Increase in MST activity correlates with visual motion learning: A functional MRI study of perceptual learning

Repeated practice of a specific task can improve visual performance, but the neural mechanisms underlying this improvement in performance are not yet well understood. Here we trained healthy participants on a visual motion task daily for 5 days in one visual hemifield. Before and after training, we used functional magnetic resonance imaging (fMRI) to measure the change in neural activity. We also imaged a control group of participants on two occasions who did not receive any task training. While in the MRI scanner, all participants completed the motion task in the trained and untrained visual hemifields separately. Following training, participants improved their ability to discriminate motion direction in the trained hemifield and, to a lesser extent, in the untrained hemifield. The amount of task learning correlated positively with the change in activity in the medial superior temporal (MST) area. MST is the anterior portion of the human motion complex (hMT+). MST changes were localized to the hemisphere contralateral to the region of the visual field, where perceptual training was delivered. Visual areas V2 and V3a showed an increase in activity between the first and second scan in the training group, but this was not correlated with performance. The contralateral anterior hippocampus and bilateral dorsolateral prefrontal cortex (DLPFC) and frontal pole showed changes in neural activity that also correlated with the amount of task learning. These findings emphasize the importance of MST in perceptual learning of a visual motion task. Hum Brain Mapp 39:145–156, 2018. © 2017 Wiley Periodicals, Inc.     

Differential dependency on motion coherence in subregions of the human MT+ complex

The detection of coherent motion embedded in noise has been widely used as a measure of global visual motion processing. Animal studies have demonstrated that this performance is closely linked to the responses of direction-sensitive neurons in the macaque middle temporal (MT) and medial superior temporal (MST) areas. Despite the strong similarities between the visual cortex of human and that of non-human primates, the human middle temporal complex (area MT+), located in the posterior part of the inferior temporal sulcus and presumably comprising both area MT and area MST, has not consistently been found to share the functional hallmark of MT and MST neurons, i.e. their preference for coherent rather than incoherent visual motion. In order to search for such preferences in human area MT+, blood oxygen level-dependent responses to random dot kinematograms presented in the right visual hemifield were studied here as a function of stimulus size and dot density. The stimulus extensions were varied in such a way as to cover an area either equaling, exceeding or falling below the mean receptive field size of macaque area MT. Unlike the posterior part of human area MT+, the anterior part and its right-hemisphere homolog showed significantly stronger responses to coherent than to incoherent motion. These differences were only present for large stimuli that presumably exceeded the receptive field size of neurons in area MT. Our results suggest that functional magnetic resonance imaging may reveal stronger responses to coherent visual motion in human area MST, provided that the stimulus allows for sufficient summation within the receptive fields. In contrast, functional magnetic resonance imaging may fail to reveal the same dependency for human area MT.     

Spatiotemporal frequency and speed tuning in the owl visual wulst

The avian visual wulst is hodologically equivalent to the mammalian primary visual cortex (V1). In contrast to most birds, owls have a massive visual wulst, which shares striking functional similarities with V1. To provide a better understanding of how motion is processed within this area, we used sinusoidal gratings to characterize the spatiotemporal frequency and speed tuning profiles of 131 neurones recorded from awake burrowing owls. Cells were found to be clearly tuned to both spatial and temporal frequencies, and in a way that is similar to what has been reported in the striate cortex of primates and carnivores. Our results also suggest the presence of spatial frequency tuning domains in the wulst. Speed tuning was assessed by several methods devised to measure the degree of dependence between spatial and temporal frequency tuning. Although many neurones were found to be independently tuned, a significant proportion of cells showed at least some degree of dependence, compatible with the idea that some kind of initial transformation towards an explicit representation of speed is being carried out by the owl wulst. Interestingly, under certain constraints, a higher incidence of spatial frequency-invariant speed tuned profiles was obtained by combining our experimentally measured responses using a recent cortical model of speed tuning. Overall, our findings reinforce the notion that, like V1, the owl wulst is an important initial stage for motion processing, a function that is usually attributed to areas of the tectofugal pathway in lateral-eyed birds.     

Mechanisms of speed encoding in the human middle temporal cortex measured by 7T fMRI

Perception of dynamic scenes in our environment results from the evaluation of visual features such as the fundamental spatial and temporal frequency components of a moving object. The ratio between these two components represents the object''s speed of motion. The human middle temporal cortex hMT+ has a crucial biological role in the direct encoding of object speed. However, the link between hMT+ speed encoding and the spatiotemporal frequency components of a moving object is still under explored. Here, we recorded high resolution 7T blood oxygen level‐dependent BOLD responses to different visual motion stimuli as a function of their fundamental spatial and temporal frequency components. We fitted each hMT+ BOLD response with a 2D Gaussian model allowing for two different speed encoding mechanisms: (1) distinct and independent selectivity for the spatial and temporal frequencies of the visual motion stimuli; (2) pure tuning for the speed of motion. We show that both mechanisms occur but in different neuronal groups within hMT+, with the largest subregion of the complex showing separable tuning for the spatial and temporal frequency of the visual stimuli. Both mechanisms were highly reproducible within participants, reconciling single cell recordings from MT in animals that have showed both encoding mechanisms. Our findings confirm that a more complex process is involved in the perception of speed than initially thought and suggest that hMT+ plays a primary role in the evaluation of the spatial features of the moving visual input.     

Disentangling neural structures for processing of high- and low-speed visual motion

Human psychophysical and electrophysiological evidence suggests at least two separate visual motion pathways, one tuned to a lower and one tuned to a broader and partly overlapping range of higher speeds. It remains unclear whether these two different channels are represented by different cortical areas or by sub-populations within a single area. We recorded evoked potentials at 59 scalp locations to the onset of a slow (3.5 degrees /s) and fast (32 degrees /s) moving test pattern, preceded by either a slow or fast adapting pattern that moved in either the same direction or opposite to the test motion. Baseline potentials were recorded for slow and fast moving test patterns after adaptation to a static pattern. Comparison of adapted responses with baseline responses revealed that the N2 peak around 180 ms after test stimulus onset was modulated by the preceding adaptation. This modulation depended on both direction and speed. Source localization of baseline potentials as well as direction-independent motion adaptation revealed cortical areas activated by fast motion to be more dorsal, medial and posterior compared with neural structures underlying slow motion processing. For both speeds, the direction-dependent component of this adaptation modulation occurred in the same area, located significantly more dorsally compared with neural structures that were adapted in a direction-independent manner. These results demonstrate for the first time the cortical separation of more ventral areas selectively activated by visual motion at low speeds (and not high speeds) and dorsal motion-sensitive cortical areas that are activated by both high and low speeds.     

Representation of illusory and physical rotations in human MST: A cortical site for the pinna illusion

Visual illusions have fascinated mankind since antiquity, as they provide a unique window to explore the constructive nature of human perception. The Pinna illusion is a striking example of rotation perception in the absence of real physical motion. Upon approaching or receding from the Pinna‐Brelstaff figure, the observer experiences vivid illusory counter rotation of the two rings in the figure. Although this phenomenon is well known as an example of integration from local cues to a global percept, the visual areas mediating the illusory rotary perception in the human brain have not yet been identified. In the current study we investigated which cortical area in the human brain initially mediates the Pinna illusion, using psychophysical tests and functional magnetic resonance imaging (fMRI) of visual cortices V1, V2, V3, V3A, V4, and hMT+ of the dorsal and ventral visual pathways. We found that both the Pinna‐Brelstaff figure (illusory rotation) and a matched physical rotation control stimulus predominantly activated subarea MST in hMT+ with a similar response intensity. Our results thus provide neural evidence showing that illusory rotation is initiated in human MST rather than MT as if it were physical rotary motion. The findings imply that illusory rotation in the Pinna illusion is mediated by rotation‐sensitive neurons that normally encode physical rotation in human MST, both of which may rely on a cascade of similar integrative processes from earlier visual areas. Hum Brain Mapp 37:2097–2113, 2016. © 2016 Wiley Periodicals, Inc.     

Changes of spatial and temporal frequency tuning properties of neurons in the middle temporal area of aged rhesus monkeys

Aged humans exhibit severe deficits in visual motion perception and contrast sensitivity under various levels of spatial and temporal modulation. Previous studies indicated that many of these deficits are probably mediated by the neural degradation of the central visual system. To clarify the neuronal response mechanisms underlying the visual degradation during aging, we examined the spatial and temporal frequency tuning properties of neurons from anesthetised and paralysed aged monkeys at the middle temporal area (area MT), which is downstream of the primary visual cortex in the visual processing pathway and thought to be critical for motion perception. We found that the preferred spatial and temporal frequencies, spatial resolution and high temporal frequency cutoff of area MT neurons were reduced in aged monkeys, and were accompanied by the broadened tuning width of spatial frequency, elevated spontaneous activity, and decreased signal‐to‐noise ratio. These results showed that, for neurons in area MT, aging significantly changed both the spatial and temporal frequency response tuning properties. Such evidence provides new insight into the changes occurring at the electrophysiological level that may be related to the aging‐related visual deficits, especially in processing spatial and temporal information.     

Brain activation associated with visual motion studied by functional magnetic resonance imaging in humans

Localized brain activation in response to moving visual stimuli was studied by functional magnetic resonance imaging (fMRI). Stimuli were 100 small white dots randomly arranged on a visual display. During the Motion condition, the dots moved along random, noncoherent linear trajectories at different velocities. During the Blink condition, the dots remained stationary but blinked on and off every 500 ms. The Motion and Blink conditions continuously alternated with 10 cycles per run and 6–8 runs per experiment. In half of the runs, the starting stimulus condition was Motion, while in the remaining runs it was Blink. A series of 128 gradient echo echoplanar images were acquired from 5–7 slices during each run using a 1.5 T GE Signa with an Advanced NMR echoplanar subsystem. The time series for each voxel were analyzed in the frequency domain. Voxels which demonstrated a significant spectral peak at the alternation frequency and whose phase changed in response to stimulus order were considered activated. These activated voxels were displayed upon high resolution anatomical images to determine the sites of activation and were also transformed into the coordinates of Talairach and Tournoux ([1988] Co-planar Stereotaxic Atlas of the Human Brain, New York: Thieme) for comparison to prior neuroimaging studies. Seven of ten subjects showed clusters of activation bilaterally at the junction of the temporal and occipital lobes (area 37) in response to moving stimuli. Most activated voxels were located within or adjacent to a region designated the parietal-temporal-occipital fossa, or PTOF. Five subjects also showed activation to moving stimuli in midline occipital cortex. The activated voxels in midline cortex had a significantly shorter phase delay in their MR signal change relative to voxels in PTOF. © 1995 Wiley-Liss, Inc. 1

1 This article is a US Government work and, as such, is in the public domain in the United States of America

     

Asymmetry of the human visual field in magnetic response to apparent motion

Predominance of the lower visual field has been shown in various visual tasks, but whether the upper visual field is involved in a specific neural process is unknown. We used magnetoencephalography to study the effect of orientation and direction on the responses of five subjects to apparent motion from the human extrastriate cortex. The first magnetic response always was the largest, and the peak latency of about 200 ms did not change with the stimulus conditions. Amplitudes of the first responses were highest when motions were oriented at the horizontal meridian, decreasing with the degree of the angle between motion orientation and the horizontal meridian. There was no difference in amplitude between the two directions in the lower visual field, whereas the value of the response to downward motion in the upper visual field was significantly larger than that to upward motion. These amplitude changes are not due to differences in the anatomical distribution of neural activities because the estimated origins for the first responses always were in the same cortical area (around the occipito-parieto-temporal region) and the directions of the current vectors did not change with the stimulus conditions, and the estimated current strength changed with the stimulus conditions as did the response amplitude. These findings suggest that the human extrastriate cortex has a directional preference for downward versus upward motion in the upper visual field.     

Stimulus-contrast-induced biases in activation order reveal interaction between V1/V2 and human MT+

The luminance contrast of a visual stimulus is known to modulate the response properties of areas V1 and the human MT complex (hMT+), but has not been shown to modulate interactions between these two areas. We examined the direction of information transfer between V1/V2 and hMT+ at different stimulus contrasts by measuring magnetoencephalographic (MEG) responses to moving and stationary stimuli presented centrally or peripherally. To determine the direction of information flow, the different response latencies among stimuli and hemispheres in V1/V2 was compared with those of hMT+. At high contrast, responses to stimulus motion and position began in V1/V2, and were followed in hMT+ with a delay between 34 and 55 ms. However, at low contrast, lateralized responses in hMT+ came first, with those in V1/V2 lagging with a delay of 27 ms. Also, at high contrast, stationary stimuli produced greater responses than motion stimuli in V1/V2, while the reverse was true in hMT+, whose response lagged behind the initial response in V1/V2. The same activation order was found using Mutual Information Analysis of the response variances for each condition. Here, the response variances in hMT+ mimicked and trailed those of V1/V2 at high contrast, whereas the reverse was true at low contrast. Such consistent interactions found using two different methodologies strongly supports a processing link between these two areas. The results also suggest that feedback from hMT+ for low-contrast stimuli compensates for unresolved processing in V1/V2 when the input of a visual image is weak.     

Sensitivity to optic flow in human cortical areas MT and MST

The macaque V5/MT complex comprises several sub-regions but little is known of their human homologues. We examined human V5/MT with fMRI in terms of specificity to optic flow stimuli, a key characteristic of macaque MST. Stimuli were large fields of moving dots, forming coherent global flow patterns. Random motion was used as a control. Retinotopic mapping was also conducted. The previously suggested existence of at least two distinct sub-regions, MT and MST, within the V5/MT complex was confirmed. Human MT is activated about equally by all moving dot patterns, including random motion, suggesting that it has little sensitivity to global flow structure. As previously described, this region shows strong signs of retinotopic organization and is only weakly activated by stimuli confined to the ipsilateral hemifield. In human MST, located immediately anterior to MT and strongly driven by ipsilateral stimuli, activation varies markedly with optic flow structure. The strongest activation is produced by complex flow that contains multiple flow components (expansion, contraction and rotation). Single components produce rather less response, while rigid translation and random motion produce less still. The results suggest that human MST is strongly specialized for encoding global flow properties, while human MT is less so.     

The temporal sequence of evoked and induced cortical responses to implied-motion processing in human motion area V5/MT+

Previous functional magnetic resonance imaging (fMRI) studies have demonstrated that the human visual motion area V5/MT+ is differentially activated by stimuli in which the presence of motion is implied by the content of static photographs, compared with similar static scenes in which no motion is implied. Here, using a group magnetoencephalography study, we confirm the role of V5/MT+ in the perception of implied motion (IM) by the measurement and localization of task-related evoked and induced oscillatory responses, and demonstrate the temporal sequence of these responses. Within the lateral occipital complex, including V5/MT+, statistically significant differential oscillatory responses to IM and implied-static (IS) stimuli were only found in the beta band (15-20 Hz). An early, evoked, beta power increase (IM>IS) occurred at about 150 ms, whilst a power decrease (IM相似文献   

Spatial and temporal frequency tuning in striate cortex: functional uniformity and specializations related to receptive field eccentricity

In light of anatomical evidence suggesting differential connection patterns in central vs. peripheral representations of cortical areas, we investigated the extent to which the response properties of cells in the primary visual area (V1) of the marmoset change as a function of eccentricity. Responses to combinations of the spatial and temporal frequencies of visual stimuli were quantified for neurons with receptive fields ranging from 3° to 70° eccentricity. Optimal spatial frequencies and stimulus speeds reflected the expectation that the responses of cells throughout V1 are essentially uniform, once scaled according to the cortical magnification factor. In addition, temporal frequency tuning was similar throughout V1. However, spatial frequency tuning curves depended both on the cell’s optimal spatial frequency and on the receptive field eccentricity: cells with peripheral receptive fields showed narrower bandwidths than cells with central receptive fields that were sensitive to the same optimal spatial frequency. Although most V1 cells had separable spatial and temporal frequency tuning, the proportion of neurons displaying significant spatiotemporal interactions increased in the representation of far peripheral vision (> 50°). In addition, of the fewer than 5% of V1 cells that showed robust (spatial frequency independent) selectivity to stimulus speed, most were concentrated in the representation of the far periphery. Spatiotemporal interactions in the responses of many cells in the peripheral representation of V1 reduced the ambiguity of responses to high‐speed (> 30°/s) signals. These results support the notion of a relative specialization for motion processing in the far peripheral representations of cortical areas, including V1.     

The selectivity of responses to red‐green colour and achromatic contrast in the human visual cortex: an fMRI adaptation study

There is controversy as to how responses to colour in the human brain are organized within the visual pathways. A key issue is whether there are modular pathways that respond selectively to colour or whether there are common neural substrates for both colour and achromatic (Ach) contrast. We used functional magnetic resonance imaging (fMRI) adaptation to investigate the responses of early and extrastriate visual areas to colour and Ach contrast. High‐contrast red–green (RG) and Ach sinewave rings (0.5 cycles/degree, 2 Hz) were used as both adapting stimuli and test stimuli in a block design. We found robust adaptation to RG or Ach contrast in all visual areas. Cross‐adaptation between RG and Ach contrast occurred in all areas indicating the presence of integrated, colour and Ach responses. Notably, we revealed contrasting trends for the two test stimuli. For the RG test, unselective processing (robust adaptation to both RG and Ach contrast) was most evident in the early visual areas (V1 and V2), but selective responses, revealed as greater adaptation between the same stimuli than cross‐adaptation between different stimuli, emerged in the ventral cortex, in V4 and VO in particular. For the Ach test, unselective responses were again most evident in early visual areas but Ach selectivity emerged in the dorsal cortex (V3a and hMT+). Our findings support a strong presence of integrated mechanisms for colour and Ach contrast across the visual hierarchy, with a progression towards selective processing in extrastriate visual areas.     

Visual detection of motion speed in humans: spatiotemporal analysis by fMRI and MEG

Humans take a long time to respond to the slow visual motion of an object. It is not known what neural mechanism causes this delay. We measured magnetoencephalographic neural responses to light spot motion onset within a wide speed range (0.4-500 degrees /sec) and compared these with human reaction times (RTs). The mean response latency was inversely related to the speed of motion up to 100 degrees /sec, whereas the amplitude increased with the speed. The response property at the speed of 500 degrees /sec was different from that at the other speeds. The speed-related latency change was observed when the motion duration was 10 msec or longer in the speed range between 5 and 500 degrees /sec, indicating that the response is directly related to the speed itself. The source of the response was estimated to be around the human MT+ and was validated by functional magnetic imaging study using the same stimuli. The results indicate that the speed of motion is encoded in the neural activity of MT+ and that it can be detected within 10 msec of motion observation. RT to the same motion onset was also inversely related to the speed of motion but the delay could not be explained by the magnetic response latency change. Instead, the reciprocal of RT was linearly related to the reciprocal of the magnetic response latency, suggesting that the visual process interacts with other neural processes for decision and motor preparation.