Abstract
Although EEG alpha (α; 8–13 Hz) rhythms are often considered to reflect an “idling” brain state, numerous studies indicate that they are also related to many aspects of perception. Recently, we outlined a potential cellular substrate by which such aspects of perception might be linked to basic α rhythm mechanisms. This scheme relies on a specialized subset of rhythmically bursting thalamocortical (TC) neurons (high-threshold bursting cells) in the lateral geniculate nucleus (LGN) which are interconnected by gap junctions (GJs). By engaging GABAergic interneurons, that in turn inhibit conventional relay-mode TC neurons, these cells can lead to an effective temporal framing of thalamic relay-mode output. Although the role of GJs is pivotal in this scheme, evidence for their involvement in thalamic α rhythms has thus far mainly derived from experiments in in vitro slice preparations. In addition, direct anatomical evidence of neuronal GJs in the LGN is currently lacking. To address the first of these issues we tested the effects of the GJ inhibitors, carbenoxolone (CBX), and 18β-glycyrrhetinic acid (18β-GA), given directly to the LGN via reverse microdialysis, on spontaneous LGN and EEG α rhythms in behaving cats. We also examined the effect of CBX on α rhythm-related LGN unit activity. Indicative of a role for thalamic GJs in these activities, 18β-GA and CBX reversibly suppressed both LGN and EEG α rhythms, with CBX also decreasing neuronal synchrony. To address the second point, we used electron microscopy to obtain definitive ultrastructural evidence for the presence of GJs between neurons in the cat LGN. As interneurons show no phenotypic evidence of GJ coupling (i.e., dye-coupling and spikelets) we conclude that these GJs must belong to TC neurons. The potential significance of these findings for relating macroscopic changes in α rhythms to basic cellular processes is discussed.
Highlights
The customary view of EEG α (8–13 Hz) rhythms is that they are a definitive marker of quiet or relaxed wakefulness, there is a large body of evidence indicating that they are closely linked to several important aspects of perception (VanRullen and Koch, 2003; Fingelkurts and Fingelkurts, 2006; Mathewson et al, 2009)
Thalamic delivery of gap junction blockers disrupts lateral geniculate nucleus (LGN) and EEG a rhythms In order to assess the role of thalamic gap junctions (GJs) in the generation of LGN and EEG α rhythms we examined the effects of carbenoxolone (CBX) and 18β-glycyrrhetinic acid (18β-GA; both at 1 mM), delivered directly to the LGN via reverse microdialysis, on spontaneous oscillatory activity
In contrast to the suppressive effects of CBX and 18β-GA, the glycyrrhetinic acid derivative that is inactive as a GJ blocker, glycyrrhizic acid (GZA, 1 mM), had no effect on either the density, power, or frequency of LGN and EEG α rhythms (Figures 2B,D,F; Table 1)
Summary
The customary view of EEG α (8–13 Hz) rhythms is that they are a definitive marker of quiet or relaxed wakefulness, there is a large body of evidence indicating that they are closely linked to several important aspects of perception (VanRullen and Koch, 2003; Fingelkurts and Fingelkurts, 2006; Mathewson et al, 2009). The central tenet of these studies is that α rhythms provide “excitability cycles” that act to temporally frame or gate perceptual events (Bartley, 1940; Lindsley, 1952; Lansing, 1957; Wiener, 1985; Crick and Koch, 2003; VanRullen and Koch, 2003; Fingelkurts and Fingelkurts, 2006; Mathewson et al, 2009) Such “excitability cycles” are considered to be a potential basis for explaining discrete perceptual processing in the brain, an idea whereby perception is considered to occur in discrete snapshots or processing epochs lasting around 70–100 ms (Stroud, 1955; Efron, 1970), and which itself can be traced back to the work of William James over a century ago (James, 1890)
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