scholarly journals Anatomical organization of presubicular head-direction circuits

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Patricia Preston-Ferrer ◽  
Stefano Coletta ◽  
Markus Frey ◽  
Andrea Burgalossi
Keyword(s):  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Retrosplenial Cortex ◽  
Theta Oscillations ◽  
Head Direction ◽  
Medial Entorhinal Cortex ◽  
Directional Information ◽  
Passive Rotation ◽  
A Cell ◽  
Fast Spiking

Neurons coding for head-direction are crucial for spatial navigation. Here we explored the cellular basis of head-direction coding in the rat dorsal presubiculum (PreS). We found that layer2 is composed of two principal cell populations (calbindin-positive and calbindin-negative neurons) which targeted the contralateral PreS and retrosplenial cortex, respectively. Layer3 pyramidal neurons projected to the medial entorhinal cortex (MEC). By juxtacellularly recording PreS neurons in awake rats during passive-rotation, we found that head-direction responses were preferentially contributed by layer3 pyramidal cells, whose long-range axons branched within layer3 of the MEC. In contrast, layer2 neurons displayed distinct spike-shapes, were not modulated by head-direction but rhythmically-entrained by theta-oscillations. Fast-spiking interneurons showed only weak directionality and theta-rhythmicity, but were significantly modulated by angular velocity. Our data thus indicate that PreS neurons differentially contribute to head-direction coding, and point to a cell-type- and layer-specific routing of directional and non-directional information to downstream cortical targets.

scholarly journals Anterior thalamic excitation and feed-forward inhibition of presubicular neurons projecting to medial entorhinal cortex

2018 ◽  
Author(s):  
Mérie Nassar ◽  
Jean Simonnet ◽  
Li-Wen Huang ◽  
Bertrand Mathon ◽  
Ivan Cohen ◽  
...  
Keyword(s):  
Entorhinal Cortex ◽  
Pyramidal Cells ◽  
Fine Tuning ◽  
Head Direction ◽  
Thalamic Nuclei ◽  
Medial Entorhinal Cortex ◽  
Directional Information ◽  
Feed Forward ◽  
Anterior Thalamic Nuclei ◽  
Feed Forward Inhibition

ABSTRACTThe presubiculum contains head direction cells that are crucial for spatial navigation. Here, we examined the connectivity and strengths of thalamic inputs to presubicular layer 3 neurons projecting to the medial entorhinal cortex in the mouse. We recorded pairs of projection neurons and interneurons while optogenetically stimulating afferent fibers from the anterior thalamic nuclei (ATN). Thalamic input differentially affects presubicular neurons: layer 3 pyramidal neurons and fast-spiking parvalbumin expressing (PV) interneurons are directly and monosynaptically activated, with depressing dynamics, while somatostatin (SST) expressing interneurons are indirectly excited, during repetitive ATN activity. This arrangement ensures that the thalamic excitation of layer 3 cells is often followed by disynaptic inhibition. Feed-forward inhibition is largely mediated by PV interneurons which have a high probability of connection to presubicular pyramidal cells. Our data point to a specific role of presubicular microcircuits in shaping thalamic head-direction signals transmitted to medial entorhinal cortex: Short-latency PV cell activation may enforce temporally precise head direction tuning during fast turns. However, depression at ATN-PV synapses during repeated activation tends to facilitate pyramidal cell firing when head direction is maintained. Operations performed in presubicular layer 3 circuits seem well-adapted for spatial fine-tuning of head direction signals sent to the medial entorhinal cortex.SIGNIFICANCE STATEMENTHow microcircuits participate in shaping neural inputs is crucial to understanding information processing in the brain. Here, we show how the presubiculum may process thalamic head directional information before transmitting it to the medial entorhinal cortex. Synaptic inputs from the anterior thalamic nuclei (ATN) excite layer 3 pyramidal cells (PC) and parvalbumin (PV) interneurons, which mediate disynaptic feed-forward inhibition. Somatostatin (SST) interneurons are excited indirectly. Presubicular circuits may switch between two regimes according to the angular velocity of head movements. During immobility, SST-PC interactions support maintained head directional firing with attractor-like dynamics. During rapid head turns, in contrast, PV mediated feed-forward inhibition acts to tune the head direction signal transmitted to medial entorhinal cortex.

scholarly journals Spatially structured inhibition defined by polarized parvalbumin interneuron axons promotes head direction tuning

2021 ◽  
Vol 7 (25) ◽  
pp. eabg4693
Author(s):  
Yangfan Peng ◽  
Federico J. Barreda Tomas ◽  
Paul Pfeiffer ◽  
Moritz Drangmeister ◽  
Susanne Schreiber ◽  
...  
Keyword(s):  
Spatial Organization ◽  
Pyramidal Cells ◽  
Brain Regions ◽  
Head Direction ◽  
Spatial Connectivity ◽  
Parvalbumin Interneurons ◽  
Parvalbumin Interneuron ◽  
Network Simulations ◽  
Fast Spiking ◽  
Direction Tuning

In cortical microcircuits, it is generally assumed that fast-spiking parvalbumin interneurons mediate dense and nonselective inhibition. Some reports indicate sparse and structured inhibitory connectivity, but the computational relevance and the underlying spatial organization remain unresolved. In the rat superficial presubiculum, we find that inhibition by fast-spiking interneurons is organized in the form of a dominant super-reciprocal microcircuit motif where multiple pyramidal cells recurrently inhibit each other via a single interneuron. Multineuron recordings and subsequent 3D reconstructions and analysis further show that this nonrandom connectivity arises from an asymmetric, polarized morphology of fast-spiking interneuron axons, which individually cover different directions in the same volume. Network simulations assuming topographically organized input demonstrate that such polarized inhibition can improve head direction tuning of pyramidal cells in comparison to a “blanket of inhibition.” We propose that structured inhibition based on asymmetrical axons is an overarching spatial connectivity principle for tailored computation across brain regions.

scholarly journals Uniquely excitable neurons enable precise and persistent information transmission through the retrosplenial cortex

2019 ◽  
Author(s):  
Ellen K.W. Brennan ◽  
Shyam Kumar Sudhakar ◽  
Izabela Jedrasiak-Cape ◽  
Omar J. Ahmed
Keyword(s):  
Input Resistance ◽  
Retrosplenial Cortex ◽  
Inhibitory Neurons ◽  
Head Direction ◽  
Cell Type ◽  
Intrinsic Properties ◽  
High Input ◽  
Biophysical Models ◽  
High Input Resistance ◽  
Fast Spiking

ABSTRACTThe retrosplenial cortex (RSC) is essential for both memory and navigation, but the neural codes underlying these functions remain largely unknown. Here, we show that the most prominent cell type in layers 2/3 (L2/3) of the granular RSC is a uniquely excitable, small pyramidal cell. These cells have a low rheobase (LR), high input resistance, lack of spike-frequency adaptation, and spike widths intermediate to those of neighboring fast-spiking (FS) inhibitory neurons and regular-spiking (RS) excitatory neurons. LR cells are excitatory but rarely synapse onto neighboring neurons. Instead, L2/3 of RSC is an inhibition-dominated network with dense connectivity between FS cells and from FS to LR neurons. Biophysical models of LR but not RS cells precisely and continuously encode sustained input from afferent postsubicular head-direction cells. Thus, the unique intrinsic properties of LR neurons can support both the precision and persistence necessary to encode information over multiple timescales in the RSC.

scholarly journals Diversity amongst human cortical pyramidal neurons revealed via their sag currents and frequency preferences

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Homeira Moradi Chameh ◽  
Scott Rich ◽  
Lihua Wang ◽  
Fu-Der Chen ◽  
Liang Zhang ◽  
...  
Keyword(s):  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Theta Oscillations ◽  
Cortical Layers ◽  
Electrophysiological Properties ◽  
Theta Frequency ◽  
Subthreshold Resonance ◽  
Cortical Pyramidal Neurons ◽  
Whole Cell Recordings

AbstractIn the human neocortex coherent interlaminar theta oscillations are driven by deep cortical layers, suggesting neurons in these layers exhibit distinct electrophysiological properties. To characterize this potential distinctiveness, we use in vitro whole-cell recordings from cortical layers 2 and 3 (L2&3), layer 3c (L3c) and layer 5 (L5) of the human cortex. Across all layers we observe notable heterogeneity, indicating human cortical pyramidal neurons are an electrophysiologically diverse population. L5 pyramidal cells are the most excitable of these neurons and exhibit the most prominent sag current (abolished by blockade of the hyperpolarization activated cation current, Ih). While subthreshold resonance is more common in L3c and L5, we rarely observe this resonance at frequencies greater than 2 Hz. However, the frequency dependent gain of L5 neurons reveals they are most adept at tracking both delta and theta frequency inputs, a unique feature that may indirectly be important for the generation of cortical theta oscillations.

scholarly journals Organization of cortical and thalamic input to inhibitory neurons in mouse motor cortex

2021 ◽  
Author(s):  
Sandra U Okoro ◽  
Roman U Goz ◽  
Brigdet W. Njeri ◽  
Madhumita Harish ◽  
Catherine F. Ruff ◽  
...  
Keyword(s):  
Motor Cortex ◽  
Primary Motor Cortex ◽  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Inhibitory Neurons ◽  
Inhibitory Interneurons ◽  
Thalamic Input ◽  
Thalamic Projections ◽  
A Cell ◽  
Feedforward Inhibition

Understanding how feedforward inhibition regulates movement requires knowing how cortical and thalamic projections connect to inhibitory interneurons in primary motor cortex (M1). We quantified excitatory synaptic input from sensory cortex and thalamus onto two main classes of M1 inhibitory interneurons across all cortical layers: parvalbumin (PV) expressing fast-spiking cells and somatostatin (SOM) expressing low-threshold-spiking cells. Each projection innervated M1 interneurons with a unique laminar profile. While pyramidal neurons were excited by these cortical and thalamic inputs in the same layers, different interneuron types were excited in a distinct, complementary manner, suggesting feedforward inhibition from different inputs proceeds selectively via distinct circuits. Specifically, somatosensory cortex (S1) inputs primarily targeted PV+ neurons in upper layers (L2/3) but SOM+ neurons in middle layers (L5). Somatosensory thalamus (PO) inputs primarily targeted PV+ neurons in middle layers (L5). Our results show that long-range excitatory inputs target inhibitory neurons in a cell type-specific manner which contrasts with input to neighboring pyramidal cells. In contrast to feedforward inhibition providing generic inhibitory tone in cortex, circuits are selectively organized to recruit inhibition matched to incoming excitatory circuits.

scholarly journals Hypoxia-inducible factor-2α is crucial for proper brain development

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Kira Kleszka ◽  
Tristan Leu ◽  
Theresa Quinting ◽  
Holger Jastrow ◽  
Sonali Pechlivanis ◽  
...  
Keyword(s):  
Cognitive Abilities ◽  
Pyramidal Neurons ◽  
Cell Damage ◽  
Expression Patterns ◽  
Hypoxia Inducible Factor ◽  
Pyramidal Cells ◽  
Retrosplenial Cortex ◽  
Altered Expression ◽  
Adult Mice ◽  
Behavioral Studies

Abstract Sufficient tissue oxygenation is required for regular brain function; thus oxygen supply must be tightly regulated to avoid hypoxia and irreversible cell damage. If hypoxia occurs the transcription factor complex hypoxia-inducible factor (HIF) will accumulate and coordinate adaptation of cells to hypoxia. However, even under atmospheric O2 conditions stabilized HIF-2α protein was found in brains of adult mice. Mice with a neuro-specific knockout of Hif-2α showed a reduction of pyramidal neurons in the retrosplenial cortex (RSC), a brain region responsible for a range of cognitive functions, including memory and navigation. Accordingly, behavioral studies showed disturbed cognitive abilities in these mice. In search of the underlying mechanisms for the specific loss of pyramidal cells in the RSC, we found deficits in migration in neural stem cells from Hif-2α knockout mice due to altered expression patterns of genes highly associated with neuronal migration and positioning.

scholarly journals Control of impulsivity by Gi-protein signalling in layer-5 pyramidal neurons of the anterior cingulate cortex

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Bastiaan van der Veen ◽  
Sampath K. T. Kapanaiah ◽  
Kasyoka Kilonzo ◽  
Peter Steele-Perkins ◽  
Martin M. Jendryka ◽  
...  
Keyword(s):  
Gene Expression ◽  
Anterior Cingulate Cortex ◽  
Expression Analysis ◽  
Gene Expression Analysis ◽  
Pyramidal Neurons ◽  
Treatment Options ◽  
Pyramidal Cells ◽  
Cingulate Cortex ◽  
Cell Types ◽  
Anterior Cingulate

AbstractPathological impulsivity is a debilitating symptom of multiple psychiatric diseases with few effective treatment options. To identify druggable receptors with anti-impulsive action we developed a systematic target discovery approach combining behavioural chemogenetics and gene expression analysis. Spatially restricted inhibition of three subdivisions of the prefrontal cortex of mice revealed that the anterior cingulate cortex (ACC) regulates premature responding, a form of motor impulsivity. Probing three G-protein cascades with designer receptors, we found that the activation of Gi-signalling in layer-5 pyramidal cells (L5-PCs) of the ACC strongly, reproducibly, and selectively decreased challenge-induced impulsivity. Differential gene expression analysis across murine ACC cell-types and 402 GPCRs revealed that - among Gi-coupled receptor-encoding genes - Grm2 is the most selectively expressed in L5-PCs while alternative targets were scarce. Validating our approach, we confirmed that mGluR2 activation reduced premature responding. These results suggest Gi-coupled receptors in ACC L5-PCs as therapeutic targets for impulse control disorders.

scholarly journals Two Populations of Layer V Pyramidal Cells of the Mouse Neocortex: Development and Sensitivity to Anesthetics

2005 ◽  
Vol 94 (5) ◽  
pp. 3357-3367 ◽  
Author(s):  
Elodie Christophe ◽  
Nathalie Doerflinger ◽  
Daniel J. Lavery ◽  
Zoltán Molnár ◽  
Serge Charpak ◽  
...  
Keyword(s):  
Action Potential ◽  
Calcium Binding ◽  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Membrane Properties ◽  
Subcortical Structures ◽  
Contralateral Cortex ◽  
Layer V ◽  
Intrinsic Membrane Properties ◽  
Two Populations

Previous studies have shown that layer V pyramidal neurons projecting either to subcortical structures or the contralateral cortex undergo different morphological and electrophysiological patterns of development during the first three postnatal weeks. To isolate the determinants of this differential maturation, we analyzed the gene expression and intrinsic membrane properties of layer V pyramidal neurons projecting either to the superior colliculus (SC cells) or the contralateral cortex (CC cells) by combining whole cell recordings and single-cell RT-PCR in acute slices prepared from postnatal day (P) 5–7 or P21–30 old mice. Among the 24 genes tested, the calcium channel subunits α1B and α1C, the protease Nexin 1, and the calcium-binding protein calbindin were differentially expressed in adult SC and CC cells and the potassium channel subunit Kv4.3 was expressed preferentially in CC cells at both stages of development. Intrinsic membrane properties, including input resistance, amplitude of the hyperpolarization-activated current, and action potential threshold, differed quantitatively between the two populations as early as from the first postnatal week and persisted throughout adulthood. However, the two cell types had similar regular action potential firing behaviors at all developmental stages. Surprisingly, when we increased the duration of anesthesia with ketamine–xylazine or pentobarbital before decapitation, a proportion of mature SC cells, but not CC cells, fired bursts of action potentials. Together these results indicate that the two populations of layer V pyramidal neurons already start to differ during the first postnatal week and exhibit different firing capabilities after anesthesia.

Differential Impact of Miniature Synaptic Potentials on the Soma and Dendrites of Pyramidal Neurons In Vivo

1997 ◽  
Vol 78 (3) ◽  
pp. 1735-1739 ◽  
Author(s):  
Denis Paré ◽  
Elen Lebel ◽  
Eric J. Lang
Keyword(s):  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Input Resistance ◽  
Differential Impact ◽  
Synaptic Potentials ◽  
Ampa Antagonists ◽  
Intact Brain ◽  
The Impact

Paré, Denis, Elen LeBel, and Eric J. Lang. Differential impact of miniature synaptic potentials on the somata and dendrites of pyramidal neurons in vivo. J. Neurophysiol. 78: 1735–1739, 1997. We studied the impact of transmitter release resistant to tetrodotoxin (TTX) in morphologically identified neocortical pyramidal neurons recorded intracellularly in barbiturate-anesthetized cats. It was observed that TTX-resistant release occurs in pyramidal neurons in vivo and at much higher frequencies than was previously reported in vitro. Further, in agreement with previous findings indicating that GABAergic and glutamatergic synapses are differentially distributed in the somata and dendrites of pyramidal cells, we found that most miniature synaptic potentials were sensitive to γ-aminobutyric acid-A (GABAA) or α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) antagonists in presumed somatic and dendritic impalements, respectively. Pharmacological blockage of spontaneous synaptic events produced large increases in input resistance that were more important in dendritic (≈50%) than somatic (≈10%) impalements. These findings imply that in the intact brain, pyramidal neurons are submitted to an intense spike-independent synaptic bombardment that decreases the space constant of the cells. These results should be taken into account when extrapolating in vitro findings to intact brains.

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