scholarly journals Learning enhances behaviorally relevant representations in apical dendrites

2021 ◽  
Author(s):  
Sam E. Benezra ◽  
Kripa B. Patel ◽  
Citlali Pérez Campos ◽  
Elizabeth M. C. Hillman ◽  
Randy M Bruno
Keyword(s):  
Pyramidal Neurons ◽  
Animal Movement ◽  
Apical Dendrite ◽  
Stimulus Exposure ◽  
Biophysical Properties ◽  
Two Photon ◽  
Apical Tuft ◽  
Whisker Stimulation ◽  
Cortical Representations ◽  
Apical Dendrites

Learning alters cortical representations and improves perception. Apical tuft dendrites in Layer 1, which are unique in their connectivity and biophysical properties, may be a key site of learning-induced plasticity. We used both two-photon and SCAPE microscopy to longitudinally track tuft-wide calcium spikes in apical dendrites of Layer 5 pyramidal neurons as mice learned a tactile behavior. Mice were trained to discriminate two orthogonal directions of whisker stimulation. Reinforcement learning, but not repeated stimulus exposure, enhanced tuft selectivity for both directions equally, even though only one was associated with reward. Selective tufts emerged from initially unresponsive or low-selectivity populations. Animal movement and choice did not account for changes in stimulus selectivity. Enhanced selectivity persisted even after rewards were removed and animals ceased performing the task. We conclude that learning produces long-lasting realignment of apical dendrite tuft responses to behaviorally relevant dimensions of a task.

scholarly journals Apical length governs computational diversity of L5 pyramidal neurons

2019 ◽  
Author(s):  
Alessandro R. Galloni ◽  
Aeron Laffere ◽  
Ede Rancz
Keyword(s):  
Action Potentials ◽  
Pyramidal Neurons ◽  
Apical Dendrite ◽  
Common Assumption ◽  
Dendritic Excitability ◽  
Visual Cortices ◽  
The Common ◽  
Channel Dependent ◽  
Apical Dendrites ◽  
The Brain

AbstractAnatomical similarity across the neocortex has led to the common assumption that the circuitry is modular and performs stereotyped computations. Layer 5 pyramidal neurons (L5PNs) in particular are thought to be central to cortical computation because of their extensive arborisation and nonlinear dendritic operations. Here, we demonstrate that computations associated with dendritic Ca2+ plateaus in L5PNs vary substantially between the primary and secondary visual cortices. L5PNs in the secondary visual cortex show reduced dendritic excitability and smaller propensity for burst firing. This reduced excitability is correlated with shorter apical dendrites. Using numerical modelling, we uncover a universal principle underlying the influence of apical length on dendritic backpropagation and excitability, based on a Na+ channel-dependent broadening of backpropagating action potentials. In summary, we provide new insights into the modulation of dendritic excitability by apical dendrite length and show that the operational repertoire of L5 neurons is not universal throughout the brain.

scholarly journals Site Independence of EPSP Time Course Is Mediated by DendriticI h in Neocortical Pyramidal Neurons

2000 ◽  
Vol 83 (5) ◽  
pp. 3177-3182 ◽  
Author(s):  
Stephen R. Williams ◽  
Greg J. Stuart
Keyword(s):  
Sodium Channels ◽  
Temporal Summation ◽  
Time Course ◽  
Pyramidal Neurons ◽  
Apical Dendrite ◽  
Linear Increase ◽  
Nonuniform Distribution ◽  
Excitatory Synaptic Input ◽  
Pharmacological Blockade ◽  
Apical Dendrites

Neocortical layer 5 pyramidal neurons possess long apical dendrites that receive a significant portion of the neurons excitatory synaptic input. Passive neuronal models indicate that the time course of excitatory postsynaptic potentials (EPSPs) generated in the apical dendrite will be prolonged as they propagate toward the soma. EPSP propagation may, however, be influenced by the recruitment of dendritic voltage-activated channels. Here we investigate the properties and distribution of I h channels in the axon, soma, and apical dendrites of neocortical layer 5 pyramidal neurons, and their effect on EPSP time course. We find a linear increase (9 pA/100 μm) in the density of dendritic I hchannels with distance from soma. This nonuniform distribution of I h channels generates site independence of EPSP time course, such that the half-width at the soma of distally generated EPSPs (up to 435 μm from soma) was similar to somatically generated EPSPs. As a corollary, a normalization of temporal summation of EPSPs was observed. The site independence of somatic EPSP time course was found to collapse after pharmacological blockade of I h channels, revealing pronounced temporal summation of distally generated EPSPs, which could be further enhanced by TTX-sensitive sodium channels. These data indicate that an increasing density of apical dendritic I hchannels mitigates the influence of cable filtering on somatic EPSP time course and temporal summation in neocortical layer 5 pyramidal neurons.

scholarly journals Learning from unexpected events in the neocortical microcircuit

2021 ◽  
Author(s):  
Colleen J. Gillon ◽  
Jason E. Pina ◽  
Jérôme A. Lecoq ◽  
Ruweida Ahmed ◽  
Yazan Billeh ◽  
...  
Keyword(s):  
Pyramidal Neurons ◽  
Top Down ◽  
Unexpected Events ◽  
Unexpected Event ◽  
Bottom Up ◽  
Two Photon ◽  
Cortical Responses ◽  
To Receive ◽  
Hierarchical Computation ◽  
Apical Dendrites

AbstractScientists have long conjectured that the neocortex learns the structure of the environment in a predictive, hierarchical manner. To do so, expected, predictable features are differentiated from unexpected ones by comparing bottom-up and top-down streams of data. It is theorized that the neocortex then changes the representation of incoming stimuli, guided by differences in the responses to expected and unexpected events. Such differences in cortical responses have been observed; however, it remains unknown whether these unexpected event signals govern subsequent changes in the brain’s stimulus representations, and, thus, govern learning. Here, we show that unexpected event signals predict subsequent changes in responses to expected and unexpected stimuli in individual neurons and distal apical dendrites that are tracked over a period of days. These findings were obtained by observing layer 2/3 and layer 5 pyramidal neurons in primary visual cortex of awake, behaving mice using two-photon calcium imaging. We found that many neurons in both layers 2/3 and 5 showed large differences between their responses to expected and unexpected events. These unexpected event signals also determined how the responses evolved over subsequent days, in a manner that was different between the somata and distal apical dendrites. This difference between the somata and distal apical dendrites may be important for hierarchical computation, given that these two compartments tend to receive bottom-up and top-down information, respectively. Together, our results provide novel evidence that the neocortex indeed instantiates a predictive hierarchical model in which unexpected events drive learning.

scholarly journals Long-term Transverse Imaging of the Hippocampus with Glass Microperiscopes

2021 ◽  
Author(s):  
William T Redman ◽  
Nora S Wolcott ◽  
Luca Montelisciani ◽  
Gabriel Luna ◽  
Tyler D Marks ◽  
...  
Keyword(s):  
Cognitive Processes ◽  
Calcium Imaging ◽  
Pyramidal Neurons ◽  
Spatial Information ◽  
Anatomical Distribution ◽  
Two Photon ◽  
Information Finding ◽  
Apical Dendrites

The hippocampus consists of a stereotyped neuronal circuit repeated along the septal-temporal axis. This transverse circuit contains distinct subfields with stereotyped connectivity that support crucial cognitive processes, including episodic and spatial memory. However, comprehensive measurements across the transverse hippocampal circuit in vivo are intractable with existing techniques. Here, we developed an approach for two-photon imaging of the transverse hippocampal plane in awake mice via implanted glass microperiscopes, allowing optical access to the major hippocampal subfields and to the dendritic arbor of pyramidal neurons. Using this approach, we tracked dendritic morphological dynamics on CA1 apical dendrites and characterized spine turnover. We then used calcium imaging to quantify the prevalence of place and speed cells across subfields. Finally, we measured the anatomical distribution of spatial information, finding a non-uniform distribution of spatial selectivity along the DG-to-CA1 axis. This approach extends the existing toolbox for structural and functional measurements of hippocampal circuitry.

Glutamate Receptors Form Hot Spots on Apical Dendrites of Neocortical Pyramidal Neurons

2001 ◽  
Vol 86 (3) ◽  
pp. 1412-1421 ◽  
Author(s):  
A. Frick ◽  
W. Zieglgänsberger ◽  
H.-U. Dodt
Keyword(s):  
Glutamate Receptors ◽  
Hot Spots ◽  
Pyramidal Neurons ◽  
Flash Photolysis ◽  
Apical Dendrite ◽  
Brain Regions ◽  
Branch Points ◽  
Cortical Pyramidal Neurons ◽  
Layer V ◽  
Apical Dendrites

Apical dendrites of layer V cortical pyramidal neurons are a major target for glutamatergic synaptic inputs from cortical and subcortical brain regions. Because innervation from these regions is somewhat laminar along the dendrites, knowing the distribution of glutamate receptors on the apical dendrites is of prime importance for understanding the function of neural circuits in the neocortex. To examine this issue, we used infrared-guided laser stimulation combined with whole cell recordings to quantify the spatial distribution of glutamate receptors along the apical dendrites of layer V pyramidal neurons. Focally applied (<10 μm) flash photolysis of caged glutamate on the soma and along the apical dendrite revealed a highly nonuniform distribution of glutamate responsivity. Up to four membrane areas (extent 22 μm) of enhanced glutamate responsivity (hot spots) were detected on the dendrites with the amplitude and integral of glutamate-evoked responses at hot spots being three times larger than responses evoked at neighboring sites. We found no association of these physiological hot spots with dendritic branch points. It appeared that the larger responses evoked at hot spots resulted from an increase in activation of both α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) and N-methyl-d-aspartate (NMDA) receptors and not a recruitment of voltage-activated sodium or calcium conductances. Stimulation of hot spots did, however, facilitate the triggering of both Na+ spikes and Ca2+ spikes, suggesting that hot spots may serve as dendritic initiation zones for regenerative spikes.

High I h Channel Density in the Distal Apical Dendrite of Layer V Pyramidal Cells Increases Bidirectional Attenuation of EPSPs

2001 ◽  
Vol 85 (2) ◽  
pp. 855-868 ◽  
Author(s):  
Thomas Berger ◽  
Matthew E. Larkum ◽  
Hans-R. Lüscher
Keyword(s):  
Temporal Summation ◽  
Pyramidal Neurons ◽  
Brain Slices ◽  
Pyramidal Cells ◽  
Signal Propagation ◽  
Apical Dendrite ◽  
Distal Dendrite ◽  
Channel Density ◽  
Apical Tuft ◽  
Layer V

Despite the wealth of recent research on active signal propagation along the dendrites of layer V neocortical pyramidal neurons, there is still little known regarding the traffic of subthreshold synaptic signals. We present a study using three simultaneous whole cell recordings on the apical dendrites of these cells in acute rat brain slices to examine the spread and attenuation of spontaneous excitatory postsynaptic potentials (sEPSPs). Equal current injections at each of a pair of sites separated by ∼500 μm on the apical dendrite resulted in equal voltage transients at the other site (“reciprocity”), thus disclosing linear behavior of the neuron. The mean apparent “length constants” of the apical dendrite were 273 and 446 μm for somatopetal and somatofugal sEPSPs, respectively. Trains of artificial EPSPs did not show temporal summation. Blockade of the hyperpolarization-activated cation current ( I h) resulted in less attenuation by 17% for somatopetal and by 47% for somatofugal sEPSPs. A pronounced location-dependent temporal summation of EPSP trains was seen. The subcellular distribution and biophysical properties of I h were studied in cell-attached patches. Within less than ∼400 μm of the soma, a low density of ∼3 pA/μm2 was found, which increased to ∼40 pA/μm2 in the apical distal dendrite. I h showed activation and deactivation kinetics with time constants faster than 40 ms and half-maximal activation at −95 mV. These findings suggest that integration of synaptic input to the apical tuft and the basal dendrites occurs spatially independently. This is due to a high I h channel density in the apical tuft that increases the electrotonic distance between these two compartments in comparison to a passive dendrite.

Inter-Ictal- and Ictal-Like Epileptic Discharges in the Dendritic Tree of Neocortical Pyramidal Neurons

2002 ◽  
Vol 88 (6) ◽  
pp. 2954-2962 ◽  
Author(s):  
Yitzhak Schiller
Keyword(s):  
Calcium Imaging ◽  
Pyramidal Neurons ◽  
Dendritic Tree ◽  
Apical Dendrite ◽  
Peak Amplitude ◽  
Peak Voltage ◽  
Voltage Gated ◽  
Epileptic Discharges ◽  
Electrographic Seizures ◽  
Apical Dendrites

Dendritic mechanisms have been implied to play a key role in the formation of epileptic discharges. However, presently only a handful of direct dendritic recordings have been reported during epileptic discharges. In this study, I performed simultaneous voltage recordings from the soma and apical dendrite of the same neuron combined with calcium-imaging measurements to investigate inter-ictal- and ictal-like epileptic discharges in dendrites of layer 5 pyramidal neurons. Neocortical brain slices treated with bicuculline (BCC) produced both isolated “inter-ictal” paroxysymal depolarization shift (PDS) responses and electrographic seizures. Concomitant voltage recordings from the soma and apical dendrite revealed that PDS responses developed in both the apical dendrites and soma. However, the two responses differed from one another. In apical dendrites, the PDS was significantly higher in amplitude and shorter in duration compared with the somatic PDS. The PDS response in dendrites had a peak amplitude of 68.9 ± 2.2 (SD) mV, peak voltage value of 9.3 ± 2.7 mV, and half-width of 203.8 ± 38.4 ms. In contrast, the somatic PDS had a peak amplitude of 48.7 ± 2.7 mV, peak voltage value of −11.9 ± 3.1 mV, and half-width of 247.8 ± 57.3 ms ( P < 0.01, n = 18). In addition the apical dendritic PDS always preceded the somatic counterpart in all 18 neurons examined. Concomitant calcium-imaging measurements showed the PDS evoked large calcium influx into the entire dendritic tree including the apical tuft, basal, and oblique dendrites. The PDS evoked [Ca2+]i were not uniform along the dendritic tree, being highest in the oblique dendrites (71.3 ± 14.5 μM) and lowest at the distal tuft branches (9.3 ± 0.7 μM). The PDS responses persisted after blockade of voltage-gated sodium channels by intracellular QX-314 but became narrower (by 69.6 ± 9.7%) following intracellular administration of the voltage-gated calcium channel blocker D600. Electrographic seizures recorded in the soma and apical dendrites were composed of recurrent bursts. The initial bursts represented PDS responses. During the seizure the amplitude of bursts gradually attenuated and reached an average value of 26 ± 13% of the initial ictal PDS burst. Double recordings during electrographic seizures revealed the initial one to four ictal bursts appeared first at the apical dendrite while later ictal bursts were always observed first at the soma. In conclusion, the results of this study show “inter-ictal” PDS responses originated in the apical dendritic tree, were partially mediated by voltage-gated calcium channels and spread throughout the dendritic tree including the fine tuft, basal, and oblique dendrites. During electrographic seizures the origin of epileptic bursts shifted from the apical dendritic tree to the soma-basal region.

scholarly journals Freeze-Frame Imaging of Dendritic Calcium Signals With TubuTag

2021 ◽  
Vol 14 ◽  
Author(s):  
Alberto Perez-Alvarez ◽  
Florian Huhn ◽  
Céline D. Dürst ◽  
Andreas Franzelin ◽  
Paul J. Lamothe-Molina ◽  
...  
Keyword(s):  
Pyramidal Neurons ◽  
Apical Dendrite ◽  
Large Field ◽  
Metabotropic Receptors ◽  
Calcium Signals ◽  
Two Photon ◽  
Rich Diversity ◽  
Large Populations ◽  
Subcellular Resolution ◽  
Large Neurons

The extensive dendritic arbor of neurons is thought to be actively involved in the processing of information. Dendrites contain a rich diversity of ligand- and voltage-activated ion channels as well as metabotropic receptors. In addition, they are capable of releasing calcium from intracellular stores. Under specific conditions, large neurons produce calcium spikes that are locally restricted to a dendritic section. To investigate calcium signaling in dendrites, we introduce TubuTag, a genetically encoded ratiometric calcium sensor anchored to the cytoskeleton. TubuTag integrates cytoplasmic calcium signals by irreversible photoconversion from green to red fluorescence when illuminated with violet light. We used a custom two-photon microscope with a large field of view to image pyramidal neurons in CA1 at subcellular resolution. Photoconversion was strongest in the most distal parts of the apical dendrite, suggesting a gradient in the amplitude of dendritic calcium signals. As the read-out of fluorescence can be performed several hours after photoconversion, TubuTag will help investigating dendritic signal integration and calcium homeostasis in large populations of neurons.

scholarly journals Apical length governs computational diversity of layer 5 pyramidal neurons

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Alessandro R Galloni ◽  
Aeron Laffere ◽  
Ede Rancz
Keyword(s):  
Pyramidal Neurons ◽  
Apical Dendrite ◽  
Na Channel ◽  
Common Assumption ◽  
Dendritic Excitability ◽  
Visual Cortices ◽  
The Common ◽  
Channel Dependent ◽  
Apical Dendrites ◽  
The Brain

Anatomical similarity across the neocortex has led to the common assumption that the circuitry is modular and performs stereotyped computations. Layer 5 pyramidal neurons (L5PNs) in particular are thought to be central to cortical computation because of their extensive arborisation and nonlinear dendritic operations. Here, we demonstrate that computations associated with dendritic Ca2+ plateaus in mouse L5PNs vary substantially between the primary and secondary visual cortices. L5PNs in the secondary visual cortex show reduced dendritic excitability and smaller propensity for burst firing. This reduced excitability is correlated with shorter apical dendrites. Using numerical modelling, we uncover a universal principle underlying the influence of apical length on dendritic backpropagation and excitability, based on a Na+ channel-dependent broadening of backpropagating action potentials. In summary, we provide new insights into the modulation of dendritic excitability by apical dendrite length and show that the operational repertoire of L5PNs is not universal throughout the brain.

scholarly journals Neuronal pannexin-1 channels are not molecular routes of water influx during spreading depolarization-induced dendritic beading

2016 ◽  
Vol 37 (5) ◽  
pp. 1626-1633 ◽  
Author(s):  
Jeremy Sword ◽  
Deborah Croom ◽  
Phil L Wang ◽  
Roger J Thompson ◽  
Sergei A Kirov
Keyword(s):  
Pyramidal Neurons ◽  
Transport Mechanisms ◽  
Coupled Transport ◽  
Pannexin 1 ◽  
Two Photon ◽  
Spreading Depolarization ◽  
Water Influx ◽  
Membrane Bound ◽  
Genetic Deletion

Spreading depolarization-induced focal dendritic swelling (beading) is an early hallmark of neuronal cytotoxic edema. Pyramidal neurons lack membrane-bound aquaporins posing a question of how water enters neurons during spreading depolarization. Recently, we have identified chloride-coupled transport mechanisms that can, at least in part, participate in dendritic beading. Yet transporter-mediated ion and water fluxes could be paralleled by water entry through additional pathways such as large-pore pannexin-1 channels opened by spreading depolarization. Using real-time in vivo two-photon imaging in mice with pharmacological inhibition or conditional genetic deletion of pannexin-1, we showed that pannexin-1 channels are not required for spreading depolarization-induced focal dendritic swelling.

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