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Role of Posterior Parietal Gamma Activity in Planning Prosaccades and Antisaccades

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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. Role of Posterior Parietal Gamma Activity in Planning Prosaccades and Antisaccades 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 ac- tion 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.
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