Fig 1.
Schematic of synchronized and non-synchronized responses from auditory cortical neurons in response to acoustic pulse trains generating flutter and fusion percepts.
Each plot is subdivided (from top to bottom) into an illustration of the acoustic pulse train (gray), and the evoked neural response from synchronized neurons (red) and non-synchronized neurons (blue). The inset plot in (a) shows a single acoustic pulse (5 kHz carrier frequency). a. An acoustic pulse train generating a flutter percept (interpulse interval = 50 ms). b. An acoustic pulse train generating a fusion percept (interpulse interval = 10 ms).
Fig 2.
Computational model of an auditory cortical neuron.
Error bars indicate SEM. a. The acoustic stimulus (top) used in our neurophysiological experiments was a narrowband acoustic pulse train. Each pulse was converted into an excitatory and inhibitory conductance in our computational model, using an alpha function with a time constant of 5 ms (middle). Three parameters could be altered (I-E delay, E input, and I/E ratio). Above threshold changes in the membrane voltage generated spikes (bottom), which could be further analyzed to measure the response properties of the simulated neuron. b. Classification of neural coding regime based on the two criteria (dashed lines)- y axis: Rayleigh statistic at an IPI of 75 ms>13.8, x axis: Discharge rate ratio>1. Neurons were classified as having a non-synchronized (o), synchronized (x), or mixed (+) response. c. Comparison of stimulus synchronization in real (gray) and simulated (red) synchronized neurons across different IPIs (3–75 ms). d. Comparison of normalized discharge rate in real (gray) and simulated (blue) non-synchronized neurons across different IPIs (3–75 ms).
Fig 3.
Dependence on input parameters of computational model.
Classification of neuron-type [non-sync (o), sync (x), mixed (+), atypical (square)] across all three parameters (I-E delay, Excitatory input, and I/E ratio). If pure tone responses were less than 1 spk/s or greater than 50 spk/s, neurons were considered to have responses outside the allowable range (cyan) and were not included in our analysis.
Fig 4.
Simulated synchronized neuron.
a. Classification of neuron-type [non-sync (o), sync (x), mixed (+), atypical (square)] across two parameters (Excitatory input and I/E ratio), with a fixed I-E delay of 5 ms. The two arrows indicate the parameters used for the simulated neurons in Fig. 4c (left arrow) and Fig. 4d (right arrow). b. Dependence of Rayleigh statistic (at an IPI of 75 ms) on the amplitude of excitatory inputs in simulated synchronized neurons. Spearman correlation coefficient: r = 0.99, P<3.1x10-87. c-e. Examples of simulated and real synchronized neurons. Each plot is subdivided into a raster plot (left), IPI vs discharge rate plot (top right), and IPI vs vector strength plot (bottom right). The stimulus is played for 500 ms, which is indicated with the gray rectangle in the raster plot. The dashed line in the IPI vs discharge rate plot indicates a significant evoked response above the spontaneous rate (2σ). Error bars indicate SEM. c. Simulated neuron: I-E delay = 5 ms, E strength = 1.8 nS, I/E ratio = 2. d. Simulated neuron: I-E delay = 5 ms, E strength = 6 nS, I/E ratio = 2. e. Real neuron (unit m2p31.1) from awake marmoset auditory cortex.
Fig 5.
Simulated non-synchronized neuron.
a. Classification of neuron-type [non-sync (o), sync (x), mixed (+), atypical (square)] across two parameters (Excitatory input and I/E ratio), with a fixed I-E delay of 0 ms. The two arrows indicate the parameters used for the simulated neurons in Fig. 5c (right arrow) and Fig. 5d (left arrow). b. Dependence of discharge rate ratio on net excitatory input (excitation-inhibition). Spearman correlation coefficient: r = 0.87, P<1.5 x 10-17 in simulated non-synchronized neurons. c-e. Examples of simulated and real non-synchronized neurons. Each plot is subdivided into a raster plot (left), IPI vs discharge rate plot (top right), and IPI vs vector strength plot (bottom right). The stimulus is played for 500 ms, which is indicated with the gray rectangle in the raster plot. The dashed line in the IPI vs discharge rate plot indicates a significant evoked response above the spontaneous rate (2σ). Error bars indicate SEM. c. Simulated neuron: I-E delay = 0 ms, E strength = 1.8 nS, I/E ratio = 1.3. d. Simulated neuron: I-E delay = 0 ms, E strength = 0.3 nS, I/E ratio = 0. e. Real neuron: (unit m32q3.1) from awake marmoset auditory cortex.
Fig 6.
Temporal dynamics of synchronized and non-synchronized neurons.
a. Net excitation (excitatory-inhibitory conductance) for a single acoustic pulse in a simulated synchronized neuron. I-E delay = 5 ms, E strength = 3 nS, I/E ratio = 1.5. b. Net excitation (excitatory-inhibitory conductance) for a single acoustic pulse in a simulated non-synchronized neuron. I-E delay = 0 ms, E strength = 0.6 nS, I/E ratio = 0.9. c. Minimum latency distribution for acoustic pulse train responses in simulated neurons. Mean: sync = 10.8 ms, nonsync = 16.6 ms, Wilcoxon rank sum test: P < 1.4 x 10-89. d. Minimum latency distribution for acoustic pulse train responses in real neurons. Mean: sync = 18.1 ms, nonsync = 51.1 ms, Wilcoxon rank sum test: P<4.6 x 10-9. e. Onset/sustained ratio distribution for pure tone responses in simulated neurons. Mean: sync = 0.69, nonsync = 0.18, Wilcoxon rank sum test: P < 6.1 x 10-124. f. Onset/sustained ratio distribution for pure tone responses in real neurons. Mean: sync = 0.60, nonsync = 0.25, Wilcoxon rank sum test: P<2.3 x 10-9.
Fig 7.
Discharge rates across mixed, synchronized, and non-synchronized neurons.
Mean discharge rates for simulated (left) and real (right) neuronal populations, grouped according to their neural coding regime: synchronized (red), non-synchronized (blue), and mixed (green). Error bars indicate SEM. Wilcoxon rank sum test: * P<0.003 Bonferonni corrected, ** P<1.2x10-76 Bonferonni corrected, NS = not significant (P>0.05 uncorrected). a. Pure tone responses of simulated neurons. b. Pure tone responses of real neurons.
Fig 8.
Temporal fidelity of synchronized and mixed neurons.
Only simulated neurons with an excitatory input strength between 3–6 nS were used in this analysis, such that synchronized and mixed neurons had a similar distribution of excitatory levels. a. Max vector strength distribution for acoustic pulse train responses in simulated neurons. Mean: sync = 0.93, mixed = 0.79, Wilcoxon rank sum test: P < 3.3 x 10-52. b. IPI synchronization limit distribution for acoustic pulse train responses in simulated neurons. Mean: sync = 10.2 ms, mixed = 7.7 ms, Wilcoxon rank sum test: P < 1.3 x 10-43. c. Max vector strength distribution for acoustic pulse train responses in real neurons. Mean: sync = 0.68, mixed = 0.60, Wilcoxon rank sum test: P = 0.16. d. IPI synchronization limit distribution for acoustic pulse train responses in real neurons. Mean: sync = 25.7 ms, mixed = 13.4 ms, Wilcoxon rank sum test: P < 0.02.
Fig 9.
Impact of spontaneous rate on computational model.
a. Relationship between spontaneous rate of simulated neuron and the amplitude of the Gaussian noise added to the excitatory and inhibitory conductances. The arrow indicates the amplitude of noise used for the simulated neurons in analyses conducted in Figs. 2–8. The gray dashed lines indicate spontaneous rates of 0 spk/s (bottom) and 40 spk/s (top). b-c. Classification of neuron-type [non-sync (o), sync (x), mixed (+), atypical (square)] for two different spontaneous rates: a low spontaneous rate (b) of 0 spk/s (noise input of 3x10-8) and a high spontaneous rate (c) of ~40 spk/s (noise input of 6x10-8). Responses outside the allowable range (pure tone response between 1–50 spk/s) are indicated in cyan.
Fig 10.
Invariance of response type across varying spontaneous rates.
Response type invariance across varying spontaneous rates (between 0–40 spk/s). Model parameters yielding one response type across all spontaneous rates tested are indicated [non-sync (o), sync (x), mixed (+)]. Model parameters where neurons changed between response types (e.g. sync → non-sync) are shown in cyan.