Temporal Frequency Tuning Curves Research Articles

Spatiotemporal resonance in mouse primary visual cortex

Human primary visual cortex (V1) responds more strongly, or resonates, when exposed to ∼10, ∼15-20, and ∼40-50Hz rhythmic flickering light. Full-field flicker also evokes the perception of hallucinatory geometric patterns, which mathematical models explain as standing-wave formations emerging from periodic forcing at resonant frequencies of the simulated neural network. However, empirical evidence for such flicker-induced standing waves in the visual cortex was missing. We recorded cortical responses to flicker in awake mice using high-spatial-resolution widefield imaging in combination with high-temporal-resolution glutamate-sensing fluorescent reporter (iGluSnFR). The temporal frequency tuningcurves in the mouse V1 were similar to those observed in humans, showing a banded structure with multiple resonance peaks (8, 15, and 33Hz). Spatially, all flicker frequencies evoked responses inV1 corresponding to retinotopic stimulus location, but some evoked additional peaks. These flicker-induced cortical patterns displayed standing-wave characteristics and matched linear wave equationsolutions in an area restricted to the visual cortex. Taken together, the interaction of periodic traveling waves with cortical area boundaries leads to spatiotemporal activity patterns that may affect perception.

Temporal properties of colour opponent receptive fields in the cat lateral geniculate nucleus.

The primordial form of mammalian colour vision relies on opponent interactions between inputs from just two cone types, 'blue' (S-) and 'green' (ML-) cones. We recently described the spatial receptive field structure of colour opponent blue-ON cells from the lateral geniculate nucleus of cats. Functional inputs from the opponent cone types were spatially coextensive and equally weighted, supporting their high chromatic and low achromatic sensitivity. Here, we studied relative cone weights, temporal frequency tuning and visual latency of cat blue-ON cells and non-opponent achromatic cells to temporally modulated cone-isolating and achromatic stimuli. We confirmed that blue-ON cells receive equally weighted antagonistic inputs from S- and ML-cones whereas achromatic cells receive exclusive ML-cone input. The temporal frequency tuning curves of S- and ML-cone inputs to blue-ON cells were tightly correlated between 1 and 48Hz. Optimal temporal frequencies of blue-ON cells were around 3Hz, whereas the frequency optimum of achromatic cells was close to 10Hz. Most blue-ON cells showed negligible response to achromatic flicker across all frequencies tested. Latency to visual stimulation was significantly greater in blue-ON than in achromatic cells. The S- and ML-cone responses of blue-ON cells had on average, similar latencies to each other. Altogether, cat blue-ON cells showed remarkable balance of opponent cone inputs. Our results also confirm similarities to primate blue-ON cells suggesting that colour vision in mammals evolved on the basis of a sluggish pathway that is optimized for chromatic sensitivity at a wide range of spatial and temporal frequencies.

The Representation of Complex Images in Spatial Frequency Domains of Primary Visual Cortex

The organization of cat primary visual cortex has been well mapped using simple stimuli such as sinusoidal gratings, revealing superimposed maps of orientation and spatial frequency preferences. However, it is not yet understood how complex images are represented across these maps. In this study, we ask whether a linear filter model can explain how cortical spatial frequency domains are activated by complex images. The model assumes that the response to a stimulus at any point on the cortical surface can be predicted by its individual orientation, spatial frequency, and temporal frequency tuning curves. To test this model, we imaged the pattern of activity within cat area 17 in response to stimuli composed of multiple spatial frequencies. Consistent with the predictions of the model, the stimuli activated low and high spatial frequency domains differently: at low stimulus drift speeds, both domains were strongly activated, but activity fell off in high spatial frequency domains as drift speed increased. To determine whether the filter model quantitatively predicted the activity patterns, we measured the spatiotemporal tuning properties of the functional domains in vivo and calculated expected response amplitudes from the model. The model accurately predicted cortical response patterns for two types of complex stimuli drifting at a variety of speeds. These results suggest that the distributed activity of primary visual cortex can be predicted from cortical maps like those of orientation and SF preference generated using simple, sinusoidal stimuli, and that dynamic visual acuity is degraded at or before the level of area 17.

Spatial and temporal frequency selectivity of neurons in the middle temporal visual area of new world monkeys (Callithrix jacchus)

Information about the responses of neurons to the spatial and temporal frequencies of visual stimuli is important for understanding the types of computations being performed in different visual areas. We characterized the spatiotemporal selectivity of neurons in the middle temporal area (MT), which is deemed central for the processing of direction and speed of motion. Recordings obtained in marmoset monkeys using high-contrast sine-wave gratings as stimuli revealed that the majority of neurons had bandpass spatial and temporal frequency tuning, and that the selectivity for these parameters was largely separable. Only in about one-third of the cells was inseparable spatiotemporal tuning detected, this typically being in the form of an increase in the optimal temporal frequency as a function of increasing grating spatial frequency. However, most of these interactions were weak, and only 10% of neurons showed spatial frequency-invariant representation of speed. Cells with inseparable spatiotemporal tuning were most commonly found in the infragranular layers, raising the possibility that they form part of the feedback from MT to caudal visual areas. While spatial frequency tuning curves were approximately scale-invariant on a logarithmic scale, temporal frequency tuning curves covering different portions of the spectrum showed marked and systematic changes. Thus, MT neurons can be reasonably described as similarly built spatial frequency filters, each covering a different dynamic range. The small proportion of speed-tuned neurons, together with the laminar position of these units, are compatible with the idea that an explicit neural representation of speed emerges from computations performed in MT.

Functional Maturation of the Macaque's Lateral Geniculate Nucleus

Vision in infant primates is poor, but it is not known which structures in the eye or brain set the main limits to its development. We studied the visual response properties of 348 neurons recorded in the lateral geniculate nucleus (LGN) of macaque monkeys aged 1 week to adult. We measured spatial and temporal frequency tuning curves and contrast responses with drifting achromatic sinusoidal gratings. Even in animals as young as 1 week, the main visual response properties of neurons in the magnocellular (M) and parvocellular (P) divisions of the LGN were qualitatively normal, including the spatial organization of receptive fields and the characteristic response properties that differentiate M- and P-cells. At 1 and 4 weeks, spatial and temporal resolution were less than one-half of adult values, whereas contrast gain and peak response rates for optimal stimuli were about two-thirds of adult values. Adult levels were reached by 24 weeks. Analysis of correlations between S-potentials representing retinal inputs and LGN cells suggested that the LGN follows retinal input as faithfully in infants as in adults, implicating retinal development as the main driving force in LGN development. Comparisons with previously published psychophysical data and ideal observer models suggest that the relatively modest changes in LGN responses during maturation impose no significant limits on visual performance. In contrast to previous studies, we conclude that these limits are set by neural development in the visual cortex, not in or peripheral to the LGN.

Influence of contrast on orientation and temporal frequency tuning in ferret primary visual cortex.

Neurons in primary visual cortex are highly sensitive to the contrast, orientation, and temporal frequency of a visual stimulus. These three stimulus properties can be varied independently of one another, raising the question of how they interact to influence neuronal responses. We recorded from individual neurons in ferret primary visual cortex to determine the influence of stimulus contrast on orientation tuning, temporal-frequency tuning, and latency to visual response. Results show that orientation-tuning bandwidth is not affected by contrast level. Thus neurons in ferret visual cortex display contrast-invariant orientation tuning. Stimulus contrast does, however, influence the structure of orientation-tuning curves as measures of circular variance vary inversely with contrast for both simple and complex cells. This change in circular variance depends, in part, on a contrast-dependent change in the ratio of null to preferred orientation responses. Stimulus contrast also has an influence on the temporal-frequency tuning of cortical neurons. Both simple and complex cells display a contrast-dependent rightward shift in their temporal frequency-tuning curves that results in an increase in the highest temporal frequency needed to produce a half-maximum response (TF(50)). Results show that the degree of the contrast-dependent increase in TF(50) is similar for cortical neurons and neurons in the lateral geniculate nucleus (LGN) and indicate that subcortical mechanisms likely play a major role in establishing the degree of effect displayed by downstream neurons. Finally, results show that LGN and cortical neurons experience a contrast-dependent phase advance in their visual response. This phase advance is most pronounced for cortical neurons indicating a role for both subcortical and cortical mechanisms.

The temporal frequency tuning of human visual cortex investigated using synthetic aperture magnetometry

Using synthetic aperture magnetometry (SAM) analyses of magnetoencephalographic (MEG) data, we investigated the variation in cortical response magnitude and frequency as a function of stimulus temporal frequency. In two separate experiments, a reversing checkerboard stimulus was used in the right or left lower visual field at frequencies from 0 to 21 Hz. Average temporal frequency tuning curves were constructed for regions-of-interest located within medial visual cortex and V5/MT. In medial visual cortex, it was found that both the frequency and magnitude of the steady-state response varied as a function of the stimulus frequency, with multiple harmonics of the stimulus frequency being found in the response. The maximum fundamental response was found at a stimulus frequency of 8 Hz, whilst the maximum broadband response occurred at 4 Hz. In contrast, the magnitude and frequency content of the evoked onset response showed no dependency on stimulus frequency. Whilst medial visual cortex showed a power increase during stimulation, extra-striate areas such as V5/MT exhibited a bilateral event-related desynchronisation (ERD). The frequency content of this ERD did not depend on the stimulus frequency but was a broadband power reduction across the 5–20 Hz frequency range. The magnitude of this ERD within V5/MT was strongly low-pass tuned for stimulus frequency, and showed only a moderate preference for stimuli in the contralateral visual field.

A model of visual cortical temporal frequency tuning

There are several response properties that distinguish cortical simple cells of cat V1 layer 4 from the geniculate cells that provide their input. We have recently demonstrated that a developmentally motivated pattern of intracortical inhibition, in conjunction with the observed pattern of geniculocortical connections, can robustly account for the contrast-invariance of simple cell orientation tuning. We now show that this same model circuit unexpectedly accounts for the low-pass shift in the temporal frequency tuning curves of cortical cells relative to geniculate cells. This arises when NMDA-mediated excitatory conductances are included in the thalamocortical synapses, at levels observed experimentally.

Recursive implementations of temporal filters for image motion computation.

Efficient algorithms for image motion computation are important for computer vision applications and the modelling of biological vision systems. Intensity-based image motion computation proceeds in two stages: the convolution of linear spatiotemporal filter kernels with the image sequence, followed by the non-linear combination of the filter outputs. If the spatiotemporal extent of the filter kernels is large, then the convolution stage can be very intensive computationally. One effective means of reducing the storage required and computation involved in implementing the temporal convolutions is the introduction of recursive filtering. Non-recursive methods require the number of frames of the image sequence stored at any given time to be equal to the temporal extent of the slowest temporal filter. In contrast, recursive methods encode recent stimulus history implicitly in the values of a small number of variables updated through a series of feedback equations. Recursive filtering reduces the number of values stored in memory during convolution and the number of mathematical operations involved in computing the filters' outputs. This paper extends previous recursive implementations of gradient- and correlation-based motion analysis algorithms [Fleet DJ, Langley K (1995) IEEE PAMI 17: 61-67; Clifford CWG, Ibbotson MR, Langley K (1997) Vis Neurosci 14: 741-749], describing a recursive implementation of causal band-pass temporal filters suitable for use in energy- and phase-based algorithms for image motion computation. It is shown that the filters' temporal frequency tuning curves fit psychophysical estimates of the temporal properties of human visual filters.

Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation.

1. We have tested the hypothesis that simple cells in the cat's visual cortex perform a linear spatiotemporal filtering of the visual image. To conduct this study we note that a visual neuron behaves linearly if the responses to small, brief flashes of light are mathematically related, via the Fourier transform, to the responses elicited by sinusoidal grating stimuli. 2. We have evaluated the linearity of temporal and spatial summation for 118 simple cells recorded from the striate cortex (area 17) of adult cats and kittens at ages 4 and 8 wk postnatal. These neurons represent a subset of the population of cells for which we have described the postnatal development of spatiotemporal receptive-field structure in the preceding paper. Spatiotemporal receptive-field profiles are constructed, with the use of a reverse correlation technique, from the responses to random sequences of small bar stimuli that are brighter or darker than the background. Fourier analysis of spatiotemporal receptive-field profiles yields linear predictions of the cells' spatial and temporal frequency tuning. These predicted responses are compared with spatial and temporal frequency tuning curves measured by the use of drifting, sinusoidal-luminance grating stimuli. 3. For most simple cells, there is good agreement between spatial and temporal frequency tuning curves predicted from the receptive-field profile and those measured by the use of sinusoidal gratings. These results suggest that both spatial and temporal summation within simple cells are approximately linear. There is a tendency for predicted tuning curves to be slightly broader than measured tuning curves, a finding that is consistent with the effects of a threshold nonlinearity at the output of these neurons. In some cases, however, predicted tuning curves deviate from measured responses only at low spatial and temporal frequencies. This cannot be explained by a simple threshold nonlinearity. 4. If linearity is assumed, it should be possible to predict the direction selectivity of simple cells from the structure of their spatiotemporal receptive-field profiles. For virtually all cells, linear predictions correctly determine the preferred direction of motion of a visual stimulus. However, the strength of the directional bias is typically underestimated by a factor of about two on the basis of linear predictions. Consideration of the expansive exponential nonlinearity revealed in the contrast-response function permits a reconciliation of the discrepancy between measured and predicted direction selectivity indexes. 5. Overall, these findings show that spatiotemporal receptive-field profiles obtained with the use of reverse correlation may be used to predict a variety of response properties for simple cells.(ABSTRACT TRUNCATED AT 400 WORDS)

Effects of convergent strabismus on spatio-temporal response properties of neurons in cat area 18.

Single-cell recording experiments were carried out to determine whether rearing kittens with surgically induced convergent strabismus (esotropia) alters the development of receptive field (RF) properties of neurons in area 18. In agreement with previous work on kittens with divergent strabismus (exotropia), there was a marked loss of binocularly driven cells in area 18 of esotropic cats. In contrast to the striate cortex of strabismic cats, the spatial properties of area 18 neurons, including receptive-field size and spatial frequency tuning, did not differ from those in normal controls. On the other hand, we found that contrast thresholds, measured at an optimal spatial frequency, were significantly elevated, and that the contrast gain in many cells was reduced in strabismic cats. These deficits were observed in both eyes, though the cells dominated by the deviating eye had a lower response amplitude at all contrasts. Furthermore, temporal frequency tuning curves were abnormal in strabismic cats in that the optimal frequencies and temporal resolutions were shifted to lower values. These effects were also bilateral. Velocity tuning, measured with a high-contrast bar stimulus, revealed that area 18 neurons in strabismic cats were unable to respond to very high velocities compared to normals. This reduced response was more severe when measured with the deviating eye in spite of the bilateral nature of the deficit. Finally, latencies to electrical stimulation of the optic chiasm or the optic radiation were significantly longer in strabismic cats. The magnitude of these effects was virtually the same for both eyes. From these observations, we conclude that the temporal properties of area 18 neurons, particularly the cells abilities to follow fast temporal modulations, are affected by raising kittens with surgically induced convergent strabismus.

The role of gabaergic inhibition in the response properties of neurones in cat visual area 18

Bicuculline methiodide was iontophoretically applied to single neurones in cat area 18 to investigate how removal of γ-aminobutyrate mediated inhibition affects the visual response properties. Moving sinusoidal gratings were used to study spatial and temporal response characteristics. Orientation sensitivity and spatial and temporal frequency tuning curves were determined with and without iontophoretically applied bicuculline. In most neurones, orientation sensitivity and spatial frequency tuning remained largely unaffected, whereas temporal frequency tuning was very much broadened. It is suggested that the dominant excitatory input to area 18 cells is a spatially organized input from area 17 and local inhibition in area 18 sharpens primarily temporal selectivity. An alternative explanation of our results would be that the distribution of synapses mediating temporal tuning in area 18 is fundamentally different from that mediating spatial frequency and orientation tuning, which may be located at sites distant from the cell body and relatively inaccessible to the drug application.

Effects of rearing kittens with convergent strabismus on development of receptive-field properties in striate cortex neurons.

Convergent strabismus was induced surgically in seven kittens at 3 wk of age. Recordings were made in 131 cells in the striate cortex of these strabismic kittens after maturation, and the results were compared to the data obtained from 140 striate neurons in normally reared cats. All our samples had receptive fields (RFs) within 5 degrees of the area centralis. The spatial and temporal response properties were quantitatively analyzed by using drifting sinusoidal gratings of various contrasts as well as spatial and temporal frequencies. In contrast to other reports, the receptive-field properties of the striate neurons exclusively driven or dominated by the deviating eye were quite abnormal. The spatial frequency tuning curves in strabismic cats were different from those obtained from normals in that the optimal spatial frequencies and spatial resolutions were shifted to lower values and the bandwidths were significantly broader. The contrast-response functions show that contrast thresholds, measured at the optimal spatial frequency, were significantly higher and the slope of the functions much flatter in strabismic animals. Moreover, receptive-field sizes were much larger and the sharpness of orientation tuning was reduced in strabismic cats. Direction selectivity, however, was normal in those animals. The temporal frequency tuning curves were also abnormal, particularly in that temporal resolution was considerably reduced in strabismic cats compared with normally reared cats. In addition, many cells in strabismic animals exhibited much longer latencies to visual and optic chiasm (OX) stimulations. All these effects, to our great surprise, were also observed in the striate units controlled by the nondeviating eye, although the magnitude of the alteration depends on the receptive-field property. The abnormalities found in spatial frequency tuning, contrast thresholds, and RF sizes were as severe as those revealed in the deviating eye. On the other hand, the effects on other RF properties were minimal or less severe. These physiological findings correspond very well with results from behavioral measurements of spatial contrast sensitivity in the same cats reported elsewhere. It is concluded from these results that the nondeviating eye in convergent strabismic animals, and perhaps humans, should not always be presumed "normal."

Spatial frequency and temporal frequency selectivity of single cells in the pigeon optic tectum

The spatial and the temporal tuning characteristics of cells in the pigeon optic tectum to drifting sine-wave gratings were analysed quantitatively. Most cells could be identified as having temporal frequency tuning curves with shallow cut to both low and high temporal frequencies. The results indicate that the cells' spatial frequency selectivity to moving sine-wave gratings is independent of the temporal modulation of the stimulus. All the cells but one were tuned to velocity rather than to temporal frequency.

Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex.

1. We have examined the spatial and temporal tuning properties of 238 cortical neurones, recorded using conventional techniques from acutely prepared anaesthetized cats. We determined spatial and temporal frequency tuning curves using sinusoidal grating stimuli presented to each neurone's receptive field by a digital computer on a cathode ray tube. 2. We measured tuning curves either by determining response amplitude as a function of spatial or temporal frequency, or by measuring contrast sensitivity (the inverse of the contrast of the grating that just elicited a detectable response). The two measures give very similar tuning curves in all cases. 3. We recorded from 184 neurones in area 17; of these 156 had receptive fields within 5 degrees of the area centralis. The range of preferred spatial frequency for these neurones was 0.3--3 c/deg, and their spatial frequency tuning band widths varied from 0.7 to 3.2 octaves at half-amplitude. The most common band width was roughly 1.3 octaves. Simple and complex cells in area 17 did not differ in their distributions of preferred spatial frequency, although complex cells were, on average, slightly less selective for spatial frequency than simple cells. 4. We recorded from fifty-four neurones from area 18, and performed several experiments in which we recorded from corresponding portions of both area 17 and area 18 in the same electrode penetration. Neurones in area 18 preferred spatial frequencies that were, on average, one third as high as those preferred by area 17 neurones at the same retinal eccentricity. Thus the range of preferred spatial frequency in area eighteen cells having receptive fields within 5 deg of the area centralis was between less than 0.1 and 0.5 c/deg. The distributions of optimum spatial frequency in the two areas were practically non-overlapping at eccentricities as high as 15 deg, the greatest eccentricity we examined. Neurones in area 18 were about as selective for spatial frequency as were neurones in area 17. 5. We determined temporal frequency tuning characteristics for some neurones from each area, using gratings that moved steadily across the screen. Neurones from area 17 all responded well to low temporal frequencies, and less well to higher frequencies (in excess of, usually, 2 or 4 Hz). In contrast, neurones recorded from area 18 sometimes had similar tuning properties, but more commonly showed a pronounced reduction in response as the temporal frequency was moved either above or below some optimum value (usually 2--8 Hz). 6. We conclude from these results that areas 17 and 18 act in parallel to process different aspects of the visual information relayed from the retina via the lateral geniculate complex. Some or all of the differences between the areas may be attributable to the predominance of Y cell input to area 18 and the predominance of X cell input to area 17...

Spatial and temporal properties of ?sustained? and ?transient? neurones in area 17 of the cat's visual cortex

Receptive field properties of cells in area 17 of the visual cortex in the cat have been studied by quantitative methods. The cortical cells were classified as ‘sustained’ or ‘transient’ according to their response to a stationary, optimal bar at the receptive field centre, this being analogous to the classification of retinal ganglion cells according to their response to a stationary, optimal spot. Evidence is presented that the ‘sustained/transient’ classification is independent of the ‘simple/complex’ classification. ‘Sustained’ cells of both ‘simple’ and ‘complex’ types had spatial frequency tuning curves with a sharp low-frequency cut, whereas ‘transient’ cells, both ‘simple’ and ‘complex’, had tuning curves with a shallow low-frequency cut, and on average were tuned to lower spatial frequencies than ‘sustained’ cells. ‘Sustained’ cells of both ‘simple’ and ‘complex’ types, had temporal frequency tuning curves with a shallow low-frequency cut, whereas ‘transient’ cells had curves with a sharp low-frequency cut, and on average were tuned to higher temporal frequencies than ‘sustained’ cells. The results indicate that ‘sustained’ and ‘transient’ cortical cells retain the spatial and temporal properties of ‘sustained’ and ‘transient’ retinal ganglion cells, respectively, and thus the two groups of neurones are organised in parallel throughout the visual system, the ‘sustained’ channel providing high spatial resolution and the ‘transient’ channel, high temporal resolution.