Spike-phase coupling patterns reveal laminar identity in primate cortex
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The authors present a novel and precise method for determining boundaries of cortical layers from multi-electrode recordings in marmosets and macaques. Their method requires less data than current approaches to finding a systematic relationship between slow local field potentials and spiking across cortical columns. This approach may be broadly useful to those doing electrophysiological recordings in the primate brain.
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Abstract
The cortical column is one of the fundamental computational circuits in the brain. In order to understand the role neurons in different layers of this circuit play in cortical function it is necessary to identify the boundaries that separate the laminar compartments. While histological approaches can reveal ground truth they are not a practical means of identifying cortical layers in vivo. The gold standard for identifying laminar compartments in electrophysiological recordings is current-source density (CSD) analysis. However, laminar CSD analysis requires averaging across reliably evoked responses that target the input layer in cortex, which may be difficult to generate in less well-studied cortical regions. Further, the analysis can be susceptible to noise on individual channels resulting in errors in assigning laminar boundaries. Here, we have analyzed linear array recordings in multiple cortical areas in both the common marmoset and the rhesus macaque. We describe a pattern of laminar spike–field phase relationships that reliably identifies the transition between input and deep layers in cortical recordings from multiple cortical areas in two different non-human primate species. This measure corresponds well to estimates of the location of the input layer using CSDs, but does not require averaging or specific evoked activity. Laminar identity can be estimated rapidly with as little as a minute of ongoing data and is invariant to many experimental parameters. This method may serve to validate CSD measurements that might otherwise be unreliable or to estimate laminar boundaries when other methods are not practical.
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eLife assessment
The authors present a novel and precise method for determining boundaries of cortical layers from multi-electrode recordings in marmosets and macaques. Their method requires less data than current approaches to finding a systematic relationship between slow local field potentials and spiking across cortical columns. This approach may be broadly useful to those doing electrophysiological recordings in the primate brain.
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Reviewer #1 (Public Review):
This is a very interesting and timely paper and one of very few that crosses species. Linear multielectrode array recordings are rapidly becoming state-of-the-art. This means that there is a greater need for finding motifs and/or reliable markers that characterize activity in different cortical layers.
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Reviewer #2 (Public Review):
The authors present a new method of determining the boundaries of superficial, input, and deep cortical layers from laminar multielectrode recordings in non-human primates.
It is based on using the generalized phase (GP) of the LFP (filtered between 5-50Hz) in conjunction with phase coupling (to the GP) of spiking activity (from single or multi-units). They report that phase coupling differs between layers. Critically the preferred LFP phase differs between the deep layers and layers above (input/superficial layers), and this measure can be reliably used to infer input/deep layer boundaries.Spiking on a given channel (for all channels) tended to occur at +/- pi relative to LFPs recorded at superficial/input layers, but at 0pi relative to deep-layer LFPs. This relationship can be used to estimate the …
Reviewer #2 (Public Review):
The authors present a new method of determining the boundaries of superficial, input, and deep cortical layers from laminar multielectrode recordings in non-human primates.
It is based on using the generalized phase (GP) of the LFP (filtered between 5-50Hz) in conjunction with phase coupling (to the GP) of spiking activity (from single or multi-units). They report that phase coupling differs between layers. Critically the preferred LFP phase differs between the deep layers and layers above (input/superficial layers), and this measure can be reliably used to infer input/deep layer boundaries.Spiking on a given channel (for all channels) tended to occur at +/- pi relative to LFPs recorded at superficial/input layers, but at 0pi relative to deep-layer LFPs. This relationship can be used to estimate the input/deep layer boundary. Generally, the estimate obtained was well correlated with measures derived from traditional CSD analysis. Where discrepancies occurred between CSD and phase coupling-based depth estimates, phase coupling-based depth estimates correlated better with additional measures such as firing rates, and low/high-frequency spectral power cross-over, that have been previously reported to align with cortical depth.
These results were present in areas MT (marmoset), V4 (macaque), and PFC (marmoset), and can be performed on short sequences of data under multiple experimental conditions.
This is a novel, easier, and potentially more precise way to assign cortical depth in non-human primates, which may prove useful to the wider research community.
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