Neocortical Layer 1: An Elegant Solution to Top-Down and Bottom-Up Integration.

Many of our daily activities, such as riding a bike to work or reading a book in a noisy cafe, and highly skilled activities, such as a professional playing a tennis match or a violin concerto, depend upon the ability of the brain to quickly make moment-to-moment adjustments to our behavior in response to the results of our actions. Particularly, they depend upon the ability of the neocortex to integrate the information provided by the sensory organs (bottom-up information) with internally generated signals such as expectations or attentional signals (top-down information). This integration occurs in pyramidal cells (PCs) and their long apical dendrite, which branches extensively into a dendritic tuft in layer 1 (L1). The outermost layer of the neocortex, L1 is highly conserved across cortical areas and species. Importantly, L1 is the predominant input layer for top-down information, relayed by a rich, dense mesh of long-range projections that provide signals to the tuft branches of the PCs. Here, we discuss recent progress in our understanding of the composition of L1 and review evidence that L1 processing contributes to functions such as sensory perception, cross-modal integration, controlling states of consciousness, attention, and learning.

Human-like scene interpretation by a guided counterstream processing.

In modeling vision, there has been a remarkable progress in recognizing a range of scene components, but the problem of analyzing full scenes, an ultimate goal of visual perception, is still largely open. To deal with complete scenes, recent work focused on the training of models for extracting the full graph-like structure of a scene. In contrast with scene graphs, humans' scene perception focuses on selected structures in the scene, starting with a limited interpretation and evolving sequentially in a goal-directed manner [G. L. Malcolm, I. I. A. Groen, C. I. Baker, Trends. Cogn. Sci. 20, 843-856 (2016)]. Guidance is crucial throughout scene interpretation since the extraction of full scene representation is often infeasible. Here, we present a model that performs human-like guided scene interpretation, using an iterative bottom-up, top-down processing, in a "counterstream" structure motivated by cortical circuitry. The process proceeds by the sequential application of top-down instructions that guide the interpretation process. The results show how scene structures of interest to the viewer are extracted by an automatically selected sequence of top-down instructions. The model shows two further benefits. One is an inherent capability to deal well with the problem of combinatorial generalization-generalizing broadly to unseen scene configurations, which is limited in current network models [B. Lake, M. Baroni, 35th International Conference on Machine Learning, ICML 2018 (2018)]. The second is the ability to combine visual with nonvisual information at each cycle of the interpretation process, which is a key aspect for modeling human perception as well as advancing AI vision systems.

Neural substrates of top-down processing during perceptual duration-based timing and beat-based timing.

Temporal context is a crucial factor in timing. Previous studies have revealed that the timing of regular stimuli, such as isochronous beats or rhythmic sequences (termed beat-based timing), activated the basal ganglia, whereas the timing of single intervals or irregular stimuli (termed duration-based timing) activated the cerebellum. We conducted a functional magnetic resonance imaging (fMRI) experiment to determine whether top-down processing of perceptual duration-based and beat-based timings affected brain activation patterns. Our participants listened to auditory sequences containing both single intervals and isochronous beats and judged either the duration of the intervals or the tempo of the beats. Whole-brain analysis revealed that both duration judgments and tempo judgments activated similar areas, including the basal ganglia and cerebellum, with no significant difference in the activated regions between the two conditions. In addition, an analysis of the regions of interest revealed no significant differences between the activation levels measured for the two tasks in the basal ganglia as well as the cerebellum. These results suggested that a set of common brain areas were involved in top-down processing of both duration judgments and tempo judgments. Our findings indicate that perceptual duration-based timing and beat-based timing are driven by stimulus regularity irrespective of top-down processing.

Using EEG to investigate the influence of boredom on prospective memory in top-down and bottom-up processing mechanisms for intelligent interaction.

We aimed to investigate the alpha (α) activity in operators experiencing boredom while performing prolonged monitoring and prospective memory tasks using different processing mechanisms. Fifty-four participants underwent electroencephalography (EEG) and were found to have poorer prospective memory performance under top-down conditions. Further, α power and synchronisation were higher during bottom-up than in top-down processes, revealing an inhibition effect of the former. Significant differences in brain regions and hemispheres were identified to distinguish different cognitive processes in both information-processing mechanisms. Thus, people are likely to cope with boredom differently in terms of top-down and bottom-up processes. Specifically, a higher attention level was reported during top-down processing, to mitigate the negative influences of boredom. Overall, this study provides EEG evidence which suggests that prospective memory can be enhanced in top-down processing during prolonged monitoring tasks by increasing the salience of cues.

Boredom is a growing problem as tasks requiring monitoring increase. We explored how people process information to perform prospective memory tasks while monitoring. The prospective memory was poorer during top-down processing, but stronger cortical activation indicated an inhibitory effect on inattention. Information-processing mechanisms are suggested for designing boredom interventions.

Information-seeking across auditory scenes by an echolocating dolphin.

Dolphins gain information through echolocation, a publicly accessible sensory system in which dolphins produce clicks and process returning echoes, thereby both investigating and contributing to auditory scenes. How their knowledge of these scenes contributes to their echoic information-seeking is unclear. Here, we investigate their top-down cognitive processes in an echoic matching-to-sample task in which targets and auditory scenes vary in their decipherability and shift from being completely unfamiliar to familiar. A blind-folded adult male dolphin investigated a target sample positioned in front of a hydrophone to allow recording of clicks, a measure of information-seeking and effort; the dolphin received fish for choosing an object identical to the sample from 3 alternatives. We presented 20 three-object sets, unfamiliar in the first five 18-trial sessions with each set. Performance accuracy and click counts varied widely across sets. Click counts of the four lowest-performance-accuracy/low-discriminability sets (X = 41%) and the four highest-performance-accuracy/high-discriminability sets (X = 91%) were similar at the first sessions' starts and then decreased for both kinds of scenes, although the decrease was substantially greater for low-discriminability sets. In four challenging-but-doable sets, number of clicks remained relatively steady across the 5 sessions. Reduced echoic effort with low-discriminability sets was not due to overall motivation: the differential relationship between click number and object-set discriminability was maintained when difficult and easy trials were interleaved and when objects from originally difficult scenes were grouped with more discriminable objects. These data suggest that dolphins calibrate their echoic information-seeking effort based on their knowledge and expectations of auditory scenes.

Evidence and implications of abnormal predictive coding in dementia.

The diversity of cognitive deficits and neuropathological processes associated with dementias has encouraged divergence in pathophysiological explanations of disease. Here, we review an alternative framework that emphasizes convergent critical features of cognitive pathophysiology. Rather than the loss of 'memory centres' or 'language centres', or singular neurotransmitter systems, cognitive deficits are interpreted in terms of aberrant predictive coding in hierarchical neural networks. This builds on advances in normative accounts of brain function, specifically the Bayesian integration of beliefs and sensory evidence in which hierarchical predictions and prediction errors underlie memory, perception, speech and behaviour. We describe how analogous impairments in predictive coding in parallel neurocognitive systems can generate diverse clinical phenomena, including the characteristics of dementias. The review presents evidence from behavioural and neurophysiological studies of perception, language, memory and decision-making. The reformulation of cognitive deficits in terms of predictive coding has several advantages. It brings diverse clinical phenomena into a common framework; it aligns cognitive and movement disorders; and it makes specific predictions on cognitive physiology that support translational and experimental medicine studies. The insights into complex human cognitive disorders from the predictive coding framework may therefore also inform future therapeutic strategies.

Flexible top-down modulation in human ventral temporal cortex.

Visual neuroscientists have long characterized attention as inducing a scaling or additive effect on fixed parametric functions describing neural responses (e.g., contrast response functions). Here, we instead propose that top-down effects are more complex and manifest in ways that depend not only on attention but also other cognitive processes involved in executing a task. To substantiate this theory, we analyze fMRI responses in human ventral temporal cortex (VTC) in a study where stimulus eccentricity and cognitive task are varied. We find that as stimuli are presented farther into the periphery, bottom-up stimulus-driven responses decline but top-down attentional enhancement increases substantially. This disproportionate enhancement of weak responses cannot be easily explained by conventional models of attention. Furthermore, we find that attentional effects depend on the specific cognitive task performed by the subject, indicating the influence of additional cognitive processes other than attention (e.g., decision-making). The effects we observe replicate in an independent experiment from the same study, and also generalize to a separate study involving different stimulus manipulations (contrast and phase coherence). Our results suggest that a quantitative understanding of top-down modulation requires more nuanced characterization of the multiple cognitive factors involved in completing a perceptual task.

Predictive processing: Is the future just a memory?

Predictive processing seems like a radical departure from traditional theories of information processing in the brain, but a broader view of predictions highlights many similarities with standard frameworks. Predictive processing is memory and competitive bias in a new outlook-and we should use this correspondence to advance research on both fronts.

Please empathize! Instructions to empathise strengthen response facilitation after pain observation.

Recent research has shown that observing others in pain leads to a general facilitation of reaction times. The current study sheds further light on the relationship between pain observation and reaction time by exploring how bottom-up processes, in the form of perceived pain intensity, and top-down processes, in the form of explicit instructions to empathise, influence response facilitation after pain observation. Participants watched videos of a hand getting pierced by a needle or touched by a Q-tip. To manipulate bottom-up information, participants saw videos depicting either deep or shallow insertion of the needle. To investigate potential top-down modulation, half the participants were explicitly requested to empathise with the person in the video, while the other half were told to simply watch and attend to the video. Results from two experiments corroborate previous results showing response facilitation after pain observation. Critically, experiment 2 provides robust evidence that explicit instructions to empathise with a person in pain strengthen response facilitation. We discuss these results considering social cognitive neuroscience and experimental psychology studies of empathy and pain observation.

Electrophysiological Evidence for Top-Down Lexical Influences on Early Speech Perception.

An unresolved issue in speech perception concerns whether top-down linguistic information influences perceptual responses. We addressed this issue using the event-related-potential technique in two experiments that measured cross-modal sequential-semantic priming effects on the auditory N1, an index of acoustic-cue encoding. Participants heard auditory targets (e.g., "potatoes") following associated visual primes (e.g., "MASHED"), neutral visual primes (e.g., "FACE"), or a visual mask (e.g., "XXXX"). Auditory targets began with voiced (/b/, /d/, /g/) or voiceless (/p/, /t/, /k/) stop consonants, an acoustic difference known to yield differences in N1 amplitude. In Experiment 1 (N = 21), semantic context modulated responses to upcoming targets, with smaller N1 amplitudes for semantic associates. In Experiment 2 (N = 29), semantic context changed how listeners encoded sounds: Ambiguous voice-onset times were encoded similarly to the voicing end point elicited by semantic associates. These results are consistent with an interactive model of spoken-word recognition that includes top-down effects on early perception.

An Upward-Facing Surface Appears Darker: The Role Played by the Light-From-Above Assumption in Lightness Perception.

The human visual system can extract information on surface reflectance (lightness) from light intensity; this, however, confounds information on reflectance and illumination. We hypothesized that the visual system, to solve this lightness problem, utilizes the internally held prior assumption that illumination falls from above. Experiment 1 showed that an upward-facing surface is perceived to be darker than a downward-facing surface, proving our hypothesis. Experiment 2 showed the same results in the absence of explicit illumination cues. The effect of the light-from-left prior assumption was not observed in Experiment 3. The upward- and downward-facing surface stimuli in Experiments 1 and 2 showed no difference in a two-dimensional configuration or three-dimensional structure, and the participants' perceived lightness appeared to be affected by the observers' prior assumption that illumination is always from above. Other studies have not accounted for this illusory effect, and this study's finding provides additional insights into the study of lightness perception.

Mechanically Induced Shaping of Organic Single Crystals: Facile Fabrication of Fluorescent and Elastic Crystal Fibers.

Mechanically induced shaping (i.e., top-down processing) of organic single crystals is an undeveloped area of research because applying stress to such nonflexible crystalline materials generally causes them to disintegrate. Herein, we present a mechanically induced splitting phenomenon of elastic organic single crystals, and study on a facile shaping processing method of centimeter-scale elastic organic single crystal of fluorescent π-conjugated molecule into various fine crystal fibers (thickness: ≈50 µm; width: ≈150 µm; length: ≈25 mm). The fibers produced maintained their original crystal structure and properties (i.e., fluorescence efficiency and elastic flexibility).

Delayed processing of global shape information is associated with weaker top-down effects in developmental prosopagnosia.

In previous studies we have shown that a group of individuals with developmental prosopagnosia (DP): (i) were impaired at recognizing objects when presented as silhouettes or fragmented forms; stimuli which place particular demands on global shape processing, (ii) that these impairments correlated with their face recognition deficit, (iii) that they showed a reduced global precedence effect in Navon's paradigm, and (iv) that the magnitude of their global precedence effect correlated with their face and object recognition performance. This pattern of deficits points towards a delay in the processing of global shape information; a delay that may weaken top-down influences on recognition performance. Here we show that the DPs show reduced real object superiority effects (faster responses to real objects than nonobjects) compared with controls. Given that real object superiority effects reflect top-down processing, these findings support the notion of impaired global shape based top-down processing in DP.

Reduced mind wandering in experienced meditators and associated EEG correlates.

One outstanding question in the contemplative science literature relates to the direct impact of meditation experience on the monitoring of internal states and its respective correspondence with neural activity. In particular, to what extent does meditation influence the awareness, duration and frequency of the tendency of the mind to wander. To assess the relation between mind wandering and meditation, we tested 2 groups of meditators, one with a moderate level of experience (non-expert) and those who are well advanced in their practice (expert). We designed a novel paradigm using self-reports of internal mental states based on an experiential sampling probe paradigm presented during ~1 h of seated concentration meditation to gain insight into the dynamic measures of electroencephalography (EEG) during absorption in meditation as compared to reported mind wandering episodes. Our results show that expert meditation practitioners report a greater depth and frequency of sustained meditation, whereas non-expert practitioners report a greater depth and frequency of mind wandering episodes. This is one of the first direct behavioral indices of meditation expertise and its associated impact on the reduced frequency of mind wandering, with corresponding EEG activations showing increased frontal midline theta and somatosensory alpha rhythms during meditation as compared to mind wandering in expert practitioners. Frontal midline theta and somatosensory alpha rhythms are often observed during executive functioning, cognitive control and the active monitoring of sensory information. Our study thus provides additional new evidence to support the hypothesis that the maintenance of both internal and external orientations of attention may be maintained by similar neural mechanisms and that these mechanisms may be modulated by meditation training.

Shift toward prior knowledge confers a perceptual advantage in early psychosis and psychosis-prone healthy individuals.

Many neuropsychiatric illnesses are associated with psychosis, i.e., hallucinations (perceptions in the absence of causative stimuli) and delusions (irrational, often bizarre beliefs). Current models of brain function view perception as a combination of two distinct sources of information: bottom-up sensory input and top-down influences from prior knowledge. This framework may explain hallucinations and delusions. Here, we characterized the balance between visual bottom-up and top-down processing in people with early psychosis (study 1) and in psychosis-prone, healthy individuals (study 2) to elucidate the mechanisms that might contribute to the emergence of psychotic experiences. Through a specialized mental-health service, we identified unmedicated individuals who experience early psychotic symptoms but fall below the threshold for a categorical diagnosis. We observed that, in early psychosis, there was a shift in information processing favoring prior knowledge over incoming sensory evidence. In the complementary study, we capitalized on subtle variations in perception and belief in the general population that exhibit graded similarity with psychotic experiences (schizotypy). We observed that the degree of psychosis proneness in healthy individuals, and, specifically, the presence of subtle perceptual alterations, is also associated with stronger reliance on prior knowledge. Although, in the current experimental studies, this shift conferred a performance benefit, under most natural viewing situations, it may provoke anomalous perceptual experiences. Overall, we show that early psychosis and psychosis proneness both entail a basic shift in visual information processing, favoring prior knowledge over incoming sensory evidence. The studies provide complementary insights to a mechanism by which psychotic symptoms may emerge.

How to (and how not to) think about top-down influences on visual perception.

The question of whether cognition can influence perception has a long history in neuroscience and philosophy. Here, we outline a novel approach to this issue, arguing that it should be viewed within the framework of top-down information-processing. This approach leads to a reversal of the standard explanatory order of the cognitive penetration debate: we suggest studying top-down processing at various levels without preconceptions of perception or cognition. Once a clear picture has emerged about which processes have influences on those at lower levels, we can re-address the extent to which they should be considered perceptual or cognitive. Using top-down processing within the visual system as a model for higher-level influences, we argue that the current evidence indicates clear constraints on top-down influences at all stages of information processing; it does, however, not support the notion of a boundary between specific types of information-processing as proposed by the cognitive impenetrability hypothesis.

Task context impacts visual object processing differentially across the cortex.

Perception reflects an integration of "bottom-up" (sensory-driven) and "top-down" (internally generated) signals. Although models of visual processing often emphasize the central role of feed-forward hierarchical processing, less is known about the impact of top-down signals on complex visual representations. Here, we investigated whether and how the observer's goals modulate object processing across the cortex. We examined responses elicited by a diverse set of objects under six distinct tasks, focusing on either physical (e.g., color) or conceptual properties (e.g., man-made). Critically, the same stimuli were presented in all tasks, allowing us to investigate how task impacts the neural representations of identical visual input. We found that task has an extensive and differential impact on object processing across the cortex. First, we found task-dependent representations in the ventral temporal and prefrontal cortex. In particular, although object identity could be decoded from the multivoxel response within task, there was a significant reduction in decoding across tasks. In contrast, the early visual cortex evidenced equivalent decoding within and across tasks, indicating task-independent representations. Second, task information was pervasive and present from the earliest stages of object processing. However, although the responses of the ventral temporal, prefrontal, and parietal cortex enabled decoding of both the type of task (physical/conceptual) and the specific task (e.g., color), the early visual cortex was not sensitive to type of task and could only be used to decode individual physical tasks. Thus, object processing is highly influenced by the behavioral goal of the observer, highlighting how top-down signals constrain and inform the formation of visual representations.

Visual Priming and Visual Hallucinations in Parkinson's Disease. Evidence for Normal Top-Down Processes.

BACKGROUND: Visual hallucinations (VH) are common in Parkinson's disease (PD) and are associated with increased morbidity and mortality. Current explanations for VH in PD suggest combined impairments in top-down attentional and bottom-up perceptual processes, which allow the passive "release" of stored images. Alternative models in other disorders have suggested that top-down factors may actively encourage hallucinations. In order to explore the interaction between top-down and bottom-up visual processing in PDVH, we developed novel experimental priming tasks in which top-down verbal cues were used to prime the bottom-up recognition of partial or ambiguous pictures. METHOD: Two groups of PD participants with (PD + VH, n = 16), and without VH (PD - VH, n = 20) were compared to a group of healthy older adults (NC, n = 20) on 3 novel measures of visual priming. RESULTS: All tasks showed significant priming effects. The PD + VH group was more impaired at accurately identifying silhouette and fragmented images compared to the PD - VH group. There were no differences in priming between the 2 PD groups. CONCLUSIONS: The study showed that VH in PD are not associated with relatively greater top-down activation, and that the interaction between top-down and bottom-up processes is intact.

Relationships between trait impulsivity and cognitive control: the effect of attention switching on response inhibition and conflict resolution.

This study examined the relationship between trait impulsivity and cognitive control, as measured by the Barratt Impulsiveness Scale (BIS) and a focused attention dichotic listening to words task, respectively. In the task, attention was manipulated in two attention conditions differing in their cognitive control demands: one in which attention was directed to one ear at a time for a whole block of trials (blocked condition) and another in which attention was switched pseudo-randomly between the two ears from trial to trial (mixed condition). Results showed that high impulsivity participants exhibited more false alarm and intrusion errors as well as a lesser ability to distinguish between stimuli in the mixed condition, as compared to low impulsivity participants. In the blocked condition, the performance levels of the two groups were comparable with respect to these measures. In addition, total BIS scores were correlated with intrusions and laterality index in the mixed but not the blocked condition. The findings suggest that high impulsivity individuals may be less prone to attentional difficulties when cognitive load is relatively low. In contrast, when attention switching is involved, high impulsivity is associated with greater difficulty in inhibiting responses and resolving cognitive conflict than is low impulsivity, as reflected in error-prone information processing. The conclusion is that trait impulsivity in a non-clinical population is manifested more strongly when attention switching is required than during maintained attention. This may have important implications for the conceptualization and treatment of impulsivity in both non-clinical and clinical populations.

Convergence of cortical and sensory driver inputs on single thalamocortical cells.

Ascending and descending information is relayed through the thalamus via strong, "driver" pathways. According to our current knowledge, different driver pathways are organized in parallel streams and do not interact at the thalamic level. Using an electron microscopic approach combined with optogenetics and in vivo physiology, we examined whether driver inputs arising from different sources can interact at single thalamocortical cells in the rodent somatosensory thalamus (nucleus posterior, POm). Both the anatomical and the physiological data demonstrated that ascending driver inputs from the brainstem and descending driver inputs from cortical layer 5 pyramidal neurons converge and interact on single thalamocortical neurons in POm. Both individual pathways displayed driver properties, but they interacted synergistically in a time-dependent manner and when co-activated, supralinearly increased the output of thalamus. As a consequence, thalamocortical neurons reported the relative timing between sensory events and ongoing cortical activity. We conclude that thalamocortical neurons can receive 2 powerful inputs of different origin, rather than only a single one as previously suggested. This allows thalamocortical neurons to integrate raw sensory information with powerful cortical signals and transfer the integrated activity back to cortical networks.