scholarly journals Aberrant development of excitatory circuits to inhibitory neurons in the primary visual cortex after neonatal binocular enucleation

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Rongkang Deng ◽  
Joseph P. Y. Kao ◽  
Patrick O. Kanold
Keyword(s):  
Visual Cortex ◽  
Nmda Receptors ◽  
Laser Scanning ◽  
Inhibitory Neurons ◽  
Gabaergic Interneurons ◽  
Cortical Circuits ◽  
Retinal Input ◽  
Layer 4 ◽  
Ampa And Nmda Receptors ◽  
Laser Scanning Photostimulation

AbstractThe development of GABAergic interneurons is important for the functional maturation of cortical circuits. After migrating into the cortex, GABAergic interneurons start to receive glutamatergic connections from cortical excitatory neurons and thus gradually become integrated into cortical circuits. These glutamatergic connections are mediated by glutamate receptors including AMPA and NMDA receptors and the ratio of AMPA to NMDA receptors decreases during development. Since previous studies have shown that retinal input can regulate the early development of connections along the visual pathway, we investigated if the maturation of glutamatergic inputs to GABAergic interneurons in the visual cortex requires retinal input. We mapped the spatial pattern of glutamatergic connections to layer 4 (L4) GABAergic interneurons in mouse visual cortex at around postnatal day (P) 16 by laser-scanning photostimulation and investigated the effect of binocular enucleations at P1/P2 on these patterns. Gad2-positive interneurons in enucleated animals showed an increased fraction of AMPAR-mediated input from L2/3 and a decreased fraction of input from L5/6. Parvalbumin-expressing (PV) interneurons showed similar changes in relative connectivity. NMDAR-only input was largely unchanged by enucleation. Our results show that retinal input sculpts the integration of interneurons into V1 circuits and suggest that the development of AMPAR- and NMDAR-only connections might be regulated differently.

scholarly journals Functional selectivity and specific connectivity of inhibitory neurons in primary visual cortex

2018 ◽  
Author(s):  
Petr Znamenskiy ◽  
Mean-Hwan Kim ◽  
Dylan R. Muir ◽  
Maria Florencia Iacaruso ◽  
Sonja B. Hofer ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Pyramidal Cells ◽  
Fine Tuning ◽  
Inhibitory Neurons ◽  
Local Network ◽  
Cortical Circuits ◽  
Sensory Stimuli ◽  
Excitatory Neurons ◽  
Strong Excitation

In the cerebral cortex, the interaction of excitatory and inhibitory synaptic inputs shapes the responses of neurons to sensory stimuli, stabilizes network dynamics1 and improves the efficiency and robustness of the neural code2–4. Excitatory neurons receive inhibitory inputs that track excitation5–8. However, how this co-tuning of excitation and inhibition is achieved by cortical circuits is unclear, since inhibitory interneurons are thought to pool the inputs of nearby excitatory cells and provide them with non-specific inhibition proportional to the activity of the local network9–13. Here we show that although parvalbumin-expressing (PV) inhibitory cells in mouse primary visual cortex make connections with the majority of nearby pyramidal cells, the strength of their synaptic connections is structured according to the similarity of the cells’ responses. Individual PV cells strongly inhibit those pyramidal cells that provide them with strong excitation and share their visual selectivity. This fine-tuning of synaptic weights supports co-tuning of inhibitory and excitatory inputs onto individual pyramidal cells despite dense connectivity between inhibitory and excitatory neurons. Our results indicate that individual PV cells are preferentially integrated into subnetworks of inter-connected, co-tuned pyramidal cells, stabilising their recurrent dynamics. Conversely, weak but dense inhibitory connectivity between subnetworks is sufficient to support competition between them, de-correlating their output. We suggest that the history and structure of correlated firing adjusts the weights of both inhibitory and excitatory connections, supporting stable amplification and selective recruitment of cortical subnetworks.

Thalamocortical Specificity and the Synthesis of Sensory Cortical Receptive Fields

2005 ◽  
Vol 94 (1) ◽  
pp. 26-32 ◽  
Author(s):  
Jose-Manuel Alonso ◽  
Harvey A. Swadlow
Keyword(s):  
Visual Cortex ◽  
Barrel Cortex ◽  
Receptive Fields ◽  
High Specificity ◽  
Inhibitory Neurons ◽  
Simple Cells ◽  
Layer 4 ◽  
Different Response ◽  
Cortical Receptive Fields ◽  
Visual Cortical

A persistent and fundamental question in sensory cortical physiology concerns the manner in which receptive fields of layer-4 neurons are synthesized from their thalamic inputs. According to a hierarchical model proposed more than 40 years ago, simple receptive fields in layer 4 of primary visual cortex originate from the convergence of highly specific thalamocortical inputs (e.g., geniculate inputs with on-center receptive fields overlap the on subregions of layer 4 simple cells). Here, we summarize studies in the visual cortex that provide support for this high specificity of thalamic input to visual cortical simple cells. In addition, we review studies of GABAergic interneurons in the somatosensory “barrel” cortex with receptive fields that are generated by a very different mechanism: the nonspecific convergence of thalamic inputs with different response properties. We hypothesize that these 2 modes of thalamocortical connectivity onto subpopulations of excitatory and inhibitory neurons constitute a general feature of sensory neocortex and account for much of the diversity seen in layer-4 receptive fields.

scholarly journals Transient coupling between subplate and subgranular layers to L1 neurons before and during the critical period

2020 ◽  
Author(s):  
Xiangying Meng ◽  
Yanqing Xu ◽  
Joseph P. Y. Kao ◽  
Patrick O. Kanold
Keyword(s):  
Similar Pattern ◽  
Critical Period ◽  
Laser Scanning ◽  
Primary Auditory Cortex ◽  
Excitatory Input ◽  
Cortical Layer ◽  
Cortical Circuits ◽  
Inhibitory Circuits ◽  
Sensory Activity ◽  
Laser Scanning Photostimulation

AbstractCortical layer 1 (L1) contains a diverse population of interneurons which can modulate processing in superficial cortical layers but the intracortical sources of synaptic input to these neurons and how these inputs change over development is unknown. We here investigated the changing intracortical connectivity to L1 in primary auditory cortex (A1) in slices of mouse A1 across development using laser-scanning photostimulation. Before P10 L1 cells receive most excitatory input from within L1, L2/3, L4 and L5/6 as well as the subplate. Excitatory inputs from all layers increase and peak during P10-P16, the peak of the critical period. Inhibitory inputs followed a similar pattern. Functional circuit diversity in L1 emerges after P16. In adult, L1 neurons receive ascending inputs from superficial L2/3 and subgranular L5/6, but only few inputs from L4. A subtype of L1 neurons, NDNF+ neurons, follow a similar pattern, suggesting that transient hyperconnectivity is a universal feature of developing cortical circuits. Our results demonstrate that deep excitatory and superficial inhibitory circuits are tightly linked in early development and might provide a functional scaffold for the layers in between. These results suggest that early thalamic driven spontaneous and sensory activity in subplate can be relayed to L1 from the earliest ages on, that the critical period is characterized by high transient columnar hyperconnectivity, and that in particular circuits originating in L5/6 and subplate might play a key role.

Consistent mapping of orientation preference across irregular functional domains in ferret visual cortex

2001 ◽  
Vol 18 (1) ◽  
pp. 65-76 ◽  
Author(s):  
LEONARD E. WHITE ◽  
WILLIAM H. BOSKING ◽  
DAVID FITZPATRICK
Keyword(s):  
Visual Cortex ◽  
Activity Patterns ◽  
Ocular Dominance ◽  
Visual Space ◽  
Visual Environment ◽  
Cortical Circuits ◽  
Orientation Preference ◽  
Intrinsic Signals ◽  
Layer 4 ◽  
Consistent Mapping

The mammalian visual cortex harbors a number of functional maps that represent distinct attributes of stimuli in the visual environment. How different functional maps are accommodated within the same cortical space, especially in species that show marked irregularities in one or more functional maps, remains poorly understood. We used optical imaging of intrinsic signals and electrophysiological techniques to investigate the organization of the maps of orientation preference, ocular dominance, and visual space in ferret. This species shows striking nonuniformity in the arrangement of ocular dominance domains and disruption of the mapping of visual space along the V1/V2 border. We asked whether these irregularities would be reflected in the organization of the map of orientation preference. The results show that orientation preference is mapped consistently within both V1 and V2, and across the interareal boundary, with no reflection of the irregularities in the other maps. These observations demonstrate the accommodation of multiple functional maps within the same cortical space without systematic geometrical relationships that necessarily constrain the organization of each representation. Furthermore, they imply that the structure of the map of orientation preference reflects the architecture and activity patterns of cortical circuits that are independent of other columnar systems established in layer 4.

scholarly journals Head Movements Control the Activity of Primary Visual Cortex in a Luminance Dependent Manner

2020 ◽  
Author(s):  
Guy Bouvier ◽  
Yuta Senzai ◽  
Massimo Scanziani
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Head Movements ◽  
Inhibitory Neurons ◽  
Dependent Manner ◽  
Ambient Light ◽  
Cortical Circuits ◽  
Cortical Layers ◽  
Visual Cortical ◽  
The Brain

AbstractThe vestibular system broadcasts head-movement related signals to sensory areas throughout the brain, including visual cortex. These signals are crucial for the brain’s ability to assess whether motion of the visual scene results from the animal’s head-movements. How head-movements impact visual cortical circuits remains, however, poorly understood. Here, we discover that ambient luminance profoundly transforms how mouse primary visual cortex (V1) processes head-movements. While in darkness, head movements result in an overall suppression of neuronal activity, in ambient light the same head movements trigger excitation across all cortical layers. This light-dependent switch in how V1 processes head-movements is controlled by somatostatin expressing (SOM) inhibitory neurons, which are excited by head movements in dark but not in light. This study thus reveals a light-dependent switch in the response of V1 to head-movements and identifies a circuit in which SOM cells are key integrators of vestibular and luminance signals.

scholarly journals Transient Subgranular Hyperconnectivity to L2/3 and Enhanced Pairwise Correlations During the Critical Period in the Mouse Auditory Cortex

2019 ◽  
Vol 30 (3) ◽  
pp. 1914-1930 ◽  
Author(s):  
Xiangying Meng ◽  
Krystyna Solarana ◽  
Zac Bowen ◽  
Ji Liu ◽  
Daniel A Nagode ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Critical Period ◽  
Laser Scanning ◽  
Primary Auditory Cortex ◽  
Excitatory Input ◽  
Two Photon ◽  
Layer 4 ◽  
Neuronal Connections ◽  
Laser Scanning Photostimulation

Abstract During the critical period, neuronal connections are shaped by sensory experience. While the basis for this temporarily heightened plasticity remains unclear, shared connections introducing activity correlations likely play a key role. Thus, we investigated the changing intracortical connectivity in primary auditory cortex (A1) over development. In adult, layer 2/3 (L2/3) neurons receive ascending inputs from layer 4 (L4) and also receive few inputs from subgranular layer 5/6 (L5/6). We measured the spatial pattern of intracortical excitatory and inhibitory connections to L2/3 neurons in slices of mouse A1 across development using laser-scanning photostimulation. Before P11, L2/3 cells receive most excitatory input from within L2/3. Excitatory inputs from L2/3 and L4 increase after P5 and peak during P9–16. L5/6 inputs increase after P5 and provide most input during P12–16, the peak of the critical period. Inhibitory inputs followed a similar pattern. Functional circuit diversity in L2/3 emerges after P16. In vivo two-photon imaging shows low pairwise signal correlations in neighboring neurons before P11, which peak at P15–16 and decline after. Our results suggest that the critical period is characterized by high pairwise activity correlations and that transient hyperconnectivity of specific circuits, in particular those originating in L5/6, might play a key role.

scholarly journals Accelerated Hyper-Maturation of Parvalbumin Circuits in the Absence of MeCP2

2019 ◽  
Vol 30 (1) ◽  
pp. 256-268 ◽  
Author(s):  
Annarita Patrizi ◽  
Patricia N Awad ◽  
Bidisha Chattopadhyaya ◽  
Chloe Li ◽  
Graziella Di Cristo ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Genetic Manipulation ◽  
Neurodevelopmental Disorder ◽  
Structural Complexity ◽  
Pyramidal Cells ◽  
Gabaergic Interneurons ◽  
Cortical Circuits ◽  
Structure Complexity ◽  
Deficient Mice

Abstract Methyl-CpG-binding protein 2 (MeCP2) mutations are the primary cause of Rett syndrome, a severe neurodevelopmental disorder. Cortical parvalbumin GABAergic interneurons (PV) make exuberant somatic connections onto pyramidal cells in the visual cortex of Mecp2-deficient mice, which contributes to silencing neuronal cortical circuits. This phenotype can be rescued independently of Mecp2 by environmental, pharmacological, and genetic manipulation. It remains unknown how Mecp2 mutation can result in abnormal inhibitory circuit refinement. In the present manuscript, we examined the development of GABAergic circuits in the primary visual cortex of Mecp2-deficient mice. We identified that PV circuits were the only GABAergic interneurons to be upregulated, while other interneurons were downregulated. Acceleration of PV cell maturation was accompanied by increased PV cells engulfment by perineuronal nets (PNNs) and by an increase of PV cellular and PNN structural complexity. Interestingly, selective deletion of Mecp2 from PV cells was sufficient to drive increased structure complexity of PNN. Moreover, the accelerated PV and PNN maturation was recapitulated in organotypic cultures. Our results identify a specific timeline of disruption of GABAergic circuits in the absence of Mecp2, indicating a possible cell-autonomous role of MeCP2 in the formation of PV cellular arbors and PNN structures in the visual cortex.

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