Early Sensory Regions Research Articles

Manipulating attentional priority creates a trade-off between memory and sensory representations in human visual cortex.

People often remember visual information over brief delays while actively engaging with ongoing inputs from the surrounding visual environment. Depending on the situation, one might prioritize mnemonic contents (i.e., remembering details of a past event), or preferentially attend sensory inputs (i.e., minding traffic while crossing a street). Previous fMRI work has shown that early sensory regions can simultaneously represent both mnemonic and passively viewed sensory information. Here we test the limits of such simultaneity by manipulating attention towards sensory distractors during a working memory task performed by human subjects during fMRI scanning. Participants remembered the orientation of a target grating while a distractor grating was shown during the middle portion of the memory delay. Critically, there were several subtle changes in the contrast and the orientation of the distractor, and participants were cued to either ignore the distractor, detect a change in contrast, or detect a change in orientation. Despite sensory stimulation being matched in all three conditions, the fidelity of memory representations in early visual cortex was highest when the distractor was ignored, intermediate when participants attended distractor contrast, and lowest when participants attended the orientation of the distractor during the delay. In contrast, the fidelity of distractor representations was lowest when ignoring the distractor, intermediate when attending distractor-contrast, and highest when attending distractor-orientation. These data suggest a trade-off in early sensory representations when engaging top-down feedback to attend both seen and remembered features and may partially explain memory failures that occur when subjects are distracted by external events.

Task-specific invariant representation in auditory cortex.

Categorical sensory representations are critical for many behaviors, including speech perception. In the auditory system, categorical information is thought to arise hierarchically, becoming increasingly prominent in higher-order cortical regions. The neural mechanisms that support this robust and flexible computation remain poorly understood. Here, we studied sound representations in the ferret primary and non-primary auditory cortex while animals engaged in a challenging sound discrimination task. Population-level decoding of simultaneously recorded single neurons revealed that task engagement caused categorical sound representations to emerge in non-primary auditory cortex. In primary auditory cortex, task engagement caused a general enhancement of sound decoding that was not specific to task-relevant categories. These findings are consistent with mixed selectivity models of neural disentanglement, in which early sensory regions build an overcomplete representation of the world and allow neurons in downstream brain regions to flexibly and selectively read out behaviorally relevant, categorical information.

Sleep-like changes in neural processing emerge during sleep deprivation in early auditory cortex.

Insufficient sleep is commonplace in modern lifestyle and can lead to grave outcomes, yet the changes in neuronal activity accumulating over hours of extended wakefulness remain poorly understood. Specifically, which aspects of cortical processing are affected by sleep deprivation (SD), and whether they also affect early sensory regions, remain unclear. Here, we recorded spiking activity in the rat auditory cortex along with polysomnography while presenting sounds during SD followed by recovery sleep. We found that frequency tuning, onset responses, and spontaneous firing rates were largely unaffected by SD. By contrast, SD decreased entrainment to rapid (≥20Hz) click trains, increased population synchrony, and increased the prevalence of sleep-like stimulus-induced silent periods, even when ongoing activity was similar. Recovery NREM sleep was associated with similar effects as SD with even greater magnitude, while auditory processing during REM sleep was similar to vigilant wakefulness. Our results show that processes akin to those in NREM sleep invade the activity of cortical circuits during SD, even in the early sensory cortex.

Differences in working memory coding of biological motion attributed to oneself and others.

The question how the brain distinguishes between information about self and others is of fundamental interest to both philosophy and neuroscience. In this functional magnetic resonance imaging (fMRI) study, we sought to distinguish the neural substrates of representing a full‐body movement as one's movement and as someone else's movement. Participants performed a delayed match‐to‐sample working memory task where a retained full‐body movement (displayed using point‐light walkers) was arbitrarily labeled as one's own movement or as performed by someone else. By using arbitrary associations we aimed to address a limitation of previous studies, namely that our own movements are more familiar to us than movements of other people. A searchlight multivariate decoding analysis was used to test where information about types of movement and about self‐association was coded. Movement specific activation patterns were found in a network of regions also involved in perceptual processing of movement stimuli, however not in early sensory regions. Information about whether a memorized movement was associated with the self or with another person was found to be coded by activity in the left middle frontal gyrus (MFG), left inferior frontal gyrus (IFG), bilateral supplementary motor area, and (at reduced threshold) in the left temporoparietal junction (TPJ). These areas are frequently reported as involved in action understanding (IFG, MFG) and domain‐general self/other distinction (TPJ). Finally, in univariate analysis we found that selecting a self‐associated movement for retention was related to increased activity in the ventral medial prefrontal cortex.

Bifocal high-definition tACS over early sensory regions modulates crossmodal matching: Combined evidence from EEG and tACS/behavioral studies

Cross-talk between distant brain regions is an integral part of complex brain dynamics. In order to study such interactions, bifocal high-definition tACS (hd-tACS) represents a promising tool to modulate oscillatory synchrony between distant brain regions in a phase- and frequency-specific manner. Here, we investigated cortico-cortical synchronization in alpha and gamma bands underlying multisensory integration. First, we employed a paradigm on crossmodal matching in an EEG study to show that stimulus-driven benefits of crossmodal congruence are paralleled by decreases in gamma band coherence between early sensory cortices. Second, we used bifocal hd-tACS to target visual and somatosensory regions in a similar crossmodal matching paradigm. In- or anti-phase stimulation between the two regions (0°/180° phase shift) was applied with either 10 or 40 Hz and was controlled by sham. As an additional control, electrical stimulation was applied ipsilateral or contralateral to the presentation of visual-tactile stimuli. As hypothesized based on our EEG data, we found contralateral gamma stimulation to decrease behavioral benefits of crossmodal congruence compared with sham. To our surprise, both in- and anti-phase stimulation showed such an effect. We conclude that 40 Hz stimulation might have synchronized gamma band activity across modalities irrespective of stimulation phase. Ipsilateral stimulation showed no interaction with stimulus congruence. Yet, overall performance was increased by ipsilateral alpha and decreased by ipsilateral gamma stimulation. We suggest that, in the absence of sensory input, tACS modulated general cortical excitation/inhibition and related hemispheric competition. Taken together, we present evidence for the involvement of gamma synchronization in crossmodal matching. Our results further suggest that conventional approaches to decrease functional coupling by anti-phase tACS might not always be effective. Our study design – incorporating both EEG and behavioral studies – also demonstrates how acute effects of tACS can be studied bypassing the unsolved problem of tACS-related artifacts in electrophysiological recordings.

What you saw is what you will hear: Two new illusions with audiovisual postdictive effects.

Neuroscience investigations are most often focused on the prediction of future perception or decisions based on prior brain states or stimulus presentations. However, the brain can also process information retroactively, such that later stimuli impact conscious percepts of the stimuli that have already occurred (called “postdiction”). Postdictive effects have thus far been mostly unimodal (such as apparent motion), and the models for postdiction have accordingly been limited to early sensory regions of one modality. We have discovered two related multimodal illusions in which audition instigates postdictive changes in visual perception. In the first illusion (called the “Illusory Audiovisual Rabbit”), the location of an illusory flash is influenced by an auditory beep-flash pair that follows the perceived illusory flash. In the second illusion (called the “Invisible Audiovisual Rabbit”), a beep-flash pair following a real flash suppresses the perception of the earlier flash. Thus, we showed experimentally that these two effects are influenced significantly by postdiction. The audiovisual rabbit illusions indicate that postdiction can bridge the senses, uncovering a relatively-neglected yet critical type of neural processing underlying perceptual awareness. Furthermore, these two new illusions broaden the Double Flash Illusion, in which a single real flash is doubled by two sounds. Whereas the double flash indicated that audition can create an illusory flash, these rabbit illusions expand audition’s influence on vision to the suppression of a real flash and the relocation of an illusory flash. These new additions to auditory-visual interactions indicate a spatio-temporally fine-tuned coupling of the senses to generate perception.

Gray matter volumes of early sensory regions are associated with individual differences in sensory processing.

Sensory processing (i.e., the manner in which the nervous system receives, modulates, integrates, and organizes sensory stimuli) is critical when humans are deciding how to react to environmental demands. Although behavioral studies have shown that there are stable individual differences in sensory processing, the neural substrates that implement such differences remain unknown. To investigate this issue, structural magnetic resonance imaging scans were acquired from 51 healthy adults and individual differences in sensory processing were assessed using the Sensory Profile questionnaire (Brown et al.: Am J Occup Ther 55 (2001) 75-82). There were positive relationships between the Sensory Profile modality-specific subscales and gray matter volumes in the primary or secondary sensory areas for the visual, auditory, touch, and taste/smell modalities. Thus, the present results suggest that individual differences in sensory processing are implemented by the early sensory regions. Hum Brain Mapp 38:6206-6217, 2017. © 2017 Wiley Periodicals, Inc.

Population imaging at subcellular resolution supports specific and local inhibition by granule cells in the olfactory bulb.

Information processing in early sensory regions is modulated by a diverse range of inhibitory interneurons. We sought to elucidate the role of olfactory bulb interneurons called granule cells (GCs) in odor processing by imaging the activity of hundreds of these cells simultaneously in mice. Odor responses in GCs were temporally diverse and spatially disperse, with some degree of non-random, modular organization. The overall sparseness of activation of GCs was highly correlated with the extent of glomerular activation by odor stimuli. Increasing concentrations of single odorants led to proportionately larger population activity, but some individual GCs had non-monotonic relations to concentration due to local inhibitory interactions. Individual dendritic segments could sometimes respond independently to odors, revealing their capacity for compartmentalized signaling in vivo. Collectively, the response properties of GCs point to their role in specific and local processing, rather than global operations such as response normalization proposed for other interneurons.

Thalamocortical rhythms during a vibrotactile detection task

To explore the role of oscillatory dynamics of the somatosensory thalamocortical network in perception and decision making, we recorded the simultaneous neuronal activity in the ventral posterolateral nucleus (VPL) of the somatosensory thalamus and primary somatosensory cortex (S1) in two macaque monkeys performing a vibrotactile detection task. Actively detecting a vibrotactile stimulus and reporting its perception elicited a sustained poststimulus beta power increase in VPL and an alpha power decrease in S1, in both stimulus-present and stimulus-absent trials. These oscillatory dynamics in the somatosensory thalamocortical network depended on the behavioral context: they were stronger for the active detection condition than for a passive stimulation condition. Furthermore, contrasting stimulus-present vs. stimulus-absent responses, we found that poststimulus theta power increased in both VPL and S1, and alpha/beta power decreased in S1, reflecting the monkey's perceptual decision but not the motor response per se. Additionally, higher prestimulus alpha power in S1 correlated with an increased probability of the monkey reporting a stimulus, regardless of the actual presence of a stimulus. Thus, we found task-related modulations in oscillatory activity, not only in the neocortex but also in the thalamus, depending on behavioral context. Furthermore, oscillatory modulations reflected the perceptual decision process and subsequent behavioral response. We conclude that these early sensory regions, in addition to their primary sensory functions, may be actively involved in perceptual decision making.

Temporal scaling of neural responses to compressed and dilated natural speech

Different brain areas integrate information over different timescales, and this capacity to accumulate information increases from early sensory areas to higher order perceptual and cognitive areas. It is currently unknown whether the timescale capacity of each brain area is fixed or whether it adaptively rescales depending on the rate at which information arrives from the world. Here, using functional MRI, we measured brain responses to an auditory narrative presented at different rates. We asked whether neural responses to slowed (speeded) versions of the narrative could be compressed (stretched) to match neural responses to the original narrative. Temporal rescaling was observed in early auditory regions (which accumulate information over short timescales) as well as linguistic and extra-linguistic brain areas (which can accumulate information over long timescales). The temporal rescaling phenomenon started to break down for stimuli presented at double speed, and intelligibility was also impaired for these stimuli. These data suggest that 1) the rate of neural information processing can be rescaled according to the rate of incoming information, both in early sensory regions as well as in higher order cortexes, and 2) the rescaling of neural dynamics is confined to a range of rates that match the range of behavioral performance.

Multisensory Representation of Frequency across Audition and Touch: High Density Electrical Mapping Reveals Early Sensory-Perceptual Coupling

The frequency of environmental vibrations is sampled by two of the major sensory systems, audition and touch, notwithstanding that these signals are transduced through very different physical media and entirely separate sensory epithelia. Psychophysical studies have shown that manipulating frequency in audition or touch can have a significant cross-sensory impact on perceived frequency in the other sensory system, pointing to intimate links between these senses during computation of frequency. In this regard, the frequency of a vibratory event can be thought of as a multisensory perceptual construct. In turn, electrophysiological studies point to temporally early multisensory interactions that occur in hierarchically early sensory regions where convergent inputs from the auditory and somatosensory systems are to be found. A key question pertains to the level of processing at which the multisensory integration of featural information, such as frequency, occurs. Do the sensory systems calculate frequency independently before this information is combined, or is this feature calculated in an integrated fashion during preattentive sensory processing? The well characterized mismatch negativity, an electrophysiological response that indexes preattentive detection of a change within the context of a regular pattern of stimulation, served as our dependent measure. High-density electrophysiological recordings were made in humans while they were presented with separate blocks of somatosensory, auditory, and audio-somatosensory "standards" and "deviants," where the deviant differed in frequency. Multisensory effects were identified beginning at ∼200 ms, with the multisensory mismatch negativity (MMN) significantly different from the sum of the unisensory MMNs. This provides compelling evidence for preattentive coupling between the somatosensory and auditory channels in the cortical representation of frequency.

Evaluative vs. trait representation in intergroup social judgments: Distinct roles of anterior temporal lobe and prefrontal cortex

When interacting with someone from another social group, one's responses may be influenced by both stereotypes and evaluations. Given behavioral results suggesting that stereotypes and evaluative associations operate independently, we used fMRI to test whether these biases are mediated by distinct brain systems. White participants viewed pairs of Black or White faces and judged them based on an evaluation (who would you befriend?) or a stereotype-relevant trait (who is more likely to enjoy athletic activities?). Multi-voxel pattern analysis revealed that a predominantly occipital network represented race in a context-invariant manner. However, lateral orbitofrontal cortex preferentially represented race during friendship judgments, whereas anterior medial prefrontal cortex preferentially represented race during trait judgments. Furthermore, representation of race in left temporal pole correlated with a behavioral measure of evaluative bias during friendship judgments and, independently, a measure of stereotyping during trait judgments. Whereas early sensory regions represent race in an apparently invariant manner, representations in higher-level regions are multi-componential and context-dependent.

Task dependent anatomical connections underlie multisensory processing

Our senses interact in daily life through multisensory integration, facilitating perceptual processes and behavioral responses. Numerous multisensory regions have been identified in humans and animals, raising the question of whether a single mechanism can support the dynamic range of experiences and behaviors multisensory processing engenders. The most common neural mechanisms proposed to underlie multisensory processing include anatomical connections directly linking early sensory areas, indirect connections to higher-order multisensory regions, and functional connectivity between cortical areas. Here we examine the relationship between white matter connectivity, as assessed with diffusion tensor imaging and individual differences in two divergent forms of multisensory processing: the redundant-target effect (RTE), in which subjects’ behavior is facilitated by congruent multisensory information, and the sound-induced illusory flash (SIIF) paradigm, in which incongruent multisensory information elicits a novel percept. Behavioral results demonstrated strong intra-subject reliability of the RTE and SIIF paradigms, but no correlation in performance between the two tasks. Consistent with this behavioral finding, we identified distinct anatomical networks underlying these two forms of multisensory processing. Using a whole-brain analysis and contrasting anatomical models of multisensory processing, increased behavioral performance on the RTE was associated with increased connectivity between the superior parietal lobe and early sensory regions. Conversely, increased incidence of illusion on the SIIF paradigm was associated with increased connectivity directly between early auditory and visual areas. These results implicate a broad network of anatomical connections involved in task-dependent multisensory processes.

Sensitive Period for a Multimodal Response in Human Visual Motion Area MT/MST

The middle temporal complex (MT/MST) is a brain region specialized for the perception of motion in the visual modality. However, this specialization is modified by visual experience: after long-standing blindness, MT/MST responds to sound. Recent evidence also suggests that the auditory response of MT/MST is selective for motion. The developmental time course of this plasticity is not known. To test for a sensitive period in MT/MST development, we used fMRI to compare MT/MST function in congenitally blind, late-blind, and sighted adults. MT/MST responded to sound in congenitally blind adults, but not in late-blind or sighted adults, and not in an individual who lost his vision between ages of 2 and 3 years. All blind adults had reduced functional connectivity between MT/MST and other visual regions. Functional connectivity was increased between MT/MST and lateral prefrontal areas in congenitally blind relative to sighted and late-blind adults. These data suggest that early blindness affects the function of feedback projections from prefrontal cortex to MT/MST. We conclude that there is a sensitive period for visual specialization in MT/MST. During typical development, early visual experience either maintains or creates a vision-dominated response. Once established, this response profile is not altered by long-standing blindness.

General to specific development of functional activation in the cerebral cortexes of 2- to 3-month-old infants

A critical issue in the functional development of the cerebral cortex is whether cortical regions are functionally differentiated in early infancy. Although a growing number of neuroimaging studies have revealed that functional differentiation between early sensory and association regions of the cortex is already present at 3 months of age, it is unclear how functional regions per se emerge in the earlier developmental period. Here, we present 3 possible hypotheses regarding the functional development of the cerebral cortex as follows: (1) functionally differentiated regions are prespecified in the early developmental period; (2) functional activations appear in a hierarchical order from early sensory regions to the association regions; and (3) functional activation patterns change in a general-to-specific manner, thereby increasing the localization of regions activated by a particular stimulus and increasing the exclusivity of the response to specific stimuli within a particular cortical region. In the present study, we used multichannel near-infrared spectroscopy (NIRS) to measure cortical hemodynamic responses to 2 different video images of colorful mobile objects and black-and-white checkerboard pattern reversals over the occipital and prefrontal regions in awake 2-month-old infants. Both visual stimuli produced comparative activations over broad regions of the cortex including the early sensory and association regions, supporting the general-to-specific development (Hypothesis 3). This result suggests that functional cortical regions emerge between 2 and 3 months of age for visual perception.

Reductions in neural activity underlie behavioral components of repetition priming

Repetition priming is a nonconscious form of memory that is accompanied by reductions in neural activity when an experience is repeated. To date, however, there is no direct evidence that these neural reductions underlie the behavioral advantage afforded to repeated material. Here we demonstrate a causal linkage between neural and behavioral priming in humans. fMRI (functional magnetic resonance imaging) was used in combination with transcranial magnetic stimulation (TMS) to target and disrupt activity in the left frontal cortex during repeated classification of objects. Left-frontal TMS disrupted both the neural and behavioral markers of priming. Neural priming in early sensory regions was unaffected by left-frontal TMS--a finding that provides evidence for separable conceptual and perceptual components of priming.