Category-selective Responses Research Articles

Distinct and distributed functional connectivity patterns across cortex reflect the domain-specific constraints of object, face, scene, body, and tool category-selective modules in the ventral visual pathway

Primate occipitotemporal cortex (OTC) is composed of a mosaic of highly specialized brain regions each involved in the high-level visual analysis and recognition of particular stimulus categories (e.g., objects, faces, scenes, bodies and tools). Whereas theories attempting to account for this modular organization of category-selective responses in OTC have largely focused on visually driven, bottom-up inputs to OTC (e.g., dimensions related to the visual structure of the world and how it is experienced), other proposals have instead focused on the connectivity of OTC's outputs, emphasizing how the information processed by different OTC regions might be used by the rest of the brain. The latter proposals underscore the importance of interpreting the activity (and selectivity) of individual OTC areas within the greater context of the widely distributed network of areas in which they are embedded and that use OTC information to support behavior. Here, using resting-state fMRI, we investigated the functional connectivity (FC) patterns of OTC regions associated with object-, face-, scene-, body- and tool-related processing defined from task-based localizers acquired in the same cohort of participants. We observed notable differences in the whole-brain FC patterns, not only across OTC regions, but even between areas thought to form part of the same category-selective network. Furthermore, we found that the neuroanatomical location of OTC regions (e.g., adjacency) had little, if any, bearing on the FC networks observed. FC between certain OTC areas and other regions traditionally implicated in sensory-, motor-, affective- and/or cognitive-related processing and the associated theoretical implications is discussed.

Alternating Zones Selective to Faces and Written Words in the Human Ventral Occipitotemporal Cortex

Recognition of faces and written words is associated with category-specific brain activation in the ventral occipitotemporal cortex (vOT). However, topological and functional relationships between face-selective and word-selective vOT regions remain unclear. In this study, we collected data from patients with intractable epilepsy who underwent high-density recording of surface field potentials in the vOT. "Faces" and "letterstrings" induced outstanding category-selective responses among the 24 visual categories tested, particularly in high-γ band powers. Strikingly, within-hemispheric analysis revealed alternation of face-selective and letterstring-selective zones within the vOT. Two distinct face-selective zones located anterior and posterior portions of the mid-fusiform sulcus whereas letterstring-selective zones alternated between and outside of these 2 face-selective zones. Further, a classification analysis indicated that activity patterns of these zones mostly represent dedicated categories. Functional connectivity analysis using Granger causality indicated asymmetrically directed causal influences from face-selective to letterstring-selective regions. These results challenge the prevailing view that different categories are represented in distinct contiguous regions in the vOT.

Neuronal integration in visual cortex elevates face category tuning to conscious face perception

The human brain has the extraordinary capability to transform cluttered sensory input into distinct object representations. For example, it is able to rapidly and seemingly without effort detect object categories in complex natural scenes. Surprisingly, category tuning is not sufficient to achieve conscious recognition of objects. What neural process beyond category extraction might elevate neural representations to the level where objects are consciously perceived? Here we show that visible and invisible faces produce similar category-selective responses in the ventral visual cortex. The pattern of neural activity evoked by visible faces could be used to decode the presence of invisible faces and vice versa. However, only visible faces caused extensive response enhancements and changes in neural oscillatory synchronization, as well as increased functional connectivity between higher and lower visual areas. We conclude that conscious face perception is more tightly linked to neural processes of sustained information integration and binding than to processes accommodating face category tuning.

Person- and Place-Selective Neural Substrates for Entity-Specific Semantic Access

Object-category has a pronounced effect on the representation of objects in higher level visual cortex. However, the influence of category on semantic/conceptual processes is less well characterized. In the present study, we conduct 2 fMRI experiments to investigate the semantic processing of information specific to individual people and places (entities). First, during picture presentation, we determined which brain regions show category-selective increases during access to entity-specific semantic information (i.e., nationality) in comparison to general-category discrimination (person vs. place). In the second experiment, we presented either words or pictures to assess the independence of entity-specific category-selective semantic representations from the processes used to access those representations. Convergent results from these 2 experiments show that brain regions exhibiting a category-selective increase during entity-specific semantic access are the same as those that show a supramodal (word/picture) category-selective response during the same task. These responses were different from classical "perceptual" category-selective responses and were evident in the medial precuneus for people and in the retrosplenial complex as well as anterior/superior sections of the transverse occipital sulcus and parahippocampal gyrus for places. These results reveal the pervasive influence of object-category in cortical organization, which extends to aspects of semantic knowledge arbitrarily related to physical/perceptual properties.

Neuronal integration in visual cortex elevates face category tuning to conscious face perception

The human brain has the extraordinary capability to transform cluttered sensory input into distinct object representations. For example, it is able to rapidly and seemingly without effort detect object categories in complex natural scenes. Surprisingly, category tuning is not sufficient to achieve conscious recognition of objects. What neural process beyond category extraction might elevate neural representations to the level where objects are consciously perceived? Here we show that visible and invisible faces produce similar category-selective responses in the ventral visual cortex. The pattern of neural activity evoked by visible faces could be used to decode the presence of invisible faces and vice versa. However, only visible faces caused extensive response enhancements and changes in neural oscillatory synchronization, as well as increased functional connectivity between higher and lower visual areas. We conclude that conscious face perception is more tightly linked to neural processes of sustained information integration and binding than to processes accommodating face category tuning.

100ms to Category-Selective Response Patterns: Ultra-rapid Categorization in Occipitotemporal Cortex as a Result of Extensive Category Learning

Event Abstract Back to Event 100ms to Category-Selective Response Patterns: Ultra-rapid Categorization in Occipitotemporal Cortex as a Result of Extensive Category Learning Benedikt Ehinger1*, Danja Porada1, Andreas K. Engel1, 2, Peter Konig1, 2 and Tim Kietzmann1 1 University Osnabrück, Institute of Cognitive Science, Germany 2 University Clinics Hamburg Eppendorf, Institute of Neurophysiology and Pathophysiology, Germany Although the categorization of visual input is a most common and essential task of everyday behavior, the underlying cortical mechanisms and their localization are poorly understood. Specifically it was suggested that categorization is accomplished in prefrontal cortex [1,2], yet categoryselective representations were found in the ventral temporal cortex [3,4]. As most studies employed fMRI measurements with low temporal resolution, both views could be reconciled based on cortical feedback from prefrontal cortex. Here, we investigate dynamics of categorization by an EEG/MEG adaptation paradigm jointly with extensive training of controlled categories of faces (Fig. 1a, Ref 5,6). This tests the prediction that the response is larger in cases of cross-category stimulation, leading to a release of adaptation, compared to the case when first and second stimuli belong to the same category. The analyses of post training EEG data revealed a significant difference in the P100 evoked potential (Fig. 1b). This is evident in four occipitotemporal electrodes (Fig. 1c, p<0.007, two-tailed t-test) over the right hemisphere. Consistent with the prediction of category selective representations, the amplitude in these electrodes was significantly larger for the cross-category condition. The right-lateralization of the effect is in line with previous reports for the processing of faces [7,8]. Importantly, no frontal electrodes showed significant effects of category membership. Taken together, the finding of such early category effects in occipitotemporal and no significant differences in prefrontal electrodes render the possibility of feedback from prefrontal cortex unlikely and rather suggests the origin of category selective representations in the ventral stream.

First-Pass Selectivity for Semantic Categories in Human Anteroventral Temporal Lobe

How the brain encodes the semantic concepts represented by words is a fundamental question in cognitive neuroscience. Hemodynamic neuroimaging studies have robustly shown that different areas of posteroventral temporal lobe are selectively activated by images of animals versus manmade objects. Selective responses in these areas to words representing animals versus objects are sometimes also seen, but they are task-dependent, suggesting that posteroventral temporal cortex may encode visual categories, while more anterior areas encode semantic categories. Here, using the spatiotemporal resolution provided by intracranial macroelectrode and microelectrode arrays, we report category-selective responses to words representing animals and objects in human anteroventral temporal areas including inferotemporal, perirhinal, and entorhinal cortices. This selectivity generalizes across tasks and sensory modalities, suggesting that it represents abstract lexicosemantic categories. Significant category-specific responses are found in measures sensitive to synaptic activity (local field potentials, high gamma power, current sources and sinks) and unit-firing (multiunit and single-unit activity). Category-selective responses can occur at short latency (as early as 130 ms) in middle cortical layers and thus are extracted in the first pass of activity through the anteroventral temporal lobe. This activation may provide input to posterior areas for iconic representations when required by the task, as well as to the hippocampal formation for categorical encoding and retrieval of memories, and to the amygdala for emotional associations. More generally, these results support models in which the anteroventral temporal lobe plays a primary role in the semantic representation of words.

Haptic perception and body representation in lateral and medial occipito-temporal cortices

Although vision is the primary sensory modality that humans and other primates use to identify objects in the environment, we can recognize crucial object features (e.g., shape, size) using the somatic modality. Previous studies have shown that the occipito-temporal areas dedicated to the visual processing of object forms, faces and bodies also show category-selective responses when the preferred stimuli are haptically explored out of view. Visual processing of human bodies engages specific areas in lateral (extrastriate body area, EBA) and medial (fusiform body area, FBA) occipito-temporal cortex. This study aimed at exploring the relative involvement of EBA and FBA in the haptic exploration of body parts. During fMRI scanning, participants were asked to haptically explore either real-size fake body parts or objects. We found a selective activation of right and left EBA, but not of right FBA, while participants haptically explored body parts as compared to real objects. This suggests that EBA may integrate visual body representations with somatosensory information regarding body parts and form a multimodal representation of the body. Furthermore, both left and right EBA showed a comparable level of body selectivity during haptic perception and visual imagery. However, right but not left EBA was more activated during haptic exploration than visual imagery of body parts, ruling out that the response to haptic body exploration was entirely due to the use of visual imagery. Overall, the results point to the existence of different multimodal body representations in the occipito-temporal cortex which are activated during perception and imagery of human body parts.

"What" precedes "which": developmental neural tuning in face- and place-related cortex.

Although category-specific activation for faces in the ventral visual pathway appears adult-like in adolescence, recognition abilities for individual faces are still immature. We investigated how the ability to represent "individual" faces and houses develops at the neural level. Category-selective regions of interest (ROIs) for faces in the fusiform gyrus (FG) and for places in the parahippocampal place area (PPA) were identified individually in children, adolescents, and adults. Then, using an functional magnetic resonance imaging adaptation paradigm, we measured category selectivity and individual-level adaptation for faces and houses in each ROI. Only adults exhibited both category selectivity and individual-level adaptation bilaterally for faces in the FG and for houses in the PPA. Adolescents showed category selectivity bilaterally for faces in the FG and houses in the PPA. Despite this profile of category selectivity, adolescents only exhibited individual-level adaptation for houses bilaterally in the PPA and for faces in the "left" FG. Children only showed category-selective responses for houses in the PPA, and they failed to exhibit category-selective responses for faces in the FG and individual-level adaptation effects anywhere in the brain. These results indicate that category-level neural tuning develops prior to individual-level neural tuning and that face-related cortex is disproportionately slower in this developmental transition than is place-related cortex.

Top-Down Spatial Categorization Signal from Prefrontal to Posterior Parietal Cortex in the Primate

In the present study we characterized the strength and time course of category-selective responses in prefrontal cortex and area 7a of the posterior parietal cortex during a match-to-sample spatial categorization task. A monkey was trained to categorize whether the height of a horizontal sample bar, presented in rectangular frame at one of three vertical locations, was “high” or “low,” depending on whether its position was above or below the frame's midline. After the display of this sample bar, and after a delay, choice bars were sequentially flashed in two locations: at the top and at the bottom of the frame (“choice” epoch). If the monkey timed its response to the display of the choice bar that matched the sample bar, he was rewarded. We found that cells in prefrontal cortex discriminated category early after the initial sample bar was shown, and continued to differentiate “up” from “down” trials throughout the delay and choice periods. In contrast, parietal cells did not differentiate category until the choice period. Therefore, our results support the notion of a top-down categorical signal that originates in prefrontal cortex and that is only represented in parietal cortex when it is necessary to express the categorical decision through a movement.

High prevalence of functional clustering in human cortex revealed by intracranial EEG during naturalistic audiovisual movies

Event Abstract Back to Event High prevalence of functional clustering in human cortex revealed by intracranial EEG during naturalistic audiovisual movies Meir Meshulam1*, Michal Ramot2, Michal Harel1, Svetlana Kipervasser3, Miri Neufeld3, Uri Kramer3, 4 and Itzhak Fried3, 5 1 Weizmann Institute of Science, Israel 2 The Hebrew University of Jerusalem, Israel 3 Tel Aviv Medical Center, Tel Aviv University, Israel 4 University of Wisconsin, United States 5 University of California at Los Angeles, United States Neurons in human high-order sensory areas are clustered by functional properties. This was typically demonstrated using stimulus-response paradigms and functional Magnetic Resonance Imaging (fMRI), which revealed specific responses to specific image categories such as faces and houses. Here, we showed an audio-visual movie clip to patients implanted with intracranial EEG electrodes (590 in total) which covered large parts of the cortex. The complex naturalistic stimulus and the superior spatial and temporal resolution of iEEG compared to fMRI allowed us to gain new insights into the prevalence of functional selectivity in the human cortex. We found that only a small minority of electrodes showed highly reliable responses the movie clip, with only 15% of electrodes having a between-presentations correlation coefficient r > .27, while 71% of electrodes had a correlation coefficient r < .13. Using a “reverse correlation” approach (Hasson et al., 2004) we found conspicuous examples of category-selective responses to faces, body movements and actions. However, since neurons may be clustered according to functional features that are not easily recognized, we correlated the signals recorded from electrodes across our pool. Our results show that the electrode response selectivity was extremely narrow, so that 99.6% of the electrode population showed a significant difference in response profile. Given that the iEEG signals reflect the averaged response of a large number of neurons, these results provide clear evidence for functional clustering of cortical neurons in human sensory cortex. Funding: Supported by ISF, Bikura, and Mark Scher’s estate grants to RM. Keywords: EEG, fMRI, Perception Conference: XI International Conference on Cognitive Neuroscience (ICON XI), Palma, Mallorca, Spain, 25 Sep - 29 Sep, 2011. Presentation Type: Poster Presentation Topic: Poster Sessions: Neurophysiology of Sensation and Perception Citation: Meshulam M, Ramot M, Harel M, Kipervasser S, Neufeld M, Kramer U and Fried I (2011). High prevalence of functional clustering in human cortex revealed by intracranial EEG during naturalistic audiovisual movies. Conference Abstract: XI International Conference on Cognitive Neuroscience (ICON XI). doi: 10.3389/conf.fnhum.2011.207.00343 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 23 Nov 2011; Published Online: 28 Nov 2011. * Correspondence: Dr. Meir Meshulam, Weizmann Institute of Science, Rehovot, Israel, meir.meshulam@weizmann.ac.il Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Meir Meshulam Michal Ramot Michal Harel Svetlana Kipervasser Miri Neufeld Uri Kramer Itzhak Fried Google Meir Meshulam Michal Ramot Michal Harel Svetlana Kipervasser Miri Neufeld Uri Kramer Itzhak Fried Google Scholar Meir Meshulam Michal Ramot Michal Harel Svetlana Kipervasser Miri Neufeld Uri Kramer Itzhak Fried PubMed Meir Meshulam Michal Ramot Michal Harel Svetlana Kipervasser Miri Neufeld Uri Kramer Itzhak Fried Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Cortical Representation of Natural Complex Sounds: Effects of Acoustic Features and Auditory Object Category

How the brain processes complex sounds, like voices or musical instrument sounds, is currently not well understood. The features comprising the acoustic profiles of such sounds are thought to be represented by neurons responding to increasing degrees of complexity throughout auditory cortex, with complete auditory "objects" encoded by neurons (or small networks of neurons) in anterior superior temporal regions. Although specialized voice and speech-sound regions have been proposed, it is unclear how other types of complex natural sounds are processed within this object-processing pathway. Using functional magnetic resonance imaging, we sought to demonstrate spatially distinct patterns of category-selective activity in human auditory cortex, independent of semantic content and low-level acoustic features. Category-selective responses were identified in anterior superior temporal regions, consisting of clusters selective for musical instrument sounds and for human speech. An additional subregion was identified that was particularly selective for the acoustic-phonetic content of speech. In contrast, regions along the superior temporal plane closer to primary auditory cortex were not selective for stimulus category, responding instead to specific acoustic features embedded in natural sounds, such as spectral structure and temporal modulation. Our results support a hierarchical organization of the anteroventral auditory-processing stream, with the most anterior regions representing the complete acoustic signature of auditory objects.

Prior auditory information shapes visual category-selectivity in ventral occipito-temporal cortex

Objects in our natural environment generate signals in multiple sensory modalities. This fMRI study investigated the influence of prior task-irrelevant auditory information on visually-evoked category-selective activations in the ventral occipito-temporal cortex. Subjects categorized pictures as landmarks or animal faces, while ignoring the preceding congruent or incongruent sound. Behaviorally, subjects responded slower to incongruent than congruent stimuli. At the neural level, the lateral and medial prefrontal cortices showed increased activations for incongruent relative to congruent stimuli consistent with their role in response selection. In contrast, the parahippocampal gyri combined visual and auditory information additively: activation was greater for visual landmarks than animal faces and landmark-related sounds than animal vocalizations resulting in increased parahippocampal selectivity for congruent audiovisual landmarks. Effective connectivity analyses showed that this amplification of visual landmark-selectivity was mediated by increased negative coupling of the parahippocampal gyrus with the superior temporal sulcus for congruent stimuli. Thus, task-irrelevant auditory information influences visual object categorization at two stages. In the ventral occipito-temporal cortex auditory and visual category information are combined additively to sharpen visual category-selective responses. In the left inferior frontal sulcus, as indexed by a significant incongruency effect, visual and auditory category information are integrated interactively for response selection.

Object Representations for Multiple Visual Categories Overlap in Lateral Occipital and Medial Fusiform Cortex

How representations of visual objects are maintained across changes in viewpoint is a central issue in visual perception. Whether neural processes underlying view-invariant recognition involve distinct subregions within extrastriate visual cortex for distinct categories of visual objects remains unresolved. We used event-related functional magnetic resonance imaging in 16 healthy volunteers to map visual cortical areas responding to a large set (156) of exemplars from 3 object categories (faces, houses, and chairs), each repeated once after a variable time lag (3-7 intervening stimuli). Exemplars were repeated with the same viewpoint (but different retinal size) or with different viewpoint and size. The task was kept constant across object categories (judging items as "young" vs. "old"). We identified object-selective adaptation effects by comparing neural responses to the first presentation versus repetition of each individual exemplar. We found that exemplar-specific adaptation effects partly overlapped with regions showing category-selective responses (as identified using a separate localizer scan). These included the lateral fusiform gyrus (FG) for faces, parahippocampal gyrus for houses, and lateral occipital complex (LOC) for chairs. In face-selective fusiform gyrus (FG), adaptation effects occurred only for faces repeated with the same viewpoint, but not with a different viewpoint, confirming previous studies using faces only. By contrast, a region in right medial FG, adjacent to but nonoverlapping with the more lateral and face-selective FG, showed repetition effects for faces and to a lesser extent for other objects, regardless of changes in viewpoint or in retinal image-size. Category- and viewpoint-independent repetition effects were also found in bilateral LOC. Our results reveal a common neural substrate in bilateral LOC and right medial FG underlying view-invariant and category-independent recognition for multiple object identities, with only a relative preference for faces in medial FG but no selectivity in LOC.

Neuronal encoding of meaning: Establishing category-selective response patterns in the avian ‘prefrontal cortex’

Forebrain association areas interweave perceived stimuli with acquired representations of own actions and their outcome. Often, relevant stimuli come in a bewildering variety of shapes and sizes and we slowly have to learn to group them into meaningful categories. Therefore, the aim of the present study was twofold: First, to reveal how single units in the pigeon's nidopallium caudolaterale (NCL), a functional analogue of the mammalian prefrontal cortex (PFC), encode stimuli that differ in visual features but not in behavioral relevance. The second aim was to understand how these categorical representations are established during learning. Recordings were made from NCL neurons while pigeons performed a go–nogo categorization paradigm. Responses during presentation of the two S+ stimuli and non-responding during presentation of the two S− stimuli were followed by reward. We recorded from two pigeons at different learning stages. In the beginning of the learning process, neurons were active during and shortly before reward, but only in go trials. These data suggest that during the early phase of learning avian ‘prefrontal’ neurons code for rewards associated with the same behavioral demand, while ignoring feature differences of stimuli within one category. When learning progressed, (1) category selectivity became stronger, (2) responses selective for nogo stimuli appeared, and (3) reward-related responses disappeared in favor of category-selective responses during the stimulus phase. This backward shift in time resembles response patterns assumed by the temporal difference (TD) model of reinforcement learning, but goes beyond it, since it reflects the neuronal correlate of functional categories.

Alternate Task Inhibits Single-neuron Category-selective Responses in the Human Hippocampus while Preserving Selectivity in the Amygdala

One fifth of neurons in the medial-temporal lobe of human epilepsy patients respond selectively to categories of images, such as faces or cars. Here we show that responses of hippocampal neurons are rapidly modified as subjects alternate (over 60 sec) between two tasks (1) identifying images from a category, or (2) playing a simple video game superimposed on the same images. Category-selective responses, present when a subject identifies categories, are eliminated when the subject shifts to playing the game for 87% of category-selective hippocampal neurons. By contrast, responses in the amygdala are present during both tasks for 72% of category-selective amygdalar neurons. These results suggest that attention to images is required to evoke selective responses from single neurons in the hippocampus, but is not required by neurons in the amygdala.

Two Distinct Neural Mechanisms for Category-selective Responses

The cognitive and neural mechanisms mediating category-selective responses in the human brain remain controversial. Using functional magnetic resonance imaging and effective connectivity analyses (Dynamic Causal Modelling), we investigated animal- and tool-selective responses by manipulating stimulus modality (pictures versus words) and task (implicit versus explicit semantic). We dissociated two distinct mechanisms that engender category selectivity: in the ventral occipito-temporal cortex, tool-selective responses were observed irrespective of task, greater for pictures and mediated by bottom-up effects. In a left temporo-parietal action system, tool-selective responses were observed irrespective of modality, greater for explicit semantic tasks and mediated by top-down modulation from the left prefrontal cortex. These distinct activation and connectivity patterns suggest that the two systems support different cognitive operations, with the ventral occipito-temporal regions engaged in structural processing and the dorsal visuo-motor system in strategic semantic processing. Consistent with current semantic theories, explicit semantic processing of tools might thus rely on reactivating their associated action representations via top-down modulation. In terms of neuronal mechanisms, the category selectivity may be mediated by distinct top-down (task-dependent) and bottom-up (stimulus-dependent) mechanisms.

1704 Linear and nonlinear color processing in striate cortex of the macaque monkey

Objects in our natural environment generate signals in multiple sensory modalities. This fMRI study investigated the influence of prior task-irrelevant auditory information on visually-evoked category-selective activations in the ventral occipito-temporal cortex. Subjects categorized pictures as landmarks or animal faces, while ignoring the preceding congruent or incongruent sound. Behaviorally, subjects responded slower to incongruent than congruent stimuli. At the neural level, the lateral and medial prefrontal cortices showed increased activations for incongruent relative to congruent stimuli consistent with their role in response selection. In contrast, the parahippocampal gyri combined visual and auditory information additively: activation was greater for visual landmarks than animal faces and landmark-related sounds than animal vocalizations resulting in increased parahippocampal selectivity for congruent audiovisual landmarks. Effective connectivity analyses showed that this amplification of visual landmark-selectivity was mediated by increased negative coupling of the parahippocampal gyrus with the superior temporal sulcus for congruent stimuli. Thus, task-irrelevant auditory information influences visual object categorization at two stages. In the ventral occipito-temporal cortex auditory and visual category information are combined additively to sharpen visual category-selective responses. In the left inferior frontal sulcus, as indexed by a significant incongruency effect, visual and auditory category information are integrated interactively for response selection.