Modeling apical and basal tree contribution to orientation selectivity in a mouse primary visual cortex layer 2/3 pyramidal cell

  1. Konstantinos-Evangelos Petousakis
  2. Jiyoung Park
  3. Athanasia Papoutsi
  4. Stelios Smirnakis  Is a corresponding author
  5. Panayiota Poirazi  Is a corresponding author
  1. Department of Biology, University of Crete, Greece
  2. IMBB, FORTH, Greece
  3. Department of Neurology, Brigham and Women’s Hospital and Jamaica Plain Veterans Administration Hospital, Harvard Medical School, United States
6 figures, 4 tables and 1 additional file

Figures

Figure 1 with 1 supplement
Dendritic properties of a L2/3 V1 neuron model.

(A) Graphical representation of the iterative paired-pulse protocol. Green dots represent allocated synapses. Synapses were activated only within the designated (red) dendritic segment, with all …

Figure 1—figure supplement 1
Visualization of dendritic non-linear properties.

(A) Expected vs Actual plot for all basal dendrites undergoing the I3P protocol for 1–200 synapses. Blue line represents the dendrite in Figure 1B (basal dendrite #0). (B) Same as A, but for all …

Figure 2 with 5 supplements
Neuronal orientation preference is robust and resists dendritic tuning disparity.

(A) Orientation tuning curve for the ‘biologically plausible’ model. (B) Example from a configuration of a model neuron set to a disparity of 40°. Right-side polar plots display the distribution of …

Figure 2—figure supplement 1
Comparing model output with two-photon imaging data.

Simultaneous recordings from basal dendritic segments and somata of L2/3 V1 pyramidal neurons were performed in anesthetized mice (spontaneous activity of 11 neurons from 2 mice, see Extended …

Figure 2—figure supplement 2
Properties of the GcaMP6s kernel.

(A) Illustration of the output of the kernel function for a single event (AP) occurring at t0 = 500ms. (marked as a red line). (B) Response intensity as a function of the number of events (APs) …

Figure 2—figure supplement 3
Waveforms of detected calcium fluorescence events.

Somatic waveforms in blue, basal dendritic waveforms in red. Spike onset detected at t=5 dt. (A) Waveforms from all detected events from both mice. (B) Waveforms from all detected events in mouse 1. …

Figure 2—figure supplement 4
Event-triggered averages of detected events and statistical testing of event pairs.

(A) Event-triggered averages for somatic (blue) and basal dendrite (red) events in mouse 1. (B) Event-triggered averages for somatic (blue) and basal dendrite (red) events in mouse 2. Note the …

Figure 2—figure supplement 5
Comparison of orientation tuning behavior seen in the model under control (blue) and apical dendrite ablation (red) configurations.

Note that the y-axis shows the normalized response (firing rate values divided by their corresponding maximum). Error bars: standard error of the mean.

Figure 3 with 1 supplement
Neuronal output relies disproportionately on apical sodium conductance.

(A) Diagram describing the ionic intervention protocol, with example traces on the right. Shaded areas on the traces denote the pre-spike (grey) and post-spike (red) intervention time windows. (B) …

Figure 3—figure supplement 1
Example traces showing the spatiotemporal evolution of somatodendritic voltage before, during and after the generation of a dendritic-sodium-mediated somatic spike, across different dendritic paths.

(A) Visualization of basal dendrites. Colors correspond to traces in panels B and C. (B) Voltage traces from the basal dendrites and soma (blue) around the occurrence of an apically driven somatic …

Figure 4 with 1 supplement
Orientation tuning critically depends on apical sodium conductance and ampa/nmda activity.

(A) Orientation tuning curves (left) and mean OSI values (right) for the experiment where stimulus-driven synapses are completely absent on either the apical (‘apical target’; red) or basal (‘basal …

Figure 4—figure supplement 1
Results from experiments similar to Figure 4C, only with a reduction in apical sodium conductance.

(A) Apical gNa decreased by 5%. Elimination of the apical sodium component results in total loss of tuning. (B) Apical gNa decreased by 10%. Unlike A, elimination of the apical or basal sodium …

Figure 5 with 1 supplement
Dendritic morphological and electrophysiological properties affect both local and somatic behavior.

(A) Left: Attenuation of a 20 mV dendritic EPSP (measured at the soma) as a function of dendritic segment length. Right: Comparison of length-normalized EPSP attenuation at the soma between apical …

Figure 5—figure supplement 1
Results from analyses similar to Figure 5.

Dendritic segments were stimulated with a number of synapses sufficient to elicit dendritic sodium spiking, and the attenuation at the soma was measured. (A) Somatic sodium spike attenuation as a …

Graphical representation of AP generation via bimodal Input coincidence in a L2/3 V1 pyramidal neuron model.

Action potential generation requires the spatiotemporal coincidence of apical sodium spikes with either basal sodium spikes or significant basal depolarizations, allowing the neuron to respond to …

Tables

Table 1
Outline of passive, active, and synaptic mechanisms present in the model neuron.
Compartment typePassive/active mechanismsSynaptic mechanisms
SomaHodgkin/Huxley voltage-gated Na+ channels
Hodgkin/Huxley voltage-gated K+ channels
Muscarinic voltage-gated K+ channels
A-Type voltage-gated K+ channels
T-Type Ca++ channels
High voltage activated (HVA) Ca++ channels
Calcium-dependent K+ channels
Active ATP Ca++ pumps
GABAA (background-driven)
Basal dendritesAMPA (background-driven)
NMDA (background-driven)
GABAA (background-driven)
AMPA (stimulus-driven)
NMDA (stimulus-driven)
GABAA (stimulus-driven)
Apical dendrites
Table 2
Outline of membrane mechanism conductances (not synaptic).

Reproduced from Park et al., 2019.

Conductance (mS/cm2)SomaApicalBasal
gNa0.5050.3030.303
gKdr0.051.5*10–31.5*10–3
gKm2.8*10–31.27*10–31.27*10–3
gA5.4Diameter ≤0.8 μm: 108
Diameter >0.8 μm: 10.8
Diameter ≤0.8 μm: 108
Diameter >0.8 μm: 10.8
gT0.03x≤260 μm: 0.029*sin(0.009*x+0.88)
x>260 μm: 0.012
0.03+6*10–5*x
gHVA0.05*10–3x≤260 μm:
0.049*10–3*sin(0.009*x+0.88)
x>260 μm: 0.02*10–3
0.05*10–3+10–7*x
gKCa2.1*10–32.1*10–32.1*10–3
Table 3
Outline of model electrophysiological properties.

RMP: resting membrane potential, IR: Input Resistance measured at hyperpolarizing current (–0.04 nA), AP: action potential, AHP: after hyperpolarization measured at depolarizing current (0.16 nA), …

ModelCho et al., 2010
RMP, mV–79–78.56 ± 1.34
IR, MΩ123.6125.2 ± 8.2
τ, ms17.316 ± 0.7
AP amplitude, mV66.167.8 ± 1.8
AP threshold, mV–41.8–37.7 ± 1.3
AHP, mV17.913.3 ± 0.5
P-T time, ms38.655.3 ± 2.7
AP adaptation1.161.18 ± 0.02
Table 4
Outline of synaptic mechanism conductances and time constants.

Reproduced from Park et al., 2019.

Conductance (nS)τ1, msτ2, ms
NMDA1.15230
AMPA0.840.12.5
GABAA1.250.21.4

Additional files

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