The first published report of human electroencephalographic (EEG) data described elevated oscillations centered at the frequency of 10
Hz over posterior electrode sites, which increased in magnitude when the eyes were closed, and decreased when the eyes were opened (Berger, 1929
). Replications and extensions of this finding have led to the widely held view that posterior alpha-band oscillations correspond to an “idling” state of the brain (Pfurtscheller et al., 1996
), with higher frequency oscillations (e.g., in the beta- and gamma-band) predominating when the same networks are engaged in, for example, active visual processing. Subsequent studies have revealed alpha-band power modulations in both attention and working memory tasks, suggesting a larger role for alpha-band oscillations in cognition than the idling account would suggest. For instance, several studies have shown that shifts of covert spatial attention are accompanied by increased alpha-band oscillations over posterior sensors ipsilateral to the direction of attention, and decreased alpha contralateral to the focus of attention (see, e.g., Worden et al., 2000
; Kelly et al., 2006
; Thut et al., 2006
). That is, alpha-band power decreases at attended and increases at unattended locations, suggesting a functional inhibitory role for shifts in posterior alpha-band power. Consistent with this possibility, spontaneous fluctuations in occipital alpha-band power have been found to predict cortical excitability, as indexed by the perception of TMS-induced visual phosphenes (Romei et al., 2008
). Additionally, the detection of at-threshold visual stimuli is predicted by the pre-stimulus power (Hanslmayr et al., 2007
; Van Dijk et al., 2008
; Mathewson et al., 2009
) and phase angle (Mathewson et al., 2009
; Busch and VanRullen, 2010
) of spontaneous posterior alpha-band oscillations.
Increased alpha-band power has also been observed throughout the delay period of tasks requiring the short-term retention of visual information (see, e.g., Klimesch et al., 1999
; Jensen et al., 2002
; Jokisch and Jensen, 2007
; Tuladhar et al., 2007
; Hamidi et al., 2009
). For instance, Klimesch et al. (1999
) observed increased posterior delay-period alpha-band power (DPABP) during the retention of unique alpha-numeric strings in working memory. Additionally, Jensen et al. (2002
) found that DPABP parametrically increases as a function of memory load during performance of a modified Sternberg (1966
These memory-related alpha-band power increases have been proposed to reflect either functional inhibition (Klimesch et al., 2007
), or active processing related to the short-term retention of information in working memory (Palva and Palva, 2007
). For example, Klimesch et al. (1999
) has argued that increased DPABP reflects a mechanism of inhibitory top-down control that prevents the retrieval of stimuli that were remembered on previous trials, which could interfere with the encoding and maintenance of new information. Another proposal, emphasized in the work of Jensen and colleagues (Jokisch and Jensen, 2007
; Jensen and Mazaheri, 2010
), holds that task-specific increases in alpha-band power reflect the functional inhibition of cortical areas representing potentially disruptive task-irrelevant information. For instance, when remembering an object's shape or color, optimal performance may depend on our ability to ignore task-irrelevant information, such as the object's location, orientation, or direction of motion. If this were the case, elevated alpha-band power should be present over task-irrelevant cortical areas during the delay period. It is this version of the “alpha inhibition” hypothesis that will be the focus of this report.
In keeping with the idea of filtering out stimulus dimensions that are trial irrelevant, elevated DPABP has been observed over dorsal stream visual areas during the retention of face identities, which engages the ventral stream (Jokisch and Jensen, 2007
). Similarly, Hamidi et al. (2009
) observed a pronounced sustained posterior increase in DPABP during the retention of abstract shapes in working memory. Additionally, smaller but reliable elevations in DPABP were also observed on trials in which participants were instructed to remember the location, rather than the identity, of each shape. In another study (Grimault et al., 2009
), participants were cued to remember stimuli appearing in either the left or right visual field, ignoring stimuli in the opposite visual field (as in Vogel and Machizawa, 2005
). In keeping with findings from studies of spatial attention, DPABP increased at parietal electrodes ipsilateral to the remembered hemifield. That is, alpha-band power increased over visual areas representing locations that were to be ignored on that trial.
However, findings from the visual cognition literature raise questions about the functional inhibition interpretation of alpha-band power. First, although it is true that, when given enough time (~1000–1500
ms for location, and 500–1000
ms for features), task-irrelevant changes in object properties can be ignored when they occur at test (Logie et al., 2011
), numerous studies exploring memory for object properties, such as shape, color, and orientation, have suggested that when objects are attended, spatial, and non-spatial features are spontaneously integrated in working memory (see, e.g., Jiang et al., 2000
; Treisman and Zhang, 2006
; Hollingworth and Rasmussen, 2010
). Moreover, although changes in task-irrelevant information can have an impact on performance (see, e.g., Jiang et al., 2000
), there is no evidence that we are aware of suggesting that the mere presence of task-irrelevant though non-distracting information (e.g., the task-irrelevant shape and location information in the studies described above) adversely affects performance.
Additionally, if alpha power increases reflect a general inhibitory mechanism that suppresses task-irrelevant cortical areas, increased alpha would be expected to be present over task-irrelevant areas whether the primary task is spatial or
non-spatial in nature. However, in the experiments of Jokisch and Jensen (2007
), alpha increases were observed over the dorsal stream in a face identity task that engaged the ventral stream, but were not seen over the ventral stream during retention of face orientations, which engaged the dorsal stream. Increased alpha was observed in the location-memory condition of Hamidi et al. (2009
), but the magnitude of the increase was much lower than observed during shape retention, and our own unpublished observations suggest that these increases are only present when individual locations are marked by unique shapes, being largely absent when locations are marked by uniform circles.
An alternative account of DPABP, therefore, is that instead of, or in addition to, reflecting the inhibition of task-irrelevant information, sustained increases in alpha power observed in working memory tasks may be a critical component of the distributed network activity underlying the selection and maintenance of objects in working memory, as proposed by Palva and Palva (2007
). By this view, load dependent increases in alpha-band power reflect increasing demands on attention- and maintenance-related neural systems, rather than inhibition.
In keeping with this possibility memory-load dependent increases in high alpha-, beta-, and gamma-band oscillations have been observed in frontal and parietal regions implicated in attentional and executive aspects of working memory, although the amplitudes of these oscillations were suppressed below baseline levels (Palva et al., 2011
). Additionally, a role for alpha-band oscillations in object processing has received support from a recent study examining local field potentials and multi-unit activity in the inferior temporal (IT) cortex of macaques performing an intermodal (visual versus auditory) selective attention task (Mo et al., 2011
). On each trial, monkeys received bimodal stimulation, but attention was directed to either visual or auditory information in alternating trial blocks. Results revealed higher pre-stimulus LFP power and multi-unit activity when monkeys attended to visual versus auditory stimuli. Moreover, increased pre-stimulus LFP alpha was predictive of stronger stimulus-evoked responses, suggesting that, in contrast to alpha activity observed in the occipital cortex, alpha oscillations in IT may play a direct role in amplifying task-relevant information.
In the present study, we test the predictions of the inhibitory view of alpha-band oscillations proposed by Jensen and Mazaheri (2010
) and those of the object selection and maintenance hypothesis using a delayed-recognition paradigm in which the presence and task relevance of shape information was systematically manipulated across trial blocks and EEG was recorded to measure DPABP. In the first trial block, participants remembered locations marked by identical black circles. The second block featured the same instructions, but locations were marked by unique shapes. The third block consisted of two memory conditions featuring identical stimulus presentation, but with pretrial instructions indicating, on a trial-by-trial basis, whether memory for shape or location was required, the other dimension being irrelevant. In the final block, stimuli once again consisted of unique shapes appearing at distinct locations, as in Blocks 2–3. However, in this block participants were required to remember the unique pairing of shape and location for each stimulus, rather than shape or location alone, as in Block 3. Thus, Blocks 2–4 consisted of identical stimulus presentation, with the only difference being whether memory for location, memory for shape, or memory for shapes in specific locations was required.
If increased DPABP reflects the functional inhibition of task-irrelevant cortical areas, it should be observed in each condition that includes the presence of task-irrelevant information. Thus, DPAPB should be absent in Block 1, in which no unique task-irrelevant information was present to be inhibited. Conversely, alpha-band power should be elevated in Block 2, and in both conditions of Block 3, in which irrelevant shape information was present in the location task, and irrelevant location information was present in the shape task. Finally, DPABP should be reduced in Block 4, in which both shape and location were task relevant, and thus neither should be inhibited.
By contrast, the object selection and maintenance hypothesis makes the following predictions. Elevated DPABP should not be observed in Block 1, because no unique shape information was present. Conversely, DPABP should be elevated in Block 2, and in both conditions of Block 3. However, on the basis of our previous observations (Hamidi et al., 2009
), we expect DPAPB to be greater in the shape-memory condition of Block 3, in which shapes were task relevant, than in any of the location-memory conditions, in which shape was present but did not need to be actively maintained. Finally, in contrast to the predictions of the functional inhibition account, DPABP should remain elevated in Block 4, which required the retention of shape–location associations.