Ventral Striatal Pathway Determines Actions Employed: A Computational Model

Despite their anatomical and functional distinctions, there is growing evidence that the dorsal and ventral visual pathways interact to support object recognition. However, the exact nature of these interactions remains poorly understood. Is the presence of identity-relevant object information in the dorsal pathway simply a byproduct of ventral input? Or, might the dorsal pathway be a source of input to the ventral pathway for object recognition? In the current study, we used high-density EEG—a technique with high temporal precision and spatial resolution sufficient to distinguish parietal and temporal lobes—to characterise the dynamics of dorsal and ventral pathways during object viewing. Using multivariate analyses, we found that category decoding in the dorsal pathway preceded that in the ventral pathway. Importantly, the dorsal pathway predicted the multivariate responses of the ventral pathway in a time-dependent manner, rather than the other way around. Together, these findings suggest that the dorsal pathway is a critical source of input to the ventral pathway for object recognition.

Reading proficiency influences the effects of transcranial direct current stimulation: Evidence from selective modulation of dorsal and ventral pathways of reading in bilinguals

Although shape perception is primarily considered a function of the ventral visual pathway, previous research has shown that both dorsal and ventral pathways represent shape information. Here, we examine whether the shape-selective electrophysiological signals observed in dorsal cortex are a product of the connectivity to ventral cortex or are independently computed. We conducted multiple EEG studies in which we manipulated the input parameters of the stimuli so as to bias processing to either the dorsal or ventral visual pathway. Participants viewed displays of common objects with shape information parametrically degraded across five levels. We measured shape sensitivity by regressing the amplitude of the evoked signal against the degree of stimulus scrambling. Experiment 1, which included grayscale versions of the stimuli, served as a benchmark establishing the temporal pattern of shape processing during typical object perception. These stimuli evoked broad and sustained patterns of shape sensitivity beginning as early as 50 msec after stimulus onset. In Experiments 2 and 3, we calibrated the stimuli such that visual information was delivered primarily through parvocellular inputs, which mainly project to the ventral pathway, or through koniocellular inputs, which mainly project to the dorsal pathway. In the second and third experiments, shape sensitivity was observed, but in distinct spatio-temporal configurations from each other and from that elicited by grayscale inputs. Of particular interest, in the koniocellular condition, shape selectivity emerged earlier than in the parvocellular condition. These findings support the conclusion of distinct dorsal pathway computations of object shape, independent from the ventral pathway.

Early involvement of dorsal and ventral pathways in visual word recognition: An ERP study

Absolute pitch (AP) is the ability to recognize pitch chroma of tonal sound without external references, providing a unique model of the human auditory system (Zatorre: Nat Neurosci 6 () 692-695). In a previous study (Kim and Knösche: Hum Brain Mapp () 3486-3501), we identified enhanced intracortical myelination in the right planum polare (PP) in musicians with AP, which could be a potential site for perceptional processing of pitch chroma information. We speculated that this area, which initiates the ventral auditory pathway, might be crucially involved in the perceptual stage of the AP process in the context of the "dual pathway hypothesis" that suggests the role of the ventral pathway in processing nonspatial information related to the identity of an auditory object (Rauschecker: Eur J Neurosci 41 () 579-585). To test our conjecture on the ventral pathway, we investigated resting state functional connectivity (RSFC) using functional magnetic resonance imaging (fMRI) from musicians with varying degrees of AP. Should our hypothesis be correct, RSFC via the ventral pathway is expected to be stronger in musicians with AP, whereas such group effect is not predicted in the RSFC via the dorsal pathway. In the current data, we found greater RSFC between the right PP and bilateral anteroventral auditory cortices in musicians with AP. In contrast, we did not find any group difference in the RSFC of the planum temporale (PT) between musicians with and without AP. We believe that these findings support our conjecture on the critical role of the ventral pathway in AP recognition. Hum Brain Mapp 38:3899-3916, 2017. © 2017 Wiley Periodicals, Inc.

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The purpose of this study is to return to Freud’s original descriptions of the primary and secondary processes in the light of modern neurosciences. In his Project for a Scientific Psychology, Freud draws the axes of the architecture of a mental apparatus: on a horizontal plane, the primary process transfers the excitation by impinging stimuli over a sequence of analogous states towards their discharge; thus, the primary process is essentially characterized by its associative tendency. On a vertical plane, the secondary process opposes the primary bottom-up pressure by a top-down inhibition with its origins in the purposive idea: the secondary process is essentially characterized by its inhibitory interventions. Freud later proposed that the primary and secondary process are seeking for perceptual, respectively thought identity. These different elements are coherent with the dynamics of the ventral and dorsal brain pathways respectively. Moreover, the dorsal pathway has an inhibitory influence upon the ventral pathway, much like the secondary has upon the primary. This influence is exerted thanks to what Freud called the “indications of reality.” We propose to equate these indications with the efference copies in modern neurosciences since they proceed from the same physiology and have the same function, besides originating from the same Helmholtzian source. Finally, even if both primary and secondary processes serve the death drive through the pleasure and the reality principle respectively, only the secondary process, requiring the bearing of an accumulation of excitations, also serves the life drive.

Traumatic brain injury (TBI) produces microstructural damage to white matter pathways connecting neural structures in pre-frontal and striatal regions involved in self-regulation (SR). Dorsal and ventral frontostriatal pathways have been linked to cognitive ("cool") and emotional ("hot") SR, respectively. We evaluated the relation of frontostriatal pathway fractional anisotropy (FA) 2 months post-TBI on cool and hot SR assessed 7 months post-TBI. Participants were 8-15 years of age, including children with uncomplicated mild TBI (mTBI; n = 24), more severe TBI (complicated-mild, moderate, severe [cms]TBI; n = 60), and typically developing (TD) children (n = 55). Diffusion tensor tractography was used to map frontostriatal pathways. Cool SR included focused and sustained attention performance, and parent-reported attention, whereas hot SR included risk-taking performance and parent-reported emotional control. Multivariate general linear models showed that children with cmsTBI had greater parent-reported cool and hot SR difficulties and lower dorsal and ventral FA than TD children. Focused attention, risk taking, and emotional control correlated with FA of specific dorsal and ventral pathways; however, only the effect of TBI on focused attention was mediated by integrity of dorsal pathways. Results suggest that frontostriatal FA may serve as a biomarker of risk for SR difficulties or to assess response to interventions targeting SR in pediatric TBI and in broader neurodevelopmental populations.

Although shape perception is considered a function of the ventral visual pathway, evidence suggests that the dorsal pathway also derives shape-based representations. In two psychophysics and neuroimaging experiments, we characterized the response properties, topographical organization and perceptual relevance of these representations. In both pathways, shape sensitivity increased from early visual cortex to extrastriate cortex but then decreased in anterior regions. Moreover, the lateral aspect of the ventral pathway and posterior regions of the dorsal pathway were sensitive to the availability of fundamental shape properties, even for unrecognizable images. This apparent representational similarity between the posterior-dorsal and lateral-ventral regions was corroborated by a multivariate analysis. Finally, as with ventral pathway, the activation profile of posterior dorsal regions was correlated with recognition performance, suggesting a possible contribution to perception. These findings challenge a strict functional dichotomy between the pathways and suggest a more distributed model of shape processing.

The division of labor between the dorsal and ventral visual pathways has been well studied, but not often with direct comparison at the single-neuron resolution with matched stimuli. Here we directly compared how single neurons in MT and V4, mid-tier areas of the two pathways, process binocular disparity, a powerful cue for 3D perception and actions. We found that MT neurons transmitted disparity signals more quickly and robustly, whereas V4 or its upstream neurons transformed the signals into sophisticated representations more prominently. Therefore, signaling speed and robustness were traded for transformation between the dorsal and ventral pathways. The key factor in this tradeoff was disparity-tuning shape: V4 neurons had more even-symmetric tuning than MT neurons. Moreover, the tuning symmetry predicted the degree of signal transformation across neurons similarly within each area, implying a general role of tuning symmetry in the stereoscopic processing by the two pathways.

An expanded neural framework for shape perception.

Reading normal and degraded words: Contribution of the dorsal and ventral visual pathways

A recently developed anatomical model describes how the intensity of reward-seeking and misery-fleeing behaviours is regulated. The first type of behaviours is regulated within an extrapyramidal cortical-subcortical circuit containing as first relay stations, the caudate nucleus, putamen and core of the accumbens nucleus. The second type of behaviours is controlled by a limbic cortical-subcortical circuit with as first stations, the centromedial amygdala, extended amygdala, bed nucleus of the stria terminalis and shell of the accumbens nucleus. We hypothesize that sudden cessation of hyperactivity of the first circuit results in feelings of pleasure and of the second circuit in feelings of happiness. The insular cortex has probably an essential role in the perception of these and other emotions. Motivation to show these behaviours is regulated by monoaminergic neurons projecting to the accumbens from the midbrain: dopaminergic ventral tegmental nuclei, adrenergic locus coeruleus and serotonergic upper raphe nuclei. The activity of these monoaminergic nuclei is in turn regulated through a ventral pathway by the prefrontal cortex and through a dorsal pathway by the medial and lateral habenula. The habenula has this role since the first vertebrate human ancestors with a brain comparable to that of modern lampreys. The lateral habenula promotes or inhibits reward-seeking behaviours depending upon the gained reward being larger or smaller than expected. It is suggested that the ventral pathway is essential for maintaining addiction based on the observation of specific cues, while the dorsal pathway is essential for becoming addicted and relapsing during periods of abstinence.

An evolving view in cognitive neuroscience is that the dorsal visual pathway not only plays a key role in visuomotor behavior but that it also contributes functionally to the recognition of objects. To characterize the nature of the object representations derived by the dorsal pathway, we assessed perceptual performance in the context of the continuous flash suppression paradigm, which suppresses object processing in the ventral pathway while sparing computation in the dorsal pathway. In a series of experiments, prime stimuli, which were rendered imperceptible by the continuous flash suppression, still contributed to perceptual decisions related to the subsequent perceptible target stimuli. However, the contribution of the prime to perception was contingent on the prime's structural coherence, in that a perceptual advantage was observed only for targets primed by objects with legitimate 3-D structure. Finally, we obtained additional evidence to demonstrate that the processing of the suppressed objects was contingent on the magnocellular, rather than the parvocellular, system, further linking the processing of the suppressed stimuli to the dorsal pathway. Together, these results provide novel evidence that the dorsal pathway does not only support visuomotor control but, rather, that it also derives the structural description of 3-D objects and contributes to shape perception.

Functional object use requires the integration of visuomotor representations processed in the dorsal visual pathway with representations of surface texture and material composition of objects, processed in the ventral visual pathway. Do regions in the ventral visual pathway project outputs to dorsal visual pathway action systems, or are the outputs of the dorsal visual pathway communicated to the ventral visual pathway to modulate processing? And what are the white matter pathways that mediate structural connectivity in support of functional object use? Here we show that the left inferior parietal cortex, a region within the dorsal visual pathway, exerts a direct effect on neural responses in ventral occipital-temporal cortex during visual processing of manipulable objects. We studied a series of consecutively enrolled participants in the pre-operative phase of their neurosurgical care (N = 109) with lesions principally distributed throughout the left hemisphere. Participants completed an object processing category localizer functional MRI experiment in which they viewed images of manipulable objects, animals, faces, and places. We then used Voxel-based Lesion-Activity Mapping (VLAM), a technique in which functional responses in a region-of-interest are used to predict variance in voxel-wise lesion incidence throughout the brain. In the VLAM analyses performed here, we found that lesions to the left anterior intraparietal sulcus and left supramarginal gyrus, two inferior parietal regions known to support object-directed grasping and manipulation, respectively, cause reduced neural responses for manipulable objects (compared to faces, places and animals) in the fusiform gyrus. Parietal lesions do not affect neural responses during visual processing of places in the same region of the fusiform gyrus, even though places elicit stronger responses in the fusiform gyrus than manipulable objects. Seventy-five of 109 participants took part in a common diffusion MRI protocol, permitting a connectome-wide analyses relating white matter fiber integrity to the strength of functional responses for manipulable objects in the left fusiform gyrus. This analysis demonstrated that the descending portion of the left arcuate fasciculus mediates parietal-totemporal lobe connectivity for manipulable objects, supporting the integration of action representations with conceptual and perceptual attributes of objects. By combining voxel-based and connectome-wide lesion-symptom mapping methods with functional MRI, we have demonstrated that structural connectivity to dorsal visual pathway areas supporting skilled manual action shape category-specific neural responses for manipulable objects within the ventral visual pathway.