Parallel Processing Streams Research Articles

Primate brain: A unique connection between dorsal and ventral visual cortex

In humans and other primates, vision is subserved by at least two parallel processing streams that are interconnected through a pathway known as the vertical occipital fasciculus. New research reveals that this white matter pathway may be a unique feature of the primate brain.

A prominent vertical occipital white matter fasciculus unique to primate brains

Vision in humans and other primates enlists parallel processing streams in the dorsal and ventral visual cortex, known to support spatial and object processing, respectively. These streams are bridged, however, by a prominent white matter tract, the vertical occipital fasciculus (VOF), identified in both classical neuroanatomy and recent diffusion-weighted magnetic resonance imaging (dMRI) studies. Understanding the evolution of the VOF may shed light on its origin, function, and role in visually guided behaviors. To this end, we acquired high-resolution dMRI data from the brains of select mammalian species, including anthropoid and strepsirrhine primates, a tree shrew, rodents, and carnivores. In each species, we attempted to delineate the VOF after first locating the optic radiations in the occipital white matter. In all primate species examined, the optic radiation was flanked laterally by a prominent and coherent white matter fasciculus recognizable as the VOF. By contrast, the equivalent analysis applied to four non-primate species from the same superorder as primates (tree shrew, ground squirrel, paca, and rat) failed to reveal white matter tracts in the equivalent location. Clear evidence for a VOF was also absent in two larger carnivore species (ferret and fox). Although we cannot rule out the existence of minor or differently organized homologous fiber pathways in the non-primate species, the results suggest that the VOF has greatly expanded, or possibly emerged, in the primate lineage. This adaptation likely facilitated the evolution of unique visually guided behaviors in primates, with direct impacts on manual object manipulation, social interactions, and arboreal locomotion.

Scene-selectivity in CA1/subicular complex: Multivoxel pattern analysis at 7T

Prior univariate functional magnetic resonance imaging (fMRI) studies in humans suggest that the anteromedial subicular complex of the hippocampus is a hub for scene-based cognition. However, it is possible that univariate approaches were not sufficiently sensitive to detect scene-related activity in other subfields that have been implicated in spatial processing (e.g., CA1). Further, as connectivity-based functional gradients in the hippocampus do not respect classical subfield boundary definitions, category selectivity may be distributed across anatomical subfields. Region-of-interest approaches, therefore, may limit our ability to observe category selectivity across discrete subfield boundaries. To address these issues, we applied searchlight multivariate pattern analysis to 7T fMRI data of healthy adults who undertook a simultaneous visual odd-one-out discrimination task for scene and non-scene (including face) visual stimuli, hypothesising that scene classification would be possible in multiple hippocampal regions within, but not constrained to, anteromedial subicular complex and CA1. Indeed, we found that the scene-selective searchlight map overlapped not only with anteromedial subicular complex (distal subiculum, pre/para subiculum), but also inferior CA1, alongside posteromedial (including retrosplenial) and parahippocampal cortices. Probabilistic overlap maps revealed gradients of scene category selectivity, with the strongest overlap located in the medial hippocampus, converging with searchlight findings. This was contrasted with gradients of face category selectivity, which had stronger overlap in more lateral hippocampus, supporting ideas of parallel processing streams for these two categories. Our work helps to map the scene, in contrast to, face processing networks within, and connected to, the human hippocampus.

Poster Session: The impact of retinal excitotoxic lesions on parallel visual streams in the ferret dorsal lateral geniculate nucleus.

Attesting to the relative strength of retinal inputs to the dorsal lateral geniculate nucleus (LGN) of the thalamus, in cats, acute retinal lesions erase responses of LGN neurons whose receptive fields fall within the retinal lesion projection zone (LPZ). Yet, thirty days later, these receptive fields appear to shift their representation to the immediate surround of the LPZ. However, little is known about whether LGN neurons in parallel streams are equally affected following retinal damage. Here, we asked whether changes in response properties of surviving LGN neurons depend on (1) their identity as either X/Y or ON/OFF cells, or (2) their receptive fields' positions relative to the LPZ. To test these hypotheses, we made retinal lesions by injecting kainic acid (KA) into one eye of ferrets and recorded from LGN neurons bilaterally in response to visual stimuli 7 days post-lesion. Area and eccentricities of retinal ganglion cell (RGC) loss in the retina were measured by RBPMS immunostaining. Relative eccentricities of recorded LGN neurons were based on electrode tracts. Our preliminary data suggest that RGC with large cell bodies are preserved in the lesioned eye. Additionally, we observed normal transient responses but altered sustained responses to flashing stimuli among contralateral responsive OFF LGN neurons. Together, these findings support the notion that acute KA lesions may differentially impact visual parallel processing streams at the surround of the LPZ in the LGN.

Deep Spiking Neural Networks with High Representation Similarity Model Visual Pathways of Macaque and Mouse

Deep artificial neural networks (ANNs) play a major role in modeling the visual pathways of primate and rodent. However, they highly simplify the computational properties of neurons compared to their biological counterparts. Instead, Spiking Neural Networks (SNNs) are more biologically plausible models since spiking neurons encode information with time sequences of spikes, just like biological neurons do. However, there is a lack of studies on visual pathways with deep SNNs models. In this study, we model the visual cortex with deep SNNs for the first time, and also with a wide range of state-of-the-art deep CNNs and ViTs for comparison. Using three similarity metrics, we conduct neural representation similarity experiments on three neural datasets collected from two species under three types of stimuli. Based on extensive similarity analyses, we further investigate the functional hierarchy and mechanisms across species. Almost all similarity scores of SNNs are higher than their counterparts of CNNs with an average of 6.6%. Depths of the layers with the highest similarity scores exhibit little differences across mouse cortical regions, but vary significantly across macaque regions, suggesting that the visual processing structure of mice is more regionally homogeneous than that of macaques. Besides, the multi-branch structures observed in some top mouse brain-like neural networks provide computational evidence of parallel processing streams in mice, and the different performance in fitting macaque neural representations under different stimuli exhibits the functional specialization of information processing in macaques. Taken together, our study demonstrates that SNNs could serve as promising candidates to better model and explain the functional hierarchy and mechanisms of the visual system.

Dual counterstream architecture may support separation between vision and predictions

According to a predictive coding framework, visual processing involves the computation of prediction errors between sensory data and a generative model that is supplied via feedback projections. This implies that vision is cognitively penetrable by all sorts of top-down influences. In this paper, we review anatomical and functional data which suggest that feedforward and feedback projections are organized into two parallel processing streams: the supragranular and the infragranular counterstreams. The supragranular counterstream computes surface and motion representation in depth. It represents the best interpretation of what is given in the input image based on physical regularities that are built into this network. By contrast, the infragranular counterstream integrates vision with cognition, because it represents what is likely to be found in the environment based on the predictions derived from learned statistical regularities. The two counterstreams work in parallel, but independently of each other. They compete for dominance, and only one is allowed to deliver its output to higher-order areas at any instance of time. Such an arrangement allows the supragranular counterstream to remain cognitively impenetrable to top-down influences.

Contextual Modulation of Feedforward Inputs to Primary Visual Cortex.

Throughout the brain, parallel processing streams compose the building blocks of complex neural functions. One of the most salient models for studying the functional specialization of parallel visual streams in the primate brain is the lateral geniculate nucleus (LGN) of the dorsal thalamus, through which the parvocellular and magnocellular channels, On-center and Off-center channels, and ipsilateral and contralateral eye channels are maintained and provide the foundation for cortical processing. We examined three aspects of neural processing in these streams: (1) the relationship between extraclassical surround suppression, a widespread visual computation thought to represent a canonical neural computation, and the parallel channels of the LGN; (2) the magnitude of binocular interaction in the parallel streams; and (3) the magnitude of suppression elicited by perceptual competition (binocular rivalry) in each stream. Our results show that surround suppression is almost exclusive to Off channel cells; further, we found evidence for two different components of monocular surround suppression—an early-stage suppression exhibited by all magnocellular cells, and a late-stage suppression exhibited only by Off cells in both the parvocellular and magnocellular pathways. This finding indicates that stream-specific circuits contribute to surround suppression in the primate LGN and suggests a distinct role for suppression in the Off channel to the cortex. We also examined the responses of LGN neurons in alert macaque monkeys to determine whether neurons that supply the cortex with visual information are influenced by stimulation of both eyes. Our results demonstrate that LGN neurons are not influenced by stimulation of the non-dominant eye. This was the case when dichoptic stimuli were presented to classical receptive fields of neurons, extraclassical receptive fields of neurons, and when stimuli were appropriate to produce the perception of binocular rivalry.

Functional Organization of Frontoparietal Cortex in the Marmoset Investigated with Awake Resting-State fMRI.

Frontoparietal networks contribute to complex cognitive functions in humans and macaques, such as working memory, attention, task-switching, response suppression, grasping, reaching, and eye movement control. However, there has been no comprehensive examination of the functional organization of frontoparietal networks using functional magnetic resonance imaging in the New World common marmoset monkey (Callithrix jacchus), which is now widely recognized as a powerful nonhuman primate experimental animal. In this study, we employed hierarchical clustering of interareal blood oxygen level-dependent signals to investigate the hypothesis that the organization of the frontoparietal cortex in the marmoset follows the organizational principles of the macaque frontoparietal system. We found that the posterior part of the lateral frontal cortex (premotor regions) was functionally connected to the anterior parietal areas, while more anterior frontal regions (frontal eye field [FEF]) were connected to more posterior parietal areas (the region around the lateral intraparietal area [LIP]). These overarching patterns of interareal organization are consistent with a recent macaque study. These findings demonstrate parallel frontoparietal processing streams in marmosets and support the functional similarities of FEF-LIP and premotor-anterior parietal pathways between marmoset and macaque.

Parallel cognitive processing streams in human prefrontal cortex: Parsing areal-level brain network for response inhibition.

Multiple cognitive processes are recruited to achieve adaptive behavior. However, it is poorly understood how such cognitive processes are implemented in temporal cascades of human cerebral cortical areas as processing streams to achieve behavior. In the present study, we identify cortical processing streams for response inhibition and examine relationships among the processing streams. Functional magnetic resonance imaging (MRI) and time-resolved single-pulse transcranial magnetic stimulation (TMS) reveal three distinct critical timings of transient disruption in the functionally essential cortical areas that belong to two distinct cerebrocortical networks. Furthermore, single-pulse TMS following suppression of the ventral posterior inferior frontal cortex (vpIFC) with repetitive TMS reveals information flow from the vpIFC to the presupplementary motor area (preSMA) within the same network but not to the dorsal posterior inferior frontal cortex (dpIFC) across different networks. These causal behavioral effects suggest two parallel processing streams (vpIFC-preSMA versus dpIFC-intraparietal sulcus) that act concurrently during response inhibition.

F3RNet: full-resolution residual registration network for deformable image registration

Deformable image registration (DIR) is essential for many image-guided therapies. Recently, deep learning approaches have gained substantial popularity and success in DIR. Most deep learning approaches use the so-called mono-stream high-to-low, low-to-high network structure and can achieve satisfactory overall registration results. However, accurate alignments for some severely deformed local regions, which are crucial for pinpointing surgical targets, are often overlooked. Consequently, these approaches are not sensitive to some hard-to-align regions, e.g., intra-patient registration of deformed liver lobes. We propose a novel unsupervised registration network, namely full-resolution residual registration network (F3RNet), for deformable registration of severely deformed organs. The proposed method combines two parallel processing streams in a residual learning fashion. One stream takes advantage of the full-resolution information that facilitates accurate voxel-level registration. The other stream learns the deep multi-scale residual representations to obtain robust recognition. We also factorize the 3D convolution to reduce the training parameters and enhance network efficiency. We validate the proposed method on a clinically acquired intra-patient abdominal CT-MRI dataset and a public inspiratory and expiratory thorax CT dataset. Experiments on both multimodal and unimodal registration demonstrate promising results compared to state-of-the-art approaches. By combining the high-resolution information and multi-scale representations in a highly interactive residual learning fashion, the proposed F3RNet can achieve accurate overall and local registration. The run time for registering a pair of images is less than 3 s using a GPU. In future works, we will investigate how to cost-effectively process high-resolution information and fuse multi-scale representations.

Mouse Higher Visual Areas Provide Both Distributed and Specialized Contributions to Visually Guided Behaviors

Cortical parallel processing streams segregate many diverse features of a sensory scene. However, some features are distributed across streams, begging the question of whether and how such distributed representations contribute to perception. We determined the necessity of the primary visual cortex (V1) and three key higher visual areas (lateromedial [LM], anterolateral [AL], and posteromedial [PM]) for perception of orientation and contrast, two features that are robustly encoded across all four areas. Suppressing V1, LM, or AL decreased sensitivity for both orientation discrimination and contrast detection, consistent with a role for these areas in sensory perception. In comparison, suppressing PM selectively increased false alarm (FA) rates during contrast detection, without any effect on orientation discrimination. This effect was not retinotopically specific, suggesting that suppression of PM altered sensory integration or the decision-making process rather than processing of local visual features. Thus, we find that distributed representations in the visual system can nonetheless support specialized perceptual roles for higher visual cortical areas.

Circuit Mechanisms Underlying the Segregation and Integration of Parallel Processing Streams in the Inferior Colliculus.

The lateral cortex of the inferior colliculus (LCIC) forms a nexus between diverse multisensory, motor, and neuromodulatory streams. Like other integration hubs, it contains repeated neurochemical motifs with distinct inputs: GABA-rich modules are innervated by somatosensory structures, while auditory inputs to the LCIC target the surrounding extramodular matrix. To investigate potential mechanisms of convergence between these input streams, we used laser photostimulation circuit mapping to interrogate local LCIC circuits in adult mice of both sexes and found that input patterns are highly dependent on cell type (GABAergic/non-GABAergic) and location (module/matrix). At the circuit level, these inputs yield a directional flow of local information, primarily from the matrix to the modules. Further, the two compartments were found to project to distinct targets in the midbrain and thalamus. These data show that, while connectional modularity in the LCIC gives rise to segregated input-output channels, local circuits provide the architecture for integration between these two streams.SIGNIFICANCE STATEMENT Modularity is a widespread motif across the brain involving the segregation of structures into discrete subregions based on dichotomies in neurochemical expression or connectivity. The inferior colliculus is one such modular structure, containing auditory-recipient matrix regions and GABA-rich modules that are innervated by somatosensory inputs. While modularity suggests segregation of processing streams, here we show that local circuits in the inferior colliculus connect the module and matrix regions, providing an avenue for integration of information across compartments.

Parallel processing streams in the hippocampus.

The hippocampus performs two complementary processes, pattern separation and pattern completion, to minimize interference and maximize the storage capacity of memories. Classic computational models have suggested that the dentate gyrus (DG) supports pattern separation and the putative attractor circuitry in CA3 supports pattern completion. However, recent evidence of functional heterogeneity along the CA3 transverse axis of the hippocampus suggests that the DG and proximal CA3 work as a functional unit for pattern separation, while distal CA3 forms an autoassociative network for pattern completion. We propose that the outputs of these functional circuits, combined with direct projections from entorhinal cortex to CA1, form interconnected, parallel processing circuits to support accurate memory storage and retrieval.

Network Architecture of Gap Junctional Coupling among Parallel Processing Channels in the Mammalian Retina.

Gap junctions are ubiquitous throughout the nervous system, mediating critical signal transmission and integration, as well as emergent network properties. In mammalian retina, gap junctions within the Aii amacrine cell-ON cone bipolar cell (CBC) network are essential for night vision, modulation of day vision, and contribute to visual impairment in retinal degenerations, yet neither the extended network topology nor its conservation is well established. Here, we map the network contribution of gap junctions using a high-resolution connectomics dataset of an adult female rabbit retina. Gap junctions are prominent synaptic components of ON CBC classes, constituting 5%-25% of all axonal synaptic contacts. Many of these mediate canonical transfer of rod signals from Aii cells to ON CBCs for night vision, and we find that the uneven distribution of Aii signals to ON CBCs is conserved in rabbit, including one class entirely lacking direct Aii coupling. However, the majority of gap junctions formed by ON CBCs unexpectedly occur between ON CBCs, rather than with Aii cells. Such coupling is extensive, creating an interconnected network with numerous lateral paths both within, and particularly across, these parallel processing streams. Coupling patterns are precise with ON CBCs accepting and rejecting unique combinations of partnerships according to robust rulesets. Coupling specificity extends to both size and spatial topologies, thereby rivaling the synaptic specificity of chemical synapses. These ON CBC coupling motifs dramatically extend the coupled Aii-ON CBC network, with implications for signal flow in both scotopic and photopic retinal networks during visual processing and disease.SIGNIFICANCE STATEMENT Electrical synapses mediated by gap junctions are fundamental components of neural networks. In retina, coupling within the Aii-ON CBC network shapes visual processing in both the scotopic and photopic networks. In retinal degenerations, these same gap junctions mediate oscillatory activity that contributes to visual impairment. Here, we use high-resolution connectomics strategies to identify gap junctions and cellular partnerships. We describe novel, pervasive motifs both within and across classes of ON CBCs that dramatically extend the Aii-ON CBC network. These motifs are highly specific with implications for both signal processing within the retina and therapeutic interventions for blinding conditions. These findings highlight the underappreciated contribution of coupling motifs in retinal circuitry and the necessity of their detection in connectomics studies.

Heterogeneous Temporal Contrast Adaptation in Drosophila Direction-Selective Circuits.

In visual systems, neurons adapt both to the mean light level and to the range of light levels, or the contrast. Contrast adaptation has been studied extensively, but it remains unclear how it is distributed among neurons in connected circuits, and how early adaptation affects subsequent computations. Here, we investigated temporal contrast adaptation in neurons across Drosophila's visual motion circuitry. Several ON-pathway neurons showed strong adaptation to changes in contrast over time. One of these neurons, Mi1, showed almost complete adaptation on fast timescales, and experiments ruled out several potential mechanisms for its adaptive properties. When contrast adaptation reduced the gain in ON-pathway cells, it was accompanied by decreased motion responses in downstream direction-selective cells. Simulations show that contrast adaptation can substantially improve motion estimates in natural scenes. The benefits are larger for ON-pathway adaptation, which helps explain the heterogeneous distribution of contrast adaptation in these circuits.

Triple model of auditory sensory processing: a novel gating stream directly links primary auditory areas to executive prefrontal cortex.

SUMMARYThe generally accepted model of sensory processing of visual and auditory stimuli assumes two major parallel processing streams, ventral and dorsal, which comprise functionally and anatomically distinct but interacting processes in which the ventral stream supports stimulus identification, and the dorsal stream is involved in recognizing the stimulus spatial location and sensori-motor integration functions. However, recent studies suggest the existence of a third, very fast sensory processing pathway, a gating stream that directly links the primary auditory cortices to the executive prefrontal cortex within the first 50 milliseconds after presentation of a stimulus, bypassing hierarchical structure of the ventral and dorsal pathways. Gating stream propagates the sensory gating phenomenon, which serves as a basic protective mechanism preventing irrelevant, repeated information from recurrent sensory processing. The goal of the present paper is to introduce the novel ‘three-stream’ model of auditory processing, including the new fast sensory processing stream, i.e. gating stream, alongside the well-affirmed dorsal and ventral sensory processing pathways. The impairments in sensory processing along the gating stream have been found to be strongly involved in the pathophysiological sensory processing in Alzheimer’s disease and could be the underlying issue in numerous neuropsychiatric disorders and diseases that are linked to the pathological sensory gating inhibition, such as schizophrenia, post-traumatic stress disorder, bipolar disorder or attention deficit hyperactivity disorder.

The Psychophysical Assessment of Hierarchical Magno-, Parvo- and Konio-Cellular Visual Stream Dysregulations in Migraineurs.

IntroductionAlthough conscious, image-forming illusions have been noted in migraine, few studies have specifically sought to collectively evaluate the role of all three parallel visual processing streams in the retinogeniculostriate pathway involved with image-forming vision and their implications in the development of migraine symptoms.MethodsWe psychophysically assessed the functionality of the inferred magnocellular (MC), parvocellular (PC), and koniocellular (KC) streams at different hierarchical loci across three clinical groups: individuals who experience migraine with aura (MA; n=13), experience migraine without aura (MWO; n=14), and Controls (n=15). Participants completed four experiments: Experiment 1 designed to assess retinal short-wavelength-sensitive (S-) cone sensitivities; Experiment 2 intended to measure postretinal temporal and spatiochromatic contrast sensitivities; Experiment 3 intended to assess postretinal spatiotemporal achromatic contrast sensitivities; and Experiment 4 designed to measure thalamocortical color discriminations along the three cone-excitation axes.ResultsS-cone deficits were revealed with greater retinal areas being affected in MA compared to MWO participants. Findings across the four experiments suggest a prominent retinal locus of dysfunction in MA (lesser in MWO) with potential feedforward compensations occurring within the KC visual stream.ConclusionComplex, integrative network compensations need to be factored in when considering the dysregulating influences of migraine along the visual pathway.

Perceiving emotion and sex from the body: evidence from the Garner task for independent processes

ABSTRACTThe appearance of the body signals socially relevant states and traits, but the how these cues are perceived is not well understood. Here we examined judgments of emotion and sex from the body’s appearance. Understanding how we extract these cues is important because they are both salient and socially relevant. Participants viewed body images and either reported the emotion expressed by each body while ignoring its sex, or else reported the sex while ignoring its emotion. Following Garner’s logic, two types of blocks were compared. In control blocks, the task-irrelevant dimension was fixed (e.g. all male in an emotion judgment task), whereas in orthogonal blocks it varied orthogonally to the task-relevant dimension (e.g. male-female). Where two dimensions draw on shared processes, interference results in relatively slower responses during orthogonal blocks. In contrast, a finding of no Garner interference – efficient selection of the task-relevant dimension – is taken to reflect independent processes. Bayesian analyses revealed evidence of no Garner interference between sex and emotion judgments, showing that extraction of these distinct signals from the body’s appearance proceeds along largely parallel processing streams. These findings are informative about the mental architecture behind our perception of socially relevant characteristics of other people.

Variability and stability of large-scale cortical oscillation patterns.

Individual differences in brain organization exist at many spatiotemporal scales and underlie the diversity of human thought and behavior. Oscillatory neural activity is crucial for these processes, but how such rhythms are expressed across the cortex within and across individuals is poorly understood. We conducted a systematic characterization of brain-wide activity across frequency bands and oscillatory features during rest and task execution. We found that oscillatory profiles exhibit sizable group-level similarities, indicating the presence of common templates of oscillatory organization. Nonetheless, well-defined subject-specific network profiles were discernible beyond the structure shared across individuals. These individualized patterns were sufficiently stable to recognize individuals several months later. Moreover, network structure of rhythmic activity varied considerably across distinct oscillatory frequencies and features, indicating the existence of several parallel information processing streams embedded in distributed electrophysiological activity. These findings suggest that network similarity analyses may be useful for understanding the role of large-scale brain oscillations in physiology and behavior.

Increased functional connectivity in the ventral and dorsal streams during retrieval of novel words in professional musicians.

Current models of speech and language processing postulate the involvement of two parallel processing streams (the dual stream model): a ventral stream involved in mapping sensory and phonological representations onto lexical and conceptual representations and a dorsal stream contributing to sound-to-motor mapping, articulation, and to how verbal information is encoded and manipulated in memory. Based on previous evidence showing that music training has an influence on language processing, cognitive functions, and word learning, we examined EEG-based intracranial functional connectivity in the ventral and dorsal streams while musicians and nonmusicians learned the meaning of novel words through picture-word associations. In accordance with the dual stream model, word learning was generally associated with increased beta functional connectivity in the ventral stream compared to the dorsal stream. In addition, in the linguistically most demanding "semantic task," musicians outperformed nonmusicians, and this behavioral advantage was accompanied by increased left-hemispheric theta connectivity in both streams. Moreover, theta coherence in the left dorsal pathway was positively correlated with the number of years of music training. These results provide evidence for a complex interplay within a network of brain regions involved in semantic processing and verbal memory functions, and suggest that intensive music training can modify its functional architecture leading to advantages in novel word learning.