Spike-phase coupling patterns reveal laminar identity in primate cortex

Davis, Zachary W.; Dotson, Nicholas M.; Franken, Tom P.; Muller, Lyle; Reynolds, John H.

doi:10.7554/elife.84512

“…This predicts that such cells are present in deep layers, in which the majority of cells that project from V4 to V2 are located 26 . As in prior studies we used current source density (CSD) analysis to estimate laminar compartments in our recordings 7,27–31 (Methods). Briefly, we recorded responses to small stimuli flashed in the cRF, and computed the CSD as the second spatial derivative of the evoked local field potentials across the electrode contacts on the probe.…”

Section: Resultsmentioning

confidence: 99%

“…The CSD was computed as the second spatial derivative of the LFP. In the resulting pattern of current sinks and current sources, we could identify the granular (input) layer as the current sink with the shortest latency based on previous physiological and histological studies 7,28,29,31,57 , and thus infer which electrode contacts were positioned respectively in superficial and in deep cortical layers.…”

Section: Star Methodsmentioning

confidence: 99%

Grouping cells in primate visual cortex

Franken,

Reynolds

2024

Preprint

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Our perception of how objects are laid out in visual scenes is remarkably stable, despite rapid shifts in the patterns of light that fall on the retina with each saccade. One mechanism that may help establish perceptual stability is border ownership assignment. Studies in macaque area V2 have identified border ownership neurons that signal which side of a border belongs to a foreground surface. This signal persists for hundreds of milliseconds after border ownership has been rendered ambiguous by deleting the stimulus features that distinguish foreground from background. Remarkably, this signal survives eye movements: border ownership neurons also exhibit border ownership signals de novo when an eye movement places the newly ambiguous border within their receptive field. The grouping cell hypothesis proposes the existence of hypothetical grouping cells in a downstream brain area. These cells would compute persistent proto-object representations and therefore have the properties to endow cells in upstream brain areas with selectivity for border ownership. Such grouping cells have been predicted to show a centripetal and persistent pattern of preferred side of ownership for a border placed parallel to the perimeter of their classical receptive field, and such a centripetal ownership preference pattern should also occur de novo in these same cells if an ambiguous border lands in their receptive field after a saccade. It is unknown if grouping cells exist. Here we used laminar multielectrodes in area V4, the main source of feedback to V2, of behaving macaques to determine whether such grouping cells exist. Consistent with the model prediction we find a substantial population of neurons with these properties, in all laminar compartments, and they exhibit a response latency that is short enough to act as the source that endows neurons in V2 with selectivity for border ownership. While grouping cell activity provides information about the location of foreground surfaces, these neurons are, counterintuitively, not as strongly tuned for luminance contrast polarity, a feature of those surfaces, as are border ownership cells. Our data suggest a division of labor in which these newly discovered grouping cells provide spatiotemporal continuity of segmented surfaces whereas border ownership cells link this location information with surface features such as luminance contrast.

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“…After lowering the probe and allowing it to settle for approximately 30 minutes, recordings are then conducted for approximately 2 hours while the marmoset performs a variety of tasks, including viewing and saccading to a perceptual illusion (Dotson et.al. 2023), visual response field mapping, and full-screen flash sessions used to calculate the current source density (CSD).…”

Section: Resultsmentioning

confidence: 99%

“…The AD recording system enables repeatable acute recordings with high optical visibility to avoid damaging blood vessels and a low risk of infection over an extended period of time. This technique has been successfully combined with marmosets performing a variety of complex behavioral tasks (e.g., Dotson et. al., 2023), to enable an exceptional ability to study laminar processing in a primate.…”

Section: Discussionmentioning

confidence: 99%

Acute Neuropixels recordings in the marmoset monkey

Dotson,

Davis,

Jendritza

et al. 2023

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High-density linear probes, like Neuropixels, provide an unprecedented opportunity to understand how neural populations within specific laminar compartments contribute to behavior. Marmoset monkeys, unlike macaque monkeys, have a lissencephalic (smooth) cortex that enables recording perpendicular to the cortical surface, thus making them an ideal animal model for studying laminar computations. Here we present a method for acute Neuropixels recordings in the common marmoset (Callithrix jacchus). The approach replaces the native dura with an artificial silicon-based dura that grants visual access to the cortical surface, which is helpful in avoiding blood vessels, ensures perpendicular penetrations, and could be used in conjunction with optical imaging or optogenetic techniques. The chamber housing the artificial dura is simple to maintain with minimal risk of infection and could be combined with semi-chronic microdrives and wireless recording hardware. This technique enables repeated acute penetrations over a period of several months. With occasional removal of tissue growth on the pial surface, recordings can be performed for a year or more. The approach is fully compatible with Neuropixels probes, enabling the recording of hundreds of single neurons distributed throughout the cortical column.

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“…1 ). The marmoset has been gaining interest as a model organism for studying cortical function due to its lissencephalic (smooth) cortex and its ability to perform complex visual tasks ( Mitchell et al, 2014 ; Solomon and Rosa, 2014 ; Selvanayagam et al, 2019 ; Cloherty et al, 2020 ; Davis et al, 2020 , 2023 ; Feizpour et al, 2021 ; Jendritza et al, 2021 , 2023 ; Dotson et al, 2023 ; Kell et al, 2023 ; Piza et al, 2023 ). However, there are still numerous technical considerations that can pose challenges to maximizing the utility of the marmoset cortex for neuroscience research.…”

Section: Introductionmentioning

confidence: 99%

Acute Neuropixels Recordings in the Marmoset Monkey

Dotson,

Davis,

Jendritza

et al. 2024

eNeuro

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High-density linear probes, like Neuropixels, provide an unprecedented opportunity to understand how neural populations within specific laminar compartments contribute to behavior. Marmoset monkeys, unlike macaque monkeys, have a lissencephalic (smooth) cortex that enables recording perpendicular to the cortical surface, thus making them an ideal animal model for studying laminar computations. Here we present a method for acute Neuropixels recordings in the common marmoset (Callithrix jacchus). The approach replaces the native dura with an artificial silicon-based dura that grants visual access to the cortical surface, which is helpful in avoiding blood vessels, ensures perpendicular penetrations, and could be used in conjunction with optical imaging or optogenetic techniques. The chamber housing the artificial dura is simple to maintain with minimal risk of infection and could be combined with semi-chronic microdrives and wireless recording hardware. This technique enables repeated acute penetrations over a period of several months. With occasional removal of tissue growth on the pial surface, recordings can be performed for a year or more. The approach is fully compatible with Neuropixels probes, enabling the recording of hundreds of single neurons distributed throughout the cortical column.Significance statementThe cerebral cortex of the macaque monkey is extensively folded, which poses a major problem for studying laminar computations in many cortical areas. Marmosets, however, have a smooth brain that allows for simultaneous recordings from all layers of the cortex in areas that are buried deep in sulci in the macaque. In this manuscript, we describe an artificial dura system that utilizes the state-of-the-art in high-density probes, Neuropixels. This system enables us to easily insert multiple Neuropixels into the marmoset cortex normal to the cortical surface permitting repeated laminar recordings for up to a year or more.

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Spike-phase coupling patterns reveal laminar identity in primate cortex

Cited by 14 publications

References 56 publications

Grouping cells in primate visual cortex

Grouping cells in primate visual cortex

Acute Neuropixels recordings in the marmoset monkey

Acute Neuropixels Recordings in the Marmoset Monkey

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