scholarly journals Diverse temporal dynamics of repetition suppression revealed by intracranial recordings in human ventral temporal cortex

2019 ◽  
Author(s):  
Vinitha Rangarajan ◽  
Corentin Jacques ◽  
Robert T. Knight ◽  
Kevin S. Weiner ◽  
Kalanit Grill-Spector

AbstractRepeated stimulus presentations commonly produce decreased neural responses - a phenomenon known as repetition suppression (RS) or adaptation – in ventral temporal cortex (VTC) in humans and nonhuman primates. However, the temporal features of RS in human VTC are not well understood. To fill this gap in knowledge, we utilized the precise spatial localization and high temporal resolution of electrocorticography (ECoG) from 9 human subjects implanted with intracranial electrodes in VTC. Subjects viewed non-repeated and repeated images of faces with long-lagged intervals and many intervening stimuli between repeats. We report three main findings: (i) robust RS occurs in VTC for activity in high-frequency broadband (HFB), but not lower frequency bands, (ii) RS of the HFB signal is associated with lower peak magnitude, lower total responses, and earlier peak responses, and (iii) RS effects occur early within initial stages of stimulus processing and persist for the entire stimulus duration. We discuss these findings in the context of early and late components of visual perception, as well as theoretical models of repetition suppression.

2020 ◽  
Vol 30 (11) ◽  
pp. 5988-6003 ◽  
Author(s):  
Vinitha Rangarajan ◽  
Corentin Jacques ◽  
Robert T Knight ◽  
Kevin S Weiner ◽  
Kalanit Grill-Spector

Abstract Repeated stimulus presentations commonly produce decreased neural responses—a phenomenon known as repetition suppression (RS) or adaptation—in ventral temporal cortex (VTC) of humans and nonhuman primates. However, the temporal features of RS in human VTC are not well understood. To fill this gap in knowledge, we utilized the precise spatial localization and high temporal resolution of electrocorticography (ECoG) from nine human subjects implanted with intracranial electrodes in the VTC. The subjects viewed nonrepeated and repeated images of faces with long-lagged intervals and many intervening stimuli between repeats. We report three main findings: 1) robust RS occurs in VTC for activity in high-frequency broadband (HFB), but not lower-frequency bands; 2) RS of the HFB signal is associated with lower peak magnitude (PM), lower total responses, and earlier peak responses; and 3) RS effects occur early within initial stages of stimulus processing and persist for the entire stimulus duration. We discuss these findings in the context of early and late components of visual perception, as well as theoretical models of repetition suppression.


2018 ◽  
Author(s):  
Mona Rosenke ◽  
Nicolas Davidenko ◽  
Kalanit Grill-Spector ◽  
Kevin S. Weiner

ABSTRACTWe have an amazing ability to categorize objects in the world around us. Nevertheless, how cortical regions in human ventral temporal cortex (VTC), which is critical for categorization, support this behavioral ability, is largely unknown. Here, we examined the relationship between neural responses and behavioral performance during the categorization of morphed silhouettes of faces and hands, which are animate categories processed in cortically adjacent regions in VTC. Our results reveal that the combination of neural responses from VTC face- and body-selective regions more accurately explains behavioral categorization than neural responses from either region alone. Furthermore, we built a model that predicts a person’s behavioral performance using estimated parameters of brain-behavioral relationships from a different group of people. We further show that this brain-behavioral model generalizes to adjacent face- and body-selective regions in lateral occipito-temporal cortex. Thus, while face- and body-selective regions are located within functionally-distinct domain-specific networks, cortically adjacent regions from both networks likely integrate neural responses to resolve competing and perceptually ambiguous information from both categories.


2020 ◽  
Vol 30 (9) ◽  
pp. 4882-4898
Author(s):  
Mona Rosenke ◽  
Nicolas Davidenko ◽  
Kalanit Grill-Spector ◽  
Kevin S Weiner

Abstract We have an amazing ability to categorize objects in the world around us. Nevertheless, how cortical regions in human ventral temporal cortex (VTC), which is critical for categorization, support this behavioral ability, is largely unknown. Here, we examined the relationship between neural responses and behavioral performance during the categorization of morphed silhouettes of faces and hands, which are animate categories processed in cortically adjacent regions in VTC. Our results reveal that the combination of neural responses from VTC face- and body-selective regions more accurately explains behavioral categorization than neural responses from either region alone. Furthermore, we built a model that predicts a person’s behavioral performance using estimated parameters of brain–behavior relationships from a different group of people. Moreover, we show that this brain–behavior model generalizes to adjacent face- and body-selective regions in lateral occipitotemporal cortex. Thus, while face- and body-selective regions are located within functionally distinct domain-specific networks, cortically adjacent regions from both networks likely integrate neural responses to resolve competing and perceptually ambiguous information from both categories.


2009 ◽  
Vol 101 (5) ◽  
pp. 2581-2600 ◽  
Author(s):  
Mark A. Pinsk ◽  
Michael Arcaro ◽  
Kevin S. Weiner ◽  
Jan F. Kalkus ◽  
Souheil J. Inati ◽  
...  

Single-cell studies in the macaque have reported selective neural responses evoked by visual presentations of faces and bodies. Consistent with these findings, functional magnetic resonance imaging studies in humans and monkeys indicate that regions in temporal cortex respond preferentially to faces and bodies. However, it is not clear how these areas correspond across the two species. Here, we directly compared category-selective areas in macaques and humans using virtually identical techniques. In the macaque, several face- and body part–selective areas were found located along the superior temporal sulcus (STS) and middle temporal gyrus (MTG). In the human, similar to previous studies, face-selective areas were found in ventral occipital and temporal cortex and an additional face-selective area was found in the anterior temporal cortex. Face-selective areas were also found in lateral temporal cortex, including the previously reported posterior STS area. Body part–selective areas were identified in the human fusiform gyrus and lateral occipitotemporal cortex. In a first experiment, both monkey and human subjects were presented with pictures of faces, body parts, foods, scenes, and man-made objects, to examine the response profiles of each category-selective area to the five stimulus types. In a second experiment, face processing was examined by presenting upright and inverted faces. By comparing the responses and spatial relationships of the areas, we propose potential correspondences across species. Adjacent and overlapping areas in the macaque anterior STS/MTG responded strongly to both faces and body parts, similar to areas in the human fusiform gyrus and posterior STS. Furthermore, face-selective areas on the ventral bank of the STS/MTG discriminated both upright and inverted faces from objects, similar to areas in the human ventral temporal cortex. Overall, our findings demonstrate commonalities and differences in the wide-scale brain organization between the two species and provide an initial step toward establishing functionally homologous category-selective areas.


2021 ◽  
Vol 21 (9) ◽  
pp. 2881
Author(s):  
Brett Bankson ◽  
Michael Ward ◽  
Edward Silson ◽  
Chris Baker ◽  
R. Mark Richardson ◽  
...  

2018 ◽  
Vol 115 (18) ◽  
pp. 4785-4790 ◽  
Author(s):  
Amy L. Daitch ◽  
Josef Parvizi

Neuroimaging evidence supports a role of the default mode network (DMN) in spontaneous thought and goal-driven internally oriented processes, such as recalling an autobiographical event, and has demonstrated its deactivation during focused, externally oriented attention. Recent work suggests that the DMN is not a homogeneous network but rather is composed of at least several subnetworks, which are engaged in distinct functions; however, it is still unclear if these different functions rely on the same neuronal populations. In this study, we used intracranial EEG to record from the posteromedial cortex (PMC), a core hub of the DMN, in 13 human subjects, during autobiographical memory retrieval (internally oriented), arithmetic processing (externally oriented), and cued rest (spontaneous thought), allowing us to measure activity from anatomically precise PMC sites with high temporal resolution. We observed a heterogeneous, yet spatially organized, pattern of activity across tasks. Many sites, primarily in the more ventral portion of PMC, were engaged during autobiographical recall and suppressed during arithmetic processing. Other more dorsal PMC sites were engaged during the cued-rest condition. Of these rest-active sites, some exhibited variable temporal dynamics across trials, possibly reflecting various forms of spontaneous thought, while others showed only transient activity at the beginning of cued-rest trials (i.e., after a switch from a task to cued rest), possibly involved in shifting the brain from a more focused to a more exploratory attentional state. These results suggest heterogeneity of function even within an individual node of the DMN.


2018 ◽  
Author(s):  
Simon Khuvis ◽  
Erin M. Yeagle ◽  
Yitzhak Norman ◽  
Shany Grossman ◽  
Rafael Malach ◽  
...  

AbstractProperties of face-responsive individual neurons in the human ventral temporal cortex (VTC) have yet to be studied, and their role in conscious perception remains unknown. To explore this, we implanted microelectrodes into the VTCs of eight human subjects undergoing invasive epilepsy monitoring. Most (26 of 33) category-selective units showed specificity for face stimuli, with a range of response profiles. Different face exemplars evoked consistent and discriminable responses in the population of units sampled. During a free recall task, face-selective units selectively reactivated in the absence of visual stimulation during the 2-second window prior to face recall events. Furthermore, the identity of the recalled face could be predicted by comparing activity preceding recall events to activity evoked by visual stimulation.


2020 ◽  
Author(s):  
Matthew J. Boring ◽  
Edward H. Silson ◽  
Michael J. Ward ◽  
R. Mark Richardson ◽  
Julie A. Fiez ◽  
...  

AbstractThe map of category-selectivity in human ventral temporal cortex (VTC) provides organizational constraints to models of object recognition. One important principle is lateral-medial response biases to stimuli that are typically viewed in the center or periphery of the visual field. However, little is known about the relative temporal dynamics and location of regions that respond preferentially to stimulus classes that are centrally viewed, like the face and word processing networks. Here, word- and face-selective regions within VTC were mapped using intracranial recordings from 36 patients. Partially overlapping, but also anatomically dissociable patches of face and word selectivity were found in ventral temporal cortex. In addition to canonical word-selective regions along the left posterior occipitotemporal sulcus, selectivity was also located medial and anterior to face-selective regions on the fusiform gyrus at the group level and within individual subjects. These regions were replicated using 7-Tesla fMRI in healthy subjects. Left hemisphere word-selective regions preceded right hemisphere responses by 125 ms, potentially reflecting the left hemisphere bias for language; with no hemispheric difference in face-selective response latency. Word-selective regions along the posterior fusiform responded first, then spread medially and laterally, then anteriorally. Face-selective responses were first seen in posterior fusiform regions bilaterally, then proceeded anteriorally from there. For both words and faces, the relative delay between regions was longer than would be predicted by purely feedforward models of visual processing. The distinct time-courses of responses across these regions, and between hemispheres, suggest a complex and dynamic functional circuit supports face and word perception.Significance StatementRepresentations of visual objects in the human brain have been shown to be organized by several principles, including whether those objects tend to be viewed centrally or in the periphery of the visual field. However, it remains unclear how regions that process objects that are viewed centrally, like words and faces, are organized relative to one another. Here, direct neural recordings and 7T fMRI demonstrate that several intermingled regions in ventral temporal cortex participate in word and face processing. These regions display differences in their temporal dynamics and response characteristics, both within and between brain hemispheres, suggesting they play different roles in perception. These results illuminate extended, bilateral, and dynamic brain pathways that support face perception and reading.


2010 ◽  
Vol 103 (6) ◽  
pp. 3349-3365 ◽  
Author(s):  
Kevin S. Weiner ◽  
Rory Sayres ◽  
Joakim Vinberg ◽  
Kalanit Grill-Spector

Repeating object images produces stimulus-specific repetition suppression referred to as functional magnetic resonance imaging-adaptation (fMRI-A) in ventral temporal cortex (VTC). However, the effects of stimulus repetition on functional selectivity are largely unknown. We investigated the effects of short-lagged (SL, immediate) and long-lagged (LL, many intervening stimuli) repetitions on category selectivity in VTC using high-resolution fMRI. We asked whether repetition produces scaling or sharpening of fMRI responses both within category-selective regions as well as in the distributed response pattern across VTC. Results illustrate that repetition effects across time scales vary quantitatively along an anterior-posterior axis and qualitatively along a lateral-medial axis. In lateral VTC, both SL and LL repetitions produce proportional fMRI-A with no change in either selectivity or distributed responses as predicted by a scaling model. Further, there is larger fMRI-A in anterior subregions irrespective of category selectivity. Medial VTC exhibits similar scaling effects during SL repetitions. However, for LL repetitions, both the selectivity and distributed pattern of responses vary with category in medial VTC as predicted by a sharpening model. Specifically, there is larger fMRI-A for nonpreferred categories compared with the preferred category, and category selectivity does not predict fMRI-A across the pattern of distributed response. Finally, simulations indicate that different neural mechanisms likely underlie fMRI-A in medial compared to lateral VTC. These results have important implications for future fMRI-A experiments because they suggest that fMRI-A does not reflect a universal neural mechanism and that results of fMRI-A experiments will likely be paradigm independent in lateral VTC but paradigm dependent in medial VTC.


2016 ◽  
Vol 113 (46) ◽  
pp. E7277-E7286 ◽  
Author(s):  
Amy L. Daitch ◽  
Brett L. Foster ◽  
Jessica Schrouff ◽  
Vinitha Rangarajan ◽  
Itır Kaşikçi ◽  
...  

Brain areas within the lateral parietal cortex (LPC) and ventral temporal cortex (VTC) have been shown to code for abstract quantity representations and for symbolic numerical representations, respectively. To explore the fast dynamics of activity within each region and the interaction between them, we used electrocorticography recordings from 16 neurosurgical subjects implanted with grids of electrodes over these two regions and tracked the activity within and between the regions as subjects performed three different numerical tasks. Although our results reconfirm the presence of math-selective hubs within the VTC and LPC, we report here a remarkable heterogeneity of neural responses within each region at both millimeter and millisecond scales. Moreover, we show that the heterogeneity of response profiles within each hub mirrors the distinct patterns of functional coupling between them. Our results support the existence of multiple bidirectional functional loops operating between discrete populations of neurons within the VTC and LPC during the visual processing of numerals and the performance of arithmetic functions. These findings reveal information about the dynamics of numerical processing in the brain and also provide insight into the fine-grained functional architecture and connectivity within the human brain.


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