Close temporal coupling of neuronal activity and tissue oxygen responses in rodent whisker barrel cortex

Abstract

Neuronal activity elicits metabolic and vascular responses, during which oxygen is first consumed and then supplied to the tissue via an increase in cerebral blood flow. Understanding the spatial and temporal dynamics of blood and tissue oxygen () responses following neuronal activity is crucial for understanding the physiological basis of functional neuroimaging signals. However, our knowledge is limited because previous measurements have been made at low temporal resolution (>100 ms). Here we recorded at high temporal resolution (1 ms), simultaneously with co-localized field potentials, at several cortical depths from the whisker region of the somatosensory cortex in anaesthetized rats and mice. Stimulation of the whiskers produced rapid, laminar-specific changes in . Positive responses (i.e. increases) were observed in the superficial layers within 50 ms of stimulus onset, faster than previously reported. Negative responses (i.e. decreases) were observed in the deeper layers, with maximal amplitude in layer IV, within 40 ms of stimulus onset. The amplitude of the negative, but not the positive, response correlated with local field potential amplitude. Disruption of neurovascular coupling, via nitric oxide synthase inhibition, abolished positive responses to whisker stimulation in the superficial layers and increased negative responses in all layers. Our data show that responses occur rapidly following neuronal activity and are laminar dependent.

Simultaneous recording of hippocampal oxygen and glucose in real time using constant potential amperometry in the freely-moving rat

“…Changes in tissue oxygen levels measured by CPEs are related to changes in regional cerebral blood flow and these changes are directly comparable to the BOLD signal from fMRI studies (Lowry et al, 2010;Francois et al, 2012). As such, tissue oxygen levels measured using CPEs can be used to assess neural activity from localised regions of the brain in freely-moving animals (Li et al, 2011;Russell et al, 2012).…”

“…Oxygen levels fluctuate considerably even across short time scales with locomotor activity being an obvious influence on hippocampal oxygen even when not engaged in a hippocampus-dependent task (McHugh et al, 2011). As it has previously been shown that oxygen measured using amperometric sensors is directly comparable to the BOLD signal in fMRI (Lowry et al, 2010;Francois et al, 2012), these fluctuations may also be due to changes in synaptic activity in a given region of the brain (Logothetis et al, 2001;Goense and Logothetis, 2008;Li et al, 2011). Therefore, these concentrations are given only as preliminary estimates and the main findings of these experiments are expressed as changes away from the baseline rather than absolute changes in concentration as we would expect the direction and extent of these changes to be similar to those found with other sampling methods.…”

“…Sensors have been previously used to show the varied metabolic characteristics of different parts of the brain including the striatum Bazzu et al, 2009;Brown et al, 2009;Calia et al, 2009), nucleus accumbens (Finnerty et al, 2012;Francois et al, 2012), motor cortex (Lowry et al, 2010), prefrontal cortex (Finnerty et al, 2012) and whisker barrel cortex (Li et al, 2011). However, there has been less attention has been afforded to the hippocampus (Freund et al, 1989;Hu and Wilson, 1997) despite its pivotal roles in declarative memory (Scoville and Milner, 1957;Cohen et al, 1999;Eacott andEaston, 2011), spatial navigation (O'Keefe andNadel, 1978;Morris et al, 1982;D'Hooge and De Deyn, 2001) and its links to various neurodegenerative/psychiatric disorders (Heckers and Konradi, 2010;Marlatt and Lucassen, 2010;Bast, 2011;Dhikav and Anand, 2011;Bonilha et al, 2012).…”

Improving estimates of the cerebral metabolic rate of oxygen from optical imaging data

“…Such a mechanism is plausible given that the responses of arterial diameter (Tian et al, 2010), BOLD-fMRI (Goense et al, 2012;Tian et al, 2010), electrophysiological signals (Devor et al, 2007;Li et al, 2011), and tissue PO 2 (Li et al, 2011) vary with cortical depth, as does the baseline activity of the oxidative metabolic enzyme cytochrome oxidase (Weber et al, 2008). Any physiological variation through cortical layers is particularly relevant for results obtained from optical imaging techniques, since their sensitivity typically decreases with cortical depth (Tian et al, 2011).…”

Investigation of events in the EEG signal correlated with changes in both oxygen and glucose in the brain

“…Implanting of amperometric micro-electrodes in a specific region of the brain, and applying a suitable potential, allows us to record the faradic current and monitor changes in the concentration of a variety of substances in the ECF for long periods [9,10]. Thus we can perform investigations on the functions and roles of specific neurochemical substances.…”