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1.  Consciousness in humans and non-human animals: recent advances and future directions 
This joint article reflects the authors' personal views regarding noteworthy advances in the neuroscience of consciousness in the last 10 years, and suggests what we feel may be promising future directions. It is based on a small conference at the Samoset Resort in Rockport, Maine, USA, in July of 2012, organized by the Mind Science Foundation of San Antonio, Texas. Here, we summarize recent advances in our understanding of subjectivity in humans and other animals, including empirical, applied, technical, and conceptual insights. These include the evidence for the importance of fronto-parietal connectivity and of “top-down” processes, both of which enable information to travel across distant cortical areas effectively, as well as numerous dissociations between consciousness and cognitive functions, such as attention, in humans. In addition, we describe the development of mental imagery paradigms, which made it possible to identify covert awareness in non-responsive subjects. Non-human animal consciousness research has also witnessed substantial advances on the specific role of cortical areas and higher order thalamus for consciousness, thanks to important technological enhancements. In addition, much progress has been made in the understanding of non-vertebrate cognition relevant to possible conscious states. Finally, major advances have been made in theories of consciousness, and also in their comparison with the available evidence. Along with reviewing these findings, each author suggests future avenues for research in their field of investigation.
PMCID: PMC3814086  PMID: 24198791
consciousness; animals; human cognition; theoretical neuroscience; biotechnology; neuroimaging
2.  Processing of Facial Emotion in the Human Fusiform Gyrus 
Journal of cognitive neuroscience  2011;24(6):1358-1370.
Electrophysiological and fMRI-based investigations of the ventral temporal cortex of primates provide strong support for regional specialization for the processing of faces. These responses are most frequently found in or near the fusiform gyrus, but there is substantial variability in their anatomical location and response properties. An outstanding question is the extent to which ventral temporal cortex participates in processing dynamic, expressive aspects of faces, a function usually attributed to regions near the superior temporal cortex. Here, we investigated these issues through intracranial recordings from eight human surgical patients. We compared several different aspects of face processing (static and dynamic faces; happy, neutral, and fearful expressions) with power in the high-gamma band (70–150 Hz) from a spectral analysis. Detailed mapping of the response characteristics as a function of anatomical location was conducted in relation to the gyral and sulcal pattern on each patient’s brain. The results document responses with high responsiveness for static or dynamic faces, often showing abrupt changes in response properties between spatially close recording sites and idiosyncratic across different subjects. Notably, strong responses to dynamic facial expressions can be found in the fusiform gyrus, just as can responses to static faces. The findings suggest a more complex, fragmented architecture of ventral temporal cortex around the fusiform gyrus, one that includes focal regions of cortex that appear relatively specialized for either static or dynamic aspects of faces.
PMCID: PMC3566877  PMID: 22185494
3.  A category-specific response to animals in the right human amygdala 
Nature neuroscience  2011;14(10):1247-1249.
The amygdala is important in emotion, but it remains unknown whether it is specialized for certain stimulus categories. We analyzed responses recorded from 489 single neurons in the amygdalae of 41 neurosurgical patients and found a categorical selectivity for pictures of animals in the right amygdala. This selectivity appeared to be independent of emotional valence or arousal and may reflect the importance that animals held throughout our evolutionary past.
PMCID: PMC3505687  PMID: 21874014
4.  Spatial Attention Is Attracted in a Sustained Fashion toward Singular Points in the Optic Flow 
PLoS ONE  2012;7(8):e41040.
While a single approaching object is known to attract spatial attention, it is unknown how attention is directed when the background looms towards the observer as s/he moves forward in a quasi-stationary environment. In Experiment 1, we used a cued speeded discrimination task to quantify where and how spatial attention is directed towards the target superimposed onto a cloud of moving dots. We found that when the motion was expansive, attention was attracted towards the singular point of the optic flow (the focus of expansion, FOE) in a sustained fashion. The effects were less pronounced when the motion was contractive. The more ecologically valid the motion features became (e.g., temporal expansion of each dot, spatial depth structure implied by distribution of the size of the dots), the stronger the attentional effects. Further, the attentional effects were sustained over 1000 ms. Experiment 2 quantified these attentional effects using a change detection paradigm by zooming into or out of photographs of natural scenes. Spatial attention was attracted in a sustained manner such that change detection was facilitated or delayed depending on the location of the FOE only when the motion was expansive. Our results suggest that focal attention is strongly attracted towards singular points that signal the direction of forward ego-motion.
PMCID: PMC3414468  PMID: 22905096
5.  The Role of Risk Aversion in Non-Conscious Decision Making 
To what extent can people choose advantageously without knowing why they are making those choices? This hotly debated question has capitalized on the Iowa Gambling Task (IGT), in which people often learn to choose advantageously without appearing to know why. However, because the IGT is unconstrained in many respects, this finding remains debated and other interpretations are possible (e.g., risk aversion, ambiguity aversion, limits of working memory, or insensitivity to reward/punishment can explain the finding of the IGT). Here we devised an improved variant of the IGT in which the deck-payoff contingency switches after subjects repeatedly choose from a good deck, offering the statistical power of repeated within-subject measures based on learning the reward contingencies associated with each deck. We found that participants exhibited low confidence in their choices, as probed with post-decision wagering, despite high accuracy in selecting advantageous decks in the task, which is putative evidence for non-conscious decision making. However, such a behavioral dissociation could also be explained by risk aversion, a tendency to avoid risky decisions under uncertainty. By explicitly measuring risk aversion for each individual, we predicted subjects’ post-decision wagering using Bayesian modeling. We found that risk aversion indeed does play a role, but that it did not explain the entire effect. Moreover, independently measured risk aversion was uncorrelated with risk aversion exhibited during our version of the IGT, raising the possibility that the latter risk aversion may be non-conscious. Our findings support the idea that people can make optimal choices without being fully aware of the basis of their decision. We suggest that non-conscious decision making may be mediated by emotional feelings of risk that are based on mechanisms distinct from those that support cognitive assessment of risk.
PMCID: PMC3286853  PMID: 22375133
decision making; consciousness; risk aversion; post-decision wagering; confidence
6.  Manifestation of ocular-muscle EMG contamination in human intracranial recordings 
NeuroImage  2010;54(1):213-233.
It is widely assumed that intracranial recordings from the brain are only minimally affected by contamination due to ocular-muscle electromyogram (oEMG). Here we show that this is not always the case. In intracranial recordings from five surgical epilepsy patients we observed that eye movements caused a transient biphasic potential at the onset of a saccade, resembling the saccadic spike potential commonly seen in scalp EEG, accompanied by an increase in broadband power between 20 and 200 Hz. Using concurrently recorded eye movements and high-density intracranial EEG (iEEG) we developed a detailed overview of the spatial distribution and temporal characteristics of the saccade-related oculomotor signal within recordings from ventral, medial and lateral temporal cortex. The occurrence of the saccadic spike was not explained solely by reference contact location, and was observed near the temporal pole for small (< 2 deg) amplitude saccades and over a broad area for larger saccades. We further examined the influence of saccade-related oEMG contamination on measurements of spectral power and interchannel coherence. Contamination manifested in both spectral power and coherence measurements, in particular, over the anterior half of the ventral and medial temporal lobe. Next, we compared methods for removing the contaminating signal and found that nearest-neighbor bipolar re-referencing and ICA filtering were effective for suppressing oEMG at locations far from the orbits, but tended to leave some residual contamination at the temporal pole. Finally, we show that genuine cortical broadband gamma responses observed in averaged data from ventral temporal cortex can bear a striking similarity in time course and band-width to oEMG contamination recorded at more anterior locations. We conclude that eye movement-related contamination should be ruled out when reporting high gamma responses in human intracranial recordings, especially those obtained near anterior and medial temporal lobe.
PMCID: PMC2975438  PMID: 20696256
intracranial EEG; ECoG; saccadic spike; EMG; gamma band; Eye Movement; Eye Muscle
8.  Abnormal social reward processing in autism as indexed by pupillary responses to happy faces 
Individuals with Autism Spectrum Disorders (ASD) typically show impaired eye contact during social interactions. From a young age, they look less at faces than typically developing (TD) children and tend to avoid direct gaze. However, the reason for this behavior remains controversial; ASD children might avoid eye contact because they perceive the eyes as aversive or because they do not find social engagement through mutual gaze rewarding.
We monitored pupillary diameter as a measure of autonomic response in children with ASD (n = 20, mean age = 12.4) and TD controls (n = 18, mean age = 13.7) while they looked at faces displaying different emotions. Each face displayed happy, fearful, angry or neutral emotions with the gaze either directed to or averted from the subjects.
Overall, children with ASD and TD controls showed similar pupillary responses; however, they differed significantly in their sensitivity to gaze direction for happy faces. Specifically, pupillary diameter increased among TD children when viewing happy faces with direct gaze as compared to those with averted gaze, whereas children with ASD did not show such sensitivity to gaze direction. We found no group differences in fixation that could explain the differential pupillary responses. There was no effect of gaze direction on pupil diameter for negative affect or neutral faces among either the TD or ASD group.
We interpret the increased pupillary diameter to happy faces with direct gaze in TD children to reflect the intrinsic reward value of a smiling face looking directly at an individual. The lack of this effect in children with ASD is consistent with the hypothesis that individuals with ASD may have reduced sensitivity to the reward value of social stimuli.
PMCID: PMC3461481  PMID: 22958650
Autism; Pupillary response; Reward processing
9.  Reading the mind's eye: decoding category information during mental imagery 
NeuroImage  2009;50(2):818-825.
Category information for visually presented objects can be read out from multi-voxel patterns of fMRI activity in ventral temporal cortex. What is the nature and reliability of these patterns in the absence of any bottom-up visual input, for example, during visual imagery? Here, we first ask how well category information can be decoded for imagined objects, and then compare the representations evoked during imagery and actual viewing. In an fMRI study, four object categories were either visually presented to subjects, or imagined by them. Using pattern classification techniques we could reliably decode category information (including for non-special categories, i.e., food and tools) from ventral temporal cortex in both conditions, but only during actual viewing from retinotopic areas. Interestingly, in temporal cortex when the classifier was trained on the viewed condition and tested on the imagined condition, or vice-versa, classification performance was comparable to within the imagined condition. The above results held even when we did not use information in the specialized category-selective areas. Thus, the patterns of representation during imagery and actual viewing are in fact surprisingly similar to each other. Consistent with this observation, the maps of “diagnostic voxels” (i.e., the classifier weights) for the perception and imagery classifiers were more similar in ventral temporal cortex than in retinotopic cortex. These results suggest that in the absence of any bottom-up input cortical back projections can selectively re-activate specific patterns of neural activity.
PMCID: PMC2823980  PMID: 20004247
imagery; perception; fMRI; multi-voxel pattern analysis; occipito-temporal cortex; object recognition
10.  Consciousness and Attention: On Sufficiency and Necessity 
Recent research has slowly corroded a belief that selective attention and consciousness are so tightly entangled that they cannot be individually examined. In this review, we summarize psychophysical and neurophysiological evidence for a dissociation between top-down attention and consciousness. The evidence includes recent findings that show subjects can attend to perceptually invisible objects. More contentious is the finding that subjects can become conscious of an isolated object, or the gist of the scene in the near absence of top-down attention; we critically re-examine the possibility of “complete” absence of top-down attention. We also cover the recent flurry of studies that utilized independent manipulation of attention and consciousness. These studies have shown paradoxical effects of attention, including examples where top-down attention and consciousness have opposing effects, leading us to strengthen and revise our previous views. Neuroimaging studies with EEG, MEG, and fMRI are uncovering the distinct neuronal correlates of selective attention and consciousness in dissociative paradigms. These findings point to a functional dissociation: attention as analyzer and consciousness as synthesizer. Separating the effects of selective visual attention from those of visual consciousness is of paramount importance to untangle the neural substrates of consciousness from those for attention.
PMCID: PMC3153822  PMID: 21833272
attention; consciousness; psychophysics; neuroimaging
11.  Intact rapid detection of fearful faces in the absence of the amygdala 
Nature neuroscience  2009;12(10):1224-1225.
The amygdala is thought to process fear-related stimuli rapidly and nonconsciously. We found that an individual with complete bilateral amygdala lesions, who cannot recognize fear from faces, nonetheless showed normal rapid detection and nonconscious processing of those same fearful faces. We conclude that the amygdala is not essential for early stages of fear processing but, instead, modulates recognition and social judgment.
PMCID: PMC2756300  PMID: 19718036
12.  Decoding Face Information in Time, Frequency and Space from Direct Intracranial Recordings of the Human Brain 
PLoS ONE  2008;3(12):e3892.
Faces are processed by a neural system with distributed anatomical components, but the roles of these components remain unclear. A dominant theory of face perception postulates independent representations of invariant aspects of faces (e.g., identity) in ventral temporal cortex including the fusiform gyrus, and changeable aspects of faces (e.g., emotion) in lateral temporal cortex including the superior temporal sulcus. Here we recorded neuronal activity directly from the cortical surface in 9 neurosurgical subjects undergoing epilepsy monitoring while they viewed static and dynamic facial expressions. Applying novel decoding analyses to the power spectrogram of electrocorticograms (ECoG) from over 100 contacts in ventral and lateral temporal cortex, we found better representation of both invariant and changeable aspects of faces in ventral than lateral temporal cortex. Critical information for discriminating faces from geometric patterns was carried by power modulations between 50 to 150 Hz. For both static and dynamic face stimuli, we obtained a higher decoding performance in ventral than lateral temporal cortex. For discriminating fearful from happy expressions, critical information was carried by power modulation between 60–150 Hz and below 30 Hz, and again better decoded in ventral than lateral temporal cortex. Task-relevant attention improved decoding accuracy more than10% across a wide frequency range in ventral but not at all in lateral temporal cortex. Spatial searchlight decoding showed that decoding performance was highest around the middle fusiform gyrus. Finally, we found that the right hemisphere, in general, showed superior decoding to the left hemisphere. Taken together, our results challenge the dominant model for independent face representation of invariant and changeable aspects: information about both face attributes was better decoded from a single region in the middle fusiform gyrus.
PMCID: PMC2588533  PMID: 19065268
13.  Orienting to Social Stimuli Differentiates Social Cognitive Impairment in Autism and Schizophrenia 
Neuropsychologia  2007;45(11):2580-2588.
Both autism and schizophrenia feature deficits in aspects of social cognition that may be related to amygdala dysfunction, but it is unclear whether these are similar or different patterns of impairment. We compared the visual scanning patterns and emotion judgments of individuals with autism, individuals with schizophrenia and controls on a task well characterized with respect to amygdala functioning. On this task, eye movements of participants are recorded as they assess emotional content within a series of complex social scenes where faces are either included or digitally erased. Results indicated marked abnormalities in visual scanning for both disorders. Controls increased their gaze on face regions when faces were present to a significantly greater degree than both the autism or schizophrenia groups. While the control and the schizophrenia groups oriented to face regions faster when faces were present compared to when they were absent, the autism group oriented at the same rate in both conditions. The schizophrenia group, meanwhile, exhibited a delay in orienting to face regions across both conditions, although whether anti-psychotic medication contributed to this effect is unclear. These findings suggest that while processing emotional information in social scenes, both individuals with autism and individuals with schizophrenia fixate faces less than controls, although only those with autism fail to orient to faces more rapidly based on the presence of facial information. Autism and schizophrenia may therefore share an abnormality in utilizing facial information for assessing emotional content in social scenes, but differ in the ability to seek out socially relevant cues from complex stimuli. Impairments in social orienting are discussed within the context of evidence suggesting the role of the amygdala in orienting to emotionally meaningful information.
PMCID: PMC2128257  PMID: 17459428
Autism; Schizophrenia; eyetracking; social cognition; emotion; perception

Results 1-13 (13)