Highly Dynamic Spatiotemporal Organization of Low-Frequency Activities During Behavioral States in the Mouse Cerebral Cortex

Abstract

Although low-frequency (LF < 10 Hz) activities have been considered as a hallmark of nonrapid eye movement (NREM) sleep, several studies have recently reported LF activities in the membrane potential of cortical neurons from different areas in awake mice. However, little is known about the spatiotemporal organization of LF activities across cortical areas during wakefulness and to what extent it differs during NREM sleep. We have thus investigated the dynamics of LF activities across cortical areas in awake and sleeping mice using chronic simultaneous local field potential recordings. We found that LF activities had higher amplitude in somatosensory and motor areas during quiet wakefulness and decreased in most areas during active wakefulness, resulting in a global state change that was overall correlated with motor activity. However, we also observed transient desynchronization of cortical states between areas, indicating a more local state regulation. During NREM sleep, LF activities had higher amplitude in all areas but slow-wave activity was only poorly correlated across cortical areas. Despite a maximal amplitude during NREM sleep, the coherence of LF activities between areas that are not directly connected dropped from wakefulness to NREM sleep, potentially reflecting a breakdown of long-range cortical integration associated with loss of consciousness.

Differential Recordings of Local Field Potential:A Genuine Tool to Quantify Functional Connectivity

“…However, some studies have used RR to quantify functional connectivity between 369 cortical areas [7,20]. Although, coherence and cross-correlation differences have been 370 observed between vigilance states, our results, as well as others, suggest that RR does 371 not measure the true functional connectivity between cortical areas.…”

“…We propose here to compare monopolar or RR 23 mode to bipolar or differential recording (DR), which consists in setting a pair of 24 electrodes in the same cortical area and measuring the voltage difference between 25 them. The main historical reasons why RR is widely used [7,20] are: 1) its simplicity 26 because of the low number of wires that needs to be implanted (contributing to the 27 preservation of brain tissue), 2) the number of available channels to connect to the 28 acquisition devices to record the signals, and 3) the method is sufficient to identify 29 global brain states and oscillations in extracellular space. However, to our knowledge, 30 no study has compared both recording methods in freely moving rats in order to define 31 the best suited configuration to record the activity of different brain areas and quantify 32 their interactions, as well as to extract the genuine meaning of the signals recorded in 33 a specific brain region during a behavioral task [1,7,[20][21][22][23][24][25][26][27][28].…”

“…Indeed, as illustrated in figure (7), we oberve that Hz is bigger than the 10 Hz to 14 Hz in CA1, because of the phasic (ie occasional) 218 nature of this 10 − 14Hz oscillation. In order to show that DR and RR modes do not 219 measure the same things, we have also reported the time-frequency of the same period 220 of CA1 and P F C in RR and DR mode in figure (7). Even if figure (7.DR) and figure 221 (7.RR) share some similarities, we can observe that P F C recording in DR presents no 222 θ rythm unlike in RR mode (7.P F C RR).…”

“…Nowadays, RR is still used [7,20] despite the advent of high density linear 351 electrodes [9,18,30] allowing to reconstruct the current-source density topology and 352 location (iCSD) [16,20]. However, when the experimental protocol is more complex 353 because of the number of cortical sites simultaneoulsy explored in a same animal, RR 354 should be used with caution.…”

“…To our knowledge, no study has compared both recording methods (i.e. RR and 358 DR) in freely moving rats in order to define the best suited configuration to record 359 cortical areas activity and quantify their interactions, as well as to extract the genuine 360 meaning of signals recorded in a specific cortical region during a behavioral 361 task [7,[20][21][22][23][24][25][26][27]. In this study, we clarify what is possible to assess according to the 362 recording mode.…”