Human visual consciousness involves large scale cortical and subcortical networks independent of task report and eye movement activity.

The full neural circuits of conscious perception remain unknown. Using a visual perception task, we directly recorded a subcortical thalamic awareness potential (TAP). We also developed a unique paradigm to classify perceived versus not perceived stimuli using eye measurements to remove confounding signals related to reporting on conscious experiences. Using fMRI, we discovered three major brain networks driving conscious visual perception independent of report: first, increases in signal detection regions in visual, fusiform cortex, and frontal eye fields; and in arousal/salience networks involving midbrain, thalamus, nucleus accumbens, anterior cingulate, and anterior insula; second, increases in frontoparietal attention and executive control networks and in the cerebellum; finally, decreases in the default mode network. These results were largely maintained after excluding eye movement-based fMRI changes. Our findings provide evidence that the neurophysiology of consciousness is complex even without overt report, involving multiple cortical and subcortical networks overlapping in space and time.

More than a feeling: Scalp EEG and eye signals in conscious tactile perception.

Understanding the neural basis of consciousness is a fundamental goal of neuroscience, and sensory perception is often used as a proxy for consciousness in empirical studies. However, most studies rely on reported perception of visual stimuli. Here we present behavior, high density scalp EEG and eye metric recordings collected simultaneously during a novel tactile threshold perception task. We found significant N80, N140 and P300 event related potentials in perceived trials and in perceived versus not perceived trials. Significance was limited to a P100 and P300 in not perceived trials. We also found an increase in pupil diameter and blink rate and a decrease in microsaccade rate following perceived relative to not perceived tactile stimuli. These findings support the use of eye metrics as a measure of physiological arousal associated with conscious perception. Eye metrics may also represent a novel path toward the creation of tactile no-report tasks in the future.

Early cortical signals in visual stimulus detection.

During visual conscious perception, the earliest responses linked to signal detection are little known. The current study aims to reveal the cortical neural activity changes in the earliest stages of conscious perception using recordings from intracranial electrodes. Epilepsy patients (N=158) were recruited from a multi-center collaboration and completed a visual word recall task. Broadband gamma activity (40-115Hz) was extracted with a band-pass filter and gamma power was calculated across subjects on a common brain surface. Our results show early gamma power increases within 0-50ms after stimulus onset in bilateral visual processing cortex, right frontal cortex (frontal eye fields, ventral medial/frontopolar, orbital frontal) and bilateral medial temporal cortex regardless of whether the word was later recalled. At the same early times, decreases were seen in the left rostral middle frontal gyrus. At later times after stimulus onset, gamma power changes developed in multiple cortical regions. These included sustained changes in visual and other association cortical networks, and transient decreases in the default mode network most prominently at 300-650ms. In agreement with prior work in this verbal memory task, we also saw greater increases in visual and medial temporal regions as well as prominent later (> 300ms) increases in left hemisphere language areas for recalled versus not recalled stimuli. These results suggest an early signal detection network in the frontal, medial temporal, and visual cortex is engaged at the earliest stages of conscious visual perception.

The Contribution of Primary Auditory Cortex to Auditory Categorization in Behaving Monkeys.

The specific contribution of core auditory cortex to auditory perception -such as categorization- remains controversial. To identify a contribution of the primary auditory cortex (A1) to perception, we recorded A1 activity while monkeys reported whether a temporal sequence of tone bursts was heard as having a "small" or "large" frequency difference. We found that A1 had frequency-tuned responses that habituated, independent of frequency content, as this auditory sequence unfolded over time. We also found that A1 firing rate was modulated by the monkeys' reports of "small" and "large" frequency differences; this modulation correlated with their behavioral performance. These findings are consistent with the hypothesis that A1 contributes to the processes underlying auditory categorization.

Contribution of spiking activity in the primary auditory cortex to detection in noise.

A fundamental problem in hearing is detecting a "target" stimulus (e.g., a friend's voice) that is presented with a noisy background (e.g., the din of a crowded restaurant). Despite its importance to hearing, a relationship between spiking activity and behavioral performance during such a "detection-in-noise" task has yet to be fully elucidated. In this study, we recorded spiking activity in primary auditory cortex (A1) while rhesus monkeys detected a target stimulus that was presented with a noise background. Although some neurons were modulated, the response of the typical A1 neuron was not modulated by the stimulus- and task-related parameters of our task. In contrast, we found more robust representations of these parameters in population-level activity: small populations of neurons matched the monkeys' behavioral sensitivity. Overall, these findings are consistent with the hypothesis that the sensory evidence, which is needed to solve such detection-in-noise tasks, is represented in population-level A1 activity and may be available to be read out by downstream neurons that are involved in mediating this task.NEW & NOTEWORTHY This study examines the contribution of A1 to detecting a sound that is presented with a noisy background. We found that population-level A1 activity, but not single neurons, could provide the evidence needed to make this perceptual decision.

Neural correlates of auditory scene analysis and perception.

The auditory system is designed to transform acoustic information from low-level sensory representations into perceptual representations. These perceptual representations are the computational result of the auditory system's ability to group and segregate spectral, spatial and temporal regularities in the acoustic environment into stable perceptual units (i.e., sounds or auditory objects). Current evidence suggests that the cortex-specifically, the ventral auditory pathway-is responsible for the computations most closely related to perceptual representations. Here, we discuss how the transformations along the ventral auditory pathway relate to auditory percepts, with special attention paid to the processing of vocalizations and categorization, and explore recent models of how these areas may carry out these computations.

Natural variability in species-specific vocalizations constrains behavior and neural activity.

A listener's capacity to discriminate between sounds is related to the amount of acoustic variability that exists between these sounds. However, a full understanding of how this natural variability impacts neural activity and behavior is lacking. Here, we tested monkeys' ability to discriminate between different utterances of vocalizations from the same acoustic class (i.e., coos and grunts), while neural activity was simultaneously recorded in the anterolateral belt region (AL) of the auditory cortex, a brain region that is a part of a pathway that mediates auditory perception. Monkeys could discriminate between coos better than they could discriminate between grunts. We also found AL activity was more informative about different coos than different grunts. This difference could be attributed, in part, to our finding that coos had more acoustic variability than grunts. Thus, intrinsic acoustic variability constrained the discriminability of AL spike trains and the ability of rhesus monkeys to discriminate between vocalizations.

Behavioral correlates of auditory streaming in rhesus macaques.

Perceptual representations of auditory stimuli (i.e., sounds) are derived from the auditory system's ability to segregate and group the spectral, temporal, and spatial features of auditory stimuli-a process called "auditory scene analysis". Psychophysical studies have identified several of the principles and mechanisms that underlie a listener's ability to segregate and group acoustic stimuli. One important psychophysical task that has illuminated many of these principles and mechanisms is the "streaming" task. Despite the wide use of this task to study psychophysical mechanisms of human audition, no studies have explicitly tested the streaming abilities of non-human animals using the standard methodologies employed in human-audition studies. Here, we trained rhesus macaques to participate in the streaming task using methodologies and controls similar to those presented in previous human studies. Overall, we found that the monkeys' behavioral reports were qualitatively consistent with those of human listeners, thus suggesting that this task may be a valuable tool for future neurophysiological studies.

Modulation of cross-frequency coupling by novel and repeated stimuli in the primate ventrolateral prefrontal cortex.

Adaptive behavior depends on an animal's ability to ignore uninformative stimuli, such as repeated presentations of the same stimulus, and, instead, detect informative, novel stimuli in its environment. The primate prefrontal cortex (PFC) is known to play a central role in this ability. However, the neural mechanisms underlying the ability to differentiate between repeated and novel stimuli are not clear. We hypothesized that the coupling between different frequency bands of the local field potential (LFP) underlies the PFC's role in differentiating between repeated and novel stimuli. Specifically, we hypothesized that whereas the presentation of a novel-stimulus induces strong cross-frequency coupling, repeated presentations of the same stimulus attenuates this coupling. To test this hypothesis, we recorded LFPs from the ventrolateral PFC (vPFC) of rhesus monkeys while they listened to a novel vocalization and repeated presentations of the same vocalization. We found that the cross-frequency coupling between the gamma-band amplitude and theta-band phase of the LFP was modulated by repeated presentations of a stimulus. During the first (novel) presentation of a stimulus, gamma-band activity was modulated by the theta-band phase. However, with repeated presentations of the same stimulus, this cross-frequency coupling was attenuated. These results suggest that cross-frequency coupling may play a role in the neural computations that underlie the differentiation between novel and repeated stimuli in the vPFC.