Does primate motion perception depend on the magnocellular pathway?

This study examined the importance of the primate magnocellular retinocortical pathway in the perception of moving stimuli. A portion of the magnocellular pathway was permanently and selectively interrupted by ibotenic acid injections in the LGN of macaque monkeys. We then tested contrast sensitivity for detecting moving stimuli, as well as two indices of motion perception, contrast sensitivity for opposite direction discrimination and speed difference thresholds, in the affected portion of the visual field. Magnocellular lesions greatly reduced detection contrast sensitivity at high temporal and low spatial frequencies and had a similar effect on contrast sensitivity for opposite direction discrimination under these same stimulus conditions. Consequently, opposite direction discriminations could be made at contrast threshold, suggesting that magnocellular lesions reduced the visibility of stimuli used to test direction perception, but did not act directly on direction perception. Magnocellular lesions also elevated speed difference thresholds under some stimulus conditions. However, this deficit was reduced or eliminated by raising the contrast of the test stimulus. Together, these findings suggest that magnocellular lesions reduce the visibility of stimuli used to test motion perception but that they do not appear to alter motion perception otherwise.     

Motion integration deficits are independent of magnocellular impairment in Parkinson's disease

Motion processing involves multiple hierarchical steps, from the magnocellular pathway, sensitive to high temporal frequency modulations, to subsequent motion integration within the visual cortical dorsal stream. We have tested whether motion integration deficits in mild Parkinson disease (PD) can be explained by visual deficits in earlier processing nodes. Contrast sensitivity deficits in the magnocellular pathway, were compared with speed discrimination of local dots moving in random directions, speed and direction discrimination of moving surfaces and motion integration as measured by 2D coherence thresholds (n = 27). We have found that low-level magnocellular impairment in PD does not explain deficits in subsequent steps in motion processing. High-level performance was abnormal in particular for tasks requiring perception of coherently moving surfaces. Motion coherence deficits were predictive of visuomotor impairment, corroborating a previous magnetic stimulation study in normal subjects. We conclude that dorsal stream deficits in PD have a high-level visual cortical basis independent of low-level magnocellular damage.     

A few remarks on attention and magnocellular deficits in schizophrenia

In connection with schizophrenia, it has been proposed that the magnocellular system is specifically linked to the guiding of covert visual attention. The argument is that the magnocellular pathway provides input to the dorsal cortical stream which then projects back to area V1. We review problems with this model. (1) It requires that responses in the magnocellular system have a lead time over responses in the parvocellular system. However, measurements indicate that the actual response time difference between the two systems is small or negligible when entering the visual cortex. (2) Attention can be modified by stimuli that do not activate the magnocellular system. And, (3) lesions to area MT in the dorsal stream impair smooth pursuit eye movements, but not saccadic eye movements which are associated with shifts in attention. For these reasons, it is difficult to link attention defects in schizophrenia to potential magnocellular deficits.     

Perhaps correlational but not causal: no effect of dyslexic readers' magnocellular system on their eye movements during reading

During reading, dyslexic readers exhibit more and longer fixations and a higher percentage of regressions than normal readers. It is still a matter of debate, whether these divergent eye movement patterns of dyslexic readers reflect an underlying problem in word processing or whether they are - as the proponents of the magnocellular deficit hypothesis claim - associated with deficient visual perception that is causal for dyslexia. To overcome problems in the empirical linkage of the magnocellular theory with reading, a string processing task is presented that poses similar demands on visual perception (in terms of letter identification) and oculomotor control as reading does. Two experiments revealed no differences in the eye movement patterns of dyslexic and control readers performing this task. Furthermore, no relationship between the functionality of the participants' magnocellular system assessed by the coherent motion task and string processing were found. The perceptual and oculomotor demands required during string processing were functionally equivalent to those during reading and the presented consonant strings had similar visual characteristics as reading material. Thus, a strong inference can be drawn: Dyslexic readers do not seem to have difficulties with the accurate perception of letters and the control of their eye movements during reading - their reading difficulties therefore cannot be explained in terms of oculomotor and visuo-perceptual problems.     

Differential impact of parvocellular and magnocellular pathways on visual impairment in apperceptive agnosia?

The term "visual form agnosia" describes a disorder characterized by problems recognizing objects, poor copying,and distinguishing between simple geometric shapes despite normal intellectual abilities. Visual agnosia has been interpreted as a disorder of the magnocellular visual system, caused by an inability to separate figure from ground by sampling information from extended regions of space and to integrate it with fine-grain local information. However,this interpretation has hardly been tested with neuropsychological or functional brain imaging methods, mainly because the magnocellular and parvocellular structures are highly interconnected in the visual system. We studied a patient (AM) who had suffered a sudden heart arrest, causing hypoxic brain damage. He was/is severely agnosic, as apparent in both the Birmingham Object Recognition Battery and the Visual Object and Space Battery. First- and especially second-order motion perception was also impaired, but AM experienced no problems in grasping and navigating through space. The patient revealed a normal P100 in visual evoked potentials both with colored and fine-grained achromatic checkerboards. But the amplitude of the P100 was clearly decreased if a coarse achromatic checkerboard was presented.The physiological and neuropsychological findings indicate that AM experienced problems integrating information over extended regions of space and in detecting second-order motion. This may be interpreted as a disorder of the magnocellular system, with intact parvocellular system and therefore preserved ability to detect both local features and colors.     

Differential inhibition of chromatic and achromatic perception by transcranial magnetic stimulation of the human visual cortex.

The magnocellular visual pathway is devoted to low-contrast achromatic and motion perception whereas the parvocellular pathway deals with chromatic and high resolution spatial vision. To specifically separate perception mediated by these pathways we have used low-contrast Gaussian filtered black-white or coloured visual stimuli. By use of transcranial magnetic stimulation (TMS) over the visual cortex inhibition of magnocellular stimuli was achieved distinctly earlier by about 40 ms compared with parvocellular information. A nonspecific inhibition of all stimuli could be seen peaking at 75-90 ms, significantly higher for magnocellular stimuli. The particular vulnerability of magnocellular stimuli to TMS is correlated with distinct physiological properties of this pathway such as faster conduction velocity and non-linear stimulus encoding.     

Abnormal global processing along the dorsal visual pathway in autism: a possible mechanism for weak visuospatial coherence?

Frith and Happe (Frith, U., & Happe, F. (1994). Autism: Beyond theory of mind. Cognition, 50, 115-132) argue that individuals with autism exhibit 'weak central coherence': an inability to integrate elements of information into coherent wholes. Some authors have speculated that a high-level impairment might be present in the dorsal visual pathway in autism, and furthermore, that this might account for weak central coherence, at least at the visuospatial level. We assessed the integrity of the dorsal visual pathway in children diagnosed with an autism spectrum disorder (ASD), and in typically developing children, using two visual tasks, one examining functioning at higher levels of the dorsal cortical stream (Global Dot Motion (GDM)), and the other assessing lower-level dorsal stream functioning (Flicker Contrast Sensitivity (FCS)). Central coherence was tested using the Children's Embedded Figures Test (CEFT). Relative to the typically developing children, the children with ASD had shorter CEFT latencies and higher GDM thresholds but equivalent FCS thresholds. Additionally, CEFT latencies were inversely related to GDM thresholds in the ASD group. These outcomes indicate that the elevated global motion thresholds in autism are the result of high-level impairments in dorsal cortical regions. Weak visuospatial coherence in autism may be in the form of abnormal cooperative mechanisms in extra-striate cortical areas, which might contribute to differential performance when processing stimuli as Gestalts, including both dynamic (i.e., global motion perception) and static (i.e., disembedding performance) stimuli.     

Impaired acquisition of limb flexion reflex and eyeblink classical conditioning in a cerebellar patient

The term “visual form agnosia” describes a disorder characterized by problems recognizing objects, poor copying, and distinguishing between simple geometric shapes despite normal intellectual abilities. Visual agnosia has been interpreted as a disorder of the magnocellular visual system, caused by an inability to separate figure from ground by sampling information from extended regions of space and to integrate it with fine-grain local information. However, this interpretation has hardly been tested with neuropsychological or functional brain imaging methods, mainly because the magnocellular and parvocellular structures are highly interconnected in the visual system.

We studied a patient (AM) who had suffered a sudden heart arrest, causing hypoxic brain damage. He was/is severely agnosic, as apparent in both the Birmingham Object Recognition Battery and the Visual Object and Space Battery. First- and especially second-order motion perception was also impaired, but AM experienced no problems in grasping and navigating through space. The patient revealed a normal P100 in visual evoked potentials both with colored and fine-grained achromatic checkerboards. But the amplitude of the P100 was clearly decreased if a coarse achromatic checkerboard was presented.

The physiological and neuropsychological findings indicate that AM experienced problems integrating information over extended regions of space and in detecting second-order motion. This may be interpreted as a disorder of the magnocellular system, with intact parvocellular system and therefore preserved ability to detect both local features and colors.     

Coherent motion, magnocellular sensitivity and the causation of dyslexia

The central tenet of the magnocellular deficit theory of dyslexia is that dyslexia is caused by a magnocellular deficit. A number of investigators have found deficiencies in visual coherent motion perception among dyslexic readers. These deficiencies have been attributed to magnocellular deficits, which means that they directly reflect the cause of dyslexia. However, similar perceptual deficiencies have been found in association with autism, Williams's syndrome, hemiplegia, and schizophrenia. These findings appear to undermine at least one of the following claims: (1) that a magnocellular deficit is the cause of dyslexia, and (2) that coherent motion is a reliable test of magnocellular sensitivity.     

Principles of visual motion detection

Motion information is required for the solution of many complex tasks of the visual system such as depth perception by motion parallax and figure/ground discrimination by relative motion. However, motion information is not explicitly encoded at the level of the retinal input. Instead, it has to be computed from the time-dependent brightness patterns of the retinal image as sensed by the two-dimensional array of photoreceptors. Different models have been proposed which describe the neural computations underlying motion detection in various ways. To what extent do biological motion detectors approximate any of these models? As will be argued here, there is increasing evidence from the different disciplines studying biological motion vision, that, throughout the animal kingdom ranging from invertebrates to vertebrates including man, the mechanisms underlying motion detection can be attributed to only a few, essentially equivalent computational principles. Motion detection may, therefore, be one of the first examples in computational neurosciences where common principles can be found not only at the cellular level (e.g., dendritic integration, spike propagation, synaptic transmission) but also at the level of computations performed by small neural networks.     

COHERENT MOTION,MAGNOCELLULAR SENSITIVITY AND THE CAUSATION OF DYSLEXIA

The central tenet of the magnocellular deficit theory of dyslexia is that dyslexia is caused by a magnocellular deficit. A number of investigators have found deficiencies in visual coherent motion perception among dyslexic readers. These deficiencies have been attributed to magnocellular deficits, which means that they directly reflect the cause of dyslexia. However, similar perceptual deficiencies have been found in association with autism, Williams's syndrome, hemiplegia, and schizophrenia. These findings appear to undermine at least one of the following claims: (1) that a magnocellular deficit is the cause of dyslexia, and (2) that coherent motion is a reliable test of magnocellular sensitivity.     

A subcortical magnocellular pathway is responsible for the fast processing of topological properties of objects: A transcranial magnetic stimulation study

Rapid object recognition has survival significance. The extraction of topological properties (TP) is proposed as the starting point of object perception. Behavioral evidence shows that TP processing takes precedence over other geometric properties and can accelerate object recognition. However, the mechanism of the fast TP processing remains unclear. The magnocellular (M) pathway is well known as a fast route to convey “coarse” information, compared with the slow parvocellular (P) pathway. Here, we hypothesize that the fast processing of TP occurs in a subcortical M pathway. We applied single‐pulse transcranial magnetic stimulation (TMS) over the primary visual cortex to temporarily disrupt cortical processing. Besides, stimuli were designed to preferentially engage M or P pathways (M‐ or P‐biased conditions). We found that, when TMS disrupted cortical function at the early stages of stimulus processing, non‐TP shape discrimination was strongly impaired in both M‐ and P‐biased conditions, whereas TP discrimination was not affected in the M‐biased condition, suggesting that early M processing of TP is independent of the visual cortex, but probably occurs in a subcortical M pathway. Using an unconscious priming paradigm, we further found that early M processing of TP can accelerate object recognition by speeding up the processing of other properties, e.g., orientation. Our findings suggest that the human visual system achieves efficient object recognition by rapidly processing TP in the subcortical M pathway.     

Perception of stationary and moving sound following unilateral cortectomy

The perception of motion is an essential prerequisite to responding adequately to the dynamic aspects of sensory information in the environment. The neural substrates of auditory motion processing are, at present, still a matter of debate. It has been hypothesized that motion information is, as in the visual system, processed separately from other aspects of auditory information, such as stationary location. Here we report data on auditory perception of stationary and motion stimuli from a subject with right-sided resection of the anterior temporal-lobe region including medial aspects of Heschl's gyrus, and from three subjects with unilateral (right-sided or left-sided) hemispherectomy. All these subjects had undergone cortectomy decades earlier. The subjects with hemispherectomy were completely unable to perceive auditory motion, but showed slight to moderate deficits in judging stationary location. The subject with temporal lobectomy exhibited quite similar stationary auditory deficits as found in the subjects with hemispherectomy, but was completely normal in judging auditory motion. Thus, there was a clear dissociation of the effects of unilateral temporal lobectomy and hemispherectomy on auditory motion perception. Collectively, these findings suggest that the unilateral anterior temporal-lobe region plays a significant role in the analysis of stationary, but not moving, sound. One may assume that the cortical “motion network” is distinct from the “stationary network”, and is located either in the most posterior aspects of temporal lobe, or in non-temporal, most likely parietal, areas.     

Abnormal visual phenomena in posterior cortical atrophy

Individuals with posterior cortical atrophy (PCA) report a host of unusual and poorly explained visual disturbances. This preliminary report describes a single patient (CRO), and documents and investigates abnormally prolonged colour afterimages (concurrent and prolonged perception of colours complimentary to the colour of an observed stimulus), perceived motion of static stimuli, and better reading of small than large letters. We also evaluate CRO's visual and vestibular functions in an effort to understand the origin of her experience of room tilt illusion, a disturbing phenomenon not previously observed in individuals with cortical degenerative disease. These visual symptoms are set in the context of a 4-year longitudinal neuropsychological and neuroimaging investigation of CRO's visual and other cognitive skills. We hypothesise that prolonged colour after-images are attributable to relative sparing of V1 inhibitory interneurons; perceived motion of static stimuli reflects weak magnocellular function; better reading of small than large letters indicates a reduced effective field of vision; and room tilt illusion effects are caused by disordered integration of visual and vestibular information. This study contributes to the growing characterisation of PCA whose atypical early visual symptoms are often heterogeneous and frequently under-recognised.     

Neuronal mechanisms for detection of motion in the field of view

The visual system cannot rely only upon information from the retina to perceive object motion because identical retinal stimulations can be evoked by the movement of objects in the field of view as well as by the movements of retinal images self-evoked by eye movements. We clearly distinguish the two situations, perceiving object motion in the first case and stationarity in the second. The present work deals with the neuronal mechanisms that are likely involved in the detection of real motion. In monkeys, cells that are able to distinguish real from self-induced motion (real-motion cells) are distributed in several cortical areas of the dorsal visual stream. We suggest that the activity of these cells is responsible for motion perception, and hypothesize that these cells are the elements of a cortical network representing an internal map of a stable visual world. Supporting this view are the facts that: (i) the same cortical regions in humans are activated in brain imaging studies during perception of object motion; and (ii) lesions of these same regions produce selective impairments in motion detection, so that patients interpret any retinal image motion as object motion, even when they result from her/his eye movements. Among the areas of the dorsal visual stream rich in real-motion cells, V3A and V6, likely involved in the fast form and motion analyses needed for visual guidance of action, could use real-motion signals to orient the animal's attention towards moving objects, and/or to help grasping them. Areas MT/V5, MST and 7a, known to be involved in the control of pursuit eye movements and in the analysis of visual signals evoked by slow ocular movements, could use real-motion signals to give a proper evaluation of motion during pursuits.     

Ultra-High-Field Neuroimaging Reveals Fine-Scale Processing for 3D Perception

Binocular disparity provides critical information about three-dimensional (3D) structures to support perception and action. In the past decade significant progress has been made in uncovering human brain areas engaged in the processing of binocular disparity signals. Yet, the fine-scale brain processing underlying 3D perception remains unknown. Here, we use ultra-high-field (7T) functional imaging at submillimeter resolution to examine fine-scale BOLD fMRI signals involved in 3D perception. In particular, we sought to interrogate the local circuitry involved in disparity processing by sampling fMRI responses at different positions relative to the cortical surface (i.e., across cortical depths corresponding to layers). We tested for representations related to 3D perception by presenting participants (male and female, N = 8) with stimuli that enable stable stereoscopic perception [i.e., correlated random dot stereograms (RDS)] versus those that do not (i.e., anticorrelated RDS). Using multivoxel pattern analysis (MVPA), we demonstrate cortical depth-specific representations in areas V3A and V7 as indicated by stronger pattern responses for correlated than for anticorrelated stimuli in upper rather than deeper layers. Examining informational connectivity, we find higher feedforward layer-to-layer connectivity for correlated than anticorrelated stimuli between V3A and V7. Further, we observe disparity-specific feedback from V3A to V1 and from V7 to V3A. Our findings provide evidence for the role of V3A as a key nexus for disparity processing, which is implicated in feedforward and feedback signals related to the perceptual estimation of 3D structures.SIGNIFICANCE STATEMENT Binocular vision plays a significant role in supporting our interactions with the surrounding environment. The fine-scale neural mechanisms that underlie the brain''s skill in extracting 3D structures from binocular signals are poorly understood. Here, we capitalize on recent advances in ultra-high-field functional imaging to interrogate human brain circuits involved in 3D perception at submillimeter resolution. We provide evidence for the role of area V3A as a key nexus for disparity processing, which is implicated in feedforward and feedback signals related to the perceptual estimation of 3D structures from binocular signals. These fine-scale measurements help bridge the gap between animal neurophysiology and human fMRI studies investigating cross-scale circuits, from micro circuits to global brain networks for 3D perception.     

The use of phantom contours to isolate magnocellular and parvocellular responses

In some "flickering" spot stimuli, two kinds of percepts can be seen at different frequencies: phantom contours and "surface characteristics." It has been proposed that their perception may be used to evaluate the magnocellular and parvocellular systems. This, however, is problematic. First, the difference in temporal frequencies associated with the two percepts is large compared to that between the temporal tuning of magno- and parvocellular neurons. Second, the lack of absolute temporal phase information in the case of surface characteristics does not fit with parvocellular neuron behavior. Third, the low temporal threshold of surface characteristics suggests cortical mechanisms rather than parvocellular ones. And fourth, the relationship between the two percepts and color may reflect parvocellular responses not magno- and parvocellular ones.     

Priming of first- and second-order motion: mechanisms and neural substrates

Priming for luminance-modulated (first-order) motion has been shown to rely on the functional integrity of visual area V5/MT [Campana, G., Cowey, A., & Walsh, V. (2002). Priming of motion direction and area V5/MT: A test of perceptual memory. Cerebral Cortex, 12, 663-669; Campana, G., Cowey, A., & Walsh, V. (2006). Visual area V5/MT remembers "what" but not "where". Cerebral Cortex, 16, 1766-1770]. The high retinotopical organization of this area would predict that direction priming is sensitive to spatial position. In order to test this hypothesis, and to see whether a similar priming mechanism also exists with second-order motion, we tested motion direction priming and its interaction with spatial position with both first- and second-order motion. Indeed, whereas a number of studies have pinpointed the specific mechanisms and neural substrates for these two kinds of motion perception that appear to be (partially) non-overlapping (i.e., Lu, Z. L., & Sperling, G. (2001). Three-systems theory of human visual motion perception: Review and update. Journal of the Optical Society of America A, 18, 2331-2370; Vaina, L. M., & Soloviev, S. (2004). First-order and second-order motion: Neurological evidence for neuroanatomically distinct systems. Progress in Brain Research, 144, 197-212), the mechanisms and neural substrates mediating implicit memory for first- and second-order motion are still unknown. Our results indicate that priming for motion direction occurs not only with first-order but also with second-order motion. Priming for motion direction is position-sensitive both with first- and second-order motion, suggesting for both processes a locus of representation where retinotopicity is still maintained, that is within the V5/MT complex but earlier than MST. Cross-order motion priming also exists but is not sensitive to spatial position, suggesting that the locus where processing of first- and second-order motion converge is situated in MST or beyond.     

Visual magnocellular and structure from motion perceptual deficits in a neurodevelopmental model of dorsal stream function

Williams syndrome (WS) is a neurodevelopmental disorder of genetic origin that has been used as a model to understand visual cognition. We have investigated early deficits in the afferent magnocellular pathway and their relation to abnormal visual dorsal processing in WS. A spatiotemporal contrast sensitivity task that is known to selectively activate that pathway was used in six WS subjects. Additionally, we have compared visual performance in 2D and 3D motion integration tasks. A novel 3D motion coherence task (using spheres with unpredictable axis of rotation) was used in order to investigate possible impairment of occipitoparietal areas that are known to be involved in 3D structure from motion (SFM) perception. We have found a significant involvement of low-level magnocellular maps in WS as assessed by the contrast sensitivity task. On the contrary, no significant differences were observed between WS and the control groups in the 2D motion integration tasks. However, all WS subjects were significantly impaired in the 3D SFM task. Our findings suggest that magnocellular damage may occur in addition to dorsal stream deficits in these patients. They are also consistent with recently described genetic and neuroanatomic abnormalities in retinotopic visual areas. Finally, selective SFM coherence deficits support the proposal that there is a specific pathway in the dorsal stream that is involved in motion processing of 3D surfaces, which seems to be impaired in this disorder.     

Direction-selective patterns of activity in human visual cortex suggest common neural substrates for different types of motion

A sense of motion can be elicited by the movement of both luminance- and texture-defined patterns, what is commonly referred to as first- and second-order, respectively. Although there are differences in the perception of these two classes of motion stimuli, including differences in temporal and spatial sensitivity, it is debated whether common or separate direction-selective mechanisms are responsible for processing these two types of motion. Here, we measured direction-selective responses to luminance- and texture-defined motion in the human visual cortex by using functional MRI (fMRI) in conjunction with multivariate pattern analysis (MVPA). We found evidence of direction selectivity for both types of motion in all early visual areas (V1, V2, V3, V3A, V4, and MT+), implying that none of these early visual areas is specialized for processing a specific type of motion. More importantly, linear classifiers trained with cortical activity patterns to one type of motion (e.g., first-order motion) could reliably classify the direction of motion defined by the other type (e.g., second-order motion). Our results suggest that the direction-selective mechanisms that respond to these two types of motion share similar spatial distributions in the early visual cortex, consistent with the possibility that common mechanisms are responsible for processing both types of motion.