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A dendritic mechanism for decoding traveling waves: principles and applications to motor cortex.

Heitmann S, Boonstra T, Breakspear M - PLoS Comput. Biol. (2013)

Bottom Line: We validate this proposal in the descending motor system, where we model the large receptor fields of the pyramidal tract neurons - the principle outputs of the motor cortex - decoding motor commands encoded in the direction of traveling wave patterns in motor cortex.The model replicates key findings of the descending motor system during simple motor tasks, including variable interspike intervals and weak corticospinal coherence.By additionally showing how the nature of the wave patterns can be controlled by modulating the topology of local intra-cortical connections, we hence propose a novel integrated neuronal model of encoding and decoding motor commands.

View Article: PubMed Central - PubMed

Affiliation: School of Psychiatry, The University of New South Wales, Sydney, Australia ; The Black Dog Institute, Sydney, Australia.

ABSTRACT
Traveling waves of neuronal oscillations have been observed in many cortical regions, including the motor and sensory cortex. Such waves are often modulated in a task-dependent fashion although their precise functional role remains a matter of debate. Here we conjecture that the cortex can utilize the direction and wavelength of traveling waves to encode information. We present a novel neural mechanism by which such information may be decoded by the spatial arrangement of receptors within the dendritic receptor field. In particular, we show how the density distributions of excitatory and inhibitory receptors can combine to act as a spatial filter of wave patterns. The proposed dendritic mechanism ensures that the neuron selectively responds to specific wave patterns, thus constituting a neural basis of pattern decoding. We validate this proposal in the descending motor system, where we model the large receptor fields of the pyramidal tract neurons - the principle outputs of the motor cortex - decoding motor commands encoded in the direction of traveling wave patterns in motor cortex. We use an existing model of field oscillations in motor cortex to investigate how the topology of the pyramidal cell receptor field acts to tune the cells responses to specific oscillatory wave patterns, even when those patterns are highly degraded. The model replicates key findings of the descending motor system during simple motor tasks, including variable interspike intervals and weak corticospinal coherence. By additionally showing how the nature of the wave patterns can be controlled by modulating the topology of local intra-cortical connections, we hence propose a novel integrated neuronal model of encoding and decoding motor commands.

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Tuning curves of the PTNs.(A) Tuning curve of the PTN dendritic compartment. The amplitude of the dendritic response current (vertical axis) is modulated by the orientation of the cortical wave pattern (horizontal axis). Heavy black line indicates the mean amplitude of the dendritic response for any given wave orientation. Shaded region indicates the 90% confidence interval. The large variation is due to local defects in the wave pattern. (B) The likelihood of the soma responding at each of the dominant firing rates. (C) Net firing rates of a population of neurons in response to wave orientation.
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pcbi-1003260-g006: Tuning curves of the PTNs.(A) Tuning curve of the PTN dendritic compartment. The amplitude of the dendritic response current (vertical axis) is modulated by the orientation of the cortical wave pattern (horizontal axis). Heavy black line indicates the mean amplitude of the dendritic response for any given wave orientation. Shaded region indicates the 90% confidence interval. The large variation is due to local defects in the wave pattern. (B) The likelihood of the soma responding at each of the dominant firing rates. (C) Net firing rates of a population of neurons in response to wave orientation.

Mentions: The tuning curve of the dendritic compartment (Figure 6A) was computed by averaging the dendritic responses of PTN receptor fields at all possible locations on the cortex. The measurements were repeated over nā€Š=ā€Š20 independently generated cortical wave patterns yielding a total of 327,680 samples for each wave orientation. The large variation in the dendritic responses (gray region indicates the 95% confidence interval) is due to local defects in the wave pattern.


A dendritic mechanism for decoding traveling waves: principles and applications to motor cortex.

Heitmann S, Boonstra T, Breakspear M - PLoS Comput. Biol. (2013)

Tuning curves of the PTNs.(A) Tuning curve of the PTN dendritic compartment. The amplitude of the dendritic response current (vertical axis) is modulated by the orientation of the cortical wave pattern (horizontal axis). Heavy black line indicates the mean amplitude of the dendritic response for any given wave orientation. Shaded region indicates the 90% confidence interval. The large variation is due to local defects in the wave pattern. (B) The likelihood of the soma responding at each of the dominant firing rates. (C) Net firing rates of a population of neurons in response to wave orientation.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC3814333&req=5

pcbi-1003260-g006: Tuning curves of the PTNs.(A) Tuning curve of the PTN dendritic compartment. The amplitude of the dendritic response current (vertical axis) is modulated by the orientation of the cortical wave pattern (horizontal axis). Heavy black line indicates the mean amplitude of the dendritic response for any given wave orientation. Shaded region indicates the 90% confidence interval. The large variation is due to local defects in the wave pattern. (B) The likelihood of the soma responding at each of the dominant firing rates. (C) Net firing rates of a population of neurons in response to wave orientation.
Mentions: The tuning curve of the dendritic compartment (Figure 6A) was computed by averaging the dendritic responses of PTN receptor fields at all possible locations on the cortex. The measurements were repeated over nā€Š=ā€Š20 independently generated cortical wave patterns yielding a total of 327,680 samples for each wave orientation. The large variation in the dendritic responses (gray region indicates the 95% confidence interval) is due to local defects in the wave pattern.

Bottom Line: We validate this proposal in the descending motor system, where we model the large receptor fields of the pyramidal tract neurons - the principle outputs of the motor cortex - decoding motor commands encoded in the direction of traveling wave patterns in motor cortex.The model replicates key findings of the descending motor system during simple motor tasks, including variable interspike intervals and weak corticospinal coherence.By additionally showing how the nature of the wave patterns can be controlled by modulating the topology of local intra-cortical connections, we hence propose a novel integrated neuronal model of encoding and decoding motor commands.

View Article: PubMed Central - PubMed

Affiliation: School of Psychiatry, The University of New South Wales, Sydney, Australia ; The Black Dog Institute, Sydney, Australia.

ABSTRACT
Traveling waves of neuronal oscillations have been observed in many cortical regions, including the motor and sensory cortex. Such waves are often modulated in a task-dependent fashion although their precise functional role remains a matter of debate. Here we conjecture that the cortex can utilize the direction and wavelength of traveling waves to encode information. We present a novel neural mechanism by which such information may be decoded by the spatial arrangement of receptors within the dendritic receptor field. In particular, we show how the density distributions of excitatory and inhibitory receptors can combine to act as a spatial filter of wave patterns. The proposed dendritic mechanism ensures that the neuron selectively responds to specific wave patterns, thus constituting a neural basis of pattern decoding. We validate this proposal in the descending motor system, where we model the large receptor fields of the pyramidal tract neurons - the principle outputs of the motor cortex - decoding motor commands encoded in the direction of traveling wave patterns in motor cortex. We use an existing model of field oscillations in motor cortex to investigate how the topology of the pyramidal cell receptor field acts to tune the cells responses to specific oscillatory wave patterns, even when those patterns are highly degraded. The model replicates key findings of the descending motor system during simple motor tasks, including variable interspike intervals and weak corticospinal coherence. By additionally showing how the nature of the wave patterns can be controlled by modulating the topology of local intra-cortical connections, we hence propose a novel integrated neuronal model of encoding and decoding motor commands.

Show MeSH
Related in: MedlinePlus