Role of Posterior Parietal Gamma Activity in Planning Prosaccades and Antisaccades

The Journal of Neuroscience, December 17, 2008 • 28(51):13713–13715 • 13713

Journal Club

Editor’s Note: These short, critical reviews of recent papers in the Journal, written exclusively by graduate students or postdoctoral fellows, are intended to summarize the important findings of the paper and provide additional insight and commentary. For more information on the format and purpose of the Journal Club, please see http://www.jneurosci.org/misc/ifa_features.shtml.

Karim Jerbi,1,2 Carlos M. Hamame´,3 Toma´s Ossando´n,1,4 and Sarang S. Dalal1 1INSERM U821, Dynamique Ce´re´brale et Cognition, 69500 Lyon, France, 2Laboratoire de Physiologie de la Perception et de l’Action, UMR 7152, Colle`ge de France, CNRS, 75005 Paris, France, 3Programa de Doctorado en Ciencias Biome´dicas, Instituto de Ciencias Biome´dicas, Facultad de Medicina, Universidad de Chile, Santiago 8380453, Chile, and 4E´cole Doctorale Neurosciences et Cognition, Universite´ Claude Bernard Lyon I, 69622 Villeurbanne cedex, France Review of Van Der Werf et al. (http://www.jneurosci.org/cgi/content/full/28/34/8397)

Although the components of the cerebral arate the brain activity involved in visual after stimulus presentation, a second network mediating saccade preparation in perception (the “stimulus component”) narrowband gamma component (85– humans have been extensively outlined by from activity representing a motor goal 105 Hz) appeared to be selective to the numerous functional magnetic resonance (the “goal component”). The basic as- direction of the upcoming saccade [Van imaging (fMRI) studies (e.g., Schluppeck sumption behind this design is that sac- Der Werf et al. (2008), their Fig. 4 et al., 2006; Curtis and Connolly, 2008), cades toward the memorized location (http://www.jneurosci.org/cgi/content/ the fine temporal and spectral dynamics (prosaccade condition) and away from it full/28/34/8397/F4)]. Compared with of its underlying electrophysiology and (antisaccade condition) have the same the widespread spatial distribution of their relationship to findings reported in stimulus component but an opposite goal the transient stimulus-related activity, animal studies still remain poorly under- component. The participants were asked the cortical sources showing goal-re- stood. The delayed saccade paradigm ex- to memorize the position of a stimulus lated modulations were found more fo- plored by Van Der Werf et al. (2008) using that was flashed peripherally for 0.1 s cally in PPC [Van Der Werf et al. (2008), the high temporal precision of magne- while they maintained central fixation. their Fig. 5A,B (http://www.jneurosci. toencephalography (MEG) reveals un- After a delay of 1.5 s, the fixation cross org/cgi/content/full/28/34/8397/F5)]. precedented evidence in humans that disappeared, instructing the subjects to Finally, the dissociation between the gamma-band activity recorded in poste- perform a prosaccade or an antisaccade two components was not found for fre- rior parietal cortex (PPC) during the delay depending on the experimental condi- quencies Ͻ30 Hz, suggesting that it is period is associated with the encoding of tion. By contrasting the topographies of indeed specific to the gamma range forthcoming saccades. MEG signal power for left versus right [Van Der Werf et al. (2008), their Fig. 7 The main finding in the article is prosaccades across frequencies, the au- (http://www.jneurosci.org/cgi/content/ the emergence of sustained direction- thors found significant sustained parietal full/28/34/8397/F7)]. selective high-frequency gamma activity gamma activity contralateral to target One possible confound in the attempt over posterior parietal regions during location [Van Der Werf et al. (2008), to separate stimulus and motor compo- planning of saccades. Using a delayed sac- their Fig. 2 (http://www.jneurosci.org/ nents in delayed saccade paradigms with a cade paradigm, the authors set out to sep- cgi/content/full/28/34/8397/F2)]. Next, short response delay period is the coacti- by comparing these results to the out- vation of neural networks involved in vi- come of the same analysis obtained in sual persistence (i.e., afterimages). This Received Oct. 10, 2008; revised Nov. 4, 2008; accepted Nov. 5, 2008. the antisaccade condition [Van Der phenomenon produces an optical illusion This work was supported by European Community Research Program Werf et al. (2008), their Fig. 3 (http:// in which an image remains perceived after NeuroProbes(FP6-IST027017)toK.J.,theECMarieCurieFellowship(FP7– 221097) to S.S.D., the Comisio´n Nacional de Investigacio´n Cientı´fica y Tec- www.jneurosci.org/cgi/content/full/28/ the true visual stimulus has ended. Al- nolo´gica (Chile) Doctoral Fellowship to C.M.H., and a doctoral fellowship 34/8397/F3)], two temporally distinct though most theories explain afterimages fromtheMiniste`redel’EducationNationaleetlaRecherche(France)toT.O. gamma components were distinguish- through the adaptation of different retinal Correspondence should be addressed to Dr. Karim Jerbi, INSERM U821, able. An early broadband (40–120 Hz) cell populations to the properties of the Dynamique Ce´re´brale et Cognition, 69500 Lyon, France. E-mail: [email protected]. component was modulated by stimulus inducing stimulus [e.g., chromatic char- DOI:10.1523/JNEUROSCI.4896-08.2008 location but not by the spatial target of acteristics, luminance, or contrast as in Copyright©2008SocietyforNeuroscience 0270-6474/08/2813713-03$15.00/0 the motor goal. In contrast, ϳ500 ms the study by Wede and Francis (2006)], 13714 • J. Neurosci., December 17, 2008 • 28(51):13713–13715 Jerbi et al. • Journal Club they also recognize an important role of both mediate the selection of a portion of rect manifestations of miniature saccade cortical structures. Afterimage-related ac- the visual scene. Nevertheless, several transients. Therefore, given that micro- tivity has been observed as occipital and studies have also provided evidence in fa- saccades have been shown to be modu- temporal scalp event-related potentials vor of a putative segregation between goal lated by shifts of spatial attention (Engbert (Kobayashi et al., 2002) as well as gamma representation and spatial attention and Kliegl, 2003), it is important to rule oscillations over occipital and parietal across parietal and frontal areas (Colby out that the gamma-band activity de- sensors using MEG (Tikhonov et al., and Goldberg, 1999; Juan et al., 2004; tected by Van Der Werf et al. (2008) is of 2007). So can the persistent parietal Quian Quiroga et al., 2006). Clearly, the artifactual origin. Such an explanation is gamma activity identified by the authors attempt to fully dissociate the neural cor- unlikely for several reasons: First, it is un- after the offset of the peripheral stimulus relates of the two processes carries the in- clear if the miniature saccade artifact phe- be interpreted as a neural correlate of vi- herent risk of misrepresenting the intri- nomenon extends to MEG. In EEG re- sual persistence of the stimulus? The in- cate interaction between them. However, cordings, such an artifact may be a version of hemispheric bias that was recent findings, including the present consequence of reference electrode place- found for the late-gamma component study by Van Der Werf et al. (2008), sug- ment (Yuval-Greenberg et al., 2008); in (Ͼ500 ms) between prosaccade and anti- gest that the fine-scale spatial and tempo- contrast, MEG may not be susceptible to saccades [Van Der Werf et al. (2008), their ral resolution of gamma-band activity this problem because it is inherently Fig. 2 (http://www.jneurosci.org/cgi/ might be particularly helpful in linking reference-free. Additionally, the beam- content/full/28/34/8397/F2) and Fig. 3 the findings of animal and human studies forming source reconstruction method (http://www.jneurosci.org/cgi/content/full/ exploring the overlap and segregation be- provides a degree of protection from arti- 28/34/8397/F3)] argues against this. Fur- tween attention and intention (Pesaran et facts arising from outside the brain. thermore, results of a previous MEG study al., 2002; Brovelli et al., 2005). Beamforming estimates either the time by the same group with a delayed double- Many variants of the delayed saccade course or power modulations of neural step saccade task only show high parietal task have been reported in the literature. activity over the brain volume using adap- gamma enhancement preceding the saccade As described above, the paradigm imple- tive spatial filters (Van Veen et al., 1997). “go” signal but not after the first cue mented by Van Der Werf et al. (2008) re- This method does not require a priori as- (Medendorp et al., 2007). An explanation of quires visuospatial processing and mem- sumptions about the location or number the sustained gamma solely on the account orization of a flashed stimulus position of sources and so does not assume sources of afterimages can therefore be ruled out. (or its mirror location) in addition to mo- are restricted to the brain. Sources of ocu- Another critical factor that might re- tor planning. One way to probe the neural lar origin would therefore be localized quire additional investigation is the puta- processes underlying oculomotor inten- near the eyes rather than projected to dis- tive link between the reported gamma action while minimizing the effect of target tant parts of the brain (Bardouille et al., tivity and visuospatial attention orienting. location is to place the visual stimulus in- 2006). A third argument in favor of a cor- Clearly, subjects planning a saccade at- structing saccade direction at the center of tical origin of the reported gamma activity tend to the target location during the de- the screen, e.g., as an arrow pointing left findings is that they are in agreement with lay. In the case of a prosaccade, this is the or right toward targets that remain visible results from direct recordings in monkeys same location as the stimulus, but for an throughout the experiment (Khonsari et at several levels. For instance, the reported antisaccade, subjects likely shift and al., 2007; Milea et al., 2007). Such delayed hemisphere-specific contralateral selec- maintain their attention to the opposite saccade paradigms significantly reduce tivity of spectral power for an upcoming side of the screen. The authors note that lateralized perceptual and visuospatial saccade is in line with findings obtained this explanation is unlikely given the ten- memory demands because the instruction with gamma-range components of local dency of the sustained gamma activity to is provided centrally, and the peripheral field potentials recorded in monkey PPC increase closer toward saccade execution. targets are not flashed but remain present (Pesaran et al., 2002). Furthermore, the It is conceivable, however, that purely at- (cf. Curtis and Connolly, 2008). This timing of gamma power modulation shift tentional neural processes might also be places the emphasis during the delay on from stimulus processing to goal encod- enhanced closer toward the onset of a the motor goal and visuomotor transfor- ing appears to coincide with the average planned movement and thereby account mation rather than the visual stimulus lo- inversion time of lateral intraparietal neu- at least partially for the observed increase. cation. Whether such a paradigm reveals rons remapping from stimulus location to This question is worth pursuing in future gamma patterns comparable with those goal encoding as reported in a memory- studies using a modified delayed saccade reported by Van Der Werf et al. (2008) delayed saccade task in monkeys (Zhang paradigm that explicitly controls for spa- still remains to be shown. and Barash, 2004). Finally, the signifi- tial attention. Most importantly, the en- A further important issue which could cance of the parietal high-gamma findings deavor to elucidate whether high-gamma impact the interpretation of the findings is further enhanced by a growing body of activity in human PPC is specifically re- reported by Van Der Werf et al. (2008) is evidence linking population-level gamma lated to intention or to attention is part of the fact that scalp muscle activity and elec- activity to the blood oxygenation level- a longstanding debate on the separability tromagnetic interference can contami- dependent signal recorded in fMRI, both of neural representations of motor goals nate MEG and EEG data yielding artifac- in monkeys (Logothetis et al., 2001) and and spatial attention (preceding move- tual activity in the high-gamma frequency in humans (Lachaux et al., 2007). ment execution). Indeed, saccade plan- range. Indeed, a recent study may intro- The authors propose that parietal ning and the allocation of spatial attention duce some additional concerns; Yuval- gamma-band activity reflects visuomotor have been shown to be mediated by over- Greenberg et al. (2008) showed that with a encoding mechanisms that determine the lapping neural substrates (Kowler et al., visual EEG experiment, broadband saccade goal. Given that the neural net- 1995). This is an intuitively appealing idea gamma activity may appear to arise from work involved in oculomotor planning given that visual attention and saccades occipital regions when in fact they are di- and execution spreads across multiple ce- Jerbi et al. • Journal Club J. 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