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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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Modeling the descending motor system.(A) Major fiber tracts of the descending motor system, redrawn from [105]. Axons of the pyramidal tract neurons (red) descend from the motor cortex to monosynaptically innervate motor neurons in the spinal cord. (B) Schematic representation of the dendritic arbors of a typical pyramidal tract neuron (PTN). The apical dendrites project widely throughout the superficial layers of cortex and thus are ideally placed to detect surface wave patterns in the neural activity (top). (C) Simulated cortical wave pattern. (D) The descending motor model. Cortical wave patterns are generated by a sheet of spatially-coupled phase oscillators (circles, 1–8). These wave patterns are spatially filtered by the dendritic trees of the pyramidal tract neurons to produce an amplitude-modulated oscillatory current at the soma. Spikes initiated by the PTN are transmitted to a randomly selected pool of motor neurons (MN) in the spine. Each MN integrates the incoming spikes to produce a muscle drive spike train. Net muscle drive is quantified by simulated Electromyogram (EMG). The cortical wave model is adapted from [17]. The MN and EMG models are adapted from [41].
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pcbi-1003260-g001: Modeling the descending motor system.(A) Major fiber tracts of the descending motor system, redrawn from [105]. Axons of the pyramidal tract neurons (red) descend from the motor cortex to monosynaptically innervate motor neurons in the spinal cord. (B) Schematic representation of the dendritic arbors of a typical pyramidal tract neuron (PTN). The apical dendrites project widely throughout the superficial layers of cortex and thus are ideally placed to detect surface wave patterns in the neural activity (top). (C) Simulated cortical wave pattern. (D) The descending motor model. Cortical wave patterns are generated by a sheet of spatially-coupled phase oscillators (circles, 1–8). These wave patterns are spatially filtered by the dendritic trees of the pyramidal tract neurons to produce an amplitude-modulated oscillatory current at the soma. Spikes initiated by the PTN are transmitted to a randomly selected pool of motor neurons (MN) in the spine. Each MN integrates the incoming spikes to produce a muscle drive spike train. Net muscle drive is quantified by simulated Electromyogram (EMG). The cortical wave model is adapted from [17]. The MN and EMG models are adapted from [41].

Mentions: Traveling waves of oscillatory neuronal activity have been observed at many spatial scales although their functional role remains a matter of debate [1]. Waves have been implicated in perception [2]–[7], working memory [8], pathological seizure-like states [9], motor control [10]–[12] and neural computation [13], [14]. Waves also arise readily in neurobiological models of oscillatory activity [15], [16]. We recently proposed that the morphological properties of waves in motor cortex may serve as a neural basis for encoding movement-related information [17]. In the present study we explore how spatially-organized receptors within the dendritic field allow neurons to act as spatial filters of those wave patterns to effectively decode the information contained within their wavelength, coherence and direction. We use numerical simulation to explore this proposal in the context of the human descending motor system where we model the response of the principle output neurons of the motor cortex to simulated waves in cortex (Figure 1). The dendritic receptor field is modeled as a spatial Gabor filter which selectively initiates actions potentials in the neuron whenever it detects a specific wave pattern. Gabor filters have previously been used to characterize the receptor fields of ‘simple cells’ in visual cortex [18], [19] and here we assume that similar structures may likewise be plausible in motor cortex, giving examples of how this could be accomplished. We show that dendritic fields in cortex may serve as biological Gabor filters of internally generated patterns of oscillatory activity. Furthermore, we show how the output neurons of motor cortex may use Gabor filtering to translate those oscillatory patterns into steady motor output in the spine.


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

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

Modeling the descending motor system.(A) Major fiber tracts of the descending motor system, redrawn from [105]. Axons of the pyramidal tract neurons (red) descend from the motor cortex to monosynaptically innervate motor neurons in the spinal cord. (B) Schematic representation of the dendritic arbors of a typical pyramidal tract neuron (PTN). The apical dendrites project widely throughout the superficial layers of cortex and thus are ideally placed to detect surface wave patterns in the neural activity (top). (C) Simulated cortical wave pattern. (D) The descending motor model. Cortical wave patterns are generated by a sheet of spatially-coupled phase oscillators (circles, 1–8). These wave patterns are spatially filtered by the dendritic trees of the pyramidal tract neurons to produce an amplitude-modulated oscillatory current at the soma. Spikes initiated by the PTN are transmitted to a randomly selected pool of motor neurons (MN) in the spine. Each MN integrates the incoming spikes to produce a muscle drive spike train. Net muscle drive is quantified by simulated Electromyogram (EMG). The cortical wave model is adapted from [17]. The MN and EMG models are adapted from [41].
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003260-g001: Modeling the descending motor system.(A) Major fiber tracts of the descending motor system, redrawn from [105]. Axons of the pyramidal tract neurons (red) descend from the motor cortex to monosynaptically innervate motor neurons in the spinal cord. (B) Schematic representation of the dendritic arbors of a typical pyramidal tract neuron (PTN). The apical dendrites project widely throughout the superficial layers of cortex and thus are ideally placed to detect surface wave patterns in the neural activity (top). (C) Simulated cortical wave pattern. (D) The descending motor model. Cortical wave patterns are generated by a sheet of spatially-coupled phase oscillators (circles, 1–8). These wave patterns are spatially filtered by the dendritic trees of the pyramidal tract neurons to produce an amplitude-modulated oscillatory current at the soma. Spikes initiated by the PTN are transmitted to a randomly selected pool of motor neurons (MN) in the spine. Each MN integrates the incoming spikes to produce a muscle drive spike train. Net muscle drive is quantified by simulated Electromyogram (EMG). The cortical wave model is adapted from [17]. The MN and EMG models are adapted from [41].
Mentions: Traveling waves of oscillatory neuronal activity have been observed at many spatial scales although their functional role remains a matter of debate [1]. Waves have been implicated in perception [2]–[7], working memory [8], pathological seizure-like states [9], motor control [10]–[12] and neural computation [13], [14]. Waves also arise readily in neurobiological models of oscillatory activity [15], [16]. We recently proposed that the morphological properties of waves in motor cortex may serve as a neural basis for encoding movement-related information [17]. In the present study we explore how spatially-organized receptors within the dendritic field allow neurons to act as spatial filters of those wave patterns to effectively decode the information contained within their wavelength, coherence and direction. We use numerical simulation to explore this proposal in the context of the human descending motor system where we model the response of the principle output neurons of the motor cortex to simulated waves in cortex (Figure 1). The dendritic receptor field is modeled as a spatial Gabor filter which selectively initiates actions potentials in the neuron whenever it detects a specific wave pattern. Gabor filters have previously been used to characterize the receptor fields of ‘simple cells’ in visual cortex [18], [19] and here we assume that similar structures may likewise be plausible in motor cortex, giving examples of how this could be accomplished. We show that dendritic fields in cortex may serve as biological Gabor filters of internally generated patterns of oscillatory activity. Furthermore, we show how the output neurons of motor cortex may use Gabor filtering to translate those oscillatory patterns into steady motor output in the spine.

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