Changes in reward-related signals in the rat nucleus accumbens measured by in vivo oxygen amperometry are consistent with fMRI BOLD responses in man

Abstract

a b s t r a c t a r t i c l e i n f oReal-time in vivo oxygen amperometry, a technique that allows measurement of regional brain tissue oxygen (O 2 ) has been previously shown to bear relationship to the BOLD signal measured with functional magnetic resonance imaging (fMRI) protocols. In the present study, O 2 amperometry was applied to the study of reward processing in the rat nucleus accumbens to validate the technique with a behavioural process known to cause robust signals in human neuroimaging studies. After acquisition of a cued-lever pressing task a robust increase in O 2 tissue levels was observed in the nucleus accumbens specifically following a correct lever press to the rewarded cue. This O 2 signal was modulated by cue reversal but not lever reversal, by differences in reward magnitudes and by the motivational state of the animal consistent with previous reports of the role of the nucleus accumbens in both the anticipation and representation of reward value. Moreover, this modulation by reward value was related more to the expected incentive value rather than the hedonic value of reward, also consistent with previous reports of accumbens coding of "wanting" of reward. Altogether, these results show striking similarities to those obtained in human fMRI studies suggesting the use of oxygen amperometry as a valid surrogate for fMRI in animals performing cognitive tasks, and a powerful approach to bridge between different techniques of measurement of brain function.

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

“…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.…”

“…Carbon paste electrodes (CPEs) have been shown to detect oxygen with high sensitivity and selectivity at a sub-second temporal resolution (Bolger et al, 2011b). 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).…”

“…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).…”

Differential Contributions of Infralimbic Prefrontal Cortex and Nucleus Accumbens during Reward-Based Learning and Extinction

“…Carbon paste electrodes (CPEs) were constructed from 8 T (200 m bare diameter, 270 m coated diameter) Teflon-coated silver wire (Advent Research Materials), as described previously Francois et al, 2012). The Teflon insulation was slid along the wire to create an ϳ2-mm-deep cavity, which was packed with carbon paste.…”

“…Animal studies performed to date have typically involved lesioning of, or electrophysiological recordings in those structures after the animals have been trained to stable performance levels of a given goal-directed behavior. The present study addressed how the NAc and IFC interact at different points during the learning of a goal-directed behavior by simultaneously recording regional activity during the acquisition and extinction of a cued lever-press task using in vivo oxygen amperometry, a technique shown to serve as a valid surrogate of functional magnetic resonance imaging in behaving animals Francois et al, 2012).…”