The Time-Course of Food Representation in the Human Brain.

Humans make decisions about food every day. The visual system provides important information that forms a basis for these food decisions. Although previous research has focused on visual object and category representations in the brain, it is still unclear how visually presented food is encoded by the brain. Here, we investigate the time-course of food representations in the brain. We used time-resolved multivariate analyses of electroencephalography (EEG) data, obtained from human participants (both sexes), to determine which food features are represented in the brain and whether focused attention is needed for this. We recorded EEG while participants engaged in two different tasks. In one task, the stimuli were task relevant, whereas in the other task, the stimuli were not task relevant. Our findings indicate that the brain can differentiate between food and nonfood items from ∼112 ms after the stimulus onset. The neural signal at later latencies contained information about food naturalness, how much the food was transformed, as well as the perceived caloric content. This information was present regardless of the task. Information about whether food is immediately ready to eat, however, was only present when the food was task relevant and presented at a slow presentation rate. Furthermore, the recorded brain activity correlated with the behavioral responses in an odd-item-out task. The fast representation of these food features, along with the finding that this information is used to guide food categorization decision-making, suggests that these features are important dimensions along which the representation of foods is organized.

Mapping the dynamics of visual feature coding: Insights into perception and integration.

The basic computations performed in the human early visual cortex are the foundation for visual perception. While we know a lot about these computations, a key missing piece is how the coding of visual features relates to our perception of the environment. To investigate visual feature coding, interactions, and their relationship to human perception, we investigated neural responses and perceptual similarity judgements to a large set of visual stimuli that varied parametrically along four feature dimensions. We measured neural responses using electroencephalography (N = 16) to 256 grating stimuli that varied in orientation, spatial frequency, contrast, and colour. We then mapped the response profiles of the neural coding of each visual feature and their interactions, and related these to independently obtained behavioural judgements of stimulus similarity. The results confirmed fundamental principles of feature coding in the visual system, such that all four features were processed simultaneously but differed in their dynamics, and there was distinctive conjunction coding for different combinations of features in the neural responses. Importantly, modelling of the behaviour revealed that every stimulus feature contributed to perceptual judgements, despite the untargeted nature of the behavioural task. Further, the relationship between neural coding and behaviour was evident from initial processing stages, signifying that the fundamental features, not just their interactions, contribute to perception. This study highlights the importance of understanding how feature coding progresses through the visual hierarchy and the relationship between different stages of processing and perception.

Properties of imagined experience across visual, auditory, and other sensory modalities.

Little is known about the perceptual characteristics of mental images nor how they vary across sensory modalities. We conducted an exhaustive survey into how mental images are experienced across modalities, mainly targeting visual and auditory imagery of a single stimulus, the letter "O", to facilitate direct comparisons. We investigated temporal properties of mental images (e.g. onset latency, duration), spatial properties (e.g. apparent location), effort (e.g. ease, spontaneity, control), movement requirements (e.g. eye movements), real-imagined interactions (e.g. inner speech while reading), beliefs about imagery norms and terminologies, as well as respondent confidence. Participants also reported on the five traditional senses and their prominence during thinking, imagining, and dreaming. Overall, visual and auditory experiences dominated mental events, although auditory mental images were superior to visual mental images on almost every metric tested except regarding spatial properties. Our findings suggest that modality-specific differences in mental imagery may parallel those of other sensory neural processes.

Temporal dissociation of neural activity underlying synesthetic and perceptual colors.

Grapheme-color synesthetes experience color when seeing achromatic symbols. We examined whether similar neural mechanisms underlie color perception and synesthetic colors using magnetoencephalography. Classification models trained on neural activity from viewing colored stimuli could distinguish synesthetic color evoked by achromatic symbols after a delay of ∼100 ms. Our results provide an objective neural signature for synesthetic experience and temporal evidence consistent with higher-level processing in synesthesia.

Spatial and Feature-selective Attention Have Distinct, Interacting Effects on Population-level Tuning.

Attention can be deployed in different ways: When searching for a taxi in New York City, we can decide where to attend (e.g., to the street) and what to attend to (e.g., yellow cars). Although we use the same word to describe both processes, nonhuman primate data suggest that these produce distinct effects on neural tuning. This has been challenging to assess in humans, but here we used an opportunity afforded by multivariate decoding of MEG data. We found that attending to an object at a particular location and attending to a particular object feature produced effects that interacted multiplicatively. The two types of attention induced distinct patterns of enhancement in occipital cortex, with feature-selective attention producing relatively more enhancement of small feature differences and spatial attention producing relatively larger effects for larger feature differences. An information flow analysis further showed that stimulus representations in occipital cortex were Granger-caused by coding in frontal cortices earlier in time and that the timing of this feedback matched the onset of attention effects. The data suggest that spatial and feature-selective attention rely on distinct neural mechanisms that arise from frontal-occipital information exchange, interacting multiplicatively to selectively enhance task-relevant information.

Capacity for movement is an organisational principle in object representations.

The ability to perceive moving objects is crucial for threat identification and survival. Recent neuroimaging evidence has shown that goal-directed movement is an important element of object processing in the brain. However, prior work has primarily used moving stimuli that are also animate, making it difficult to disentangle the effect of movement from aliveness or animacy in representational categorisation. In the current study, we investigated the relationship between how the brain processes movement and aliveness by including stimuli that are alive but still (e.g., plants), and stimuli that are not alive but move (e.g., waves). We examined electroencephalographic (EEG) data recorded while participants viewed static images of moving or non-moving objects that were either natural or artificial. Participants classified the images according to aliveness, or according to capacity for movement. Movement explained significant variance in the neural data over and above that of aliveness, showing that capacity for movement is an important dimension in the representation of visual objects in humans.

The Rapid Emergence of Musical Pitch Structure in Human Cortex.

In tonal music, continuous acoustic waveforms are mapped onto discrete, hierarchically arranged, internal representations of pitch. To examine the neural dynamics underlying this transformation, we presented male and female human listeners with tones embedded within a Western tonal context while recording their cortical activity using magnetoencephalography. Machine learning classifiers were then trained to decode different tones from their underlying neural activation patterns at each peristimulus time sample, providing a dynamic measure of their dissimilarity in cortex. Comparing the time-varying dissimilarity between tones with the predictions of acoustic and perceptual models, we observed a temporal evolution in the brain's representational structure. Whereas initial dissimilarities mirrored their fundamental-frequency separation, dissimilarities beyond 200 ms reflected the perceptual status of each tone within the tonal hierarchy of Western music. These effects occurred regardless of stimulus regularities within the context or whether listeners were engaged in a task requiring explicit pitch analysis. Lastly, patterns of cortical activity that discriminated between tones became increasingly stable in time as the information coded by those patterns transitioned from low-to-high level properties. Current results reveal the dynamics with which the complex perceptual structure of Western tonal music emerges in cortex at the timescale of an individual tone.SIGNIFICANCE STATEMENT Little is understood about how the brain transforms an acoustic waveform into the complex perceptual structure of musical pitch. Applying neural decoding techniques to the cortical activity of human subjects engaged in music listening, we measured the dynamics of information processing in the brain on a moment-to-moment basis as subjects heard each tone. In the first 200 ms after onset, transient patterns of neural activity coded the fundamental frequency of tones. Subsequently, a period emerged during which more temporally stable activation patterns coded the perceptual status of each tone within the "tonal hierarchy" of Western music. Our results provide a crucial link between the complex perceptual structure of tonal music and the underlying neural dynamics from which it emerges.

The Influence of Object-Color Knowledge on Emerging Object Representations in the Brain.

The ability to rapidly and accurately recognize complex objects is a crucial function of the human visual system. To recognize an object, we need to bind incoming visual features, such as color and form, together into cohesive neural representations and integrate these with our preexisting knowledge about the world. For some objects, typical color is a central feature for recognition; for example, a banana is typically yellow. Here, we applied multivariate pattern analysis on time-resolved neuroimaging (MEG) data to examine how object-color knowledge affects emerging object representations over time. Our results from 20 participants (11 female) show that the typicality of object-color combinations influences object representations, although not at the initial stages of object and color processing. We find evidence that color decoding peaks later for atypical object-color combinations compared with typical object-color combinations, illustrating the interplay between processing incoming object features and stored object knowledge. Together, these results provide new insights into the integration of incoming visual information with existing conceptual object knowledge.SIGNIFICANCE STATEMENT To recognize objects, we have to be able to bind object features, such as color and shape, into one coherent representation and compare it with stored object knowledge. The MEG data presented here provide novel insights about the integration of incoming visual information with our knowledge about the world. Using color as a model to understand the interaction between seeing and knowing, we show that there is a unique pattern of brain activity for congruently colored objects (e.g., a yellow banana) relative to incongruently colored objects (e.g., a red banana). This effect of object-color knowledge only occurs after single object features are processed, demonstrating that conceptual knowledge is accessed relatively late in the visual processing hierarchy.

The Rapid Emergence of Auditory Object Representations in Cortex Reflect Central Acoustic Attributes.

Human listeners are bombarded by acoustic information that the brain rapidly organizes into coherent percepts of objects and events in the environment, which aids speech and music perception. The efficiency of auditory object recognition belies the critical constraint that acoustic stimuli necessarily require time to unfold. Using magnetoencephalography, we studied the time course of the neural processes that transform dynamic acoustic information into auditory object representations. Participants listened to a diverse set of 36 tokens comprising everyday sounds from a typical human environment. Multivariate pattern analysis was used to decode the sound tokens from the magnetoencephalographic recordings. We show that sound tokens can be decoded from brain activity beginning 90 msec after stimulus onset with peak decoding performance occurring at 155 msec poststimulus onset. Decoding performance was primarily driven by differences between category representations (e.g., environmental vs. instrument sounds), although within-category decoding was better than chance. Representational similarity analysis revealed that these emerging neural representations were related to harmonic and spectrotemporal differences among the stimuli, which correspond to canonical acoustic features processed by the auditory pathway. Our findings begin to link the processing of physical sound properties with the perception of auditory objects and events in cortex.

The representational dynamics of visual objects in rapid serial visual processing streams.

In our daily lives, we are bombarded with a stream of rapidly changing visual input. Humans have the remarkable capacity to detect and identify objects in fast-changing scenes. Yet, when studying brain representations, stimuli are generally presented in isolation. Here, we studied the dynamics of human vision using a combination of fast stimulus presentation rates, electroencephalography and multivariate decoding analyses. Using a presentation rate of 5 images per second, we obtained the representational structure of a large number of stimuli, and showed the emerging abstract categorical organisation of this structure. Furthermore, we could separate the temporal dynamics of perceptual processing from higher-level target selection effects. In a second experiment, we used the same paradigm at 20Hz to show that shorter image presentation limits the categorical abstraction of object representations. Our results show that applying multivariate pattern analysis to every image in rapid serial visual processing streams has unprecedented potential for studying the temporal dynamics of the structure of representations in the human visual system.

The influence of image masking on object representations during rapid serial visual presentation.

Rapid image presentations combined with time-resolved multivariate analysis methods of EEG or MEG (rapid-MVPA) offer unique potential in assessing the temporal limitations of the human visual system. Recent work has shown that multiple visual objects presented sequentially can be simultaneously decoded from M/EEG recordings. Interestingly, object representations reached higher stages of processing for slower image presentation rates compared to fast rates. This fast rate attenuation is probably caused by forward and backward masking from the other images in the stream. Two factors that are likely to influence masking during rapid streams are stimulus duration and stimulus onset asynchrony (SOA). Here, we disentangle these effects by studying the emerging neural representation of visual objects using rapid-MVPA while independently manipulating stimulus duration and SOA. Our results show that longer SOAs enhance the decodability of neural representations, regardless of stimulus presentation duration, suggesting that subsequent images act as effective backward masks. In contrast, image duration does not appear to have a graded influence on object representations. Interestingly, however, decodability was improved when there was a gap between subsequent images, indicating that an abrupt onset or offset of an image enhances its representation. Our study yields insight into the dynamics of object processing in rapid streams, paving the way for future work using this promising approach.

Untangling featural and conceptual object representations.

How are visual inputs transformed into conceptual representations by the human visual system? The contents of human perception, such as objects presented on a visual display, can reliably be decoded from voxel activation patterns in fMRI, and in evoked sensor activations in MEG and EEG. A prevailing question is the extent to which brain activation associated with object categories is due to statistical regularities of visual features within object categories. Here, we assessed the contribution of mid-level features to conceptual category decoding using EEG and a novel fast periodic decoding paradigm. Our study used a stimulus set consisting of intact objects from the animate (e.g., fish) and inanimate categories (e.g., chair) and scrambled versions of the same objects that were unrecognizable and preserved their visual features (Long et al., 2018). By presenting the images at different periodic rates, we biased processing to different levels of the visual hierarchy. We found that scrambled objects and their intact counterparts elicited similar patterns of activation, which could be used to decode the conceptual category (animate or inanimate), even for the unrecognizable scrambled objects. Animacy decoding for the scrambled objects, however, was only possible at the slowest periodic presentation rate. Animacy decoding for intact objects was faster, more robust, and could be achieved at faster presentation rates. Our results confirm that the mid-level visual features preserved in the scrambled objects contribute to animacy decoding, but also demonstrate that the dynamics vary markedly for intact versus scrambled objects. Our findings suggest a complex interplay between visual feature coding and categorical representations that is mediated by the visual system's capacity to use image features to resolve a recognisable object.

Seeing versus knowing: The temporal dynamics of real and implied colour processing in the human brain.

Colour is a defining feature of many objects, playing a crucial role in our ability to rapidly recognise things in the world around us and make categorical distinctions. For example, colour is a useful cue when distinguishing lemons from limes or blackberries from raspberries. That means our representation of many objects includes key colour-related information. The question addressed here is whether the neural representation activated by knowing that something is red is the same as that activated when we actually see something red, particularly in regard to timing. We addressed this question using neural timeseries (magnetoencephalography, MEG) data to contrast real colour perception and implied object colour activation. We applied multivariate pattern analysis (MVPA) to analyse the brain activation patterns evoked by colour accessed via real colour perception and implied colour activation. Applying MVPA to MEG data allows us here to focus on the temporal dynamics of these processes. Male and female human participants (N = 18) viewed isoluminant red and green shapes and grey-scale, luminance-matched pictures of fruits and vegetables that are red (e.g., tomato) or green (e.g., kiwifruit) in nature. We show that the brain activation pattern evoked by real colour perception is similar to implied colour activation, but that this pattern is instantiated at a later time. These results suggest that a common colour representation can be triggered by activating object representations from memory and perceiving colours.

Edge-Related Activity Is Not Necessary to Explain Orientation Decoding in Human Visual Cortex.

Multivariate pattern analysis is a powerful technique; however, a significant theoretical limitation in neuroscience is the ambiguity in interpreting the source of decodable information used by classifiers. This is exemplified by the continued controversy over the source of orientation decoding from fMRI responses in human V1. Recently Carlson (2014) identified a potential source of decodable information by modeling voxel responses based on the Hubel and Wiesel (1972) ice-cube model of visual cortex. The model revealed that activity associated with the edges of gratings covaries with orientation and could potentially be used to discriminate orientation. Here we empirically evaluate whether "edge-related activity" underlies orientation decoding from patterns of BOLD response in human V1. First, we systematically mapped classifier performance as a function of stimulus location using population receptive field modeling to isolate each voxel's overlap with a large annular grating stimulus. Orientation was decodable across the stimulus; however, peak decoding performance occurred for voxels with receptive fields closer to the fovea and overlapping with the inner edge. Critically, we did not observe the expected second peak in decoding performance at the outer stimulus edge as predicted by the edge account. Second, we evaluated whether voxels that contribute most to classifier performance have receptive fields that cluster in cortical regions corresponding to the retinotopic location of the stimulus edge. Instead, we find the distribution of highly weighted voxels to be approximately random, with a modest bias toward more foveal voxels. Our results demonstrate that edge-related activity is likely not necessary for orientation decoding. SIGNIFICANCE STATEMENT: A significant theoretical limitation of multivariate pattern analysis in neuroscience is the ambiguity in interpreting the source of decodable information used by classifiers. For example, orientation can be decoded from BOLD activation patterns in human V1, even though orientation columns are at a finer spatial scale than 3T fMRI. Consequently, the source of decodable information remains controversial. Here we test the proposal that information related to the stimulus edges underlies orientation decoding. We map voxel population receptive fields in V1 and evaluate orientation decoding performance as a function of stimulus location in retinotopic cortex. We find orientation is decodable from voxels whose receptive fields do not overlap with the stimulus edges, suggesting edge-related activity does not substantially drive orientation decoding.

Finding decodable information that can be read out in behaviour.

Multivariate decoding methods applied to neuroimaging data have become the standard in cognitive neuroscience for unravelling statistical dependencies between brain activation patterns and experimental conditions. The current challenge is to demonstrate that decodable information is in fact used by the brain itself to guide behaviour. Here we demonstrate a promising approach to do so in the context of neural activation during object perception and categorisation behaviour. We first localised decodable information about visual objects in the human brain using a multivariate decoding analysis and a spatially-unbiased searchlight approach. We then related brain activation patterns to behaviour by testing whether the classifier used for decoding can be used to predict behaviour. We show that while there is decodable information about visual category throughout the visual brain, only a subset of those representations predicted categorisation behaviour, which were strongest in anterior ventral temporal cortex. Our results have important implications for the interpretation of neuroimaging studies, highlight the importance of relating decoding results to behaviour, and suggest a suitable methodology towards this aim.

Interpreting the dimensions of neural feature representations revealed by dimensionality reduction.

Recent progress in understanding the structure of neural representations in the cerebral cortex has centred around the application of multivariate classification analyses to measurements of brain activity. These analyses have proved a sensitive test of whether given brain regions provide information about specific perceptual or cognitive processes. An exciting extension of this approach is to infer the structure of this information, thereby drawing conclusions about the underlying neural representational space. These approaches rely on exploratory data-driven dimensionality reduction to extract the natural dimensions of neural spaces, including natural visual object and scene representations, semantic and conceptual knowledge, and working memory. However, the efficacy of these exploratory methods is unknown, because they have only been applied to representations in brain areas for which we have little or no secondary knowledge. One of the best-understood areas of the cerebral cortex is area MT of primate visual cortex, which is known to be important in motion analysis. To assess the effectiveness of dimensionality reduction for recovering neural representational space we applied several dimensionality reduction methods to multielectrode measurements of spiking activity obtained from area MT of marmoset monkeys, made while systematically varying the motion direction and speed of moving stimuli. Despite robust tuning at individual electrodes, and high classifier performance, dimensionality reduction rarely revealed dimensions for direction and speed. We use this example to illustrate important limitations of these analyses, and suggest a framework for how to best apply such methods to data where the structure of the neural representation is unknown.

Decoding Dynamic Brain Patterns from Evoked Responses: A Tutorial on Multivariate Pattern Analysis Applied to Time Series Neuroimaging Data.

Multivariate pattern analysis (MVPA) or brain decoding methods have become standard practice in analyzing fMRI data. Although decoding methods have been extensively applied in brain-computer interfaces, these methods have only recently been applied to time series neuroimaging data such as MEG and EEG to address experimental questions in cognitive neuroscience. In a tutorial style review, we describe a broad set of options to inform future time series decoding studies from a cognitive neuroscience perspective. Using example MEG data, we illustrate the effects that different options in the decoding analysis pipeline can have on experimental results where the aim is to "decode" different perceptual stimuli or cognitive states over time from dynamic brain activation patterns. We show that decisions made at both preprocessing (e.g., dimensionality reduction, subsampling, trial averaging) and decoding (e.g., classifier selection, cross-validation design) stages of the analysis can significantly affect the results. In addition to standard decoding, we describe extensions to MVPA for time-varying neuroimaging data including representational similarity analysis, temporal generalization, and the interpretation of classifier weight maps. Finally, we outline important caveats in the design and interpretation of time series decoding experiments.

Asymmetric Compression of Representational Space for Object Animacy Categorization under Degraded Viewing Conditions.

Animacy is a robust organizing principle among object category representations in the human brain. Using multivariate pattern analysis methods, it has been shown that distance to the decision boundary of a classifier trained to discriminate neural activation patterns for animate and inanimate objects correlates with observer RTs for the same animacy categorization task [Ritchie, J. B., Tovar, D. A., & Carlson, T. A. Emerging object representations in the visual system predict reaction times for categorization. PLoS Computational Biology, 11, e1004316, 2015; Carlson, T. A., Ritchie, J. B., Kriegeskorte, N., Durvasula, S., & Ma, J. Reaction time for object categorization is predicted by representational distance. Journal of Cognitive Neuroscience, 26, 132-142, 2014]. Using MEG decoding, we tested if the same relationship holds when a stimulus manipulation (degradation) increases task difficulty, which we predicted would systematically decrease the distance of activation patterns from the decision boundary and increase RTs. In addition, we tested whether distance to the classifier boundary correlates with drift rates in the linear ballistic accumulator [Brown, S. D., & Heathcote, A. The simplest complete model of choice response time: Linear ballistic accumulation. Cognitive Psychology, 57, 153-178, 2008]. We found that distance to the classifier boundary correlated with RT, accuracy, and drift rates in an animacy categorization task. Split by animacy, the correlations between brain and behavior were sustained longer over the time course for animate than for inanimate stimuli. Interestingly, when examining the distance to the classifier boundary during the peak correlation between brain and behavior, we found that only degraded versions of animate, but not inanimate, objects had systematically shifted toward the classifier decision boundary as predicted. Our results support an asymmetry in the representation of animate and inanimate object categories in the human brain.

Dynamic population codes of multiplexed stimulus features in primate area MT.

The middle-temporal area (MT) of primate visual cortex is critical in the analysis of visual motion. Single-unit studies suggest that the response dynamics of neurons within area MT depend on stimulus features, but how these dynamics emerge at the population level, and how feature representations interact, is not clear. Here, we used multivariate classification analysis to study how stimulus features are represented in the spiking activity of populations of neurons in area MT of marmoset monkey. Using representational similarity analysis we distinguished the emerging representations of moving grating and dot field stimuli. We show that representations of stimulus orientation, spatial frequency, and speed are evident near the onset of the population response, while the representation of stimulus direction is slower to emerge and sustained throughout the stimulus-evoked response. We further found a spatiotemporal asymmetry in the emergence of direction representations. Representations for high spatial frequencies and low temporal frequencies are initially orientation dependent, while those for high temporal frequencies and low spatial frequencies are more sensitive to motion direction. Our analyses reveal a complex interplay of feature representations in area MT population response that may explain the stimulus-dependent dynamics of motion vision.NEW & NOTEWORTHY Simultaneous multielectrode recordings can measure population-level codes that previously were only inferred from single-electrode recordings. However, many multielectrode recordings are analyzed using univariate single-electrode analysis approaches, which fail to fully utilize the population-level information. Here, we overcome these limitations by applying multivariate pattern classification analysis and representational similarity analysis to large-scale recordings from middle-temporal area (MT) in marmoset monkeys. Our analyses reveal a dynamic interplay of feature representations in area MT population response.

Representational dynamics of object recognition: Feedforward and feedback information flows.

Object perception involves a range of visual and cognitive processes, and is known to include both a feedfoward flow of information from early visual cortical areas to higher cortical areas, along with feedback from areas such as prefrontal cortex. Previous studies have found that low and high spatial frequency information regarding object identity may be processed over different timescales. Here we used the high temporal resolution of magnetoencephalography (MEG) combined with multivariate pattern analysis to measure information specifically related to object identity in peri-frontal and peri-occipital areas. Using stimuli closely matched in their low-level visual content, we found that activity in peri-occipital cortex could be used to decode object identity from ~80ms post stimulus onset, and activity in peri-frontal cortex could also be used to decode object identity from a later time (~265ms post stimulus onset). Low spatial frequency information related to object identity was present in the MEG signal at an earlier time than high spatial frequency information for peri-occipital cortex, but not for peri-frontal cortex. We additionally used Granger causality analysis to compare feedforward and feedback influences on representational content, and found evidence of both an early feedfoward flow and later feedback flow of information related to object identity. We discuss our findings in relation to existing theories of object processing and propose how the methods we use here could be used to address further questions of the neural substrates underlying object perception.