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. 2009 Jan 28;29(4):1191-201.
doi: 10.1523/JNEUROSCI.4867-08.2009.

Contrasting activity profile of two distributed cortical networks as a function of attentional demands

Daniela Popa  1 , Andrei T Popescu, Denis Paré
Affiliations

Contrasting activity profile of two distributed cortical networks as a function of attentional demands

Daniela Popa et al. J Neurosci. .

Abstract

Recent human functional MRI (fMRI) studies have revealed that two widely distributed groups of cortical areas display inverse changes in activity when attentional demands increase, with one group showing higher (task-on) and the second lower (task-off) blood oxygen level-dependent (BOLD) signals. Moreover, task-on and task-off regions also exhibit slow (<0.2 Hz) inversely correlated fluctuations in BOLD signal at rest. However, the neuronal correlates of these reciprocal BOLD signal fluctuations are unknown. Here, we addressed this question using simultaneous recordings of unit activity and local field potentials (LFPs) in the cat homologues of task-on and task-off regions. In all states of vigilance, LFP power was lower in task-off than task-on regions with no difference in firing rates. Both sets of regions displayed slow (0.5-0.15 Hz) cyclical modulations in LFP power in all frequency bands but with large and variable phase differences such that task-on and task-off regions were often anticorrelated. Inversely correlated LFP power fluctuations were state-dependent in that they were much more frequent in waking and paradoxical sleep than in slow-wave sleep. Moreover, consistent with fMRI findings, when attentional demands increased, LFP power in task-on and task-off regions changed in opposite directions, further augmenting and decreasing, respectively. At odds with previous fMRI studies, however, the decreased LFP power in task-off regions was associated with increased firing rates, suggesting that the engagement of task-off regions might not be reduced but in fact enhanced during attention.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1.
Figure 1.
Location and histological identification of recording sites. A, Recording method. Microelectrodes (filled circles) were inserted in various cortical regions. Targeted task-on regions (red circles) included the insula as well as areas 5, 7, and 21. Task-off regions (blue circles) consisted of the medial prefrontal, cingulate, and retrosplenial cortices. In addition, we obtained recordings from the entorhinal cortex and BLA. Electrodes positioned in the SMA are shown in gray because earlier fMRI studies variously classified this area as belonging to the task-on or task-off networks. B–F, Histological verification of recording sites. Coronal (B–E) and parasagittal (F) sections showing the location of electrolytic lesions (arrows) performed at the end of the experiments to mark the position of the microelectrode tips in SMA (B), anterior cingulate cortex (C), the entorhinal cortex (D), area 5 (E) and the posterior cingulate cortex (F). A, Amygdala; CA, caudate nucleus; CC, corpus callosum; CRU, cruciate sulcus; H, hippocampus; LAT, lateral sulcus; OB, olfactory bulb; PRS, presylvian sulcus; RS, retrosplenial cortex; RhS, rhinal sulcus; SPL, splenial sulcus; SUPS, suprasylvian sulcus; V, ventricle.
Figure 2.
Figure 2.
LFP power is lower in task-off than task-on regions. A, B, LFPs recorded simultaneously in task-on (A) or task-off (B) regions in waking (W), at the transition from waking to slow-wave sleep (W→SWS), and during paradoxical sleep (REM). A3 and B3 show an expanded period of SWS. C1–3, Frequency distribution of total power in W (C1), SWS (C2), and REM sleep (C3). Note that all histograms are bimodal. Arrows indicate cutoff between low and high modes. C1 (insets), Separate frequency distributions of LFP power for task-on and task-off regions during wakefulness.
Figure 3.
Figure 3.
Task-on and task-off regions exhibit slow LFP power fluctuations. A, Average delta (continuous line) and gamma (dashed line) power fluctuations in task-on (A1) and task-off (A2) regions during a slow-wave sleep epoch. B, Correlation between unit activity and LFP power in the theta (red) and fast (black) frequency bands in task-on (B1) and task-off (B2) regions. Average of data obtained in 10 different waking epochs obtained from three cats. C, D, FFT of average unit-power crosscorrelograms shown in A for fast (C1, D1) and theta (D1, D2) LFP activity. Thick lines indicate power of actual correlogram, whereas thin solid line indicate power ±1SD (dashed lines) of shuffled correlograms. E, Same as in B but for a single waking session where the power-unit relations were particularly strong and rhythmic. F, Gamma power fluctuations of task-on (black) and task-off (red) regions in waking shown with a slow (F1) and fast (F2–3) time base. Same epoch is shown in F1–2. Arrows in F2–3 point to periods of anticorrelated fluctuations in gamma power in task-on and task-off regions.
Figure 4.
Figure 4.
Operant sensory discrimination task. A, B, Cats were presented vertical (CS−, A) or horizontal gratings (CS+, B). The CS+ had a variable duration (10–18 s) and was followed by a second grating (4 s) of shifted orientation (5–45°), during which the cat had to lick to obtain a liquid food reward at CS+ offset. Each session, ∼25 CS+ and 25 CS− were presented in random order (40 s between onset of each CS). C, D, Lick frequency (y-axis) as a function of time (x-axis) during trials where the CS+ (C) or CS− (D) were presented.
Figure 5.
Figure 5.
Compared with the CS−, LFP power during the CS+ shifts in opposite directions in task-on and task-off regions. A, Difference in LFP power during the CS+ versus the CS− (y-axis) in various frequency bands (x-axis) in task-on (thick line) and task-off (thin line) regions. B, Normalized change in total power in different task-on (thick lines) and task-off (thin lines) regions.
Figure 6.
Figure 6.
Compared with the CS−, LFP coherence during the CS+ increases both within and between task-on and task-off regions. A, LFP coherence (theta band) during the CS− (empty bars) and CS+ (solid bars) among task-on (left), task-off (middle), or between task-on and task-off regions (right). B, LFP coherence (color coded) in various frequency bands (x-axis) during the CS− (left) and CS+ (right).
Figure 7.
Figure 7.
LFP power and firing rates change in opposite directions in task-off regions during the CS+. Graphs plotting difference in total (A) or theta (B) power (y-axis) as a function of difference in firing rate (x-axis) during the CS+ versus CS− in task-on (empty circles) and task-off (filled circles) regions. B (inset), Normalized difference in firing rates during the CS− versus CS+ for neurons recorded in task-on (white bar) and task-off (black bar) regions. C, Average firing rate of a task-off neuron (y-axis, data normalized to baseline values) as a function of time (x-axis) during trials where a CS+ (red line, n = 25) or a CS− (black line, n = 47) were presented. D, Normalized difference in firing rates during the CS− versus CS+ for neurons recorded in different task-on (left, white bars) and task-off (right, black bars) regions. Area 7, n = 36; insula (INS), n = 13; area 5, n = 19; area 21, n = 11; medial prefrontal cortex (mPFC), n = 15; anterior cingulate (ACing), n = 29; posterior cingulate (PCing), n = 26; retrosplenial (Retrospl), n = 6.
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