The role of directionally selective neurons in the perception of global motion

Dynamic random dot targets consisting of many localized motion vectors have been used to study the pooling of local motion signals into a global motion percept (Williams and Sekuler, 1984). In such displays, the dots are displaced with a constant step size and the direction of motion for each dot is chosen at random from a specified distribution. When the distribution extends over 360 deg, the display consists only of local random motion of individual dots and no coherent motion is reported. However, when the distribution is less than 360 deg (biased), the stimulus appears to flow in a single direction. We examined the effects of reducing the number of directionally selective (DS) cortical neurons on this integration process. Normal cats and cats with severely reduced proportions of DS neurons were trained on 2 direction discrimination tasks. The discrimination of opposite directions was examined while varying either the range of directions of local motion, or the proportion of dots moving with biased distribution. When all dots in the display were directionally biased, cats with reduced numbers of DS neurons performed the task as well as normal cats and humans (threshold range: 280-320 deg). However, when the proportion of biased dots decreased, these animals had severe deficits. Thus, in the absence of noise, even a very small number of DS neurons can perform spatial pooling of local directional signals, and support normal discrimination of opposite directions. However, a full complement of directional detectors appears necessary when the motion signal is masked by noise. The discrimination of small differences in direction revealed far more severe deficits, even when all the dots in the display were directionally biased (no noise).(ABSTRACT TRUNCATED AT 250 WORDS)     

Construction and evaluation of an integrated dynamical model of visual motion perception

Although numerous models describe the individual neural mechanisms that may be involved in the perception of visual motion, few of them have been constructed to take arbitrary stimuli and map them to a motion percept. Here, we propose an integrated dynamical motion model (IDM), which is sufficiently general to handle diverse moving stimuli, yet sufficiently precise to account for a wide-ranging set of empirical observations made on a family of random dot kinematograms. In particular, we constructed models of the cortical areas involved in motion detection, motion integration and perceptual decision. We analyzed their parameters through dynamical simulations and numerical continuation to constrain their proper ranges. Then, empirical data from a family of random dot kinematograms experiments with systematically varying direction distribution, presentation duration and stimulus size, were used to evaluate our model and estimate corresponding model parameters. The resulting model provides an excellent account of a demanding set of parametrically varied behavioral effects on motion perception, providing both quantitative and qualitative elements of evaluation.     

Orienting attention to locations in internal representations

Three experiments investigated whether it is possible to orient selective spatial attention to internal representations held in working memory in a similar fashion to orienting to perceptual stimuli. In the first experiment, subjects were either cued to orient to a spatial location before a stimulus array was presented (pre-cue), cued to orient to a spatial location in working memory after the array was presented (retro-cue), or given no cueing information (neutral cue). The stimulus array consisted of four differently colored crosses, one in each quadrant. At the end of a trial, a colored cross (probe) was presented centrally, and subjects responded according to whether it had occurred in the array. There were equivalent patterns of behavioral costs and benefits of cueing for both pre-cues and retro-cues. A follow-up experiment used a peripheral probe stimulus requiring a decision about whether its color matched that of the item presented at the same location in the array. Replication of the behavioral costs and benefits of pre-cues and retro-cues in this experiment ruled out changes in response criteria as the only explanation for the effects. The third experiment used event-related potentials (ERPs) to compare the neural processes involved in orienting attention to a spatial location in an external versus an internal spatial representation. In this task, subjects responded according to whether a central probe stimulus occurred at the cued location in the array. There were both similarities and differences between ERPs to spatial cues toward a perception versus an internal spatial representation. Lateralized early posterior and later frontal negativities were observed for both pre- and retro-cues. Retro-cues also showed additional neural processes to be involved in orienting to an internal representation, including early effects over frontal electrodes.     

Modulation of spatial orientation processing by mental imagery instructions: a MEG study of representational momentum

Under appropriate conditions, an observer's memory for the final position of an abruptly halted moving object is distorted in the direction of the represented motion. This phenomenon is called "representational momentum" (RM). We examined the effect of mental imagery instructions on the modulation of spatial orientation processing by testing for RM under conditions of picture versus body rotation perception and imagination. Behavioral data were gathered via classical reaction time and error measurements, whereas brain activity was recorded with the help of magnetoencephalography (MEG). Due to the so-called inverse problem and to signal complexity, results were described at the signal level rather than with the source location modeling. Brain magnetic field strength and spatial distribution, as well as latency of P200m evoked fields were used as neurocognitive markers. A task was devised where a subject examined a rotating sea horizon as seen from a virtual boat in order to extrapolate either the picture motion or the body motion relative to the picture while the latter disappeared temporarily until a test-view was displayed as a final orientation candidate. Results suggest that perceptual interpretation and extrapolation of visual motion in the roll plane capitalize on the fronto-parietal cortical networks involving working memory processes. Extrapolation of the rotational dynamics of sea horizon revealed a RM effect simulating the role of gravity in rotational equilibrium. Modulation of the P200m component reflected spatial orientation processing and a non-voluntary detection of an incongruity between displayed and expected final orientations given the implied motion. Neuromagnetic properties of anticipatory (Contingent Magnetic Variation) and evoked (P200m) brain magnetic fields suggest, respectively, differential allocation of attentional resources by mental imagery instructions (picture vs. body tilt), and a communality of neural structures (in the right centro-parietal region) for the control of both RM and mental rotation processes. Finally, the RM of the body motion is less prone to forward shifts than that of picture motion evidencing an internalization of the implied mass of the virtual body of the observer.     

Pushing around the locus of selection: evidence for the flexible-selection hypothesis

Attention operates at an early stage in some experimental paradigms and at a late stage in others, which suggests that the locus of selection is flexible. The present study was designed to determine whether the locus of selection can vary flexibly within a single experimental paradigm as a function of relatively modest variations in stimulus and task parameters. In the first experiment, a new method for assessing the locus of selection was developed. Specifically, attention can influence perceptual encoding only if it is directed to the target before a perceptual representation of the target has been formed, whereas attention can influence postperceptual processes even if attention is cued after perception is complete. Event-related potentials were used to confirm the validity of this method. The subsequent experiments used cueing tasks in which subjects were required to perceive and remember a set of objects, and the difficulty of the perception and memory components of the task were varied. When the task overloaded perception but not working memory, attention influenced the formation of perceptual representations but not the storage of these representations in memory; when the task overloaded working memory but not perception, attention influenced the transfer of perceptual representations into memory but not the formation of the perceptual representations. Thus, attention operates to select relevant information at whatever stage or stages of processing are overloaded by a particular stimulus-task combination.     

Enhanced visual perception with occipital transcranial magnetic stimulation

Transcranial magnetic stimulation (TMS) over the occipital pole can produce an illusory percept of a light flash (or ‘phosphene’), suggesting an excitatory effect. Whereas previous reported effects produced by single‐pulse occipital pole TMS are typically disruptive, here we report the first demonstration of a location‐specific facilitatory effect on visual perception in humans. Observers performed a spatial cueing orientation discrimination task. An orientation target was presented in one of two peripheral placeholders. A single pulse below the phosphene threshold applied to the occipital pole 150 or 200 ms before stimulus onset was found to facilitate target discrimination in the contralateral compared with the ipsilateral visual field. At the 150‐ms time window contralateral TMS also amplified cueing effects, increasing both facilitation effects for valid cues and interference effects for invalid cues. These results are the first to show location‐specific enhanced visual perception with single‐pulse occipital pole stimulation prior to stimulus presentation, suggesting that occipital stimulation can enhance the excitability of visual cortex to subsequent perception.     

A neural circuit basis for spatial working memory.

The maintenance of a mental image in memory over a time scale of seconds is mediated by the persistent discharges of neurons in a distributed brain network. The representation of the spatial location of a remembered visual stimulus has been studied most extensively and provides the best-understood model of how mnemonic information is encoded in the brain. Neural correlates of spatial working memory are manifested in multiple brain areas, including the prefrontal and parietal association cortices. Spatial working memory ability is severely compromised in schizophrenia, a condition that has been linked to prefrontal cortical malfunction. Recent computational modeling work, in interplay with physiological studies of behaving monkeys, has begun to identify microcircuit properties and neural dynamics that are sufficient to generate memory-related persistent activity in a recurrent network of excitatory and inhibitory neurons during spatial working memory. This review summarizes recent results and discusses issues of current debate. It is argued that understanding collective neural dynamics in a recurrent microcircuit provides a key step in bridging the gap between network memory function and its underlying cellular mechanisms. Progress in this direction will shed fundamental insights into the neural basis of spatial working memory impairment associated with mental disorders.     

A neural basis for percept stabilization in binocular rivalry

When the same visual input has conflicting interpretations, conscious perception can alternate spontaneously between each competing percept. Surprisingly, such bistable perception can be stabilized by intermittent stimulus removal, suggesting the existence of perceptual "memory" across interruptions in stimulation. The neural basis of such a process remains unknown. Here, we studied binocular rivalry, one type of bistable perception, in two linked experiments in human participants. First, we showed, in a behavioral experiment using binocular rivalry between face and grating stimuli, that the stabilizing effect of stimulus removal was specific to perceptual alternations evoked by rivalry, and did not occur following physical alternations in the absence of rivalry. We then used functional magnetic resonance imaging to measure brain activity in a variable delay period of stimulus removal. Activity in the fusiform face area during the delay period following removal of rivalrous stimuli was greater following face than grating perception, whereas such a difference was absent during removal of non-rivalrous stimuli. Moreover, activity in areas of fronto-parietal regions during the delay period correlated with the degree to which individual participants tended to experience percept stabilization. Our findings suggest that percept-related activity in specialized extrastriate visual areas help to stabilize perception during perceptual conflict, and that high-level mechanisms may determine the influence of such signals on conscious perception.     

Examining encoding imprecision in spatial working memory in schizophrenia

BACKGROUND: Visuospatial working memory is not a unitary sketch pad but comprises independent dimensions of target distance and direction and at least two levels of detail (fine-grained and category level). The aim of this study was to examine these multiple aspects of encoding in patients with schizophrenia using a modified delayed response task. METHOD: 42 patients with schizophrenia and 48 healthy controls pointed, as accurately as possible from a fixed starting position, to the visual location of target stimuli presented to a touch-sensitive screen. An adaptive staircase procedure was used to equate stimulus duration for each individual. Encoding accuracy and maintenance of distance (mm) and direction ( degrees ) information was examined following a 0-second (immediate) or 4-second (unfilled) delay. Analyses utilized both absolute (unsigned) and signed data. RESULTS: The results showed that the average duration required to detect a target was significantly longer in patients than controls. When stimulus duration was equated, (a) the absolute accuracy of distance and direction responses was not significantly different between groups at 0-second delay but was significantly reduced at 4-second delay in patients with schizophrenia, and (b) signed direction errors at 4-second delay were significantly different between groups at stimulus angles greater than 90 degrees . CONCLUSIONS: The findings challenge previous suggestions of deficits in fine-grained encoding of spatial information in schizophrenia but confirm a difficulty maintaining both direction and distance details in working memory. Imprecision in spatial memory in schizophrenia also introduced greater bias from category level (prior) representations, especially in left hemi-space.     

Functional properties of parietal visual neurons: radial organization of directionalities within the visual field

Parietal visual neurons (PVNs) were studied in waking monkeys as they executed a simple fixation-detection task. Test visual stimuli of varied direction, speed, and extent were presented during the fixation period; these stimuli did not control behavior. Most PVNs subtend large, bilateral receptive fields and are exquisitely sensitive to stimulus motion and direction but insensitive to stimulus speed. The directional preferences of PVNs along meridians are opponently organized, with the preferred directions pointing either inward toward or outward away from the fixation point. Evidence presented in the preceding paper (Motter et al., 1987) indicates that opponent directionality along a single meridian is produced by a feed-forward inhibition of 20 degrees-30 degrees spatial extent. The observations fit a double-Gaussian model of superimposed but unequal excitatory and inhibitory receptive fields: When the former is larger, inward directionality results; when smaller, outward directionality results. We examine here the distribution of the meridional directional preferences in the visual field. Tests showed that opponent organization is not produced by differences in local directional properties in different parts of the receptive field. The distribution of response intensities from one meridian to another is adequately described by a sine wave function. These data indicate a best radial direction for each neuron with a broad distribution of response intensities over successive meridians. Thus, any single PVN, with rare exceptions, cannot signal radial stimulus direction precisely. We then determined how accurately the population response predicted radial stimulus direction by the application of a linear vector summation model. The resulting population vector varied from stimulus direction by an average of 9 degrees. Whether or not the perception of the direction of motion depends upon a population vector remains uncertain. PVNs are especially sensitive to object movement in the visual surround, particularly in the periphery of the visual field. This, combined with their large receptive fields and their wide but flat sensitivity to stimulus speed, makes them especially sensitive to optic flow. This is discussed in relation to the role of the parietal visual system in the visual guidance of projected movements of the arm and hand, in the guidance of locomotion, and in evoking the illusion of vection.     

When a thought equals a look: refreshing enhances perceptual memory

Cognition constantly involves retrieving and maintaining information that is not perceptually available in the current environment. Studies on visual imagery and working memory suggest that such high-level cognition might, in part, be mediated by the revival of perceptual representations in the inferior temporal cortex. Here, we provide new support for this hypothesis, showing that reflectively accessed information can have similar consequences for subsequent perception as actual perceptual input. Participants were presented with pairs of frames in which a scene could appear, and were required to make a category judgment on the second frame. In the critical condition, a scene was presented in the first frame, but the second frame was blank. Thus, it was necessary to refresh the scene from the first frame in order to make the category judgment. Scenes were then repeated in subsequent trials to measure the effect of refreshing on functional magnetic resonance imaging repetition attenuation -- a neural index of memory -- in a scene-selective region of the visual cortex. Surprisingly, the refreshed scenes produced equal attenuation as scenes that had been presented twice during encoding, and more attenuation than scenes that had been presented once during encoding, but that were not refreshed. Thus, the top-down revival of a percept had a similar effect on memory as actually seeing the stimulus again. These findings indicate that high-level cognition can activate stimulus-specific representations in the ventral visual cortex, and that such top-down activation, like that from sensory stimulation, produces memorial changes that affect perceptual processing during a later encounter with the stimulus.     

Synaptic reverberation underlying mnemonic persistent activity

Stimulus-specific persistent neural activity is the neural process underlying active (working) memory. Since its discovery 30 years ago, mnemonic activity has been hypothesized to be sustained by synaptic reverberation in a recurrent circuit. Recently, experimental and modeling work has begun to test the reverberation hypothesis at the cellular level. Moreover, theory has been developed to describe memory storage of an analog stimulus (such as spatial location or eye position), in terms of continuous 'bump attractors' and 'line attractors'. This review summarizes new studies, and discusses insights and predictions from biophysically based models. The stability of a working memory network is recognized as a serious problem; stability can be achieved if reverberation is largely mediated by NMDA receptors at recurrent synapses.     

Neural correlates of spontaneous percept switches in ambiguous stimuli: an event‐related functional magnetic resonance imaging study

When ambiguous visual stimuli are being looked at, perception alternates spontaneously between two competing interpretations of the same sensory input. One major issue in understanding the underlying neural process is whether spontaneous percept switches result from fluctuations at the level of sensory processes or whether they are initiated by higher‐order areas. To further study this question, we developed an ambiguous apparent motion paradigm that specifically focused on the generation of percept switches. The percept switches occurred either spontaneously or were experimentally triggered. The differential analysis of spontaneous and triggered percept switches was aimed at disentangling the causes and effects of percept switches. Spontaneous percept switches were associated with stronger activations at the right occipitotemporal junction, whereas prefrontal, superior temporal and inferior parietal regions showed greater activations during experimentally triggered percept switches. We propose that complex networks including both sensory and higher‐order areas are involved in percept switches, whereas stimulus‐specific sensory processes are crucial for the initiation of spontaneous percept switches.     

Moving objects appear to slow down at low contrasts.

Moving cars give the illusion of slowing down in foggy conditions, because low contrast reduces perceived speed. A grey square that drifts horizontally across a surround of black and white vertical stripes appears to stop and start as it crosses each stripe, because its contrast keeps changing. A moving square whose vertical and horizontal edges have different contrasts will show illusory distortions in perceived direction. Contrast also affects the apparent amplitude and salience of back-and-forth apparent motion. Finally, a line of black and white dots on a grey surround moves in illusory directions, because of a mismatch in the contrasts along and across the dotted line. Thus, motion signals in the early parts of the visual system are profoundly altered by stimulus luminance and contrast. This suggests that motion is coded by the relative firing rates of neural channels tuned to fast and slow motion, with contrast-dependence being a motion analog of the Bezold-Brucke hue shift.     

Prior information of stimulus location: effects on ERP measures of visual selection and response selection

This paper examines the effects of prior information of the location of an upcoming stimulus on event-related EEG potentials associated with the focusing of attention. Results of two tasks, reported in a previous publication (Praamstra, P., Boutsen, L., Humphreys, G.W., 2005. Frontoparietal control of spatial attention and motor intention in human EEG. J. Neurophysiol. 94, 764-774), were compared: one in which spatial attention was cued to the stimulus location and one in which the cue was non-informative. Only informative directional cues elicited directing-attention EEG potentials in the delay period between cue and target. Notwithstanding these electrophysiological signs of an attentional orientation prior to the occurrence of the target, there were no reaction time effects related to the presence of advance spatial information. By contrast, the advance information did have effects on EEG potentials following the target stimulus. The N2pc, reflecting an attentional selection mechanism in extrastriate cortex, was reduced in amplitude with advance spatial information. The N2cc, coinciding in time with the N2pc but measured over the motor cortex, was preempted by the advance spatial information. These results support that the N2cc is not due to overlap of the N2pc with movement execution-related activity. It is proposed that the neural activity underlying this EEG potential arises from the dorsal premotor cortex and serves an executive-attentional function that helps to ensure that the selection of a manual response is not biased by the direction of spatial attention.     

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.     

The dual nature of the BOLD signal: Responses in visual area hMT+ reflect both input properties and perceptual decision

Neuroimaging studies have suggested that hMT+ encodes global motion interpretation, but this contradicts the notion that BOLD activity mainly reflects neuronal input. While measuring fMRI responses at 7 Tesla, we used an ambiguous moving stimulus, yielding the perception of two incoherently moving surfaces—component motion—or only one coherently moving surface—pattern motion, to induce perceptual fluctuations and identify perceptual organization size‐matched domains in hMT+. Then, moving gratings, exactly matching either the direction of component or pattern motion percepts of the ambiguous stimulus, were shown to the participants to investigate whether response properties reflect the input or decision. If hMT+ responses reflect the input, component motion domains (selective to incoherent percept) should show grating direction stimulus‐dependent changes, unlike pattern motion domains (selective to the coherent percept). This hypothesis is based on the known direction‐selective nature of inputs in component motion perceptual domains versus non‐selectivity in pattern motion perceptual domains. The response amplitude of pattern motion domains did not change with grating direction (consistently with their non‐selective input), in contrast to what happened for the component motion domains (consistently with their selective input). However, when we analyzed relative ratio measures they mirrored perceptual interpretation. These findings are consistent with the notion that patterns of BOLD responses reflect both sensory input and perceptual read‐out.     

The inferior colliculus encodes the Franssen auditory spatial illusion

Illusions are effective tools for the study of the neural mechanisms underlying perception because neural responses can be correlated to the physical properties of stimuli and the subject's perceptions. The Franssen illusion (FI) is an auditory spatial illusion evoked by presenting a transient, abrupt tone and a slowly rising, sustained tone of the same frequency simultaneously on opposite sides of the subject. Perception of the FI consists of hearing a single sound, the sustained tone, on the side that the transient was presented. Both subcortical and cortical mechanisms for the FI have been proposed, but, to date, there is no direct evidence for either. The data show that humans and rhesus monkeys perceive the FI similarly. Recordings were taken from single units of the inferior colliculus in the monkey while they indicated the perceived location of sound sources with their gaze. The results show that the transient component of the Franssen stimulus, with a shorter first spike latency and higher discharge rate than the sustained tone, encodes the perception of sound location. Furthermore, the persistent erroneous perception of the sustained stimulus location is due to continued excitation of the same neurons, first activated by the transient, by the sustained stimulus without location information. These results demonstrate for the first time, on a trial‐by‐trial basis, a correlation between perception of an auditory spatial illusion and a subcortical physiological substrate.     

Nonverbal working memory deficits in schizophrenia patients: evidence of a supramodal executive processing deficit

BACKGROUND: Although there have been several investigations of spatial working memory performance in schizophrenia patients, there have been considerably fewer studies of object working memory. The purpose of the present investigation was to evaluate the domain specificity of nonverbal working memory impairment in schizophrenia patients. METHODS: Delayed match-to-sample tasks involving spatial, identity and affective information were administered to schizophrenia and schizophrenia-spectrum patients (n=36) and normal controls (n=29). RESULTS: Using visual stimuli that can be considered prototypical of object vision, namely, faces we observed that schizophrenia patients perform poorly on working memory tasks that are based on the identity and/or features of the stimulus (i.e., object-based working memory tasks) as well as on a working memory task based on the spatial location of the stimulus. We observed significant associations between global ratings of negative symptoms and working memory performance. CONCLUSIONS: These data demonstrate that the working memory deficit displayed by schizophrenia and schizophrenia-spectrum patients extends to nonspatial visual domains.     

Specific activation of the V5 brain area by auditory motion processing: an fMRI study

Previous neuroimaging studies devoted to auditory motion processing have shown the involvement of a cerebral network encompassing the temporoparietal and premotor areas. Most of these studies were based on a comparison between moving stimuli and static stimuli placed at a single location. However, moving stimuli vary in spatial location, and therefore motion detection can include both spatial localisation and motion processing. In this study, we used fMRI to compare neural processing of moving sounds and static sounds in various spatial locations in blindfolded sighted subjects. The task consisted of simultaneously determining both the nature of a sound stimulus (pure tone or complex sound) and the presence or absence of its movement. When movement was present, subjects had to identify its direction. This comparison of how moving and static stimuli are processed showed the involvement of the parietal lobules, the dorsal and ventral premotor cortex and the planum temporale during auditory motion processing. It also showed the specific recruitment of V5, the visual motion area. These results suggest that the previously proposed network of auditory motion processing is distinct from the network of auditory localisation. In addition, they suggest that the occipital cortex can process non-visual stimuli and that V5 is not restricted to visual processing.