Abstract
Spontaneous slow oscillation-associated slow wave activity represents an internally generated state which is characterized by alternations of network quiescence and stereotypical episodes of neuronal activity - slow wave events. However, it remains unclear which macroscopic signal is related to these active periods of the slow wave rhythm. We used optic fiber-based calcium recordings of local neural populations in cortex and thalamus to detect neurophysiologically defined slow calcium waves in isoflurane anesthetized rats. The individual slow wave events were used for an event-related analysis of simultaneously acquired whole-brain BOLD fMRI. We identified BOLD responses directly related to onsets of slow calcium waves, revealing a cortex-wide BOLD correlate: the entire cortex was engaged in this specific type of slow wave activity. These findings demonstrate a direct relation of defined neurophysiological events to a specific BOLD activity pattern and were confirmed for ongoing slow wave activity by independent component and seed-based analyses.
Highlights
Slow oscillation-associated slow wave activity is characterized by a waxing and waning of spontaneous neuronal firing arising from neuronal populations in deeper cortical layers (Chauvette et al, 2010; Sanchez-Vives and McCormick, 2000; Stroh et al, 2013), influencing neuronal excitability as well as stimulus-response properties of neuronal networks throughout the brain (McGinley et al, 2015b; Petersen et al, 2003; Steriade et al, 1993c; 1993b)
Cortical layers are indicated. (C) Fluorescence micrograph of a coronal brain slice depicting the area of Oregon Green BAPTA1 (OGB-1) staining at the level of primary somatosensory cortex, scale bar = 1 mm. (D) Fluorescence micrograph of co-staining with OGB-1 and sulforhodamine 101 (SR101) (E) Expression of GCaMP6f four weeks after injection of AAV1.Syn.GCaMP6f. (F–G) Expression of GCaMP6f four weeks after injection of AAV1.CamKII.GCaMP6f scale bar F = 500 mm G = 50 mm. (H) Calcium trace upon OGB-1 staining recorded in the MR scanner during slow wave activity
Recorded spontaneous stereotypical calcium waves are interrupted by periods of network quiescence. (I) Optical recordings in GCaMP6f expressing rats reveal slow calcium waves. (J–M) Quantifications of slow calcium wave parameters in OGB-1 stained vs. GCaMP6f expressing rats reveal significant differences only in rise times (p=0.0001), whereas amplitude and durations are not significantly different (p=0.13; p=0.61). (N) Simultaneous optical calcium recordings outside the MR scanner using two optic fibers implanted into left hemisphere with OGB-1 staining and with CaMKII-GCaMP6f staining
Summary
Slow oscillation-associated slow wave activity is characterized by a waxing and waning of spontaneous neuronal firing arising from neuronal populations in deeper cortical layers (Chauvette et al, 2010; Sanchez-Vives and McCormick, 2000; Stroh et al, 2013), influencing neuronal excitability as well as stimulus-response properties of neuronal networks throughout the brain (McGinley et al, 2015b; Petersen et al, 2003; Steriade et al, 1993c; 1993b). An optical fiber was lowered into the rat’s brain to transmit the fluorescence signals to a computer Monitoring these signals while the animals lay inside the scanner revealed that slow-wave activity in any one group of cortical neurons was accompanied by slowwave activity across the cortex as a whole. In order to investigate brain-wide BOLD correlates of locally occurring slow waves, these two signals have to be recorded simultaneously, and slow waves have to be detected in a spatiotemporally precise manner and directly related to BOLD activity To achieve this aim, optic fiber-based calcium recordings are well-suited as they can be performed unperturbed by the magnetic field of the MR scanner (Schmid et al, 2016; Schulz et al, 2012). We reveal the interrelation of a neurophysiological defined slow wave event and a macroscopic, network organizing signal, and find a cortex-wide BOLD fMRI correlate
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