Dissociation of neuronal and psychophysical responses to local and global motion

Most neurons in cortical area MT (V5) are strongly direction selective, and their activity is closely associated with the perception of visual motion. These neurons have large receptive fields built by combining inputs with smaller receptive fields that respond to local motion. Humans integrate motion over large areas and can perceive what has been referred to as global motion. The large size and direction selectivity of MT receptive fields suggests that MT neurons may represent global motion. We have explored this possibility by measuring responses to a stimulus in which the directions of simultaneously presented local and global motion are independently controlled. Surprisingly, MT responses depended only on the local motion and were unaffected by the global motion. Yet, under similar conditions, human observers perceive global motion and are impaired in discriminating local motion. Although local motion perception might depend on MT signals, global motion perception depends on mechanisms qualitatively different from those in MT. Motion perception therefore does not depend on a single cortical area but reflects the action and interaction of multiple brain systems.     

Spatial distribution and interaction of responses in receptive fields of cat lateral geniculate neurons

Responses of lateral geniculate neurons to local photic stimulation and to adaptation of the central, antagonistic, and disinhibiting zones of their receptive fields were compared in unanesthetized cats immobilized with D-tubocurarine. Under most conditions of local adaptation, activation of on- and off-responses of neurons occurred after stimulation of the peripheral zones and inhibition of responses after stimulation of the central zone of the receptive field. As a result most neurons acquired the ability to generate a considerable on- and off-signal in response to stimulation. Comparison of this fact with the properties of on-off neurons [7] supports the view that under light-adaptation conditions the processing of large volumes of visual information and the more sophisticated performance of visual functions are connected with activation of responses from peripheral zones of circular receptive fields. It is concluded that local adaptation to light can extend the functional capacity of circular receptive fields.Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 15, No. 5, pp. 451–456, September–October, 1983.     

A system of insect neurons sensitive to horizontal and vertical image motion connects the medulla and midbrain

Summary The response properties and gross morphologies of neurons that connect the medulla and midbrain in the butterfly Papilio aegeus are described. The neurons presented give direction-selective responses, i.e. they are excited by motion in the preferred direction and the background activity of the cells is inhibited by motion in the opposite, null, direction. The neurons are either maximally sensitive to horizontal motion or to slightly off-axis vertical upward or vertical downward motion, when tested in the frontal visual field. The responses of the cells are dependent on the contrast frequency of the stimulus with peak values at 5–10 Hz. The receptive fields of the medulla neurons are large and are most sensitive in the frontal visual field. Examination of the local and global properties of the receptive fields of the medulla neurons indicates that (1) they are fed by local elementary motion-detectors consistent with the correlation model and (2) there is a non-linear spatial integration mechanism in operation.     

Relationship between Size Summation Properties,Contrast Sensitivity and Response Latency in the Dorsomedial and Middle Temporal Areas of the Primate Extrastriate Cortex

Analysis of the physiological properties of single neurons in visual cortex has demonstrated that both the extent of their receptive fields and the latency of their responses depend on stimulus contrast. Here, we explore the question of whether there are also systematic relationships between these response properties across different cells in a neuronal population. Single unit recordings were obtained from the middle temporal (MT) and dorsomedial (DM) extrastriate areas of anaesthetized marmoset monkeys. For each cell, spatial integration properties (length and width summation, as well as the presence of end- and side-inhibition within 15° of the receptive field centre) were determined using gratings of optimal direction of motion and spatial and temporal frequencies, at 60% contrast. Following this, contrast sensitivity was assessed using gratings of near-optimal length and width. In both areas, we found a relationship between spatial integration and contrast sensitivity properties: cells that summated over smaller areas of the visual field, and cells that displayed response inhibition at larger stimulus sizes, tended to show higher contrast sensitivity. In a sample of MT neurons, we found that cells showing longer latency responses also tended to summate over larger expanses of visual space in comparison with neurons that had shorter latencies. In addition, longer-latency neurons also tended to show less obvious surround inhibition. Interestingly, all of these effects were stronger and more consistent with respect to the selectivity for stimulus width and strength of side-inhibition than for length selectivity and end-inhibition. The results are partially consistent with a hierarchical model whereby more extensive receptive fields require convergence of information from larger pools of “feedforward” afferent neurons to reach near-optimal responses. They also suggest that a common gain normalization mechanism within MT and DM is involved, the spatial extent of which is more evident along the cell’s preferred axis of motion.     

‘Vector white noise’: a technique for mapping the motion receptive fields of direction-selective visual neurons

A technique is described and tested for mapping the sensitivities and preferred directions of motion at different locations within the receptive fields of direction-selective motion-detecting visual neurons. The procedure is to record the responses to a number of visual stimuli, each stimulus presentation consisting of a set of short, randomly-oriented, moving bars arranged in a square grid. Each bar moves perpendicularly to its long axis. The vector describing the sensitivity and preferred direction of motion at each grid location is obtained as a sum of the unit vectors defining the directions of motion of the bars in each of the stimuli at that location, weighted by the strengths of the corresponding responses. The resulting vector field specifies the optimum flow field for the neuron. The advantage of this technique over the conventional approach of probing the receptive field sequentially at each grid location is that the parallel nature of the stimulus is sensitive to nonlinear interactions (such as shunting inhibition for mutual facilitation) between different regions of the visual field. The technique is used to determine accurately the motion receptive fields of direction-selective motion detecting neurons in the optic lobes of insects. It is potentially applicable to motion-sensitive neurons with highly structured receptive fields, such as those in the optic tectum of the pigeon or in area MST of the monkey.     

Feature-based attention increases the selectivity of population responses in primate visual cortex

BACKGROUND: Attending to the spatial location or to nonspatial features of visual stimuli can modulate neuronal responses in primate visual cortex. The modulation by spatial attention changes the gain of sensory neurons and strengthens the representation of attended locations without changing neuronal selectivities such as directionality, i.e., the ratio of responses to preferred and anti-preferred directions of motion. Whether feature-based attention acts in a similar manner is unknown. RESULTS: To clarify this issue, we recorded the responses of 135 direction-selective neurons in the middle temporal area (MT) of two macaques to an unattended moving random dot pattern (the distractor) positioned inside a neuron's receptive field while the animals attended to a second moving pattern positioned in the opposite hemifield. Responses to different directions of the distractor were modulated by the same factor (approximately 12%) as long as the attended direction remained unchanged. On the other hand, systematically changing the attended direction from a neuron's preferred to its anti-preferred direction caused a systematic change of the attentional modulation from an enhancement to a suppression, increasing directionality by about 20%. CONCLUSIONS: The results show that (1) feature-based attention exerts a multiplicative modulation upon neuronal responses and that the strength of this modulation depends on the similarity between the attended feature and the cell's preferred feature, in line with the feature-similarity gain model, and (2) at the level of the neuronal population, feature-based attention increases the selectivity for attended features by increasing the responses of neurons preferring this feature value while decreasing responses of neurons tuned to the opposite feature value.     

Parietal neurons encoding visual space in a head-frame of reference.

Neurons of the visual system are known to have receptive fields organized in retinotopic coordinates. We wanted to test whether visual neurons existed whose receptive fields were organized in spatial coordinates. Extracellular recordings from single cells were carried out in one area of the posterior parietal cortex (area V6) of a behaving macaque monkey. Among a great majority of retinotopically organized visual cells, neurons whose visual receptive field did not shift with gaze were also found. These cells responded to the visual stimulation of the same spatial position independently of the animal's direction of gaze, that is, their receptive field was anchored to an absolute spatial location. We suggest that these neurons directly encode visual space and are involved in programming visually-guided motor actions in space.     

Segregation of object and background motion in visual area MT: effects of microstimulation on eye movements

To track a moving object, its motion must first be distinguished from that of the background. The center-surround properties of neurons in the middle temporal visual area (MT) may be important for signaling the relative motion between object and background. To test this, we microstimulated within MT and measured the effects on monkeys' eye movements to moving targets. We found that stimulation at "local motion" sites, where receptive fields possessed antagonistic surrounds, shifted pursuit in the preferred direction of the neurons, whereas stimulation at "wide-field motion" sites shifted pursuit in the opposite, or null, direction. We propose that activating wide-field sites simulated background motion, thus inducing a target motion signal in the opposite direction. Our results support the hypothesis that neuronal center-surround mechanisms contribute to the behavioral segregation of objects from the background.     

Response properties of visual interneurons to motion stimuli in the praying mantis,Tenodera aridifolia

Intracellular responses of motion-sensitive visual interneurons were recorded from the lobula complex of the mantis, Tenodera aridifolia. The interneurons were divided into four classes according to the response polarity, spatial tuning, and directional selectivity. Neurons of the first class had small, medium, or large receptive fields and showed a strong excitation in response to a small-field motion such as a small square moving in any direction (SF neurons). The second class neurons showed non-directionally selective responses: an excitation to a large-field motion of gratings in any direction (ND neurons). Most ND neurons had small or medium-size receptive fields. Neurons of the third class had large receptive fields and exhibited directionally selective responses: an excitation to a large-field motion of gratings in preferred direction and an inhibition to a motion in opposite, null direction (DS neurons). The last class neurons had small receptive fields and showed inhibitory responses to a moving square and gratings (I neurons). The functional roles of these neurons in prey recognition and optomotor response were discussed.     

Adaptation to stimulus contrast and correlations during natural visual stimulation

In this study, we characterize the adaptation of neurons in the cat lateral geniculate nucleus to changes in stimulus contrast and correlations. By comparing responses to high- and low-contrast natural scene movie and white noise stimuli, we show that an increase in contrast or correlations results in receptive fields with faster temporal dynamics and stronger antagonistic surrounds, as well as decreases in gain and selectivity. We also observe contrast- and correlation-induced changes in the reliability and sparseness of neural responses. We find that reliability is determined primarily by processing in the receptive field (the effective contrast of the stimulus), while sparseness is determined by the interactions between several functional properties. These results reveal a number of adaptive phenomena and suggest that adaptation to stimulus contrast and correlations may play an important role in visual coding in a dynamic natural environment.     

Adaptation-dependent synchronous activity contributes to receptive field size change of bullfrog retinal ganglion cell

Nearby retinal ganglion cells of similar functional subtype have a tendency to discharge spikes in synchrony. The synchronized activity is involved in encoding some aspects of visual input. On the other hand, neurons always continuously adjust their activities in adaptation to some features of visual stimulation, including mean ambient light, contrast level, etc. Previous studies on adaptation were primarily focused on single neuronal activity, however, it is also intriguing to investigate the adaptation process in population neuronal activities. In the present study, by using multi-electrode recording system, we simultaneously recorded spike discharges from a group of dimming detectors (OFF-sustained type ganglion cells) in bullfrog retina. The changes in receptive field properties and synchronization strength during contrast adaptation were analyzed. It was found that, when perfused using normal Ringer's solution, single neuronal receptive field size was reduced during contrast adaptation, which was accompanied by weakening in synchronization strength between adjacent neurons' activities. When dopamine (1 μM) was applied, the adaptation-related receptive field area shrinkage and synchronization weakening were both eliminated. The activation of D1 receptor was involved in the adaptation-related modulation of synchronization and receptive field. Our results thus suggest that the size of single neuron's receptive field is positively related to the strength of its synchronized activity with its neighboring neurons, and the dopaminergic pathway is responsible for the modulation of receptive field property and synchronous activity of the ganglion cells during the adaptation process.     

Orientation tuning of motion-sensitive neurons shaped by vertical-horizontal network interactions

We measured the orientation tuning of two neurons of the fly lobula plate (H1 and H2 cells) sensitive to horizontal image motion. Our results show that H1 and H2 cells are sensitive to vertical motion, too. Their response depended on the position of the vertically moving stimuli within their receptive field. Stimulation within the frontal receptive field produced an asymmetric response: upward motion left the H1/H2 spike frequency nearly unaltered while downward motion increased the spike frequency to about 40% of their maximum responses to horizontal motion. In the lateral parts of their receptive fields, no such asymmetry in the responses to vertical image motion was found. Since downward motion is known to be the preferred direction of neurons of the vertical system in the lobula plate, we analyzed possible interactions between vertical system cells and H1 and H2 cells. Depolarizing current injection into the most frontal vertical system cell (VS1) led to an increased spike frequency, hyperpolarizing current injection to a decreased spike frequency in both H1 and H2 cells. Apart from VS1, no other vertical system cell (VS2-8) had any detectable influence on either H1 or H2 cells. The connectivity of VS1 and H1/H2 is also shown to influence the response properties of both centrifugal horizontal cells in the contralateral lobula plate, which are known to be postsynaptic to the H1 and H2 cells. The vCH cell receives additional input from the contralateral VS2-3 cells via the spiking interneuron V1.     

Contrast gain reduction in fly motion adaptation

In many species, including humans, exposure to high image velocities induces motion adaptation, but the neural mechanisms are unclear. We have isolated two mechanisms that act on directionally selective motion-sensitive neurons in the fly's visual system. Both are driven strongly by movement and weakly, if at all, by flicker. The first mechanism, a subtractive process, is directional and is only activated by stimuli that excite the neuron. The second, a reduction in contrast gain, is strongly recruited by motion in any direction, even if the adapting stimulus does not excite the cell. These mechanisms are well designed to operate effectively within the context of motion coding. They can prevent saturation at susceptible nonlinear stages in processing, cope with rapid changes in direction, and preserve fine structure within receptive fields.     

Pattern-dependent response modulations in motion-sensitive visual interneurons--a model study

Even if a stimulus pattern moves at a constant velocity across the receptive field of motion-sensitive neurons, such as lobula plate tangential cells (LPTCs) of flies, the response amplitude modulates over time. The amplitude of these response modulations is related to local pattern properties of the moving retinal image. On the one hand, pattern-dependent response modulations have previously been interpreted as 'pattern-noise', because they deteriorate the neuron's ability to provide unambiguous velocity information. On the other hand, these modulations might also provide the system with valuable information about the textural properties of the environment. We analyzed the influence of the size and shape of receptive fields by simulations of four versions of LPTC models consisting of arrays of elementary motion detectors of the correlation type (EMDs). These models have previously been suggested to account for many aspects of LPTC response properties. Pattern-dependent response modulations decrease with an increasing number of EMDs included in the receptive field of the LPTC models, since spatial changes within the visual field are smoothed out by the summation of spatially displaced EMD responses. This effect depends on the shape of the receptive field, being the more pronounced--for a given total size--the more elongated the receptive field is along the direction of motion. Large elongated receptive fields improve the quality of velocity signals. However, if motion signals need to be localized the velocity coding is only poor but the signal provides--potentially useful--local pattern information. These modelling results suggest that motion vision by correlation type movement detectors is subject to uncertainty: you cannot obtain both an unambiguous and a localized velocity signal from the output of a single cell. Hence, the size and shape of receptive fields of motion sensitive neurons should be matched to their potential computational task.     

Motion sensitive interneurons in the optomotor system of the fly

The functional properties of the three horizontal cells (north horizontal cell, HSN; equatorial horizontal cell, HSE; south horizontal cell, HSS) in the lobula plate of the blowflyCalliphora erythrocephala were investigated electrophysiologically. 1. The receptive fields of the HSN, HSE, and HSS cover the dorsal, equatorial and ventral part of the ipsilateral visual field, respectively. In all three cells, the sensitivity to visual stimulation is highest in the frontal visual field and decreases laterally. The receptive fields and spatial sensitivity distributions of the horizontal cells are directly determined by the position and extension of their dendritic fields in the lobula plate and the dendritic density distributions within these fields. 2. The horizontal cells respond mainly to progressive (front to back) motion and are inhibited by motion in the reverse direction, the preferred and null direction being antiparallel. The amplitudes of motion induced excitatory and inhibitory responses decline like a cosine function with increasing deviation of the direction of motion from the preferred direction. Stimulation with motion in directions perpendicular to the preferred direction is ineffective. 3. The preferred directions of the horizontal cells show characteristic gradual orientation changes in different parts of the receptive fields: they are horizontally oriented only in the equatorial region and increasingly tilted vertically towards the dorsofrontal and ventrofrontal margins of the visual field. These orientation changes can be correlated with equivalent changes in the local orientation of the lattice of ommatidial axes in the pertinent compound eye. 4. The response amplitudes of the horizontal cells under stimulation with a moving periodic grating depend strongly on the contrast frequency of the stimulus. Maximal responses were found at contrast frequencies of 2–5 Hz. 5. The spatial integration properties of the horizontal cells (studied in the HSE) are highly nonlinear. Under stimulation with extended moving patterns, their response amplitudes are nearly independent of the size of the stimuli. It is demonstrated that this response behaviour does not result from postsynaptic saturation in the dendrites of the cells. The results indicate that the horizontal system is essentially involved in the neural control of optomotor torque responses performed by the fly in order to minimize unvoluntary deviations from a straight flight course.     

Responses of primary somatosensory cortical neurons to paired stimulation of the infraorbital nerve and vibrissae in cats

Extra- and intracellular responses of 128 neurons to paired stimulation of the infraorbital nerve and vibrissae, recorded in the projection zone of the vibrissae in cortical area SI, were studied in adult cats immobilized with tubocurarine. Conditioning stimulation completely suppressed the ability of different neurons to respond for periods of between 10 and 120 msec. The duration of the period of total suppression of test responses was shown to depend on the location of the stimulated vibrissa in the peripheral receptive field of the neurons studied. Excitatory and inhibitory responses of maximal intensity arose in the neurons to stimulation of receptive field centers. The functional role of the decrease in intensity of excitatory responses during stimulation of vibrissae located at different distances from centers of the receptive fields of cortical neurons is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 13, No. 2, pp. 117–124, April, 1981.     

Antennal receptive fields of pheromone-responsive projection neurons in the antennal lobes of the male sphinx moth Manduca sexta

Stimulation of the antenna of the male moth, Manduca sexta, with a key component of the female's sex pheromone and a mimic of the second key component evokes responses in projection neurons in the sexually dimorphic macroglomerular complex of the antennal lobe. Using intracellular recording and staining techniques, we studied the antennal receptive fields of 149 such projection neurons. An antennal flagellum was stimulated in six regions along its proximo-distal axis with one or both of the pheromone-related compounds while activity was recorded in projection neurons. These neurons fell mainly into two groups, based on their responses to the two-component blend: neurons with broad receptive fields that were excited when any region of the flagellum was stimulated, and neurons selectively excited by stimulation of the proximal region of the flagellum. Projection neurons that were depolarized by stimulation of one antennal region were not inhibited by stimulation of other regions, suggesting absence of antennotopic center-surround organization. In most projection neurons, the receptive field was determined by afferent input evoked by only one of the two components. Different receptive-field properties of projection neurons may be related to the roles of these neurons in sensory control of the various phases of pheromone-modulated behavior of male moths. Accepted: 30 January 1998     

Shifts in coding properties and maintenance of information transmission during adaptation in barrel cortex

Neuronal responses to ongoing stimulation in many systems change over time, or “adapt.” Despite the ubiquity of adaptation, its effects on the stimulus information carried by neurons are often unknown. Here we examine how adaptation affects sensory coding in barrel cortex. We used spike-triggered covariance analysis of single-neuron responses to continuous, rapidly varying vibrissa motion stimuli, recorded in anesthetized rats. Changes in stimulus statistics induced spike rate adaptation over hundreds of milliseconds. Vibrissa motion encoding changed with adaptation as follows. In every neuron that showed rate adaptation, the input–output tuning function scaled with the changes in stimulus distribution, allowing the neurons to maintain the quantity of information conveyed about stimulus features. A single neuron that did not show rate adaptation also lacked input–output rescaling and did not maintain information across changes in stimulus statistics. Therefore, in barrel cortex, rate adaptation occurs on a slow timescale relative to the features driving spikes and is associated with gain rescaling matched to the stimulus distribution. Our results suggest that adaptation enhances tactile representations in primary somatosensory cortex, where they could directly influence perceptual decisions.     

The spatial substructure of visual receptive fields in the cat's superior colliculus

Although the direction selective properties of the superficial layer cells of the cat's superior colliculus have been extensively studied, the mechanisms underlying this property remain controversial. With the aim to understand the mechanism(s) underlying directional selectivity of collicular neurons we examined the substructure of their visual receptive fields. 1. The strength of cell responses and the direction selectivity indices varied in relation to the location of the tested region within the receptive field and the amplitude of stimulus movement. 2. Decrease of the amplitude of motion resulted in a decrease of direction selectivity index both in the group of direction-selective cells and in the group of cells classified as direction nonselective but with a directional bias. 3. The decrease of direction selectivity for small amplitude movement resulted mainly from increase in the magnitude of response in the nonpreferred direction of movement. 4. These results suggest that the receptive fields of most collicular cells are composed of subregions with different response profiles and indicate that inhibitory mechanisms dictate direction selectivity of collicular cells.     

Rapid dynamics of contrast responses in the cat primary visual cortex

The visual information we receive during natural vision changes rapidly and continuously. The visual system must adapt to the spatiotemporal contents of the environment in order to efficiently process the dynamic signals. However, neuronal responses to luminance contrast are usually measured using drifting or stationary gratings presented for a prolonged duration. Since motion in our visual field is continuous, the signals received by the visual system contain an abundance of transient components in the contrast domain. Here using a modified reverse correlation method, we studied the properties of responses of neurons in the cat primary visual cortex to different contrasts of grating stimuli presented statically and transiently for 40 ms, and showed that neurons can effectively discriminate the rapidly changing contrasts. The change in the contrast response function (CRF) over time mainly consisted of an increment in contrast gain (CRF shifts to left) in the developing phase of temporal responses and a decrement in response gain (CRF shifts downward) in the decay phase. When the distribution range of stimulus contrasts was increased, neurons demonstrated decrement in contrast gain and response gain. Our results suggest that contrast gain control (contrast adaptation) and response gain control mechanisms are well established during the first tens of milliseconds after stimulus onset and may cooperatively mediate the rapid dynamic responses of visual cortical neurons to the continuously changing contrast. This fast contrast adaptation may play a role in detecting contrast contours in the context of visual scenes that are varying rapidly.