Stimulus-specific Information Research Articles

Widespread, perception-related information in the human brain scales with levels of consciousness

Abstract How does the human brain generate coherent, subjective perceptions—transforming yellow and oblong visual sensory information into the perception of an edible banana? This is a hard problem. According to the standard viewpoint, processing in groups of dedicated regions—identified as active “blobs” when using functional magnetic resonance imaging (fMRI)—gives rise to perception. Here, our research reveals a new organizational concept by discovering stimulus-specific information distributed throughout the whole brain. Using fMRI, we found stimulus-specific information across the neocortex, even in voxels previously considered “noise,” challenging traditional analytical approaches. Surprisingly, these stimulus-specific signals were also present in the subcortex and cerebellum and could be detected from across-subject variances. Additionally, we observed that the widespread signal in brain regions beyond the primary and secondary sensory cortices is influenced by sedation levels, suggesting a connection to perception rather than sensory encoding. We hypothesize that these widespread, stimulus-specific, and consciousness level-dependent signals may underlie coherent and subjective perceptions.

Coherent categorical information triggers integration-related alpha dynamics.

To create coherent visual experiences, the brain spatially integrates the complex and dynamic information it receives from the environment. We previously demonstrated that feedback-related alpha activity carries stimulus-specific information when two spatially and temporally coherent naturalistic inputs can be integrated into a unified percept. In this study, we sought to determine whether such integration-related alpha dynamics are triggered by categorical coherence in visual inputs. In an EEG experiment, we manipulated the degree of coherence by presenting pairs of videos from the same or different categories through two apertures in the left and right visual hemifields. Critically, video pairs could be video-level coherent (i.e., stem from the same video), coherent in their basic-level category, coherent in their superordinate category, or incoherent (i.e., stem from videos from two entirely different categories). We conducted multivariate classification analyses on rhythmic EEG responses to decode between the video stimuli in each condition. As the key result, we significantly decoded the video-level coherent and basic-level coherent stimuli, but not the superordinate coherent and incoherent stimuli, from cortical alpha rhythms. This suggests that alpha dynamics play a critical role in integrating information across space, and that cortical integration processes are flexible enough to accommodate information from different exemplars of the same basic-level category.NEW & NOTEWORTHY Our brain integrates dynamic inputs across the visual field to create coherent visual experiences. Such integration processes have previously been linked to cortical alpha dynamics. In this study, the integration-related alpha activity was observed not only when snippets from the same video were presented, but also when different video snippets from the same basic-level category were presented, highlighting the flexibility of neural integration processes.

Perceptual comparisons modulate memory biases induced by new visual inputs.

It is well-established that stimulus-specific information in visual working memory (VWM) can be systematically biased by new perceptual inputs. These memory biases are commonly attributed to interference that arises when perceptual inputs are physically similar to VWM contents. However, recent work has suggested that explicitly comparing the similarity between VWM contents and new perceptual inputs modulates the size of memory biases above and beyond stimulus-driven effects. Here, we sought to directly investigate this modulation hypothesis by comparing the size of memory biases following explicit comparisons to those induced when new perceptual inputs are ignored (Experiment 1) or maintained in VWM alongside target information (Experiment 2). We found that VWM reports showed larger attraction biases following explicit perceptual comparisons than when new perceptual inputs were ignored or maintained in VWM. An analysis of participants' perceptual comparisons revealed that memory biases were amplified after perceptual inputs were endorsed as similar-but not dissimilar-to one's VWM representation. These patterns were found to persist even after accounting for variability in the physical similarity between the target and perceptual stimuli across trials, as well as the baseline memory precision between the distinct task demands. Together, these findings illustrate a causal role of perceptual comparisons in modulating naturally-occurring memory biases.

The Representational Dynamics of Sequential Perceptual Averaging.

It is clear that humans can extract statistical information from streams of visual input, yet how our brain processes sequential images into the abstract representation of the mean feature value remains poorly explored. Using multivariate pattern analyses of electroencephalography recorded while human observers viewed 10 sequentially presented Gabors of different orientations to estimate their mean orientation at the end, we investigated sequential averaging mechanism by tracking the quality of individual and mean orientation as a function of sequential position. Critically, we varied the sequential variance of Gabor orientations to understand the neural basis of perceptual mean errors occurring during a sequential averaging task. We found that the mean-orientation representation emerged at specific delays from each sequential stimulus onset and became increasingly accurate as additional Gabors were viewed. Especially in frontocentral electrodes, the neural representation of mean orientation improved more rapidly and to a greater degree in less volatile environments, whereas individual orientation information was encoded precisely regardless of environmental volatility. The computational analysis of behavioral data also showed that perceptual mean errors arise from the cumulative construction of the mean orientation rather than the low-level encoding of individual stimulus orientation. Thus, our findings provide neural mechanisms to differentially accumulate increasingly abstract features from a concrete piece of information across the cortical hierarchy depending on environmental volatility.SIGNIFICANCE STATEMENT The visual system extracts behaviorally relevant summary statistical representation by exploiting statistical regularity of the visual stream over time. However, how the neural representation of the abstract mean feature value develops in a temporally changing environment remains poorly identified. Here, we directly recover the mean orientation information of sequentially delivered Gabor stimuli with different orientations as a function of their positions in time. The mean orientation representation, which is regularly updated, becomes increasingly accurate with increasing sequential position especially in the frontocentral region. Further, perceptual mean errors arise from the cumulative process rather than the low-level stimulus encoding. Overall, our study reveals a role of higher cortical areas in integrating stimulus-specific information into increasingly abstract task-oriented information.

Age effects on category learning, categorical perception, and generalization

ABSTRACT Age deficits in memory for individual episodes are well established. Less is known about how age affects another key memory function: the ability to form new conceptual knowledge. Here we studied age differences in concept formation in a category-learning paradigm with face-blend stimuli, using several metrics: direct learning of category members presented during training, generalisation of category labels to new examples, and shifts in perceived similarity between category members that often follow category learning. We found that older adults were impaired in direct learning of training examples, but that there was no significant age deficit in generalisation once we accounted for the deficit in direct learning. We also found that category learning affected the perceived similarity between members of the same versus opposing categories, and age did not significantly moderate this effect. Lastly, we compared traditional category learning to categorisation after a learning task in which a category label (shared last name) was presented alongside stimulus-specific information (unique first names that individuated category members). We found that simultaneously learning stimulus-specific and category information resulted in decreased category learning, and that this decrement was apparent in both age groups.

Electrical Signaling of Plants under Abiotic Stressors: Transmission of Stimulus-Specific Information.

Plants have developed complex systems of perception and signaling to adapt to changing environmental conditions. Electrical signaling is one of the most promising candidates for the regulatory mechanisms of the systemic functional response under the local action of various stimuli. Long-distance electrical signals of plants, such as action potential (AP), variation potential (VP), and systemic potential (SP), show specificities to types of inducing stimuli. The systemic response induced by a long-distance electrical signal, representing a change in the activity of a complex of molecular-physiological processes, includes a nonspecific component and a stimulus-specific component. This review discusses possible mechanisms for transmitting information about the nature of the stimulus and the formation of a specific systemic response with the participation of electrical signals induced by various abiotic factors.

Stimulation of the left dorsolateral prefrontal cortex with slow rTMS enhances verbal memory formation.

Encoding of episodic memories relies on stimulus-specific information processing and involves the left prefrontal cortex. We here present an incidental finding from a simultaneous EEG-TMS experiment as well as a replication of this unexpected effect. Our results reveal that stimulating the left dorsolateral prefrontal cortex (DLPFC) with slow repetitive transcranial magnetic stimulation (rTMS) leads to enhanced word memory performance. A total of 40 healthy human participants engaged in a list learning paradigm. Half of the participants (N = 20) received 1 Hz rTMS to the left DLPFC, while the other half (N = 20) received 1 Hz rTMS to the vertex and served as a control group. Participants receiving left DLPFC stimulation demonstrated enhanced memory performance compared to the control group. This effect was replicated in a within-subjects experiment where 24 participants received 1 Hz rTMS to the left DLPFC and vertex. In this second experiment, DLPFC stimulation also induced better memory performance compared to vertex stimulation. In addition to these behavioural effects, we found that 1 Hz rTMS to DLPFC induced stronger beta power modulation in posterior areas, a state that is known to be beneficial for memory encoding. Further analysis indicated that beta modulations did not have an oscillatory origin. Instead, the observed beta modulations were a result of a spectral tilt, suggesting inhibition of these parietal regions. These results show that applying 1 Hz rTMS to DLPFC, an area involved in episodic memory formation, improves memory performance via modulating neural activity in parietal regions.

Visual plasticity: Illuminating the role of the hippocampus in cortical sensory encoding

The primary visual cortex has the capacity to store stimulus-specific information locally. A new study reveals a direct role for the hippocampus in experience-dependent cortical plasticity when visual stimuli are presented in a predictable temporal order.

Probabilistic discrimination of relative stimulus features in mice

During perceptual decision-making, the brain encodes the upcoming decision and the stimulus information in a mixed representation. Paradigms suitable for studying decision computations in isolation rely on stimulus comparisons, with choices depending on relative rather than absolute properties of the stimuli. The adoption of tasks requiring relative perceptual judgments in mice would be advantageous in view of the powerful tools available for the dissection of brain circuits. However, whether and how mice can perform a relative visual discrimination task has not yet been fully established. Here, we show that mice can solve a complex orientation discrimination task in which the choices are decoupled from the orientation of individual stimuli. Moreover, we demonstrate a typical discrimination acuity of 9°, challenging the common belief that mice are poor visual discriminators. We reached these conclusions by introducing a probabilistic choice model that explained behavioral strategies in 40 mice and demonstrated that the circularity of the stimulus space is an additional source of choice variability for trials with fixed difficulty. Furthermore, history biases in the model changed with task engagement, demonstrating behavioral sensitivity to the availability of cognitive resources. In conclusion, our results reveal that mice adopt a diverse set of strategies in a task that decouples decision-relevant information from stimulus-specific information, thus demonstrating their usefulness as an animal model for studying neural representations of relative categories in perceptual decision-making research.

Neuronal selectivity to complex vocalization features emerges in the superficial layers of primary auditory cortex.

Early in auditory processing, neural responses faithfully reflect acoustic input. At higher stages of auditory processing, however, neurons become selective for particular call types, eventually leading to specialized regions of cortex that preferentially process calls at the highest auditory processing stages. We previously proposed that an intermediate step in how nonselective responses are transformed into call-selective responses is the detection of informative call features. But how neural selectivity for informative call features emerges from nonselective inputs, whether feature selectivity gradually emerges over the processing hierarchy, and how stimulus information is represented in nonselective and feature-selective populations remain open question. In this study, using unanesthetized guinea pigs (GPs), a highly vocal and social rodent, as an animal model, we characterized the neural representation of calls in 3 auditory processing stages-the thalamus (ventral medial geniculate body (vMGB)), and thalamorecipient (L4) and superficial layers (L2/3) of primary auditory cortex (A1). We found that neurons in vMGB and A1 L4 did not exhibit call-selective responses and responded throughout the call durations. However, A1 L2/3 neurons showed high call selectivity with about a third of neurons responding to only 1 or 2 call types. These A1 L2/3 neurons only responded to restricted portions of calls suggesting that they were highly selective for call features. Receptive fields of these A1 L2/3 neurons showed complex spectrotemporal structures that could underlie their high call feature selectivity. Information theoretic analysis revealed that in A1 L4, stimulus information was distributed over the population and was spread out over the call durations. In contrast, in A1 L2/3, individual neurons showed brief bursts of high stimulus-specific information and conveyed high levels of information per spike. These data demonstrate that a transformation in the neural representation of calls occurs between A1 L4 and A1 L2/3, leading to the emergence of a feature-based representation of calls in A1 L2/3. Our data thus suggest that observed cortical specializations for call processing emerge in A1 and set the stage for further mechanistic studies.

Decoding Concurrent Representations of Pitch and Location in Auditory Working Memory.

Multivariate analyses of hemodynamic signals serve to identify the storage of specific stimulus contents in working memory (WM). Representations of visual stimuli have been demonstrated both in sensory regions and in higher cortical areas. While previous research has typically focused on the WM maintenance of a single content feature, it remains unclear whether two separate features of a single object can be decoded concurrently. Also, much less evidence exists for representations of auditory compared with visual stimulus features. To address these issues, human participants had to memorize both pitch and perceived location of one of two sample sounds. After a delay phase, they were asked to reproduce either pitch or location. At recall, both features showed comparable levels of discriminability. Region of interest (ROI)-based decoding of functional magnetic resonance imaging (fMRI) data during the delay phase revealed feature-selective activity for both pitch and location of a memorized sound in auditory cortex and superior parietal lobule. The latter region showed higher decoding accuracy for location than pitch. In addition, location could be decoded from angular and supramarginal gyrus and both superior and inferior frontal gyrus. The latter region also showed a trend for decoding of pitch. We found no region exclusively coding pitch memory information. In summary, the present study yielded evidence for concurrent representations of pitch and location of a single object both in sensory cortex and in hierarchically higher regions, pointing toward representation formats that enable feature integration within the same anatomic brain regions.SIGNIFICANCE STATEMENT Decoding of hemodynamic signals serves to identify brain regions involved in the storage of stimulus-specific information in working memory (WM). While to-be-remembered information typically consists of several features, most previous investigations have focused on the maintenance of one memorized feature belonging to one visual object. The present study assessed the concurrent storage of two features of the same object in auditory WM. We found that both pitch and location of memorized sounds were decodable both in early sensory areas, in higher-level superior parietal cortex and, to a lesser extent, in inferior frontal cortex. While auditory cortex is known to process different features in parallel, their concurrent representation in parietal regions may support the integration of object features in WM.

Volitional learning promotes theta phase coding in the human hippocampus

Electrophysiological studies in rodents show that active navigation enhances hippocampal theta oscillations (4-12 Hz), providing a temporal framework for stimulus-related neural codes. Here we show that active learning promotes a similar phase coding regime in humans, although in a lower frequency range (3-8 Hz). We analyzed intracranial electroencephalography (iEEG) from epilepsy patients who studied images under either volitional or passive learning conditions. Active learning increased memory performance and hippocampal theta oscillations and promoted a more accurate reactivation of stimulus-specific information during memory retrieval. Representational signals were clustered to opposite phases of the theta cycle during encoding and retrieval. Critically, during active but not passive learning, the temporal structure of intracycle reactivations in theta reflected the semantic similarity of stimuli, segregating conceptually similar items into more distant theta phases. Taken together, these results demonstrate a multilayered mechanism by which active learning improves memory via a phylogenetically old phase coding scheme.

Mice Can Learn a Stimulus-Invariant Orientation Discrimination Task

Understanding how the brain computes choice from sensory information is a central question of perceptual decision-making. Relevant behavioral tasks condition choice on abstract or invariant properties of the stimuli, thus decoupling stimulus-specific information from the decision variable. Among visual tasks, orientation discrimination is a gold standard; however, it is not clear if a mouse – a recently popular animal model in visual decision-making research – can learn an invariant orientation discrimination task and what choice strategies it would use. Here we show that mice can solve a discrimination task where choices are decoupled from the orientation of individual stimuli, depending instead on a measure of relative orientation. Mice learned this task, reaching an upper bound for discrimination acuity of 6 degrees and relying on decision-making strategies that balanced cognitive resources with history-dependent biases. We analyzed behavioral data from n=40 animals with the help of a novel probabilistic choice model that we used to interpret individual biases and behavioral strategies. The model explained variation in performance with task difficulty and identified unreported dimensions of variation associated with the circularity of the stimulus space. Furthermore, it showed a larger effect of history biases on animals’ choices during periods of lower engagement. Our results demonstrate that mice can learn invariant perceptual representations by combining decision-relevant stimulus information decoupled from low-level visual features, with the computation of the decision variable dependent on the cognitive state.

Stimulus-specific information is represented as local activity patterns across the brain

Modern neuroimaging represents three-dimensional brain activity, which varies across brain regions. It remains unknown whether activity of different brain regions has similar spatial organization to reflect similar cognitive processes. We developed a rotational cross-correlation method allowing a straightforward analysis of spatial activity patterns distributed across the brain in stimulation specific contrast images. Results of this method were verified using several statistical approaches on real and simulated random datasets. We found, for example, that the seed patterns in the fusiform face area were robustly correlated to brain regions involved in face-specific representations. These regions differed from the non-specific visual network meaning that activity structure in the brain is locally preserved in stimulus-specific regions. Our findings indicate spatially correlated perceptual representations in cerebral activity and suggest that the 3D coding of the processed information is organized using locally preserved activity patterns across the brain. More generally, our results demonstrate that information is represented and shared in the local spatial configurations of brain activity.

Tonoplast-localized Ca2+ pumps regulate Ca2+ signals during pattern-triggered immunity in Arabidopsis thaliana

One of the major events of early plant immune responses is a rapid influx of Ca2+ into the cytosol following pathogen recognition. Indeed, changes in cytosolic Ca2+ are recognized as ubiquitous elements of cellular signaling networks and are thought to encode stimulus-specific information in their duration, amplitude, and frequency. Despite the wealth of observations showing that the bacterial elicitor peptide flg22 triggers Ca2+ transients, there remain limited data defining the molecular identities of Ca2+ transporters involved in shaping the cellular Ca2+ dynamics during the triggering of the defense response network. However, the autoinhibited Ca2+-ATPase (ACA) pumps that act to expel Ca2+ from the cytosol have been linked to these events, with knockouts in the vacuolar members of this family showing hypersensitive lesion-mimic phenotypes. We have therefore explored how the two tonoplast-localized pumps, ACA4 and ACA11, impact flg22-dependent Ca2+ signaling and related defense responses. The double-knockout aca4/11 exhibited increased basal Ca2+ levels and Ca2+ signals of higher amplitude than wild-type plants. Both the aberrant Ca2+ dynamics and associated defense-related phenotypes could be suppressed by growing the aca4/11 seedlings at elevated temperatures. Relocalization of ACA8 from its normal cellular locale of the plasma membrane to the tonoplast also suppressed the aca4/11 phenotypes but not when a catalytically inactive mutant was used. These observations indicate that regulation of vacuolar Ca2+ sequestration is an integral component of plant immune signaling, but also that the action of tonoplast-localized Ca2+ pumps does not require specific regulatory elements not found in plasma membrane-localized pumps.

Alpha/beta power decreases track the fidelity of stimulus-specific information.

Massed synchronised neuronal firing is detrimental to information processing. When networks of task-irrelevant neurons fire in unison, they mask the signal generated by task-critical neurons. On a macroscopic level, such synchronisation can contribute to alpha/beta (8-30 Hz) oscillations. Reducing the amplitude of these oscillations, therefore, may enhance information processing. Here, we test this hypothesis. Twenty-one participants completed an associative memory task while undergoing simultaneous EEG-fMRI recordings. Using representational similarity analysis, we quantified the amount of stimulus-specific information represented within the BOLD signal on every trial. When correlating this metric with concurrently-recorded alpha/beta power, we found a significant negative correlation which indicated that as post-stimulus alpha/beta power decreased, stimulus-specific information increased. Critically, we found this effect in three unique tasks: visual perception, auditory perception, and visual memory retrieval, indicating that this phenomenon transcends both stimulus modality and cognitive task. These results indicate that alpha/beta power decreases parametrically track the fidelity of both externally-presented and internally-generated stimulus-specific information represented within the cortex.

Nuclear calcium signatures are associated with root development

In plants, nuclear Ca2+ releases are essential to the establishment of nitrogen-fixing and phosphate-delivering arbuscular mycorrhizal endosymbioses. In the legume Medicago truncatula, these nuclear Ca2+ signals are generated by a complex of nuclear membrane-localised ion channels including the DOES NOT MAKE INFECTIONS 1 (DMI1) and the cyclic nucleotide-gated channels (CNGC) 15s. DMI1 and CNCG15s are conserved among land plants, suggesting roles for nuclear Ca2+ signalling that extend beyond symbioses. Here we show that nuclear Ca2+ signalling initiates in the nucleus of Arabidopsis root cells and that these signals are correlated with primary root development, including meristem development and auxin homeostasis. In addition, we demonstrate that altering genetically AtDMI1 is sufficient to modulate the nuclear Ca2+ signatures, and primary root development. This finding supports the postulate that stimulus-specific information can be encoded in the frequency and duration of a Ca2+ signal and thereby regulate cellular function.

Using intersection information to map stimulus information transfer within neural networks

Analytical tools that estimate the directed information flow between simultaneously recorded neural populations, such as directed information or Granger causality, typically focus on measuring how much information is exchanged between such populations. However, understanding how sensory information is processed through the brain and how it is used to generate behaviors requires estimating specifically the amount of stimulus information that is transmitted. Here we use the concept of intersection information to make progress on how to perform this measure. We develop the concept of transmitted intersection information, which measures how much of the stimulus information present in one population at a certain time is transmitted to a second population at a later time. We show that this measure of stimulus-specific information transfer has several appealing properties, such as being non-negative, and being bounded by the amount of stimulus information present in each of the two populations and by the total amount of information transmitted between the two populations. Applying this measure to simulated neurons or pools of neurons connected by feed-forward synapses, we show that it can discern cases when the information transmitted from one population to another is about specific stimulus features encoded by the sending population from cases in which the information transmitted is not about the stimuli. We also show that this measure has a good statistical sensitivity from trial numbers that can be collected in real data. Our results highlight the promise of using the concept of intersection information to map stimulus-specific information transfer across neural populations.

Cross-decoding supramodal information in the human brain.

Perceptual decision making is the cognitive process wherein the brain classifies stimuli into abstract categories for more efficient downstream processing. A system that, during categorization, can process information regardless of the information's original sensory modality (i.e., a supramodal system) would have a substantial advantage over a system with dedicated processes for specific sensory modalities. While many studies have probed decision processes through the lens of one sensory modality, it remains unclear whether there are such supramodal brain areas that can flexibly process task-relevant information regardless of the original "format" of the information. To investigate supramodality, one must ensure that supramodal information exists somewhere within the functional architecture by rendering information from multiple sensory systems necessary but insufficient for categorization. To this aim, we tasked participants with categorizing auditory and tactile frequency-modulated sweeps according to learned, supramodal categories in a delayed match-to-category paradigm while we measured their blood-oxygen-level dependent signal with functional MRI. To detect supramodal information, we implemented a set of cross-modality pattern classification analyses, which demonstrated that the left caudate nucleus encodes category-level information but not stimulus-specific information (such as spatial directions and stimulus modalities), while the right inferior frontal gyrus, showing the opposite pattern, encodes stimulus-specific information but not category-level information. Given our paradigm, these results reveal abstract representations in the brain that are independent of motor, semantic, and sensory-specific processing, instead reflecting supramodal, categorical information, which points to the caudate nucleus as a locus of cognitive processes involved in complex behavior.

Chronometry on Spike-LFP Responses Reveals the Functional Neural Circuitry of Early Auditory Cortex Underlying Sound Processing and Discrimination.

Animals and humans rapidly detect specific features of sounds, but the time courses of the underlying neural response for different stimulus categories is largely unknown. Furthermore, the intricate functional organization of auditory information processing pathways is poorly understood. Here, we computed neuronal response latencies from simultaneously recorded spike trains and local field potentials (LFPs) along the first two stages of cortical sound processing, primary auditory cortex (A1) and lateral belt (LB), of awake, behaving macaques. Two types of response latencies were measured for spike trains as well as LFPs: (1) onset latency, time-locked to onset of external auditory stimuli; and (2) selection latency, time taken from stimulus onset to a selective response to a specific stimulus category. Trial-by-trial LFP onset latencies predominantly reflecting synaptic input arrival typically preceded spike onset latencies, assumed to be representative of neuronal output indicating that both areas may receive input environmental signals and relay the information to the next stage. In A1, simple sounds, such as pure tones (PTs), yielded shorter spike onset latencies compared to complex sounds, such as monkey vocalizations (“Coos”). This trend was reversed in LB, indicating a hierarchical functional organization of auditory cortex in the macaque. LFP selection latencies in A1 were always shorter than those in LB for both PT and Coo reflecting the serial arrival of stimulus-specific information in these areas. Thus, chronometry on spike-LFP signals revealed some of the effective neural circuitry underlying complex sound discrimination.