Temporal and spatial response characteristics of the cat superior colliculus

We have examined the responses of 72 cells of the cat superior colliculus to drifting gratings of sinusoidal luminance profile as a function of spatial frequency velocity and contrast. Of 72 cells, 66 responded to gratings either by change in mean firing rate only (58/72) or in a temporally modulated pattern in addition to the change in mean firing rate (8/72). The remaining 6 showed no change in discharge rate in response to any of the gratings tested. Many cells (24/72) were inhibited or excited by particular combinations of spatial and temporal frequencies. Some (8/72) demonstrated selective inhibition or excitation to a particular temporal frequency independent of spatial frequency and velocity and could therefore be said to be tuned specifically to temporal frequency. No cells were tuned only to a constant spatial frequency or a constant velocity. (24/72) cells displayed maximum inhibition or excitation only at a particular combination of spatial and temporal frequencies. Some cells (8/72) demonstrated a temporal modulation synchronous with the drifting grating in addition to an elevated mean discharge rate. The change in discharge rates evoked by gratings are generally less than those evoked by presentation of moving small slits or spots of light. Collicular cells often demonstrate a center-surround organization in their response to gratings. The center and surround often differ in their spatial frequency and velocity preferences. Compared to cortical and retinal ganglion cells, individual collicular cells are extremely non-linear. On a cell population basis, however, a linear Fourier analysis on grating response predicts the collicular cells' preference for movement of small objects.     

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.     

Development of spatial and temporal selectivity in the suprasylvian visual cortex of the cat

We have studied the development of the spatial and temporal properties of neurons in the medial bank of the suprasylvian visual cortex (PMLS) in kittens aged between 9 d and 8 weeks. Quantitative measurements were made of the responses to drifting high-contrast gratings of optimum orientation and direction of motion, but varying in spatial and temporal frequency. The spatial resolution ("acuity") of cells increased rapidly and was fully mature (over 2 cycles/deg for the best cells) at 3 weeks of age. The optimum spatial frequency also tended to improve and reached adult values (around 0.5 cycles/deg for the best cells) at about the end of the third week. In younger kittens, the spatial resolution of neurons was not obviously correlated with the eccentricity of their receptive fields, but in older animals acuity was clearly elevated for receptive fields in the central visual field. The proportion of "low-pass" cells (showing no obvious attenuation of response for gratings of low spatial frequency) decreased with age and simultaneously there was a slight increase in the mean spatial bandwidth of "bandpass" cells. Responses to drifting sinusoidal gratings were generally dominated by an unmodulated elevation of discharge at all ages. In tests with stationary, contrast-modulated gratings presented at different spatial positions, cells in the youngest kittens behaved nonlinearly and showed mainly an unmodulated increase in discharge, whereas in older kittens, as in adult cats, most neurons responded to contrast-modulated gratings with a small, phase-dependent response at the temporal frequency of modulation and a larger component at twice the fundamental frequency. None of the cells recorded at any age had a true "null position." As in adult PMLS, the widths of receptive fields in kittens were, on average, about twice the size of the preferred spatial period (4 times the preferred bar width). At all ages, therefore, neurons in PMLS resembled striate complex cells with respect to the nonlinearity of their responses and the spatial structure of their receptive fields. The preferred temporal frequency and high-temporal-frequency cutoff also improved, on average, during the first 3 weeks of life, and the range of temporal frequencies over which cells responded continued to increase until at least 8 weeks. Although the low-spatial-frequency inhibition that creates spatial bandpass characteristics probably depends on cortical mechanisms, the postnatal development of both temporal and spatial resolution might well be limited by maturation at the level of the retina.     

Drifting grating stimulation reveals particular activation properties of visual neurons in the caudate nucleus

The role of the caudate nucleus (CN) in motor control has been widely studied. Less attention has been paid to the dynamics of visual feedback in motor actions, which is a relevant function of the basal ganglia during the control of eye and body movements. We therefore set out to analyse the visual information processing of neurons in the feline CN. Extracellular single-unit recordings were performed in the CN, where the neuronal responses to drifting gratings of various spatial and temporal frequencies were recorded. The responses of the CN neurons were modulated by the temporal frequency of the grating. The CN units responded optimally to gratings of low spatial frequencies and exhibited low spatial resolution and fine spatial frequency tuning. By contrast, the CN neurons preferred high temporal frequencies, and exhibited high temporal resolution and fine temporal frequency tuning. The spatial and temporal visual properties of the CN neurons enable them to act as spatiotemporal filters. These properties are similar to those observed in certain feline extrageniculate visual structures, i.e. in the superior colliculus, the suprageniculate nucleus and the anterior ectosylvian cortex, but differ strongly from those of the primary visual cortex and the lateral geniculate nucleus. Accordingly, our results suggest a functional relationship of the CN to the extrageniculate tecto-thalamo-cortical system. This system of the mammalian brain may be involved in motion detection, especially in velocity analysis of moving objects, facilitating the detection of changes during the animal's movement.     

Spatial and temporal frequency tuning and contrast sensitivity of single neurons in area 21a of the cat

The spatial and temporal selectivities of single neurons in area 21a of the adult cat were investigated using sinusoidal gratings. Optimal spatial frequencies and visual acuity (high cut-off frequency) were fairly low and spatial bandwidth was mainly narrow. Contrast threshold was generally low but a substantial number of cells were only excited by high contrast stimuli. The temporal selectivity suggests that cells responded to a wide range of temporal frequencies.     

Visual acuity in hooded rats: effects of superior collicular or posterior neocortical lesions

The visual resolution acuity of hooded rats was measured with an avoidance technique, using large, high contrast square-wave gratings of high mean luminance. Measurements were taken before and after ablation of either posterior cortex or the superior colliculus. The cortical lesions included both striate and temporal cortex, and caused retrograde degeneration throughout the dorsal lateral geniculate nucleus. Neither group showed signs of detecting even coarse square-wave gratings when first tested after operation. The animals with collicular lesions quickly relearnt, and their acuity was unaltered. After extensive training 3 out of 4 cortical animals relearnt to detect gratings, and their acuity was reduced to about one-third of its preoperative value. It seems likely that in rats the geniculocortical pathway carries sufficient information for the normal detection of high spatial frequencies. Whether a pathway from superior colliculus to neocortex via a thalamic relay also carries this information is uncertain.     

Stimulus-dependent oscillations in the cat visual cortex: differences between bar and grating stimuli

We have investigated the dependence of cortical oscillations on the type of visual stimulus. Single unit recordings were performed in areas 17 and 18 of the cat visual cortex. Among 217 cortical neurons oscillations in the frequency range of 22–102 Hz were found in 29 cells (13%). The proportion of oscillating cells was higher (16%) if both bar and grating stimuli were used to stimulate cortical neurons. It was found that gratings are more effective than bars in triggering oscillatory patterns in cortical cells. Among 21 oscillating cells which were stimulated with both bar and grating stimuli, oscillations evoked with gratings were found in 17 neurons (81%) while oscillations evoked with bar stimuli were triggered in 7 cells (33%). The distributions of oscillation frequencies were statistically different for oscillations evoked with bars and gratings. Frequencies of oscillations evoked with bars were in the lower and higher range than frequencies of oscillations evoked with gratings. In 3 cells (14%), rhythmic patterns could be evoked with both bar and grating stimuli. However, the oscillations were of different frequencies. No significant correlation was found between the strength of oscillations and firing rate of cortical neurons. Both simple and complex cells manifested the same dependence on stimulus type. However, complex cells mostly exhibited oscillations in the lower frequency range while simple cells did so when neurons were stimulated with bars. The results suggest that various classes of visual stimuli can be coded by a temporal pattern of cortical responses.     

Temporal properties of spatial frequency tuning of surround suppression in the primary visual cortex and the lateral geniculate nucleus of the cat

In primary visual cortex (V1) neurons, a stimulus placed in the extraclassical receptive field suppresses the response to a stimulus within the classical receptive field (CRF), a phenomenon referred to as surround suppression. The aim of the present study was to elucidate the mechanisms of surround suppression in V1. Using stationary‐flashed sinusoidal grating as stimuli, we observed temporal changes of surround suppression in V1 and the lateral geniculate nucleus (LGN) and of the response to CRF stimulation in V1. The spatial frequency (SF) tuning of surround suppression in V1 neurons changed over time after the stimulus onset. In the early phase (< 50 ms), the SF tuning was low‐pass, but later became band‐pass that tuned to the optimal SF in response to CRF stimulation. On the other hand, the SF tuning of CRF responses in V1 was band‐pass throughout the response time whereas the SF peak shifted slightly toward high SF. Thus, SF tuning properties of the CRF response dissociated from that of surround suppression in V1 only in the early phase. We also confirmed that the temporal changes of the SF tuning of surround suppression in the LGN occurred in the same direction as surround suppression in V1, but the shift from low‐pass to band‐pass SF tuning started later than that in V1. From these results, we suggest that subcortical mechanisms contribute to early surround suppression in V1, whereas cortical mechanisms contribute to late surround suppression.     

Spatial-frequency tuning and geniculocortical projections in the visual cortex (areas 17 and 18) of the pigmented ferret

We have examined the spatial-frequency selectivity of neurons in areas 17 and 18 of the adult pigmented ferret, by measuring how the amplitude of response depends on the spatial-frequency of moving sinusoidal gratings of optimal orientation and fixed contrast. Neurons in area 17 of the ferret respond optimally to low spatial frequencies [average 0.25 cycles per degree (c/deg)], much lower than the optima for cat area 17. The tuning curves are of the same form as those found in cat and monkey: unimodal with bandwidths in the range 0.8–3.5 octaves. Neurons in area 18 of the ferret respond optimally to even lower spatial frequencies (average 0.087 c/deg) than area 17 neurons, and the distributions of optimal spatial frequency for areas 17 and 18 hardly overlap. In both cortical areas, the bandwidth of the tuning curves is inversely correlated with optimal spatial frequency. This marked difference in tuning between the two cortical areas is probably attributable to differential geniculo-cortical projections. Small injections of fluorescent latex microspheres or horseradish peroxidase (HRP) were made into area 17 or area 18 in order to investigate the populations of geniculate neurons projecting to the two cortical areas. After injections into area 17, labelled neurons are found predominantly in the geniculate A layers, with a few neurons labelled in the C layers. Conversely, after an area 18 injection, similar numbers of labelled neurons are found in the C layers as in the A layers. Soma-size analysis of the neurons in the A-layers suggests the existence of two populations of relay neurons, which project differentially to areas 17 and 18. The different geniculate inputs and the different spatial-frequency tuning in areas 17 and 18 may imply that the two cortical areas process visual information more in parallel than in series.     

Stronger responses to darks along the ventral pathway of the cat visual cortex

Light increments (brights) and decrements (darks) are differently processed throughout the early visual system. It is well known that a bias towards faster and stronger responses to darks is present in the retina, lateral geniculate nucleus and primary visual cortex. In humans, psychophysical and neurophysiological data indicate that darks are better detected than brights, suggesting that the dark bias found in early visual areas is transmitted across the cortical hierarchy. Here, we tested this assumption by investigating the spatiotemporal features of responses to brights and darks in area 21a, a gateway area of the cat ventral stream, using reverse correlation analysis of a sparse noise stimulus. The receptive field of most 21a neurons exhibited larger dark subfields. Additionally, the amplitude of the responses to darks was considerably greater than those evoked by brights. In the temporal domain, no differences were found between the response peak latency. Thus, the present study supports the notion that bright/dark asymmetries are transmitted throughout the cortical hierarchy and further, that the luminance processing varies as a function of the position in the cortical hierarchy, dark preference being strongly enhanced (in the spatial domain and response amplitude) along the ventral pathway.     

Distinct functional properties of primary and posteromedial visual area of mouse neocortex

Visual input provides important landmarks for navigating in the environment, information that in mammals is processed by specialized areas in the visual cortex. In rodents, the posteromedial area (PM) mediates visual information between primary visual cortex (V1) and the retrosplenial cortex, which further projects to the hippocampus. To understand the functional role of area PM requires a detailed analysis of its spatial frequency (SF) and temporal frequency (TF) tuning. Here, we applied two-photon calcium imaging to map neuronal tuning for orientation, direction, SF and TF, and speed in response to drifting gratings in V1 and PM of anesthetized mice. The distributions of orientation and direction tuning were similar in V1 and PM. Notably, in both areas we found a preference for cardinal compared to oblique orientations. The overrepresentation of cardinal tuned neurons was particularly strong in PM showing narrow tuning bandwidths for horizontal and vertical orientations. A detailed analysis of SF and TF tuning revealed a broad range of highly tuned neurons in V1. On the contrary, PM contained one subpopulation of neurons with high spatial acuity and a second subpopulation broadly tuned for low SFs. Furthermore, ～20% of the responding neurons in V1 and only 12% in PM were tuned to the speed of drifting gratings with PM preferring slower drift rates compared to V1. Together, PM is tuned for cardinal orientations, high SFs, and low speed and is further located between V1 and the retrosplenial cortex consistent with a role in processing natural scenes during spatial navigation.     

Spatiotemporal flow of information in the early visual pathway

The spatial components of a visual scene are processed neurally in a sequence of coarse features followed by fine features. This coarse‐to‐fine temporal stream was initially considered to be a cortical function, but has recently been demonstrated in the dorsal lateral geniculate nucleus. The goal of this study was to test the hypothesis that coarse‐to‐fine processing is present at earlier stages of visual processing in the retinal ganglion cells that supply lateral geniculate nucleus (LGN) neurons. To compare coarse‐to‐fine processing in the cat's visual system, we measured the visual responses of connected neuronal pairs from the retina and LGN, and separate populations of cells from each region. We found that coarse‐to‐fine processing was clearly present at the ganglion cell layer of the retina. Interestingly, peak and high‐spatial‐frequency cutoff responses were higher in the LGN than in the retina, indicating that there was a progressive cascade of coarse‐to‐fine information from the retina to the LGN to the visual cortex. The analysis of early visual pathway receptive field characteristics showed that the physiological response interplay between the center and surround regions was consistent with coarse‐to‐fine features and may provide a primary role in the underlying mechanism. Taken together, the results from this study provided a framework for understanding the emergence and refinement of coarse‐to‐fine processing in the visual system.     

Differences in spatial and temporal frequency interactions between central and peripheral parts of the feline area 18

The visual system demonstrates significant differences in information processing abilities between the central and peripheral parts of the visual field. Optical imaging based on intrinsic signals was used to investigate the difference in stimulus spatial and temporal frequency interactions related to receptive field eccentricity in the cat area 18. Changing either the spatial or the temporal frequency of grating stimuli had a significant impact on responses in the cortical areas corresponding to the centre of the visual field and more peripheral parts at 10 degrees eccentricity. The cortical region corresponding to the centre of the gaze was tuned to 0.4 cycles per degree (c/deg) for spatial frequency and 2 Hz for temporal frequency. In contrast, the cortical region corresponding to the periphery of the visual field was tuned to a lower spatial frequency of 0.15 c/deg and a higher temporal frequency of 4 Hz. Interestingly, when we simultaneously changed both the spatial frequency and the temporal frequency of the grating stimuli, the responses were significantly different from those estimated with an assumption of independence between the spatial and temporal frequency in the cortical region corresponding to the periphery of the visual field. However, in the cortical area corresponding to the centre of the gaze, spatial frequency showed significant independence from temporal frequency. These properties support the notion of relative specialization of visual information processing for peripheral representations in cortical areas.     

Spatial and temporal selectivity in the suprasylvian visual cortex of the cat

We recorded from single units in the medial and lateral banks of the posterolateral suprasylvian visual cortex (PMLS/PLLS) of the cat. The responses to drifting high-contrast gratings of optimum orientation and direction of motion, but varying in spatial and temporal frequency, were examined quantitatively for a sample of cells, whose receptive fields covered a wide range of eccentricities. The optimum spatial frequencies (average about 0.2 cycles/deg) were low compared to the values reported for striate cortex but similar to those for area 18. The mean spatial bandwidth (about 2 octaves) was slightly broader than that of cells in other cortical visual areas. The cut-off spatial frequencies ("acuities") covered a wide range, from 0.05 to 2.1 cycles/deg, similar to those of cells in area 18. Responses to drifting sinusoidal gratings were usually dominated by an unmodulated elevation of discharge, although some modulation occurred at the temporal frequency of drift, especially at low spatial frequencies. Modulated responses were relatively stronger in PMLS than in PLLS. For those cells that responded to flashed stimuli, stationary, contrast-modulated gratings presented at different spatial positions typically evoked small responses at the fundamental frequency (dependent on spatial phase) and a larger component at the second harmonic of temporal frequency, with no overall "null-position." The optimum spatial frequency was usually higher than would be predicted by simple summation within the dimensions of the receptive field. Thus, neurons in PMLS and PLLS, like complex cells in areas 17 and 18, behave nonlinearly and their spatial selectivity is determined by "subunits" smaller than their receptive fields. The range of preferred temporal frequencies ranged from less than 2.5 Hz to more than 10 Hz. In their temporal selectivity neurons in PMLS resembled cells in area 17, with little attenuation at low temporal frequencies, whereas there was a tendency for cells in PLLS to prefer higher temporal frequencies, as is common in area 18.     

Effect of spatial frequency on simultaneous recorded steady-state pattern electroretinograms and visual evoked potentials.

Pattern electroretinograms (P-ERGs) and visual evoked potentials (VEPs) to 4 Hz alternating square-wave gratings were simultaneously recorded in 23 subjects. Responses were Fourier analyzed and amplitude and phase of the 2nd and 4th temporal harmonics were measured. The spatial frequency-amplitude function of the P-ERG 2nd harmonic component displayed either a bandpass tuning behavior, or a low-pass behavior. The peak amplitude for subjects with bandpass tuning was at 1.5 c/deg. The phase of the P-ERG 2nd harmonic decreased monotonically as spatial frequency increased. The VEP 2nd harmonic had a bimodal spatial frequency function with a peak at 3 c/deg and a second increase at spatial frequencies below 1 c/deg, regardless of the P-ERG characteristics. The phase of VEP 2nd and 4th harmonic had an inverted U-shaped function with peak at 3 c/deg and 1.5 c/deg respectively. Comparison of simultaneously recorded P-ERG and VEP spatial frequency functions demonstrated different tuning behavior for cortical and retinal responses. It is concluded that the proposed technique permits the separate analysis of retinal and cortical processing of visual information. The 2nd and 4th harmonic components of bEP behave independently of each other suggesting they may be generated by different subsystems.     

Multiple adaptable mechanisms early in the primate visual pathway

We describe experiments that isolate and characterize multiple adaptable mechanisms that influence responses of orientation-selective neurons in primary visual cortex (V1) of anesthetized macaque (Macaca fascicularis). The results suggest that three adaptable stages of machinery shape neural responses in V1: a broadly tuned early stage and a spatio-temporally tuned later stage, both of which provide excitatory input, and a normalization pool that is also broadly tuned. The early stage and the normalization pool are revealed by adapting gratings that themselves fail to evoke a response from the neuron: either low temporal frequency gratings at the null orientation or gratings of any orientation drifting at high temporal frequencies. When effective, adapting stimuli that altered the sensitivity of these two mechanisms caused reductions of contrast gain and often brought about a paradoxical increase in response gain due to a relatively greater desensitization of the normalization pool. The tuned mechanism is desensitized only by stimuli well matched to a neuron's receptive field. We could thus infer desensitization of the tuned mechanism by comparing effects obtained with adapting gratings of preferred and null orientation modulated at low temporal frequencies.     

Spatiotemporal frequency and speed tuning in the owl visual wulst

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

Receptive fields of the visual cortex--detectors or filters of spatial frequencies?

Spatial frequency characteristics of the complex cortical visual receptive field were studied in curarized cats. It is shown that, besides the main maximum, they also have additional maxima and negative regions as predicted by the theory of piecewise Fourier-analysis. Comparison of responses of the complex receptive field to sinusoidal grating entering the field completely or incompletely together with the comparison of responses to sinusoidal and squarewave gratings shows the linear properties of the receptive field as a spatial frequency filter. The response of the complex receptive field increases with the number of periods constituting the sinusoidal grating. Several periods of optimal spatial frequency matched the size of the complex receptive field. In the columns of neurons, the receptive fields were found tuned to a broad band of spatial frequencies. The data confirm the hypothesis according to which the complex receptive fields are rather spatial frequency filters than detectors.     

Non-dominant eye responses in the dorsal lateral geniculate nucleus of the cat: an intracellular study

While binocularity has been established as an important characteristic of cat visual cortical neurons, neurons in the dorsal lateral geniculate nucleus (LGNd) are commonly believed to be monocular. To test whether binocularity exists at the level of the LGNd, postsynaptic potentials (PSPs) of 101 cells were intracellularly recorded in eight normal and eight monocularly deprived cats while presenting stimuli to either the dominant or non-dominant eyes. The results showed that: (1) About 92% of neurons (45 out of 49) responded to a flashing spot presented to the non-dominant eye. In contrast to the dominant eye responses, the non-dominant eye PSPs usually exhibited the same polarization tendency (hyperpolarization or depolarization) to flashing spot stimuli of light increment or decrement, and most of them were inhibitory (hyperpolarization, 35 out of 45, 78%). (2) The response field (RF) of the non-dominant eye overlapped that of the dominant eye. (3) For most binocular cells, peak-to-peak amplitudes of non-dominant eye PSPs were about half the size (46%) of those of the dominant eye. The peak latencies and half-peak latencies of non-dominant eye PSPs were significantly longer than those of the dominant eye (mean differences were 5.4 ms and 5.6 ms respectively). (4) Most of the binocular cells responded well to contrast reversing gratings presented to the non-dominant eye, and the responses were clearly spatial-frequency tuned. No null phase could be found for non-dominant eye PSPs, no matter the neuron was classified as X or Y type according to dominant eye elicited responses. Some of the cells responded well to drifting gratings presented to the non-dominant eye. (5) We also recorded 52 cells in monocularly deprived cats, and found that 49 cells (94%) showed significant responses to flashing spots presented to the non-dominant eye, a similar percentage to that found in normal cats (92%). CONCLUSION: as strongly monocular neurons, most of LGNd cells could also be driven by the non-dominant eye. The responses evoked by non-dominant eye stimulation differ greatly from those evoked by dominant eye stimulation, and remain intact even without visual experience. These observations suggest an important role of the perigeniculate nucleus in providing binocular inputs to LGNd cells.     

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

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