scholarly journals Dendritic domain-specific sampling of long-range axons shapes feedforward and feedback connectivity of L5 neurons

2021 ◽  
Author(s):  
Alessandro R. Galloni ◽  
Zhiwen Ye ◽  
Ede Rancz
Keyword(s):  
Visual Cortex ◽  
Long Range ◽  
Cognitive Functions ◽  
Pyramidal Neurons ◽  
Predictive Inference ◽  
Cortical Layers ◽  
Domain Specific ◽  
Axonal Projections ◽  
Deep Layers ◽  
Feedback Pathways

AbstractFeedforward and feedback pathways interact in specific dendritic domains to enable cognitive functions such as predictive inference and learning. Based on axonal projections, hierarchically lower areas are thought to form synapses primarily on dendrites in middle cortical layers, while higher-order areas are posited to target dendrites in layer 1 and in deep layers. However, the extent to which functional synapses form in regions of axo-dendritic overlap has not been extensively studied. Here, we use viral tracing in the visual cortex of mice to map brain-wide inputs to a genetically-defined population of layer 5 pyramidal neurons. Furthermore, we provide a comprehensive map of input locations through subcellular optogenetic circuit mapping. We show that input pathways target distinct dendritic domains with far greater specificity than appears from their axonal branching, often deviating substantially from the canonical patterns. Common assumptions regarding the dendrite-level interaction of feedforward and feedback inputs may thus need revisiting.

Silent Synapses in the Immature Visual Cortex: Layer-Specific Developmental Regulation

2004 ◽  
Vol 91 (2) ◽  
pp. 1097-1101 ◽  
Author(s):  
Simon Rumpel ◽  
Gunnar Kattenstroth ◽  
Kurt Gottmann
Keyword(s):  
Visual Cortex ◽  
Pyramidal Neurons ◽  
Developmental Regulation ◽  
Pyramidal Cells ◽  
Cortical Plate ◽  
Glutamatergic Synapses ◽  
Silent Synapses ◽  
Deep Layers ◽  
Further Development ◽  
Layer Vi

Central glutamatergic synapses are thought to initially form as immature, so-called silent synapses showing exclusively N-methyl-d-aspartate receptor-mediated synaptic transmission. Postsynaptic insertion of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors during further development leads to a conversion into functional, mature synapses. Here, we tested the hypothesis that, according to the “inside first–outside last” pattern of neocortical layer formation and synaptogenesis, pyramidal cells in the superficial layers might show a higher fraction of silent synapses compared with pyramidal cells in the deep layers. We performed an electrophysiological analysis of glutamatergic synapses in acute rat visual cortex slices during postnatal development. In layer VI pyramidal neurons the incidence of silent synapses was high during the first postnatal week and strongly declined during further development. Surprisingly, in superficial cortical plate pyramidal neurons (immature layers II/III), the fraction of silent synapses was initially very low and increased up to the second postnatal week. Thereafter, a similar decline as found in layer VI pyramidal neurons was observed. Thus the developmental regulation of silent synapses was clearly different in pyramidal neurons from different neocortical layers. The almost complete absence of silent synapses at early stages in layer II/III pyramidal neurons indicates that an initially formed subset of synapses is constitutively functional. This might be important to enable spontaneous activity and latter activity-dependent maturation of synapses.

scholarly journals Prior expectations evoke stimulus-specific activity in the deep layers of the primary visual cortex

PLoS Biology ◽  
2020 ◽  
Vol 18 (12) ◽  
pp. e3001023
Author(s):  
Fraser Aitken ◽  
Georgios Menelaou ◽  
Oliver Warrington ◽  
Renée S. Koolschijn ◽  
Nadège Corbin ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Specific Activity ◽  
Predictive Processing ◽  
Cortical Layers ◽  
Computational Architecture ◽  
Deep Layers ◽  
Flow Through ◽  
The Brain ◽  
The Way

The way we perceive the world is strongly influenced by our expectations. In line with this, much recent research has revealed that prior expectations strongly modulate sensory processing. However, the neural circuitry through which the brain integrates external sensory inputs with internal expectation signals remains unknown. In order to understand the computational architecture of the cortex, we need to investigate the way these signals flow through the cortical layers. This is crucial because the different cortical layers have distinct intra- and interregional connectivity patterns, and therefore determining which layers are involved in a cortical computation can inform us on the sources and targets of these signals. Here, we used ultra-high field (7T) functional magnetic resonance imaging (fMRI) to reveal that prior expectations evoke stimulus-specific activity selectively in the deep layers of the primary visual cortex (V1). These findings are in line with predictive processing theories proposing that neurons in the deep cortical layers represent perceptual hypotheses and thereby shed light on the computational architecture of cortex.

scholarly journals The relationship between oscillatory EEG activity and the laminar-specific BOLD signal

2016 ◽  
Vol 113 (24) ◽  
pp. 6761-6766 ◽  
Author(s):  
René Scheeringa ◽  
Peter J. Koopmans ◽  
Tim van Mourik ◽  
Ole Jensen ◽  
David G. Norris
Keyword(s):  
Visual Cortex ◽  
High Resolution ◽  
Blood Oxygen Level Dependent ◽  
Superficial Layer ◽  
Oscillatory Activity ◽  
Bold Signal ◽  
Cortical Layers ◽  
Differential Relation ◽  
Combining Data ◽  
Deep Layers

Electrophysiological recordings in animals have indicated that visual cortex γ-band oscillatory activity is predominantly observed in superficial cortical layers, whereas α- and β-band activity is stronger in deep layers. These rhythms, as well as the different cortical layers, have also been closely related to feedforward and feedback streams of information. Recently, it has become possible to measure laminar activity in humans with high-resolution functional MRI (fMRI). In this study, we investigated whether these different frequency bands show a differential relation with the laminar-resolved blood-oxygen level-dependent (BOLD) signal by combining data from simultaneously recorded EEG and fMRI from the early visual cortex. Our visual attention paradigm allowed us to investigate how variations in strength over trials and variations in the attention effect over subjects relate to each other in both modalities. We demonstrate that γ-band EEG power correlates positively with the superficial layers’ BOLD signal and that β-power is negatively correlated to deep layer BOLD and α-power to both deep and superficial layer BOLD. These results provide a neurophysiological basis for human laminar fMRI and link human EEG and high-resolution fMRI to systems-level neuroscience in animals.

Ocular dominance columns and local projections of layer 6 pyramidal neurons in macaque primary visual cortex

1997 ◽  
Vol 14 (2) ◽  
pp. 241-251 ◽  
Author(s):  
Anne K. Wiser ◽  
Edward M. Callaway
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Pyramidal Neurons ◽  
Ocular Dominance ◽  
Class Ii ◽  
Class I ◽  
Individual Layer ◽  
Ocular Dominance Columns ◽  
Axonal Projections ◽  
Axonal Arbors

AbstractTo study the relationship between ocular dominance columns (ODCs) and axonal projections of individual layer 6 pyramidal neurons in the primary visual cortex, neurons were intracellularly labeled with biocytin in live slices prepared from macaque monkeys that had received an intravitreal injection of tetrodotoxin (TTX). The TTX injection indirectly causes a decrease in cytochrome oxidase (CO) expression in the cortical ODCs corresponding to the treated eye (Wong-Riley & Carroll, 1984). Sections from slices with labeled layer 6 neurons were double stained for biocytin and CO, to allow visualization of neuronal processes as well as ODCs. Twenty-seven layer 6 pyramidal neurons in ODC-labeled slices were analyzed. These neurons were classified according to the criteria of Wiser and Callaway (1996). Eight of these are class I neurons, which have dense axonal projections to the monocular layer 4C. The remaining 19 are class II neurons which project primarily to the binocular layers outside 4C. Among class I neurons, two have dense axonal arbors in layer 4Cα (type Iα), one in layer 4Cβ (type Iβ), and two throughout the depth of layer 4C (type IC). None of these neurons have ODC-specific axonal arbors. The remaining three class I neurons have focused axonal projections in layers 4Cβ and 4A (type IβA). All three appear to have axonal arbors predominantly within their home ODC in layer 4C. The axonal arbors of class II neurons do not appear to relate to ODCs in any specific fashion.

scholarly journals Distinct Laminar Processing of Local and Global Context in Primate Primary Visual Cortex

2017 ◽  
Author(s):  
Maryam Bijanzadeh ◽  
Lauri Nurminen ◽  
Sam Merlin ◽  
Alessandra Angelucci
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Space ◽  
Spatial Context ◽  
Surround Suppression ◽  
Cortical Layers ◽  
Global Context ◽  
Global Signal ◽  
Deep Layers ◽  
Contextual Stimuli

Visual perception is profoundly affected by spatial context. In visual cortex, neuronal responses to stimuli inside their receptive field (RF) are suppressed by contextual stimuli in the RF surround (surround suppression). How do neuronal RFs integrate information across visual space, and what role do different cortical layers play in the processing of spatial context? By recording simultaneously across all layers of macaque primary visual cortex, while presenting visual stimuli at increasing distances from the recorded cells RF, we find that near vs. far stimuli activate distinct layers. Stimuli in the near-surround evoke the earliest subthreshold responses in superficial and deep layers, and cause the earliest surround suppression of spiking responses in superficial layers. Instead, far-surround stimuli evoke the earliest subthreshold responses in feedback-recipient layers, i.e. 1 and the lower half of the deep layers, and suppress visually-evoked spiking responses almost simultaneously in all layers, except 4C, where suppression emerges latest. Our results reveal unique contributions of the cortical layers to the processing of local and global spatial context, and suggest distinct underlying circuits for local and global signal integration.

Contributions of individual layer 2–5 spiny neurons to local circuits in macaque primary visual cortex

1996 ◽  
Vol 13 (5) ◽  
pp. 907-922 ◽  
Author(s):  
Edward M. Callaway ◽  
Anne K. Wiser
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Pyramidal Neurons ◽  
Dendritic Morphology ◽  
Projection Neurons ◽  
Axonal Projections ◽  
Spiny Neurons ◽  
Local Circuitry ◽  
Local Circuits ◽  
Axonal Arbors

AbstractWe studied excitatory local circuits in the macaque primary visual cortex (V1) to investigate their relationships to the magnocellular (M) and parvocellular (P) streams. Sixty-two intracellularly labeled spiny neurons in layers 2–5 were analyzed. We made detailed observations of the laminar and columnar specificity of axonal arbors and noted correlations with dendritic arbors. We find evidence for considerable mixing of M and P streams by the local circuitry in V1. Such mixing is provided by neurons in the primary geniculate recipient layer 4C, as well as by neurons in both the supragranular and infragranular layers. We were also interested in possible differences in the axonal projections of neurons with different dendritic morphologies. We found that layer 4B spiny stellate and pyramidal neurons have similar axonal arbors. However, we identified two types of layer 5 pyramidal neuron. The majority have a conventional pyramidal dendritic morphology, a dense axonal arbor in layers 2–4B, and do not project to the white matter. Layer 5 projection neurons have an unusual “backbranching” dendritic morphology (apical dendritic branches arc downward rather than upward) and weak or no axonal arborization in layers 2–4B, but have long horizontal axonal projections in layer 5B. We find no strong projection from layer 5 pyramidal neurons to layer 6. In macaque V1 there appears to be no single source of strong local input to layer 6; only a minority of cells in layers 2–5 have axonal branches in layer 6 and these are sparse. Our results suggest that local circuits in V1 mediate interactions between M and P input that are complex and not easily incorporated into a simple framework.

scholarly journals Spatial clustering of inhibition in mouse primary visual cortex

2019 ◽  
Author(s):  
Pawan Bista ◽  
Rinaldo D. D’Souza ◽  
Andrew M. Meier ◽  
Weiqing Ji ◽  
Andreas Burkhalter
Keyword(s):  
Visual Cortex ◽  
Long Range ◽  
Primary Visual Cortex ◽  
Pyramidal Neurons ◽  
Spatial Clustering ◽  
Muscarinic Acetylcholine Receptor ◽  
Feature Maps ◽  
Lateral Posterior ◽  
Mouse Visual Cortex ◽  
Relative Excitation

SUMMARYWhether mouse visual cortex contains orderly feature maps is debated. The overlapping pattern of geniculocortical (dLGN) inputs with M2 muscarinic acetylcholine receptor-rich patches in layer 1 (L1) suggests a non-random architecture. Here, we found that L1 inputs from the lateral posterior thalamus (LP) avoid patches and target interpatches. Channelrhodopsin-assisted mapping of EPSCs in L2/3 shows that the relative excitation of parvalbumin-expressing interneurons (PVs) and pyramidal neurons (PNs) by dLGN, LP and cortical feedback are distinct and depend on whether the neurons reside in clusters aligned with patches or interpatches. Paired recordings from PVs and PNs shows that unitary IPSCs are larger in interpatches than patches. The spatial clustering of inhibition is matched by dense clustering of PV-terminals in interpatches. The results show that the excitation/inhibition balance across V1 is organized into patch and interpatch subnetworks which receive distinct long-range inputs and are specialized for the processing of distinct spatiotemporal features.

scholarly journals A single-cell anatomical blueprint for intracortical information transfer from primary visual cortex

2017 ◽  
Author(s):  
Yunyun Han ◽  
Justus M Kebschull ◽  
Robert AA Campbell ◽  
Devon Cowan ◽  
Fabia Imhof ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Long Range ◽  
Primary Visual Cortex ◽  
Information Transfer ◽  
Target Area ◽  
V1 Neurons ◽  
Cortical Areas ◽  
Axonal Projections ◽  
High Throughput Dna Sequencing ◽  
Axonal Arbors

The wiring diagram of the neocortex determines how information is processed across dozens of cortical areas. Each area communicates with multiple others via extensive long-range axonal projections 1–6, but the logic of inter-area information transfer is unresolved. Specifically, the extent to which individual neurons send dedicated projections to single cortical targets or distribute their signals across multiple areas remains unclear5,7–20. Distinguishing between these possibilities has been challenging because axonal projections of only a few individual neurons have been reconstructed. Here we map the projection patterns of axonal arbors from 591 individual neurons in mouse primary visual cortex (V1) using two complementary methods: whole-brain fluorescence-based axonal tracing21,22 and high-throughput DNA sequencing of genetically barcoded neurons (MAPseq)23. Although our results confirm the existence of dedicated projections to certain cortical areas, we find these are the exception, and that the majority of V1 neurons broadcast information to multiple cortical targets. Furthermore, broadcasting cells do not project to all targets randomly, but rather comprise subpopulations that either avoid or preferentially innervate specific subsets of cortical areas. Our data argue against a model of dedicated lines of intracortical information transfer via “one neuron – one target area” mapping. Instead, long-range communication between a sensory cortical area and its targets may be based on a principle whereby individual neurons copy information to, and potentially coordinate activity across, specific subsets of cortical areas.

Patterns of Local Connectivity in the Neocortex

1993 ◽  
Vol 5 (5) ◽  
pp. 665-680 ◽  
Author(s):  
Andrew Nicoll ◽  
Colin Blakemore
Keyword(s):  
Visual Cortex ◽  
Pyramidal Neurons ◽  
Extreme Values ◽  
Pyramidal Cells ◽  
Excitatory Synapses ◽  
Synaptic Connections ◽  
Local Connectivity ◽  
Connection Probability ◽  
Layer 2 ◽  
Deep Layers

Dual intracellular recording of nearby pairs of pyramidal cells in slices of rat visual cortex has shown that there are significant differences in functional connectivity between the superficial and deep layers (Mason et al. 1991; Nicoll and Blakemore 1993). For pairs of cells no farther than 300 μm apart, synaptic connections between layer 2/3 pyramidal neurons were individually weaker (median peak amplitude, A, of single-fiber excitatory postsynaptic potentials, EPSPs, = 0.4 mV) but more frequent (connection probability, p = 0.087) than those between layer 5 pyramidal neurons (mean A = 0.8 mV, p < 0.015). Taken in combination with plausible estimates of the density of pyramidal cells, the total numbers of synapses on them and the number of synapses formed on their intracortical axons, the present analysis of the above data suggests that roughly 70% of the excitatory synapses on any layer 2/3 pyramid, but fewer than 1% of those on a layer 5 pyramidal neuron, are derived from neighboring pyramidal neurons in its near vicinity. Even assuming very extreme values for some parameters, chosen to erode this difference, the calculated proportion of "local synapses" for layer 5 pyramids was always markedly lower than for layer 2/3 pyramidal neurons. These results imply that local excitatory connections are much more likely to provide significant "intracortical amplification" of afferent signals in layer 2/3 than in layer 5 of rat visual cortex.

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