Functional interactions among neurons within single columns of macaque V1
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Curated by eLife
Evaluation Summary:
This paper will be of interest to readers who perform extracellular recordings with high-density electrodes. It provides a proof of principle that high-density recordings allow assessing the interactions of pairs of neurons within local cortical networks in nonhuman primates.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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Abstract
Recent developments in high-density neurophysiological tools now make it possible to record from hundreds of single neurons within local, highly interconnected neural networks. Among the many advantages of such recordings is that they dramatically increase the quantity of identifiable, functional interactions between neurons thereby providing an unprecedented view of local circuits. Using high-density, Neuropixels recordings from single neocortical columns of primary visual cortex in nonhuman primates, we identified 1000s of functionally interacting neuronal pairs using established crosscorrelation approaches. Our results reveal clear and systematic variations in the synchrony and strength of functional interactions within single cortical columns. Despite neurons residing within the same column, both measures of interactions depended heavily on the vertical distance separating neuronal pairs, as well as on the similarity of stimulus tuning. In addition, we leveraged the statistical power afforded by the large numbers of functionally interacting pairs to categorize interactions between neurons based on their crosscorrelation functions. These analyses identified distinct, putative classes of functional interactions within the full population. These classes of functional interactions were corroborated by their unique distributions across defined laminar compartments and were consistent with known properties of V1 cortical circuitry, such as the lead-lag relationship between simple and complex cells. Our results provide a clear proof-of-principle for the use of high-density neurophysiological recordings to assess circuit-level interactions within local neuronal networks.
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Evaluation Summary:
This paper will be of interest to readers who perform extracellular recordings with high-density electrodes. It provides a proof of principle that high-density recordings allow assessing the interactions of pairs of neurons within local cortical networks in nonhuman primates.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
This work employs high-density electrodes to study functional connections between pairs of neurons within local cortical networks of nonhuman primates. The work aims at providing a proof of principle that using high-density electrodes dramatically increases the number of identified functionally connected neuron pairs, which in turn allows for studying the interactions within local cortical circuits. The work also leverages the large number of identified correlated neuron pairs to study the interactions within and between cortical layers.
Strengths:
Using high-density electrodes (Neuropixels probes) to study interactions within the visual cortex in nonhuman monkeys is elegant because the Neuropixels probes allow recording neuronal activity across the entire depth of the cortical column simultaneously. …Reviewer #1 (Public Review):
This work employs high-density electrodes to study functional connections between pairs of neurons within local cortical networks of nonhuman primates. The work aims at providing a proof of principle that using high-density electrodes dramatically increases the number of identified functionally connected neuron pairs, which in turn allows for studying the interactions within local cortical circuits. The work also leverages the large number of identified correlated neuron pairs to study the interactions within and between cortical layers.
Strengths:
Using high-density electrodes (Neuropixels probes) to study interactions within the visual cortex in nonhuman monkeys is elegant because the Neuropixels probes allow recording neuronal activity across the entire depth of the cortical column simultaneously. Moreover, due to the dense sampling, the number of identified single neurons is large (115-221 neurons) and the number of measured interactions between pairs of neurons, via cross-correlation analysis, is impressive (~68000). Thus, high-density electrodes are ideally suited to study interactions within cortical circuits in animals with thick cortices, like the nonhuman primate. This work is a proof of principle that this can be achieved and will likely impact the field.Weaknesses:
Although the paper does provide rich information on interactions within local cortical circuits, the main weakness of the paper is using the term "functional connection" in an imprecise manner. Cross-correlograms (CCG) of spike trains of pairs of neurons show different shapes depending on the underlying connectivity and not all significant peaks in CCGs reflect functionally connected neuron pairs. For example, CCGs of synaptically connected neuron pairs show a transient peak that is offset from the 0-ms lag due to the synaptic delay. CCGs with this shape thus reflect "functionally connected neuron pairs". In contrast, common inputs to pairs of neurons can induce significant peaks in CCGs, despite the fact that these neurons are only correlated but not functionally connected (e.g. Ostojic et al. 2009). Therefore, taking the shape of significant CCGs into account is important when discussing "functionally connected neuron pairs". While the authors mention this point in the paper, the term "functional connection" is nonetheless used irrespective of the CCG shapes which can be confusing to the reader. Moreover, the authors claim that the method allows identifying "1000s of functionally connected neuronal pairs". This statement is likely not fully supported by the data, evident by the fact that CCGs with the shape of mono-synaptic connections (transient and non-zero lag peak) are not among the distinct classes of CCGs shown in Figure 4. -
Reviewer #2 (Public Review):
This manuscript uses spike train cross-correlation analysis to infer functional connections among neurons within a cortical column. This type of work has a long history, but it has almost always been applied to neurons in different cortical columns. In this study, the authors use the dense sampling of a cortical column afforded by Neuropixel recordings to assess functional connectivity within a column. The results largely conform to expected patterns, based on knowledge of anatomical connectivity. These results thus provide a 'proof of principle' that dense recordings and correlation analysis may be able to reveal features of cortical circuitry.
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