Limits...
The role of inhibition in a computational model of an auditory cortical neuron during the encoding of temporal information.

Bendor D - PLoS Comput. Biol. (2015)

Bottom Line: Using a computational neuronal model, we find that stimulus-locked responses are generated when sound-evoked excitation is combined with strong, delayed inhibition.In contrast to this, a non-synchronized rate representation is generated when the net excitation evoked by the sound is weak, which occurs when excitation is coincident and balanced with inhibition.Together these data suggest that feedforward inhibition provides a parsimonious explanation of the neural coding dichotomy observed in auditory cortex.

View Article: PubMed Central - PubMed

Affiliation: Institute of Behavioural Neuroscience, Department of Experimental Psychology, University College London, London, United Kingdom.

ABSTRACT
In auditory cortex, temporal information within a sound is represented by two complementary neural codes: a temporal representation based on stimulus-locked firing and a rate representation, where discharge rate co-varies with the timing between acoustic events but lacks a stimulus-synchronized response. Using a computational neuronal model, we find that stimulus-locked responses are generated when sound-evoked excitation is combined with strong, delayed inhibition. In contrast to this, a non-synchronized rate representation is generated when the net excitation evoked by the sound is weak, which occurs when excitation is coincident and balanced with inhibition. Using single-unit recordings from awake marmosets (Callithrix jacchus), we validate several model predictions, including differences in the temporal fidelity, discharge rates and temporal dynamics of stimulus-evoked responses between neurons with rate and temporal representations. Together these data suggest that feedforward inhibition provides a parsimonious explanation of the neural coding dichotomy observed in auditory cortex.

No MeSH data available.


Related in: MedlinePlus

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.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4400160&req=5

pcbi.1004197.g005: 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.

Mentions: In contrast to this, non-synchronized neurons were more common when the net excitation was weak, which occurred for I/E ratios close to one (balanced excitation and inhibition) or low I/E ratios in combination with a weak excitatory input (Fig. 5a, model with an I-E delay = 0 ms). We observed a statistically significant correlation (r = 0.87, P<1.5 x 10-17, Spearman Correlation, Fig. 5b) between the net excitatory input (excitation-inhibition) and the discharge rate ratio. In other words, as the magnitude of net excitation increased, short IPIs evoked a higher discharge rate relative to the discharge rate at longer IPIs, effectively increasing the dynamic range of the neuron’s rate code. This effect can be observed by comparing the responses of two simulated non-synchronizing neurons that differ in their net excitation (Fig. 5c-d). While both of these examples of simulated neurons differ in the dynamic range of their rate representation, they closely match the general properties of real non-synchronized neurons (Fig. 5e).


The role of inhibition in a computational model of an auditory cortical neuron during the encoding of temporal information.

Bendor D - PLoS Comput. Biol. (2015)

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.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4400160&req=5

pcbi.1004197.g005: 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.
Mentions: In contrast to this, non-synchronized neurons were more common when the net excitation was weak, which occurred for I/E ratios close to one (balanced excitation and inhibition) or low I/E ratios in combination with a weak excitatory input (Fig. 5a, model with an I-E delay = 0 ms). We observed a statistically significant correlation (r = 0.87, P<1.5 x 10-17, Spearman Correlation, Fig. 5b) between the net excitatory input (excitation-inhibition) and the discharge rate ratio. In other words, as the magnitude of net excitation increased, short IPIs evoked a higher discharge rate relative to the discharge rate at longer IPIs, effectively increasing the dynamic range of the neuron’s rate code. This effect can be observed by comparing the responses of two simulated non-synchronizing neurons that differ in their net excitation (Fig. 5c-d). While both of these examples of simulated neurons differ in the dynamic range of their rate representation, they closely match the general properties of real non-synchronized neurons (Fig. 5e).

Bottom Line: Using a computational neuronal model, we find that stimulus-locked responses are generated when sound-evoked excitation is combined with strong, delayed inhibition.In contrast to this, a non-synchronized rate representation is generated when the net excitation evoked by the sound is weak, which occurs when excitation is coincident and balanced with inhibition.Together these data suggest that feedforward inhibition provides a parsimonious explanation of the neural coding dichotomy observed in auditory cortex.

View Article: PubMed Central - PubMed

Affiliation: Institute of Behavioural Neuroscience, Department of Experimental Psychology, University College London, London, United Kingdom.

ABSTRACT
In auditory cortex, temporal information within a sound is represented by two complementary neural codes: a temporal representation based on stimulus-locked firing and a rate representation, where discharge rate co-varies with the timing between acoustic events but lacks a stimulus-synchronized response. Using a computational neuronal model, we find that stimulus-locked responses are generated when sound-evoked excitation is combined with strong, delayed inhibition. In contrast to this, a non-synchronized rate representation is generated when the net excitation evoked by the sound is weak, which occurs when excitation is coincident and balanced with inhibition. Using single-unit recordings from awake marmosets (Callithrix jacchus), we validate several model predictions, including differences in the temporal fidelity, discharge rates and temporal dynamics of stimulus-evoked responses between neurons with rate and temporal representations. Together these data suggest that feedforward inhibition provides a parsimonious explanation of the neural coding dichotomy observed in auditory cortex.

No MeSH data available.


Related in: MedlinePlus