A Dendritic Mechanism for Decoding Traveling Waves: Principles and Applications to Motor Cortex

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.

Mathematical framework for large-scale brain network modeling in The Virtual Brain

“…This anisotropic kernel is used for a single layer neural field model with a mixed population of interacting inhibitory and excitatory neurons with typical cortical connections. More recently Heitmann et al (2013) utilized an anisotropic inhibitory-surround coupling on a sheet of coupled phase oscillators. Such a model has been shown to evoke traveling waves, whose wavelength and orientation are determined by the properties of the inhibitory surround governs (Heitmann et al, 2012).…”

The rhythms of steady posture: Motor commands as spatially organized oscillation patterns

“…Furthermore, the simulated corticomuscular coherence diminishes when the orientation of the cortical wave is detuned from the preferred orientation of the motor neuron pool (not shown). That reduction of coherence is concomitant with the reduction of the motor response and the associated attenuation of the electromyogram (see [8] for examples).…”

“…Furthermore, their axons descend the spinal cord to monosynaptically innervate motor neurons. Gabor filters have previously been used to model neural responses to spatial visual stimuli [39,40] and thus we considered that pyramidal tract neurons may likewise spatially filter synaptic activity within their own dendritic receptor field (see [8] for a discussion). We hence modeled each pyramidal tract neuron as a non-spatial axonal compartment coupled to a spatially extended dendritic receptor field which was modeled by a two-dimensional Gabor filter (Fig.…”

“…Introducing anisotropy into the inhibitory coupling permits control over the spatial orientation of waves to encode motor commands [29]. The orientation of those waves can be discriminated (decoded) by the extensive dendritic arbors of the pyramidal tract neurons to selectively drive motor unit activity [8]. That motor unit activity can in turn drive muscle movement in a simulated biomechanical limb [30].…”

“…Waves and synchrony are elicited in the cortical model by manipulating the lateral inhibitory connectivity. The descending motor tracts are each (1)(2)(3)(4)(5)(6)(7)(8). The synchronization patterns formed by these oscillators are spatially filtered by the dendritic receptors of the pyramidal tract neurons (PTN).…”