Pyramidal Cells Make Specific Connections onto Smooth (GABAergic) Neurons in Mouse Visual Cortex

Bopp, Rita; Costa, Nuno Maçarico da; Kampa, Björn M.; Martin, Kevan A; Roth, Morgane M.

doi:10.1371/journal.pbio.1001932

Cited by 28 publications

(47 citation statements)

References 52 publications

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“…Within the reconstructed network, 43 functionally characterized neurons made 990 synapses, 443 of which were onto inhibitory interneurons and 547 onto other pyramidal cells (Table 1). The large fraction of synapses onto inhibitory neurons is consistent with past observations 8,20 and seems to be a characteristic of L2/3 in the mouse visual cortex. Consistent with physiological studies, connectivity between excitatory neurons was more likely for pairs with similar orientation preferences 2 (Fig.…”

supporting

confidence: 91%

Anatomy and function of an excitatory network in the visual cortex

Lee

Bonin

Reed

et al. 2016

Nature

504

499

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Circuits in the cerebral cortex consist of thousands of neurons connected by millions of synapses. A precise understanding of these local networks requires relating circuit activity with the underlying network structure. For pyramidal cells in superficial mouse visual cortex (V1), a consensus is emerging that neurons with similar visual response properties excite each other1–5, but the anatomical basis of this recurrent synaptic network is unknown. We combined physiological imaging and large-scale electron microscopy (EM) to study an excitatory network in V1. We found that layer 2/3 neurons organized into subnetworks defined by anatomical connectivity, with more connections within than between groups. More specifically, we found that pyramidal neurons with similar orientation selectivity preferentially formed synapses with each other, despite the fact that axons and dendrites of all orientation selectivities pass near (< 5 μm) each other with roughly equal probability. Therefore, we predict that mechanisms of functionally specific connectivity take place at the length scale of spines. Neurons with similar orientation tuning formed larger synapses, potentially enhancing the net effect of synaptic specificity. With the ability to study thousands of connections in a single circuit, functional connectomics is proving a powerful method to uncover the organizational logic of cortical networks.

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supporting

confidence: 91%

Anatomy and function of an excitatory network in the visual cortex

Lee

Bonin

Reed

et al. 2016

Nature

504

499

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“…In the adult, very few excitatory synapses onto excitatory neurons are located on the dendritic shaft, and the vast majority of spines contain a single type 1 excitatory synapse (Harris et al, 1992; LeVay, 1973). Excitatory synapses that have been observed on the shaft are generally formed on the dendrites of inhibitory interneurons that are typically aspiny (Ahmed et al, 1997; Bock et al, 2011; Bopp et al, 2014; Buhl et al, 1997). The minority of inhibitory interneurons that contain spines, are less spiny than pyramidal neurons (Kawaguchi et al, 2006; Kuhlman and Huang, 2008).…”

Section: Spines As Synaptic Markersmentioning

confidence: 99%

Spine Dynamics: Are They All the Same?

Berry

Nedivi

2017

Neuron

410

350

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Since Cajal’s first drawings of Golgi stained neurons, generations of researchers have been fascinated by the small protrusions, termed spines, studding many neuronal dendrites. Most excitatory synapses in the mammalian CNS are located on dendritic spines, making spines convenient proxies for excitatory synaptic presence. When in vivo imaging revealed that dendritic spines are dynamic structures, their addition and elimination were interpreted as excitatory synapse gain and loss, respectively. Spine imaging has since become a popular assay for excitatory circuit remodeling. In this review, we re-evaluate the validity of using spine dynamics as a straightforward reflection of circuit rewiring. Recent studies tracking both spines and synaptic markers in vivo reveal that 20% of spines lack PSD-95 and are short-lived. Although they account for most spine dynamics, their remodeling is unlikely to impact long-term network structure. We discuss distinct roles that spine dynamics can play in circuit remodeling depending on synaptic content.

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“…The V1 of mice and other species is structured into six layers and has retinotopic organization (Huberman and Niell, 2011). Neurons in V1 respond preferentially to a specific orientation of a line or edge, termed “orientation preference” (Bopp et al, 2014; Huberman and Niell, 2011). This process of breaking down the visual field into short line segments of different orientation contributes towards a “primal sketch” or discrimination the outline of the visual stimulus and is critical for our understanding of the analyses relevant for the measurement of visual performance (Kandel et al, 2000).…”

Section: Basic Overview Of Visual Processingmentioning

confidence: 99%

“…Receptive field size and connectivity of these primary sensory neurons and interneurons determine both visual acuity and contrast sensitivity at the level of the retina. RGCs determine contrast of a visual stimulus through their receptive fields’ center-surround organization, which is maintained in the visual pathway including the visual cortex, where neurons with the capacity to discriminate the orientation preference of a visual stimulus identify distinct patterns of the visual field and of a visual stimulus (Bopp et al, 2014). During the initial stages of disease development, RGCs are the first cells affected by neurodegeneration and cell death in the glaucomatous retina, resulting in a deficit of visual function before other cell types are affected (Burroughs et al, 2011; Kaja et al, 2011; Kaja et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Psychophysical testing in rodent models of glaucomatous optic neuropathy

Grillo

Koulen

2015

Experimental Eye Research

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Processing of visual information begins in the retina, with photoreceptors converting light stimuli into neural signals. Ultimately, signals are transmitted to the brain through signaling networks formed by interneurons, namely bipolar, horizontal and amacrine cells providing input to retinal ganglion cells (RGCs), which form the optic nerve with their axons. As part of the chronic nature of glaucomatous optic neuropathy, the increasing and irreversible damage and ultimately loss of neurons, RGCs in particular, occurs following progressive damage to the optic nerve head (ONH), eventually resulting in visual impairment and visual field loss. There are two behavioral assays that are typically used to assess visual deficits in glaucoma rodent models, the visual water task and the optokinetic drum. The visual water task can assess an animal’s ability to distinguish grating patterns that are associated with an escape from water. The optokinetic drum relies on the optomotor response, a reflex turning of the head and neck in the direction of the visual stimuli, which usually consists of rotating black and white gratings. This reflex is a physiological response critical for keeping the image stable on the retina. Driven initially by the neuronal input from direction-selective RGCs, this reflex is comprised of a number of critical sensory and motor elements. In the presence of repeatable and defined stimuli, this reflex is extremely well suited to analyze subtle changes in the circuitry and performance of retinal neurons. Increasing the cycles of these alternating gratings per degree, or gradually reducing the contrast of the visual stimuli, threshold levels can be determined at which the animal is no longer tracking the stimuli, and thereby visual function of the animal can be determined non-invasively. Integrating these assays into an array of outcome measures that determine multiple aspects of visual function is a central goal in vision research and can be realized, for example, by the combination of measuring optomotor reflex function with electroretinograms (ERGs) and optical coherence tomography (OCT) of the retina. These structure-function correlations in vivo are urgently needed to identify disease mechanisms as potential new targets for drug development. Such a combination of the experimental assessment of the optokinetic reflex (OKN) or optomotor reflex (OMR) with other measures of retinal structure and function is especially valuable for research on GON. The chronic progression of the disease is characterized by a gradual decrease in function accompanied by a concomitant increase in structural damage to the retina, therefore the assessment of subtle changes is key to determining the success of novel intervention strategies.

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Pyramidal Cells Make Specific Connections onto Smooth (GABAergic) Neurons in Mouse Visual Cortex

Abstract: Light and electron microscopy of the primary visual cortex of mice indicates that pyramidal neurons connect preferentially to inhibitory neurons.

Cited by 28 publications

References 52 publications

Anatomy and function of an excitatory network in the visual cortex

Anatomy and function of an excitatory network in the visual cortex

Spine Dynamics: Are They All the Same?

Psychophysical testing in rodent models of glaucomatous optic neuropathy

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