U-shaped arousal-performance relationship is a general and robust property of sensory processing. It might be brought about by the influence of arousal on two type of interneurons that together act as a disinhibitory pathway for the neural populations that encode the available sensory evidence used for the decision.

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“… 2004 ; Medalla et al. 2023 ). In STG, layers II-III are populated in highest number by CR neurons, followed by CB neurons, and then PV neurons ( Kondo et al.…”

Section: The Importance Of Top–down Connectivity For Controlling the ...mentioning

confidence: 99%

The meso-connectomes of mouse, marmoset, and macaque: network organization and the emergence of higher cognition

Magrou,

Joyce,

Froudist-Walsh

et al. 2024

Cerebral Cortex

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The recent publications of the inter-areal connectomes for mouse, marmoset, and macaque cortex have allowed deeper comparisons across rodent vs. primate cortical organization. In general, these show that the mouse has very widespread, “all-to-all” inter-areal connectivity (i.e. a “highly dense” connectome in a graph theoretical framework), while primates have a more modular organization. In this review, we highlight the relevance of these differences to function, including the example of primary visual cortex (V1) which, in the mouse, is interconnected with all other areas, therefore including other primary sensory and frontal areas. We argue that this dense inter-areal connectivity benefits multimodal associations, at the cost of reduced functional segregation. Conversely, primates have expanded cortices with a modular connectivity structure, where V1 is almost exclusively interconnected with other visual cortices, themselves organized in relatively segregated streams, and hierarchically higher cortical areas such as prefrontal cortex provide top–down regulation for specifying precise information for working memory storage and manipulation. Increased complexity in cytoarchitecture, connectivity, dendritic spine density, and receptor expression additionally reveal a sharper hierarchical organization in primate cortex. Together, we argue that these primate specializations permit separable deconstruction and selective reconstruction of representations, which is essential to higher cognition.

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Comparative features of calretinin, calbindin, and parvalbumin expressing interneurons in mouse and monkey primary visual and frontal cortices

Cited by 13 publications

References 126 publications

Laminar specificity and coverage of viral-mediated gene expression restricted to GABAergic interneurons and their parvalbumin subclass in marmoset primary visual cortex

Laminar specificity and coverage of viral-mediated gene expression restricted to GABAergic interneurons and their parvalbumin subclass in marmoset primary visual cortex

A disinhibitory circuit mechanism explains a general principle of peak performance during mid-level arousal

The meso-connectomes of mouse, marmoset, and macaque: network organization and the emergence of higher cognition

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