Extrastriate Area MT Research Articles

Visual Response Properties of Striate Cortical Neurons Projecting to Area MT in Macaque Monkeys

We have previously shown that some neurons in extrastriate area MT are capable of signaling the global motion of complex patterns; neurons randomly sampled from V1, on the other hand, respond only to the motion of individual oriented components. Because only a small fraction of V1 neurons projects to MT, we wished to establish the processing hierarchy more precisely by studying the properties of those neurons projecting to MT, identified by antidromic responses to electrical stimulation of MT. The neurons that project from V1 to MT were directionally selective and, like other V1 neurons, responded only to the motion of the components of complex patterns. The projection neurons were predominantly "special complex," responsive to a broad range of spatial and temporal frequencies, and sensitive to very low stimulus contrasts. The projection neurons thus comprise a homogeneous and highly specialized subset of V1 neurons, consistent with the notion that V1 acts as clearing house of basic visual measurements, distributing information appropriately to higher cortical areas for specialized analysis.

Morphology and connections of neurons in area 17 projecting to the extrastriate areas MT and 19DM and to the superior colliculus in the monkey Callithrix jacchus.

Neurons of area 17, the primary visual cortex, project to various anatomically and physiologically different extrastriate areas and subcortical regions. In the present investigation, we addressed the question of whether the efferent neurons in area 17 can contribute to functional diversity between these regions. We approached this question by analyzing the dendritic morphology of neurons in area 17 projecting to area MT, area 19DM, and the superior colliculus in the new world simian primate Callithrix jacchus, because dendritic morphology is an important factor in determining physiological properties of nerve cells. Retrograde transport of fluorochromes injected into the target regions, and intracellular injections of Lucifer yellow in the prelabelled neurons, revealed the following. 1) Morphologically identical large pyramidal cells in layer VI of area 17 project to all three targets. Some of them possess axon collaterals to two or all three targets, suggesting that they provide common information to all three areas. 2) Pyramidal cells in layer IIIc projecting to area MT form a morphologically homogeneous population. 3) Three small to medium-sized pyramidal cell types in layers IIIa-c, spiny stellate cells in layer IIIc, and another large pyramidal cell type in layer VI project to area 19DM. 4) Pyramidal cells in the lower two-thirds of layer V in area 17 project to the superior colliculus. In conclusion, we have shown that in Callithrix one efferent pathway may originate from several cell types. However, with the exception of the large cells in layer VI, efferent cells projecting to area MT, area 19DM, and the superior colliculus were morphologically distinct. This suggests that functional differences between brain regions could arise in part from morphological heterogeneity between and within the efferent cell populations.

Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey

We recorded the responses of single neurons in extrastriate area MST while rhesus monkeys discriminated the direction of motion in a set of stochastic visual displays. By varying systematically the strength of a coherent motion signal within the visual display, we were able to measure simultaneously the monkeys' psychophysical thresholds for direction discrimination and the responses of single neurons to the same motion signals. Neuronal thresholds for reliably signaling the direction of motion in the visual display were calculated from the measured responses using a method based in signal detection theory. Neurons in MST were exquisitely sensitive to motion signals in the display, having thresholds for discriminating the direction of coherent motion that were, on average, equal to the psychophysical thresholds of the monkeys. For many MST neurons, the intensity of the response was correlated with the monkey's psychophysical judgements for repeated presentations of a given near-threshold stimulus; the monkey tended to choose the preferred direction of the neuron under study when that neuron responded more strongly to the stimulus. In both of these respects, MST neurons were indistinguishable from neurons in extrastriate area MT, a major source of afferent input to MST. In a second set of experiments, we found that both of these results held true in the face of pronounced manipulations of the visual stimulus. Severe reductions in stimulus size and speed, for example, compromised neuronal and psychophysical sensitivities by similar amounts so that the average neuronal and psychophysical thresholds remained approximately equal. In addition, the trial-to-trial covariation of neuronal response and perceptual decision was unaffected by our stimulus manipulations. Thus, MST neurons carry signals appropriate for supporting psychophysical performance on our task over an impressively wide range of stimulus configurations.

Power spectrum analysis of bursting cells in area MT in the behaving monkey

It is widely held that visual cortical neurons encode information primarily in their mean firing rates. Some proposals, however, emphasize the information potentially available in the temporal structure of spike trains (Optican and Richmond, 1987; Bialek et al., 1991), in particular with respect to stimulus-related synchronized oscillations in the 30-70 Hz range (Eckhorn et al., 1988; Gray et al., 1989; Kreiter and Singer, 1992) as well as via bursting cells (Cattaneo et al., 1981a; Bonds, 1992). We investigate the temporal fine structure of spike trains recorded in extrastriate area MT of the trained macaque monkey, a region that plays a major role in processing motion information. The data were recorded while the monkey performed a near-threshold direction discrimination task so that both physiological and psychophysical data could be obtained on the same set of trials (Britten et al., 1992). We identify bursting cells and quantify their properties, in particular in relation to the behavior of the animal. We compute the power spectrum and the distribution of interspike intervals (ISIs) associated with individual spike trains from 212 cells, averaging these quantities across similar trials. (1) About 33% of the cells have a relatively flat power spectrum with a dip at low temporal frequencies. We analytically derive the power spectrum of a Poisson process with refractory period and show that it matches the observed spectrum of these cells. (2) About 62% of the cells have a peak in the 20-60 Hz frequency band. In about 10% of all cells, this peak is at least twice the height of its base. The presence of such a peak strongly correlates with a tendency of the cell to respond in bursts, that is, two to four spikes within 2-8 msec. For 93% of cells, the shape of the power spectrum did not change dramatically with stimulus conditions. (3) Both the ISI distribution and the power spectrum of the vast majority of bursting cells are compatible with the notion that these cells fire Poisson-distributed bursts, with a burst-related refractory period. Thus, for our stimulus conditions, no explicitly oscillating neuronal process is required to yield a peak in the power spectrum. (4) We found no statistically significant relationship between the peak in the power spectrum and psychophysical measures of the monkeys' performance on the direction discrimination task.(ABSTRACT TRUNCATED AT 400 WORDS)

Microstimulation in visual area MT: effects of varying pulse amplitude and frequency

We have previously shown that perceptual judgements of motion direction are based in part on the activity of direction selective neurons in extrastriate visual area MT (Salzman et al., 1990, 1992). In those experiments, we applied low-amplitude microstimulation pulses (10 microA, 200 Hz) to clusters of MT neurons whose preferred directions were similar. The effect of microstimulation was to bias the monkeys' choices on a direction discrimination task toward the preferred direction of neurons at the stimulation site. The results suggest that microstimulation generated a directionally specific cortical signal by activating selectively neurons near the electrode tip. To test this notion more directly, we have now examined the behavioral effects of varying current amplitude, current frequency, and electrode position. In the majority of experiments, the directional bias in the monkeys' choices was reduced or eliminated as current amplitude increased to 80 microA. In addition, 80 microA stimulating pulses frequently impaired overall performance as measured by the percentage of correct responses. This decrement in performance indicated that 80 microA pulses introduced "noise" into the neural circuitry encoding motion direction, presumably by increasing current spread to activate a larger population of neurons representing all directions of motion. In contrast, increasing current frequency to 500 Hz (10 microA pulses) preserved the directional specificity of microstimulation effects. The precise position of the stimulating electrode also influenced the magnitude of microstimulation effects; in some cases, differences in position on the order of 100 microns determined whether an experiment yielded a very large effect or no effect at all. Thus, directionally specific activation of cortical circuitry within MT can be disrupted by increases in current spread or by small changes in electrode position. These observations suggest that the effects of low-amplitude microstimulation depend upon direct activation of a well-localized population of neurons.

Functional anatomy of macaque striate cortex. III. Color

Using spatially diffuse stimuli (or sinusoidal gratings of very low spatial frequency), levels of 14C-2-deoxy-d-glucose (DG) uptake produced by color-varying stimuli are much greater than those produced by luminance-varying stimuli in macaque striate cortex. Such a difference in DG results is consistent with previous psychophysical and electrophysiological results from man and monkey. In DG experiments with color-varying gratings of low and middle spatial frequencies, or with spatially diffuse color variations, DG uptake was highest in the cytochrome oxidase blobs, as was also seen with low-spatial-frequency luminance gratings. High-spatial-frequency, color-varying uptake patterns were shifted to cover both blob and interblob regions in a manner similar to that of the patterns obtained with middle-spatial-frequency luminance stimuli. However, in no instance did chromatic gratings produce uptake restricted to the interblob regions, as with the pattern seen with the highest-spatial-frequency luminance gratings. Thus, DG uptake is relatively higher in the interblob regions when comparing luminance with color-varying gratings that are otherwise similar. It was also possible to show DG evidence for receptive-field double-opponency in the upper-layer blobs, but color sensitivity in layer 4Cb appears single-opponent. The DG results suggest that color sensitivity is also high in the lower-layer (layers 5 + 6) blobs, and that many layer 5 receptive fields are double-opponent. Striate layers 4Ca and 4B-appeared color-insensitive in a wide variety of DG tests; this supports the idea of a color-insensitive stream running from the magnocellular LGN layers through striate layers 4Ca and 4B to extrastriate areas MT and V3. There was also a major effect due to wavelength: long and short wavelengths produced much more uptake than did middle wavelengths, even when all colors were equated for luminance and saturation. No variation with eccentricity was seen in cortical color sensitivity, at least between 0 degrees and 10 degrees.

Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT

Mechanisms of direction selectivity and speed selectivity were studied in single neurons of the middle temporal visual area (MT) of behaving macaque monkeys. Visual stimuli were presented in both smooth and stroboscopic motion within a neuron's receptive field as the monkey fixated a stationary point of light. Direction selectivity, speed selectivity, and the spontaneous discharge characteristics of MT neurons in behaving monkeys were similar to those reported in previous studies in anesthetized monkeys. Stroboscopic motion stimuli were sequences of flashes characterized by the spatial and temporal intervals between each flash. The spatial and temporal intervals were systematically varied so that suppressive and facilitatory interactions could be studied in both the preferred and null directions. Suppression and facilitation were measured by subtracting the peak discharge rate elicited by a single flash from the peak discharge rate elicited by a stroboscopic train of flashes. The dominant mechanism of direction selectivity in MT was a pronounced suppression of discharge for motion in the null direction which we interpreted as inhibition. The inhibition was sufficiently potent to abolish the responses to single flashed stimuli when they were embedded in a series of flashes in the null direction, and it frequently reduced the neuronal discharge to a level below the spontaneous firing rate. Facilitation in the preferred direction was a prominent feature of the responses of some, but not all, MT neurons. The peak discharge rate for stroboscopic motion in the preferred direction was more than twice the peak rate to a single flash for approximately 50% of the neurons in our sample. The direction selectivity of most MT neurons showed the effects of both inhibitory and facilitatory mechanisms, and it was not possible to segregate MT neurons into distinct groups on the basis of these measures. Suppressive mechanisms contributed to speed tuning as well as direction tuning. The low-speed cutoff for motion in the preferred direction resulted from suppression in 82% of the neurons tested. The high-speed cutoff resulted from suppression in 32% of the neurons tested. The latter mechanism appeared to be distinct from the inhibitory mechanism which acted in the null direction in that large spatial intervals were required for its activation.

Motion selectivity in macaque visual cortex. III. Psychophysics and physiology of apparent motion.

We have conducted physiological and psychophysical experiments to identify possible neural substrates of the perception of apparent motion. We used identical sequences of flashed stimuli in both sets of experiments to better compare the responses of cortical neurons and psychophysical observers. Physiological data were obtained from two cortical visual areas, striate cortex (V1) and the middle temporal area (MT). In the previous paper we presented evidence that neuronal thresholds for direction selectivity in extrastriate area MT were similar to psychophysical thresholds for motion perception at the largest effective interflash interval, and thus speed, for a given eccentricity. We now examine physiological and psychophysical thresholds for a broad range of speeds to determine whether such a correspondence exists for speeds below the upper threshold considered in the previous paper. Stimuli were presented in stroboscopic motion of constant apparent speed while the spatial and temporal interflash intervals were systematically varied. For each neuron we measured the largest spatial interval that elicited directionally selective responses at each of several apparent speeds. We calculated the composite performance of neurons in both MT and V1 by averaging the spatial interval necessary for direction selectivity at each apparent speed. We employed the same apparent-motion stimuli for psychophysical experiments with human subjects in which we measured the spatial interval necessary for the perception of motion over a similar range of apparent speeds. We obtained a composite profile of psychophysical performance by averaging thresholds across subjects at each apparent speed. For high apparent speeds, physiological data from MT, but not V1, corresponded closely to the psychophysical data as suggested in the preceding paper. For low apparent speeds, however, physiological data from MT and V1 were similar to each other and to the psychophysical data. It would appear, therefore, that neurons in either V1 or MT could mediate the perceptual effect at low speeds, whereas MT is a stronger candidate for this role at high speeds. We suggest that the neuronal substrate for apparent motion may be distributed over multiple cortical areas, depending upon the speed and spatial interval of the stimulus.

Demonstration of lack of dorsal lateral geniculate nucleus input to extrastriate areas MT and Visual 2 in the macaque monkey

Injections of wheat germ conjugated and normal horseradish peroxidase in the identifiable extrastriate cortical areas MT and Visual 2 of the macaque monkey, indicate that these areas do not receive an input from the dorsal lateral geniculate nucleus as do other regions of extrastriate visual cortex.

Neurographic evidence in alcoholic neuropathy : D. Kountouris, M.E. Dughly, J. Haan and J. Milonas (Bochum, W. Germany)

The relationship between the neural processing of color and motion information has been a contentious issue in visual neuroscience. We examined this relationship directly by measuring neural responses to isoluminant S cone signals in extrastriate area MT of the macaque monkey. S cone stimuli produced robust, direction-selective responses at most recording sites, indicating that color signals are present in MT. While these responses were unequivocal, S cone contrast sensitivity was, on average, 1.0–1.3 log units lower than luminance contrast sensitivity. The presence of S cone responses and the relative sensitivity of MT neurons to S cone and luminance signals agree with functional magnetic resonance imaging (fMRI) measurements in human MT+. The results are consistent with the hypothesis that color signals in MT influence behavior in speed judgment tasks.

Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex.

Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex.