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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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The PTN model.(A) Spatial profiles of the dendritic filter. (B) Spatial contours of the dendritic filter. (C) Preferred cortical oscillation pattern for this dendritic filter. (D) Orthogonal oscillation pattern. (E) Time course of the neural response to the preferred cortical pattern. Bottom trace (red) is the dendritic current. Top trace (black) is the somatic membrane potential. Light gray traces show the responses of four other PTNs located at random positions on the same cortical pattern. (F) Time course of neural response to the orthogonal pattern. Panels E and F have the same scales.
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pcbi-1003260-g004: The PTN model.(A) Spatial profiles of the dendritic filter. (B) Spatial contours of the dendritic filter. (C) Preferred cortical oscillation pattern for this dendritic filter. (D) Orthogonal oscillation pattern. (E) Time course of the neural response to the preferred cortical pattern. Bottom trace (red) is the dendritic current. Top trace (black) is the somatic membrane potential. Light gray traces show the responses of four other PTNs located at random positions on the same cortical pattern. (F) Time course of neural response to the orthogonal pattern. Panels E and F have the same scales.

Mentions: Having verified that dendritic receptor fields can serve as Gabor filters, we next simulated the receptor field of each PTN as a two-dimensional Gabor filter using a phase-only approach (Figure 4). Here, the output of the Gabor filter directly represents the dendritic current produced by the net synaptic bombardment of the receptor field by the local activity in the cortical oscillator model. This dendritic current flows directly into the somatic compartment where action potentials are generated according to the conductance model of Izhikevich and Edelman [61] (Methods, equations 14–15). The parameters of the somatic model were tuned to match the physiological response characteristics of pyramidal tract neurons in mammals [62]–[64].


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

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

The PTN model.(A) Spatial profiles of the dendritic filter. (B) Spatial contours of the dendritic filter. (C) Preferred cortical oscillation pattern for this dendritic filter. (D) Orthogonal oscillation pattern. (E) Time course of the neural response to the preferred cortical pattern. Bottom trace (red) is the dendritic current. Top trace (black) is the somatic membrane potential. Light gray traces show the responses of four other PTNs located at random positions on the same cortical pattern. (F) Time course of neural response to the orthogonal pattern. Panels E and F have the same scales.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003260-g004: The PTN model.(A) Spatial profiles of the dendritic filter. (B) Spatial contours of the dendritic filter. (C) Preferred cortical oscillation pattern for this dendritic filter. (D) Orthogonal oscillation pattern. (E) Time course of the neural response to the preferred cortical pattern. Bottom trace (red) is the dendritic current. Top trace (black) is the somatic membrane potential. Light gray traces show the responses of four other PTNs located at random positions on the same cortical pattern. (F) Time course of neural response to the orthogonal pattern. Panels E and F have the same scales.
Mentions: Having verified that dendritic receptor fields can serve as Gabor filters, we next simulated the receptor field of each PTN as a two-dimensional Gabor filter using a phase-only approach (Figure 4). Here, the output of the Gabor filter directly represents the dendritic current produced by the net synaptic bombardment of the receptor field by the local activity in the cortical oscillator model. This dendritic current flows directly into the somatic compartment where action potentials are generated according to the conductance model of Izhikevich and Edelman [61] (Methods, equations 14–15). The parameters of the somatic model were tuned to match the physiological response characteristics of pyramidal tract neurons in mammals [62]–[64].

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