A Comparison of Partial Information Decompositions Using Data from Real and Simulated Layer 5b Pyramidal Cells
<p>Reconstruction of a biocytin-filled L5b pyramidal neuron recorded from the rat somatosensory cortex. Basal and apical tuft dendrites are indicated. These sets of dendrites directly influence two distinct integration zones that can emit spikes: the axon initial segment close to the soma of the neuron, which initiates Na <math display="inline"><semantics> <msup> <mrow/> <mo>+</mo> </msup> </semantics></math>-dependent APs, and the integration zone in the apical dendrite, which initiates dendritic Ca<math display="inline"><semantics> <msup> <mrow/> <mrow> <mn>2</mn> <mo>+</mo> </mrow> </msup> </semantics></math> spikes.</p> "> Figure 2
<p>Dual dendritic and somatic patch-clamp recording from a L5b pyramidal neuron of rat somatosensory cortex enables the study of amplification of somatic AP output by apical dendritic input and its regulation by dendritic inhibition. (<b>A</b>) Locations of dual dendritic and somatic patch-clamp recordings are indicated on a biocytin-filled L5 pyramidal neuron. After recordings in the control condition, the GABA <math display="inline"><semantics> <msub> <mrow/> <mi mathvariant="normal">B</mi> </msub> </semantics></math> agonist baclofen (50 <math display="inline"><semantics> <mi mathvariant="sans-serif">μ</mi> </semantics></math>M) was puffed onto the apical dendrite at 50 to 100 <math display="inline"><semantics> <mi mathvariant="sans-serif">μ</mi> </semantics></math>M distal to the dendritic patch pipette. Example membrane potential responses to combined current injections into soma and dendrite are shown in control condition (<b>left</b>) and during the puff of baclofen (<b>right</b>). Peak current amplitude was 1000 pA for dendritic and somatic current injections. (<b>B</b>) Top, injected current waveforms based on in vivo responses to sensory stimulation [<a href="#B54-entropy-24-01021" class="html-bibr">54</a>]. Dendritic current is shown in green, somatic in purple. Bottom, raster plot of APs emitted in individual episodes during increasing levels of dendritic and somatic stimulation strength. Control is shown on the left. A raster plot of APs emitted in the same neuron during activation of dendritic GABA <math display="inline"><semantics> <msub> <mrow/> <mi mathvariant="normal">B</mi> </msub> </semantics></math> Rs by a puff of baclofen onto the apical dendrite is shown on the right. Different levels of the injected current in 36 combinations are indicated by the right colour bars (S, somatic; D, dendritic). The peak amplitude of the current waveform was increased from 0 pA (white) to 1250 (black) in soma and dendrite, respectively. Step size was 250 pA. (<b>C</b>) Peri-stimulus time histogram of APs across all current combinations for both conditions. All data were obtained from [<a href="#B28-entropy-24-01021" class="html-bibr">28</a>].</p> "> Figure 3
<p>Physiological L5b neuronal recording data. For each of the 15 neurons under each of the Control and Baclofen conditions, the values of the four normalised classic mutual information measures that are involved in the definition of a PID are displayed. Their values are given as their relative contributions to the joint mutual information in each case.</p> "> Figure 4
<p>Physiological L5b neuronal recording data. Plots of each PID component, connected by each neuron, for the five PID methods: (<b>A</b>) UnqB, (<b>B</b>) UnqA, (<b>C</b>) Shd and (<b>D</b>) Syn. For each neuron under each experimental condition, the values of the PID components are given as proportions of the respective joint mutual information.</p> "> Figure 5
<p>Physiological L5b neuronal recording data. Within-neuron differences in each PID component for 15 neurons, taken as Baclofen minus Control. Different vertical scales are employed for each component.</p> "> Figure 6
<p>Physiological L5b neuronal recording data. A plot of the unique information asymmetries provided by each of the five PIDs for each experimental condition for 15 neurons.</p> "> Figure 7
<p>Simulated mouse L5b neuron model data. The number of action potentials emitted are provided for 651 combinations of the numbers of basal and apical inputs to the cell. The number of basal inputs ranges from 0 to 300 in steps of 10. The number of apical inputs ranges from 0 to 200 in steps of 10.</p> "> Figure 8
<p>Simulated mouse L5b neuron model data. Stacked bar plots showing the values of the components for each of the five PIDs using the full data set.</p> "> Figure 9
<p>Simulated mouse L5b neuron model data. Ibroja (<b>left column</b>), Idep (<b>middle column</b>) and Iccs (<b>right column</b>) PIDs for various combinations of increasing ranges of basal inputs and increasing ranges of apical inputs: B1 (0–100), B2 (0–130), B3 (0–150), B4 (0–170), B5 (0–200) and A1 (0–100), A2 (0–130), A3 (0–150), A4 (0–170), A5 (0–200).</p> "> Figure 10
<p>Simulated mouse L5b neuron model data. Ipm (<b>left column</b>) and Isx (<b>right column</b>) PIDs for various combinations of increasing ranges of basal inputs and increasing ranges of apical inputs: B1 (0–100), B2 (0–130), B3 (0–150), B4 (0–170), B5 (0–200) and A1 (0–100), A2 (0–130), A3 (0–150), A4 (0–170), A5 (0–200).</p> "> Figure 11
<p>Simulated mouse L5b neuron model data. Ibroja (<b>left column</b>), Idep (<b>middle column</b>) and Iccs (<b>right column</b>) PIDs for various combinations of increasing ranges of basal inputs and three fixed ranges of apical inputs: B1 (0–100), B2 (0–130), B3 (0–150), B4 (0–170), B5 (0–200), B6 (0–250), B7 (0–300) and A1 (0–100), A6 (110–150) and A7 (160–200).</p> "> Figure 12
<p>Simulated mouse L5b neuron model data. Ipm (<b>left column</b>) and Isx (<b>right column</b>) PIDs for various combinations of increasing ranges of basal inputs and three fixed ranges of apical inputs: B1 (0–100), B2 (0–130), B3 (0–150), B4 (0–170), B5 (0–200), B6 (0–250), B7 (0–300) and A1 (0–100), A6 (110–150) and A7 (160–200).</p> "> Figure A1
<p>A dependency lattice of models reproduced from [<a href="#B63-entropy-24-01021" class="html-bibr">63</a>]. Edges coloured green (b, d, i, k) correspond to adding the constraint <math display="inline"><semantics> <mrow> <msub> <mi>S</mi> <mn>1</mn> </msub> <mi>T</mi> </mrow> </semantics></math> to the model immediately below. Edges coloured red (c, f, h, j) correspond to adding the constraint <math display="inline"><semantics> <mrow> <msub> <mi>S</mi> <mn>2</mn> </msub> <mi>T</mi> </mrow> </semantics></math> to the model immediately below.</p> "> Figure A2
<p>The dependency lattice with the value of the joint mutual information attached to each of the models defined in <a href="#entropy-24-01021-f0A1" class="html-fig">Figure A1</a>. Edges coloured green (b, d, i, k) correspond to adding the constraint <math display="inline"><semantics> <mrow> <msub> <mi>S</mi> <mn>1</mn> </msub> <mi>T</mi> </mrow> </semantics></math> to the model immediately below. The values of <math display="inline"><semantics> <mrow> <mi>b</mi> <mo>,</mo> <mi>d</mi> <mo>,</mo> <mi>i</mi> <mo>,</mo> <mi>k</mi> </mrow> </semantics></math> are shown, and we can see that Unq<math display="inline"><semantics> <msub> <mi>S</mi> <mn>1</mn> </msub> </semantics></math> = 0.2296.</p> "> Figure A3
<p>Physiological L5b neuronal recording data. Plots of each PID component, connected by each neuron, for seven PID methods: (<b>A</b>) UnqB, (<b>B</b>) UnqA, (<b>C</b>) Shd and (<b>D</b>) Syn. For each neuron under each experimental condition, the values of the PID components are given as proportions of the respective joint mutual informations.</p> "> Figure A4
<p>Physiological L5b neuronal recording data. Within-neuron differences in each PID component for 15 neurons, taken as Baclofen minus Control. Different vertical scales are employed for each component.</p> ">
Abstract
:1. Introduction
2. Methods
2.1. Data
2.2. Notation and Definitions
2.3. Partial Information Decomposition
denotes the unique information that B conveys about Y; | |||
is the unique information that A conveys about Y; | |||
gives the shared (or redundant) information that both B and A have about Y; | |||
is the synergy or information that the joint variable has about Y that cannot be obtained by observing B and A separately. |
2.4. Unique Information Asymmetry
2.5. Pointwise PID Methods
2.6. Ideal Properties of Cooperative Context-Sensitivity
- CCS1:
- The drive, B, is sufficient for the output to transmit information about the input, so context, A, is not necessary.
- CCS2:
- The drive, B, is necessary for the output to transmit information about the input, so context, A, is not sufficient.
- CCS3:
- The output transmits unique information about the drive, B, but little or no unique information or misinformation about the context, A, although synergistic or shared mechanistic components, or both, are present.
- CCS4:
- The context strengthens the transmission of information about B when B is weak. As the strength of B increases, the synergy and shared mechanistic information decrease.
2.7. Statistics
2.8. Software
3. Results
3.1. Real Data from Patch-Clamp Recordings in L5b Pyramidal Neurons
3.1.1. Classic Mutual Information Measures
3.1.2. Comparison of PID Components
3.1.3. Analysis of Within-Neuron Differences in PID Components
3.1.4. Statistical Significance
3.1.5. Unique Information Asymmetry
3.2. Simulated Data from a Detailed Compartmental Model
3.2.1. PID Analysis for Varying Strengths of Basal and Apical Input
3.2.2. Cooperative Context-Sensitivity as Revealed by PID Analyses
Properties CSS1 and CSS2
Property CSS3
Property CSS4
4. Conclusions and Discussion
4.1. Rat Somatosensory Cortical L5b Pyramidal Neuron Recording Data
4.2. Simulated Mouse L5b Neuron Model Data
4.3. Biological Implications
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
Partial Information Decomposition | |
PID | Partial Information Decomposition, with components UnqB, UnqA, Shd and Syn, defined in Section 2.3 |
Ibroja | The PID developed by Bertschinger et al. [3] |
Iccs | The PID developed by Ince [5] |
Idep | The PID developed by James et al. [62] |
Iig | The PID developed by Niu and Quinn [7] |
Imin | The PID developed by Williams and Beer [1] |
Iprec | The PID developed by Kolchinsky [10,50] |
Iproj | The PID developed by Harder et al. [2] |
Ipm | The PID developed by Finn and Lizier. [6] |
Isx | The PID developed by Makkeh et al. [8] |
Others | |
AMPA | -amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid |
AP | Action potential |
GABA | gamma-aminobutyric acid |
GABA | A G protein-coupled receptor for GABA |
JMI | Joint mutual information between the output Y and the inputs , as defined in Section 2.2 |
L5b | Layer 5b |
NMDA | N-methyl-D-aspartate |
UIA | Unique information asymmetry, as defined in Section 2.4 |
Appendix A. Introduction
T | |||
---|---|---|---|
0 | 0 | 0 | |
0 | 1 | 0 | |
1 | 0 | 0 | |
1 | 1 | 1 |
(a) | (b) | (c) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
0 | 1 | 0 | 1 | t | 0 | 1 | |||||
(d) | (e) | (f) | |||||||||
t | t | ||||||||||
0 | 1 | 0 | 1 | 0 | 1 | ||||||
0 | 0 | 0 | 0 | 0 | |||||||
1 | 1 | 1 |
Appendix B. The Imin PID
Application of Imin to the AND Distribution
Appendix C. The Ibroja PID
Application of Ibroja to the AND Distribution
Appendix D. The Idep PID
Application Idep to the AND Distribution
Appendix E. The Iccs PID
Application of Iccs to the AND Distribution
Allowed? | |||||
---|---|---|---|---|---|
(0,0,0) | Yes | ||||
(0,1,0) | No | ||||
(1,0,0) | No | ||||
(1,1,1) | 1 | 1 | 2 | 0 | Yes |
Appendix F. The Ipm PID
Application of the Ipm Method to the AND Distribution
Shd | Shd | Shd | |||||
---|---|---|---|---|---|---|---|
(0,0,0) | 1 | 1 | 1 | ||||
(0,1,0) | 1 | 1 | 1 | ||||
(1,0,0) | 1 | 1 | 1 | ||||
(1,1,1) | 1 | 1 | 1 | 0 | 0 | 0 | 1 |
Appendix G. The Isx PID
Appendix G.1. Probability Mass Exclusion
Appendix G.2. Shared Exclusions
Appendix G.3. Application of the Isx Method to the AND Distribution
Realisation (0,0,0)
Realisation (0,1,0)
Shd | Shd | Shd | |
---|---|---|---|
(0,0,0) | 0 | ||
(0,1,0) | |||
(1,0,0) | |||
(1,1,1) | 0 |
Appendix H. Comparison of the Results
PID | ||||||
---|---|---|---|---|---|---|
Imin | Ibroja | Idep | Iccs | Ipm | Isx | |
Unq | 0 | 0 | 0.2296 | 0.2075 | −0.2497 | 0.1887 |
Unq | 0 | 0 | 0.2296 | 0.2075 | −0.2497 | 0.1887 |
Shd | 0.3113 | 0.3113 | 0.0817 | 0.1038 | 0.5613 | 0.1226 |
Syn | 0.5000 | 0.5000 | 0.2704 | 0.2925 | 0.7497 | 0.3113 |
Appendix I. Further Comparison of PIDs
Control | Baclofen | ||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Imin | Iproj | Ibroja | Iccs | Idep | Iig | Iprec | Imin | Iproj | Ibroja | Iccs | Idep | Iig | Iprec | ||
q | 33.3 | 33.5 | 33.7 | 41.9 | 43.7 | 44.0 | 43.4 | 64.7 | 65.2 | 65.7 | 66.4 | 67.9 | 68.5 | 66.4 | |
UnqB | Md | 44.6 | 49.2 | 49.7 | 55.0 | 56.1 | 50.3 | 53.2 | 74.5 | 74.5 | 74.5 | 73.9 | 76.3 | 75.5 | 74.7 |
q | 60.7 | 60.7 | 60.8 | 61.1 | 65.7 | 68.6 | 61.7 | 80.1 | 81.3 | 82.0 | 79.5 | 84.3 | 82.8 | 82.8 | |
q | 0.0 | 0.1 | 0.2 | 1.7 | 6.1 | 2.0 | 1.4 | 0.0 | 0.0 | 0.1 | -0.7 | 1.9 | 0.4 | 0.5 | |
UnqA | Md | 0.0 | 0.4 | 0.7 | 6.7 | 10.3 | 4.8 | 2.7 | 0.0 | 0.3 | 0.7 | -0.1 | 4.0 | 0.6 | 1.7 |
q | 0.0 | 2.4 | 5.3 | 11.4 | 13.6 | 8.2 | 11.7 | 0.0 | 1.1 | 1.9 | 1.2 | 5.0 | 1.2 | 2.7 | |
q | 11.8 | 11.0 | 9.4 | 6.4 | 3.4 | 6.4 | 3.7 | 4.3 | 3.7 | 3.5 | 3.7 | 1.5 | 3.7 | 2.8 | |
Shd | Md | 16.3 | 13.7 | 11.9 | 8.7 | 5.4 | 9.5 | 6.6 | 5.2 | 5.1 | 5.0 | 4.7 | 2.7 | 4.0 | 3.8 |
q | 19.3 | 17.4 | 17.1 | 10.1 | 6.6 | 10.9 | 11.4 | 8.0 | 6.8 | 5.5 | 7.6 | 3.2 | 5.2 | 4.8 | |
q | 30.2 | 27.5 | 25.9 | 25.1 | 19.0 | 22.9 | 24.4 | 13.8 | 12.9 | 12.7 | 16.4 | 11.3 | 12.9 | 12.2 | |
Syn | Md | 38.8 | 38.8 | 38.6 | 33.9 | 32.0 | 32.6 | 30.0 | 22.2 | 21.7 | 21.1 | 21.6 | 17.0 | 17.2 | 19.8 |
q | 47.7 | 46.4 | 44.4 | 37.3 | 36.0 | 38.4 | 37.8 | 28.4 | 27.6 | 27.2 | 27.7 | 24.7 | 22.7 | 26.1 |
Imin | Iproj | Ibroja | Iccs | Idep | Iig | Iprec | ||
---|---|---|---|---|---|---|---|---|
q | 21.8 | 21.7 | 21.7 | 14.7 | 16.9 | 16.8 | 16.0 | |
UnqB | Md | 27.9 | 28.6 | 26.6 | 22.1 | 22.1 | 20.4 | 21.4 |
q | 33.3 | 30.3 | 28.3 | 23.4 | 24.2 | 26.8 | 26.9 | |
q | 0.0 | −1.4 | −2.6 | −8.9 | −9.0 | −6.6 | −9.7 | |
UnqA | Md | 0.0 | −0.1 | −0.3 | −6.8 | −6.0 | −3.5 | −1.4 |
q | 0.0 | 0.0 | 0.0 | −5.1 | −4.0 | −1.5 | −0.5 | |
q | −11.9 | −10.8 | −10.3 | −3.6 | −3.4 | −5.9 | −7.7 | |
Shd | Md | −9.3 | −9.2 | −7.4 | −2.4 | −2.7 | −4.1 | −3.3 |
q | −7.4 | −6.4 | −4.6 | −1.8 | −1.8 | −3.4 | 0.2 | |
q | −20.7 | −20.2 | −19.0 | −14.4 | −13.0 | −16.0 | −14.9 | |
Syn | Md | −19.1 | −16.7 | −14.9 | −9.9 | −11.1 | −10.6 | −12.0 |
q | −13.4 | −13.4 | −12.6 | −6.8 | −7.5 | −8.3 | −8.1 |
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Condition | |||||
---|---|---|---|---|---|
Control | 61.2 | 16.3 | 83.7 | 38.8 | 26.9 |
(52.1, 69.8) | (11.8, 19.5) | (80.5, 88.2) | (30.2, 47.9) | (14.5, 30.0) | |
Baclofen | 77.6 | 5.2 | 94.8 | 22.4 | 13.6 |
(71.6, 86.3) | (4.3, 8.2) | (91.8, 95.7) | (13.7, 28.4) | (9.6, 22.3) |
Control | Baclofen | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Ibroja | Idep | Iccs | Ipm | Isx | Ibroja | Idep | Iccs | Ipm | Isx | ||
q | 33.7 | 43.5 | 39.7 | 13.9 | 65.7 | 65.8 | 64.3 | 13.6 | |||
UnqB | Md | 49.7 | 51.9 | 47.7 | 18.5 | 74.5 | 74.6 | 70.0 | 19.2 | ||
q | 60.8 | 65.7 | 61.1 | 28.3 | 82.0 | 84.3 | 78.4 | 24.0 | |||
q | 0.2 | 6.1 | 1.7 | 0.0 | 1.9 | ||||||
UnqA | Md | 0.7 | 10.3 | 6.7 | 0.7 | 4.0 | |||||
q | 5.3 | 13.6 | 12.2 | 1.9 | 5.5 | 2.1 | |||||
q | 9.4 | 3.9 | 6.3 | 80.0 | 36.7 | 3.5 | 1.8 | 3.6 | 85.5 | 38.8 | |
Shd | Md | 11.9 | 5.4 | 7.4 | 86.6 | 38.3 | 5.0 | 2.7 | 4.7 | 88.4 | 42.9 |
q | 17.1 | 6.6 | 10.1 | 91.9 | 43.5 | 5.5 | 3.4 | 7.6 | 94.2 | 46.0 | |
q | 25.9 | 20.3 | 26.9 | 109.3 | 62.3 | 12.7 | 11.3 | 16.7 | 101.4 | 55.8 | |
Syn | Md | 38.6 | 32.2 | 34.3 | 112.4 | 65.1 | 21.1 | 17.7 | 23.2 | 106.3 | 58.7 |
q | 44.4 | 38.6 | 39.2 | 116.6 | 66.2 | 27.2 | 25.9 | 28.5 | 110.0 | 62.3 |
Ibroja | Idep | Iccs | Ipm | Isx | ||
---|---|---|---|---|---|---|
q | 21.7 | 16.9 | 14.6 | 12.6 | 13.1 | |
UnqB | Md | 26.6 | 22.1 | 22.1 | 14.8 | 14.8 |
q | 24.2 | 24.2 | 23.4 | 19.2 | 17.8 | |
q | ||||||
UnqA | Md | |||||
q | 0.0 | |||||
q | 1.1 | |||||
Shd | Md | 2.5 | 2.7 | |||
q | 3.8 | 5.1 | ||||
q | ||||||
Syn | Md | |||||
q |
Control | Baclofen | Difference | |
---|---|---|---|
q | 33.3 | 64.7 | 21.8 |
Md | 44.6 | 74.5 | 27.9 |
q | 60.7 | 80.1 | 33.4 |
P | <0.0002 | <0.0002 | <0.0004 |
0.74 | 0.16 | 1.37 | 0.79 | 1.54 | 0.63 | 1.54 |
(48.3) | (10.7) | (89.3) | (51.7) | (100) | (41.0) | (100) |
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Kay, J.W.; Schulz, J.M.; Phillips, W.A. A Comparison of Partial Information Decompositions Using Data from Real and Simulated Layer 5b Pyramidal Cells. Entropy 2022, 24, 1021. https://doi.org/10.3390/e24081021
Kay JW, Schulz JM, Phillips WA. A Comparison of Partial Information Decompositions Using Data from Real and Simulated Layer 5b Pyramidal Cells. Entropy. 2022; 24(8):1021. https://doi.org/10.3390/e24081021
Chicago/Turabian StyleKay, Jim W., Jan M. Schulz, and William A. Phillips. 2022. "A Comparison of Partial Information Decompositions Using Data from Real and Simulated Layer 5b Pyramidal Cells" Entropy 24, no. 8: 1021. https://doi.org/10.3390/e24081021
APA StyleKay, J. W., Schulz, J. M., & Phillips, W. A. (2022). A Comparison of Partial Information Decompositions Using Data from Real and Simulated Layer 5b Pyramidal Cells. Entropy, 24(8), 1021. https://doi.org/10.3390/e24081021