Aligning the Brain in a Rhythmic World

More documents

Recommendations

Info

NoTeS 24 oscillations as an instrument for enhancing auditory processing. That is, the somatosensory input does not appear to increase the power of ongoing oscillations; however, it does increase phase coherence across trials (intertrial coherence, or ITC) in the low delta, theta, and gamma bands. The somatosensory (modulatory) input contrasts with the auditory (driving) input, which provokes both increase in oscillatory power and ITC across the spectrum, typical of an “evoked” response (Makeig et al., 2004; Shah et al., 2004). Prestimulus-to-poststimulus increase in phase concentration (in the absence of an accompanying increase in power) indicates that, in A1, somatosensory input has an effect mainly by resetting the phase of ongoing oscillations. Thus, somatosensory input “modulates” the dynamics of activity in A1 but does not cause auditory neurons to respond (Lakatos et al., 2007). Both Ghazanfar et al. (2005) and Kayser et al. (2008) found that visual input has similar effects on auditory processing in primary and secondary auditory cortical areas. Thus, it seems that this is a general mechanism whereby nonpreferred (modulatory) stimuli can affect specific stimulus processing. Attentional selection Recent findings show that when behaviorally relevant stimuli occur in predictable (rhythmic) streams, lowfrequency oscillations can function as instruments of attentional selection in primary visual cortex (V1) (Lakatos et al., 2008). For these studies, we trained monkeys to perform an intermodal selection task in which auditory and visual stimuli (beeps and flashes) were delivered in jittered but rhythmic interdigitated streams. In alternate trial blocks, the monkey had to attend to either the visual or the auditory stimulus stream, and make a manual response to an infrequently presented “oddball” stimulus. Although this paradigm is artificial, it combines the rhythmic structure and variability characteristic of many natural event patterns. The key finding of this experiment is that, whereas activity in the thalamic input (granular) layers entrains (oscillatorily phaselocks) reliably to visual input, activity in the extragranular layers entrains to the attended input stream, whether visual or auditory. The difference is most apparent in the supragranular laminae: A direct comparison of CSD responses across the attend and ignore conditions shows that delta oscillations in the supragranular layers are entrained in opposite phase in the two attention conditions. The same comparison for the granular layers shows amplitude, but not phase modulation by attention. These effects share several complexities, including concomitant theta and gamma band modulations (Lakatos et al., 2008). However, the key factor is the relationship between delta oscillation phase and neuronal excitability and the modulation (shifting) of delta phase by attention. In broad terms: (1) In the attend visual condition, the laminar CSD profile at stimulus onset reflects a high excitability state that permits the transmission of inputs from granular to extragranular laminae (and onward), whereas in the ignore visual (attend auditory) condition, the laminar CSD configuration at this time point reflects a relative depression of excitability in this circuit. (2) These differential facilitative and suppressive states are responsible for attention’s effects on visual response amplitudes. Operational mode of the brain aligns to task rhythmicity We have proposed that, depending on task demands, the brain dynamically shifts between variably rhythmic operating modes (Schroeder and Lakatos, 2009a). At the extremes are the “continuous/vigilance” mode and the “rhythmic” mode. The former may be best exemplified by the classic vigilance paradigm used in Psychology. This paradigm entails a task in which the target stimuli occur at a completely random and unpredictable time; an example is when a cat watches a mouse hole, waiting for the mouse to appear. However, as discussed above, a great deal of natural stimulation is explicitly rhythmic and predictable. Under these conditions, neuronal oscillations can entrain to the structure of the stimulus stream and become instrumental in sensory processing (Schroeder et al., 2008) (the intermodal paradigm described above is of this type). Rhythmic mode operation entails entraining activity to the temporal structure of an attended stream, resulting in the alignment of highexcitability oscillation phases with events in the attended stream. Rhythmic mode entrainment, in turn, leads to systematic enhancement of responses to attended events, and suppression of responses to events that occur out of phase with attended events. In contrast, when there is no task-relevant rhythm to which the system can entrain, low-frequency oscillations tend to blunt neuronal processing, because they entail relatively long periods of low excitability during which detection of subtle stimuli would be impaired. Under these conditions, a continuous (vigilance) mode of operation is implemented, lowfrequency oscillations are suppressed, and the system © 2009 Schroeder
is pushed as far as possible into a continuous state of high excitability. Several behavioral observations are consistent with the differential operation of these two processing modes. In continuous/vigilance mode, where the oscillatory correlates of attention are enhanced gamma amplitude/synchrony and lower frequency suppression (Fries et al., 2001), variations in gamma synchrony are predictive of reaction time variations (Womelsdorf et al., 2006). In rhythmic mode, where attention uses low-frequency rhythmic entrainment (Lakatos et al., 2008), low-frequency phase predicts reaction time. We have suggested (Schroeder and Lakatos, 2009a) that rhythmic mode is the preferred state of the system for the following reasons: (1) It is efficient because inputs that are out of phase with the attended stream are automatically suppressed; (2) Gamma-band activity appears to be more metabolically demanding than low-frequency oscillations (Mukamel et al., 2005; Niessing et al., 2005); and (3) Owing to hierarchical coupling, gamma activity is “rationed” (selectively enhanced) at critical time points, when a high-excitability state is most useful. In this sense, the gamma oscillation is a “slave” rather than a “master” operator (Schroeder and Lakatos, 2009b). Converging Theory and Reflection on Earlier Findings “Dynamic attending theory” proposes to describe many key components of rhythmic mode processing from a psychophysical perspective (Jones and Boltz, 1989; Large and Jones, 1999; Jones et al., 2006). This idea has also been developed in a motor framework (Praamstra et al., 2006). The basic hypothesis put forward by Jones and colleagues is that attending itself can be an oscillatory process that entrains to environmental rhythms, thereby improving discriminative performance. In a similar vein, Nobre and colleagues have suggested that “attention to time” is a fundamental form of attending, controlled by a parietocentric network of brain structures (Nobre et al., 2007; Correa and Nobre, 2008a,b). There is evidence (Ghose and Maunsell, 2002) that in a temporally structured (rhythmic) task, monkeys form an internal representation of task timing that can guide the temporal allocation of attentional resources in order to maximize behavioral performance. In all © 2009 Schroeder Aligning the Brain in a Rhythmic World these cases, entrained neuronal oscillations, operating in a steady-state mode and/or resetting on a trial-bytrial basis, provide likely physiological substrates for the effects of attention. The fact that, because of cross-frequency coupling, oscillations can be reset to low-excitability as well as high-excitability states on multiple time scales (Schroeder et al., 2008) increases the flexibility and range of the mechanism. The distinction between rhythmic and continuous modes of processing may be fundamental: Evidence of rhythmic mode operation can be seen in diverse varieties of attention, including “object attention” (Taylor et al., 2005), whereas “intermodal attention” (Lakatos et al., 2008) can operate in a rhythmic mode, with excitability/gamma bursting coupled to the rhythm of the task. Significantly, the most heavily studied form of attention—spatial attention— can operate either in continuous mode, with the effect of tonic increase in excitability (Fries et al., 2001; Womelsdorf et al., 2006), or in rhythmic mode, with periodic variations in excitability coupled to the temporal structure of the task (Ghose and Maunsell, 2002). The idea that several modes govern the operation of attention may help resolve discrepancies between attention effects reported by different laboratories (Moran and Desimone, 1985; Luck et al., 1997, versus results from McAdams and Maunsell, 1999; Treue and Maunsell, 1999). Examining the task structures used by these groups suggests that the former generally examine functioning in the continuous/vigilance mode, whereas the latter do so in the rhythmic mode. Phase-resetting of low-frequency oscillations may help explain cueing effects on attentional performance and pertinent event-related potentials (ERPs). The frontal contingent negative variation (CNV) (Walter et al., 1964), for example, may be generated by phase-resetting frontal low-frequency oscillations by a warning cue, which are then averaged over trials. The perceptual effects known as “attentional blink” (Raymond et al., 1992) and “inhibition of return,” or IOR (Klein, 2000), result when stimuli are delivered during the low-excitability phase of a low-frequency oscillation that has been reset by the appearance of either a salient target or a cue to attend. Outstanding questions Is rhythmic mode processing generalizable? A number of empirical predictions need to be evaluated. Sensory selection in a typical 25 NoTeS
Page 1: © 2009 Schroeder Aligning the Brai
Page 6 and 7: NoTeS 26 spatial attention paradigm
Page 8: NoTeS 28 McAuley JH, Rothwell JC, M

Aligning the Brain in a Rhythmic World

You also want an ePaper? Increase the reach of your titles

Delete template?

Save as template?