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The Journal of Neuroscience, September 28, 2005, 25(39):9046-9058; doi:10.1523/JNEUROSCI.2127-05.2005

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Behavioral/Systems/Cognitive
Separate Spatial Scales Determine Neural Activity-Dependent Changes in Tissue Oxygen within Central Visual Pathways

Jeffrey K. Thompson,^1,2 Matthew R. Peterson,^1,2 and Ralph D. Freeman^1,2,3

¹School of Optometry, ²Group in Vision Science, and ³Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, California 94720-2020

The relationship between oxygen levels and neural activity in the brain is fundamental to functional neuroimaging techniques. We have examined this relationship on a fine spatial scale in the lateral geniculate nucleus (LGN) and visual cortex of the cat using a microelectrode sensor that provides simultaneous colocalized measurements of oxygen partial pressure in tissue (tissue oxygen) and multiunit neural activity. In previous work with this sensor, we found that changes in tissue oxygen depend strongly on the location and spatial extent of neural activation. Specifically, focal neural activity near the microelectrode elicited decreases in tissue oxygen, whereas spatially extended activation, outside the field of view of our sensor, yielded mainly increases. In the current study, we report an expanded set of measurements to quantify the spatiotemporal relationship between neural responses and changes in tissue oxygen. For the purpose of data analysis, we develop a quantitative model that assumes that changes in tissue oxygen are composed of two response components (one positive and one negative) with magnitudes determined by neural activity on separate spatial scales. Our measurements from visual cortex and the LGN are consistent with this model and suggest that the positive response spreads over a distance of 1–2 mm, whereas the negative component is confined to a few hundred micrometers. These results are directly relevant to the mechanisms that generate functional brain imaging signals and place limits on their spatial properties.

Key words: neurovascular coupling; neurometabolic coupling; tissue oxygen; initial dip; lateral geniculate; LGN; microelectrode; extracellular recordings; optical imaging; fMRI

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Received Jan 24, 2005; revised August 16, 2005; accepted August 18, 2005.

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