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Where Is the Anterior Temporal Lobe and What Does It Do?

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Where Is the Anterior Temporal Lobe and What Does It Do? The Journal of Neuroscience, March 6, 2013 • 33(10):4213–4215 • 4213 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/site/misc/ifa_features.xhtml. Where Is the Anterior Temporal Lobe and What Does It Do? Michael F. Bonner1 and Amy R. Price1,2 1Department of Neurology and 2Neuroscience Graduate Group, University of Pennsylvania, Philadelphia, Pennsylvania 19104 Review of Peelen and Caramazza The anterior temporal lobe (ATL) is these findings have implicated a large re- represented (Simmons and Barsalou, thought to be critical for semantic memory– gion of the ATL in semantic memory. 2003). This work has implications for our our knowledge of objects, people, words, One might expect that complementary understanding of how ATL structures dif- and facts. However, there is substantial functional neuroimaging studies would ferentially contribute to semantic memory, disagreement over the precise role of the provide a more fine-grained picture of and how the semantic system is shaped ATL in semantic memory, and there is ATL function. Unfortunately, the evi- by the modalities of the information it considerable variability in the anatomic dence from functional neuroimaging has processes. findings that link the ATL with semantic not clearly pointed to the ATL as a critical In their study, subjects viewed images processing. The inconsistent findings across region for conceptual knowledge. Indeed, of objects. Half were objects that are typi- studies may be related to the diverse ana- fMRI examinations of semantic memory cally found in a kitchen (e.g., pepper mill), tomic structures within the ATL and their have implicated a broad cortical network and half in a garage (e.g., staple gun). Half differential contribution to distinct modali- in conceptual processing, with sensory were objects that are typically acted upon ties of semantic information (e.g., visual, au- and motor regions contributing to repre- by rotating (e.g., pepper mill), and half ditory, affective). sentations of the perceptual and action by squeezing (e.g., staple gun). Subjects Much of the evidence implicating the features of concepts (Martin, 2007), and performed a one-back task, indicating ATL in semantic memory has come from inferior parietal and posterolateral tem- whether they saw two objects in a row that neuropsychology. In particular, patients poral regions supporting multimodal shared a particular conceptual feature with semantic dementia, a neurodegen- conceptual information (Binder and De- (shared location for half of the trials, erative disease affecting the ATL, exhibit a sai, 2011). Inconsistent ATL activation shared action for the other half). The au- profound deficit in semantic knowledge can partly be explained by imaging arti- thors reasoned that if a cortical region with a relative sparing of most other cog- facts near the sinuses in fMRI, which may encodes abstract conceptual features, it nitive domains (Warrington, 1975; Pat- degrade signal detection in the ATL. should have a similar neural response to terson et al., 2007). These patients have Nonetheless, the variability of the evi- objects with a shared conceptual feature, little trouble performing episodic recall dence to date has left many unanswered even if those objects are different in all tasks, visual perceptual tasks, or numeri- questions about the functions of ATL other respects. They tested this hypothesis cal tasks, and can even retain complex be- structures. using multivoxel pattern analysis to look haviors like performing novel musical pieces—yet they have a striking impair- In a recent report in the Journal of Neu- for regions where objects with a shared ment on nearly all assessments of seman- roscience, Peelen and Caramazza (2012) conceptual feature had highly similar pat- tic knowledge. Given the broad anatomic provide fMRI evidence that a region of terns of fMRI responses. This was per- extent of disease in semantic dementia, the ventral temporal pole encodes infor- formed in regions of interest along the mation about the abstract conceptual ventral temporal lobe, and in whole-brain properties of objects. Their findings searchlight analyses. complement neuropsychological studies These analyses revealed a graded effect Received Jan. 4, 2013; revised Jan. 16, 2013; accepted Jan. 21, 2013. of the ATL and fit within a broad theoret- along the posterior–anterior axis of the This work was supported by National Institutes of Health Grant AG017586. We thank Murray Grossman and Jonathan Peelle for helpful ical framework of perception and mem- ventral temporal lobe, with the highest comments on this manuscript. ory, in which the ventral visual stream degree of similarity in bilateral ventral CorrespondenceshouldbeaddressedtoMichaelF.Bonner,Department processes a hierarchy of increasingly com- temporal pole (this anatomic region is of Neurology—2 Gibson, University of Pennsylvania, 3400 Spruce Street, plex information, culminating in anterior illustrated in Fig. 1). A similar effect was Philadelphia, PA 19104. E-mail: [email protected]. DOI:10.1523/JNEUROSCI.0041-13.2013 regions of the temporal lobe where ab- observed for both the location and action Copyright©2013theauthors 0270-6474/13/304213-03$15.00/0 stract conceptual properties of objects are features of concepts. These effects were 4214 • J. Neurosci., March 6, 2013 • 33(10):4213–4215 Bonner and Price • Journal Club concepts, sound concepts) through all their experiment, their results may nonethe- modes of reception and expression (e.g., less be consistent with this account. Their language, photos, sounds). However, the task assessed knowledge of how individual ATL is a large, heterogeneous region con- objects are used and where they are located. taining numerous cytoarchitectonically This task may have relied on highly specific distinct cortical areas (Brodmann, 1909; semantic information in the most anterior superior temporal gyrus middle temporal gyrus Blaizot et al., 2010) with a structured pat- regions of the temporal lobe, whereas a less inferior temporal gyrus tern of differential anatomic connectivity specific semantic task, like lexical decision, temporal pole rhinal cortex (Kondo et al., 2003). It is unlikely that might rely more on the fusiform or parahip- fusiform gyrus these anatomically distinct regions are pocampal gyri. parahippocampal gyrus functionally equivalent. Furthermore, the Finally, it is important to consider the visualcomplex non-visual basic spatial resolution of functional neuroimag- modality of the semantic content that was Figure 1. Structures of the anterior temporal lobe. The ing techniques is more than adequate for probed in Peelen and Caramazza’s (2012) axes indicate theoretical gradients of differential semantic identifying the differential contribution of study. Their experiment examined the processes. Along one axis, ventral structures contribute more these regions to semantic processing. conceptual processing of objects, a cate- totheprocessingofvisualinformation(e.g.,objectconcepts), One plausible account for the ana- gory of concepts with strongly associated and dorsolateral structures contribute more to the processing tomic variability in previous studies is visual features. They reasoned that their of non-visual information (e.g., abstract concepts, auditory that there is some degree of modality- ATL findings reflect an extension of the concepts).Alongthesecondaxis,posteriorstructurescontrib- ute more to basic object representations, and anterior struc- specificity in the functions of the ATL (Yi processing hierarchy in the ventral visual tures contribute more to the representation of complex et al., 2007), and more broadly through- stream. However, this interpretation dif- conceptual associations. out the temporal lobe (Bonner and Gross- fers from the hypothesis that the ATL is an man, 2012). In other words, semantic amodal semantic hub (Patterson et al., processing in the ATL may not be fully 2007). From the amodal perspective, it is present regardless of whether the task amodal. Indeed, the results of a recent proposed that the ATL represents all cat- probed location or action knowledge, meta-analysis are consistent with this per- egories of concepts, including those with suggesting that the responses were not spective, demonstrating that visual object weak visual feature associations, such as purely task-driven. By comparison, visual processing often recruits ventral ATL abstract concepts like “truth” and audi- similarity across the stimuli was encoded structures, while linguistic and auditory tory concepts like “thunder.” Yet, criti- in early visual processing regions of processing tend to recruit lateral ATL cally, most studies of ATL function have temporal-occipital cortex. Altogether, structures (Visser et al., 2010). This meta- focused on the representation of object these findings illustrate a model of hierar- analysis focused on the modality of the concepts, which depend heavily on visual chical processing along the ventral visual stimulus materials (e.g., pictures vs feature knowledge. As with Peelen and stream, with lower-level visual-perceptual words), and did not directly address ques- Caramazza’s (2012) study, these investi- features processed
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