8630 • The Journal of Neuroscience, July 8, 2009 • 29(27):8630–8632

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.

The Temporoparietal Junction as a Part of the “When” Pathway

Lucas Spierer,1 Fosco Bernasconi,1,2 and Jeremy Grivel2 1Neuropsychology and Neurorehabilitation Service and 2Community Psychiatry Service, Vaudois University Hospital Center and University of Lausanne, 1010 Lausanne, Switzerland Review of Davis et al. (http://www.jneurosci.org/cgi/content/full/29/10/3182)

Accurate perception of the timing of sen- (Battelli et al., 2007). Some of these incon- A possible confound of experiment 1 sory events is crucial in normal function- sistencies stem from divergent theories (that was acknowledged by the authors) ing and plays a key role in numerous concerning hemispheric specialization in was that resolving the temporal order re- higher-order cognitive functions, ranging attention and the resultant influence of quired subjects to process differences in from speech comprehension to motor co- any such lateralization on temporal order the onset of the items, whereas such tem- ordination. Accordingly, poor temporal judgments (e.g., Spence et al., 2001). Sec- poral selectivity was not necessary in the processing has been implicated in several ond, Davis et al. (2009) provide new in- shape discrimination task. In addition, psychiatric and neurologic conditions, in- sight into the existence of a “when” pro- the shape discrimination task called for cluding dyslexia, schizophrenia, autism, cessing stream and shed light on its longer visual search than the temporal or- and attention deficit disorder (Buhusi and multisensory nature. der judgment task. These differences in Meck, 2005). Although the encoding of Using functional magnetic resonance the temporal window during which atten- temporal information on the subsecond imaging, Davis et al. (2009) identified tion was required in the two tasks, as well time scale has been extensively studied brain regions involved in judging the tem- as differences in the duration of visual over the last several decades using tempo- poral order of rapidly presented, spatially search in which the participants engaged, ral order judgment paradigms, its neural separated visual stimuli. In experiment 1, were controlled in a second experiment. basis remains largely unresolved, because subjects were presented with sequences of In experiment 2, attention to stimulus on- the vast majority of this research involved two rectangles (one red, one green), the set was necessary in both the temporal or- psychophysical and/or electrophysiologi- onset, size, and location of which were der and shape condition. The design was cal methods with poor spatial resolution randomized across trials. Before each similar to that in experiment 1, except that (Lewandowska et al., 2008). A recent trial, the task subjects had to perform was the shape of the rectangles was kept con- study by Davis et al. (2009) constitutes a cued by the color of a centrally presented stant and that a gray line of variable width major advance toward understanding fixation point. In the shape task, partici- was initially superimposed on experiment how the brain encodes temporal informa- pants were instructed to report whether 1 items. The shape task of experiment 2 tion. First, it helps to resolve conflicting the red or the green rectangle was more was based on these gray lines, thereby results of previous literature regarding the square. In the temporal order judgment compelling participants to attend to the relative roles of the left and right hemi- condition, they reported which of the two onset of the items, as in the temporal or- spheres in the processing of event order items appeared first. This paradigm al- der judgment condition. This control ex- lowed the researchers to compare the periment is of particular importance in a Received May 5, 2009; revised May 26, 2009; accepted May 27, 2009. brain’s responses to physically identical temporal order judgment paradigm, as This work was supported by an Interdisciplinary grant from the Faculty stimulation; the experimental condition the perception of succession has been of Biology and Medicine, University of Lausanne, and by a grant from the Pierre Mercier Foundation for Science. We thank Dr. Micah Murray for his being defined by the feature (shape or shown to be strongly influenced by atten- encouragement and support. timing) on which subjects were instructed tional factors (Eagleman, 2008). It is note- Correspondence should be addressed to Dr. Lucas Spierer, Neuropsy- to focus their attention. The results of the worthy that the relative luminance of the chology and Neurorehabilitation Service, University of Lausanne and Vau- statistical contrast between the two condi- red, green, and gray colors used by Davis dois University Hospital Center, av. Pierre-Decker 5, 1011 Lausanne, Swit- zerland. E-mail: [email protected]. tions revealed differences only between et al. (2009) were individually adjusted to DOI:10.1523/JNEUROSCI.2111-09.2009 the tasks in which subject were engaged, ensure that the items’ salience did not bias Copyright©2009SocietyforNeuroscience 0270-6474/09/298630-03$15.00/0 not differences between the stimuli. responses. Moreover, the difficulty of the Spierer et al. • Journal Club J. Neurosci., July 8, 2009 • 29(27):8630–8632 • 8631 shape and temporal order judgment tasks poral features is not intrinsic to “what” by presenting stimuli at a single location was matched in a pilot study to avoid pos- processing, but rather relies on a partially and/or along the midline; both of which sible confounds induced by differences in independent module comprised within would minimize a potential interaction attentional load across experimental the temporoparietal junction. between the location of the stimuli and conditions. More importantly, the results of exper- any hemispheric specialization for the Behaviorally, the results of experi- iment 2 revealed the selective involvement processing of the attended feature or for ments 1 and 2 indicate that the difficulty of the left temporoparietal junction in spatial attention in general. levels of both temporal order judgment temporal order judgment. This result not As mentioned above, the results of and shape discrimination tasks were com- only extends, but also runs counter to pre- Davis et al. (2009) are relevant with regard parable (ϳ85%), indicating that differ- vious transcranial magnetic stimulation to current models of the anatomofunc- ences in brain activity related to the two (TMS) and neuropsychological findings tional organization of the visual system. experimental conditions were unlikely at- attributing a crucial role to right inferior Given the evidence suggesting the organi- tributable to differences in task difficulty. parietal cortex and/or inferior parietal zation of sensory processing in dual what/ Brain activation in experiment 1 in- lobule in the perception of events’ order where streams constitutes a general prin- cluded stronger bilateral activity in the (Battelli et al., 2008). The new insight pro- ciple across sensory systems that might temporoparietal junction, right fronto- vided by Davis et al. (2009) into the issue encompass multisensory aspects [see, e.g., temporal cortices, and frontal eye fields in of hemispheric dominance in fast tempo- De Santis et al. (2007) for discussion], it the temporal order judgment task than in ral processing was enabled by the joint use could be hypothesized that “when” pro- the shape task [Davis et al. (2009), their of a correlational neuroimaging method cessing follows the same architecture. Fig. 2]. However, as mentioned above, the and their experimental design, which While the temporal order judgment task possibility that this statistical contrast re- avoided two confounds. First, contrary to by Davis et al. (2009) has been conducted flects differences in the length of visual previous TMS or neuropsychological in the visual modality, the striking result search required in the two tasks (i.e., sub- studies that tested for the role of a prede- of a specific role they found for the left jects had to pay attention to the stimulus termined brain area of interest in tempo- temporoparietal junction in temporal or- onset in the temporal order judgment but ral order judgment (i.e., right temporopa- der judgment provides insight into the not shape task) cannot be excluded. In ex- rietal regions); Davis et al. (2009) screened multisensory nature of the “when” path- periment 2, in which this potential con- for temporal order judgment-related ac- way. Damage in the left temporoparietal found was controlled for by matching the tivity throughout the whole brain, in a junction causes Wernicke’s aphasia, a syn- temporal window over which the task- purely data-driven approach, allowing drome characterized by language com- relevant information could be extracted in them to reveal unexpected activation pat- prehension deficits, which in turn have the two tasks (i.e., the onset of the stim- terns. Second, because the regions of in- been explained by impaired integration uli), a similar activation pattern to that in terest selected in the lesion or TMS studies of the order within and/or between pho- experiment 1 was observed except that the are also involved in spatial attention and nemes or more generally in auditory tem- temporoparietal junction activity was re- visual search duration (Shulman et al., poral order judgment (von Steinbu¨chel et stricted to the left hemisphere [Davis et al. 2007), right temporoparietal junction in- al., 1999). Impaired responsiveness along (2009), their Fig. 3]. terference possibly impacted temporal or- the posterior superior temporal cortex By providing direct evidence for the der judgment by perturbing top-down and temporoparietal junction has also brain regions involved in processing the spatial attentional processes, resulting in been linked to deficient integration of let- order of spatially separated visual events, misinterpretation of the role of right ters and speech sounds in dyslexic indi- the study by Davis et al. (2009) is a major hemispheric structures in temporal order viduals (Blau et al., 2009), who often also step toward understanding the functional judgment [see also Wittmann et al. (2004) exhibit impaired temporal processing organization underlying temporal pro- for discussion]. The control for atten- (Tallal, 2004). Together, lesion data on cessing. Hence, their results contribute to tional factors used in Davis et al. (2009) is temporal order judgment and the study a better understanding of how the brain particularly important because previous by Davis et al. (2009) therefore suggest integrates the timing of sensory events, an data revealed that attentional variables that the left temporoparietal junction may issue receiving growing interest, as it be- can induce striking distortion in temporal comprise a multisensory (or at least audi- comes more evident that the temporal di- order judgment (Eagleman, 2008). This tory and visual) temporal order process- mension is important in sensory and mo- hypothesis is supported by the finding ing unit within an extended “when” path- tor processing (Battelli et al., 2007). that right temporoparietal junction activ- way. Although further investigations are In contrast to the classical conception ity was not observed in experiment 2 of needed to confirm that the left tem- that the anatomofunctional organization Davis et al. (2009), in which the atten- poroparietal junction indeed encodes of the visual system consists of two main tional window required to resolve the temporal order in a multisensory manner, processing streams subserving the pro- tasks was balanced across the temporal or- the work by Davis et al. (2009) supports cessing of semantic (what) and spatial/ der judgment and shape discrimination this hypothesis. action-oriented (where) information, tasks. Davis et al. (2009) correctly argue Davis et al. (2009) provide strong support that the effects of attention could be dis- References for the emerging view that the encoding of cerned in TMS-induced and real lesion Battelli L, Walsh V, Pascual-Leone A, Cavanagh P time relies on a third, partially segregated, studies as such induces biases but not de- (2008) The ‘when’ parietal pathway explored “when” network. By contrasting brain creases in temporal order judgment per- by lesion studies. Curr Opin Neurobiol activity associated with a “what” (shape formance. Additional ways for controlling 18:120–126. Battelli L, Pascual-Leone A, Cavanagh P (2007) discrimination) and a “when” (temporal the influence of spatial attention include The ‘when’ pathway of the right parietal lobe. order judgment) task, the authors dem- avoiding the use of spatially varying stim- Trends Cogn Sci 11:204–210. onstrated that the processing of the tem- uli for the temporal order judgment task Blau V, van Atteveldt N, Ekkebus M, Goebel R, 8632 • J. Neurosci., July 8, 2009 • 29(27):8630–8632 Spierer et al. • Journal Club

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