Large Size Of Receptive Fields Research Articles

Poster Session I: Digital dual-Purkinje-image eye tracking enables precise determination of visual receptive fields in fixating macaques.

Understanding the relationship between visual stimuli and neural activity is a fundamental goal in visual neuroscience. However, the study of visual neurophysiology in awake primates is complicated by the constant occurrence of eye movements, even during periods of nominal fixation. To address this challenge, we adapted a recently developed high-resolution digital dual-Purkinje-image (dDPI) eye tracker (Wu et al., 2023) for use with macaque monkeys. In addition to tracking the Purkinje images, we simultaneously estimate the pupil center and size: a first for video eye tracking. We then sought to evaluate the efficacy of dDPI eye tracking for studying visual processing in fixating macaques by recording single neurons from the lateral geniculate nucleus while a spatially-correlated noise stimulus was displayed. Our analyses show that, as a result of properly accounting for eye movements post-hoc, the predictive performance of generalized linear models improves and the estimates center radii contract to values equal to or smaller than those reported in the literature. Notably, correcting for eye movements using the locations of the pupil center and corneal reflection-the standard method in video eye tracking-yielded worse model fits and larger receptive field sizes. This finding implies that the pupil center is an inaccurate reporter of small eye movements, while the Purkinje images may be veridical during fixations.

Population receptive field (pRF) measurements of chromatic responses in human visual cortex using fMRI

The spatial sensitivity of the human visual system depends on stimulus color: achromatic gratings can be resolved at relatively high spatial frequencies while sensitivity to isoluminant color contrast tends to be more low-pass. Models of early spatial vision often assume that the receptive field size of pattern-sensitive neurons is correlated with their spatial frequency sensitivity - larger receptive fields are typically associated with lower optimal spatial frequency. A strong prediction of this model is that neurons coding isoluminant chromatic patterns should have, on average, a larger receptive field size than neurons sensitive to achromatic patterns. Here, we test this assumption using functional magnetic resonance imaging (fMRI). We show that while spatial frequency sensitivity depends on chromaticity in the manner predicted by behavioral measurements, population receptive field (pRF) size measurements show no such dependency. At any given eccentricity, the mean pRF size for neuronal populations driven by luminance, opponent red/green and S-cone isolating contrast, are identical. Changes in pRF size (for example, an increase with eccentricity and visual area hierarchy) are also identical across the three chromatic conditions. These results suggest that fMRI measurements of receptive field size and spatial resolution can be decoupled under some circumstances - potentially reflecting a fundamental dissociation between these parameters at the level of neuronal populations.

Functional selectivity in the human occipitotemporal cortex during natural vision: Evidence from combined intracranial EEG and eye-tracking

Eye movements are a constant and essential component of natural vision, yet, most of our knowledge about the human visual system comes from experiments that restrict them. This experimental constraint is mostly in place to control visual stimuli presentation and to avoid artifacts in non-invasive measures of brain activity, however, this limitation can be overcome with intracranial EEG (iEEG) recorded from epilepsy patients. Moreover, the high-frequency components of the iEEG signal (between about 50 and 150Hz) can provide a proxy of population-level spiking activity in any cortical area during free-viewing. We combined iEEG with high precision eye-tracking to study fine temporal dynamics and functional specificity in the fusiform face (FFA) and visual word form area (VWFA) while patients inspected natural pictures containing faces and text. We defined the first local measure of visual (electrophysiological) responsiveness adapted to free-viewing in humans: amplitude modulations in the high-frequency activity range (50–150Hz) following fixations (fixation-related high-frequency response). We showed that despite the large size of receptive fields in the ventral occipito-temporal cortex, neural activity during natural vision of realistic cluttered scenes is mostly dependent upon the category of the foveated stimulus — suggesting that category-specificity is preserved during free-viewing and that attention mechanisms might filter out the influence of objects surrounding the fovea.

A Two-Stage Cascade Model of BOLD Responses in Human Visual Cortex

Visual neuroscientists have discovered fundamental properties of neural representation through careful analysis of responses to controlled stimuli. Typically, different properties are studied and modeled separately. To integrate our knowledge, it is necessary to build general models that begin with an input image and predict responses to a wide range of stimuli. In this study, we develop a model that accepts an arbitrary band-pass grayscale image as input and predicts blood oxygenation level dependent (BOLD) responses in early visual cortex as output. The model has a cascade architecture, consisting of two stages of linear and nonlinear operations. The first stage involves well-established computations—local oriented filters and divisive normalization—whereas the second stage involves novel computations—compressive spatial summation (a form of normalization) and a variance-like nonlinearity that generates selectivity for second-order contrast. The parameters of the model, which are estimated from BOLD data, vary systematically across visual field maps: compared to primary visual cortex, extrastriate maps generally have larger receptive field size, stronger levels of normalization, and increased selectivity for second-order contrast. Our results provide insight into how stimuli are encoded and transformed in successive stages of visual processing.

Peripheral Advantage in Texture Segmentation: The Role of Spatial and Temporal Factors

Previous studies (eg Kehrer, 1989 Spatial Vision4 45 – 62; Gurnsey et al, 1996 Journal of Experimental Psychology: Human Perception and Performance22 738 – 757) have shown that performance peaks several degrees from fixation in texture segmentation tasks, and performance falls as the target texture moves closer to the fovea or further into the periphery. There are two theories for this phenomenon: (1) neural processing speed in the fovea is slower than in the periphery (Kehrer 1989), and (2) the spatial frequency band of the texture is too low (ie too coarse) for the foveal receptive fields (Gurnsey et al 1996). However, the use of backward masking in previous studies made it impossible to decide between the two factors. The purpose of the present study was to isolate them. In experiment 1 a new stimulus configuration with backward masking was used, and previous reports were replicated. In experiment 2, the same texture was presented for 110 ms without a mask, but with added random-dot noise. Without limitations on processing time, the mid-peripheral advantage disappeared, which indicated that the previous findings were due to slower neural processing in the fovea. In experiment 3, a new type of texture was devised consisting of pairs of vertical lines with a horizontal offset. The offset was reversed for the target. Performance for unmasked 110 ms presentation was worst near the fovea and improved monotonically up to 12 deg. This peripheral advantage was spatial, not temporal, because it arose from larger receptive field sizes in periphery. When these results are taken together, the present study demonstrates that there are two independent causes for the mid-peripheral advantage in texture segregation.

The characteristics of slowly adapting mechanical sensory neurons in the trigeminal ganglia of crotaline snakes

Mechanical pressure (P) and touch (M) neurons, two types of slowly adapting neurons, can be distinguished in the trigeminal ganglion of crotaline snakes, Trimeresurus flavoviridis, by their electrophysiological membrane properties. Intracellular stimulation and the recording of the responses from P and M neurons in vivo was performed with microelectrodes. The characteristics of the receptive field (RF) of both types of neurons were examined. P neurons had a much larger RF size and a higher mechanical threshold than those of M neurons. Both of them responded with discharges to mechanical stimulation. The active and passive electrophysiological membrane properties were measured from nine P and 18 M neurons. The active membrane properties of P neurons showed a larger amplitude and longer duration of action potential, a larger after-hyperpolarization with a longer duration to half-decay, and a higher electric threshold in response to intracellularly injected depolarizing current than M neurons. The passive membrane properties of P neurons showed a higher input resistance, much longer time constant, and larger capacitance than M neurons. The rebound spike which responded to injecting sufficient hyperpolarizing current was sometimes observed, and had a longer latency in P neurons than M neurons. These results indicated that some electrophysiological membrane properties of primary sensory neurons are dependent on their sensory modalities.

Retinotopic order is surprisingly good within cell columns in the cat's lateral suprasylvian cortex.

The retinotopic map in the striate-recipient region of the cat's lateral suprasylvian cortex (referred to here as the lateral suprasylvian area (LS)) has generally been described as quite disorderly. The disorder is commonly attributed to receptive field scatter within cell columns, reflecting the very large size of receptive fields. However, scatter within columns has never been investigated. In the experiments reported here, we examined the receptive field scatter of cells in columns, and also the scatter of a limited sample of their afferents arising from areas 17 and 18. To measure post-synaptic receptive field scatter, electrode penetrations were made parallel to columns in LS, with the electrode approaching from the medial side, traversing the suprasylvian gyrus and emerging into the suprasylvian sulcus. In all 13 such penetrations, receptive fields were clustered together despite their large size. Their centers were scattered over a region that occupied on average less than 20% of the largest field in the column. In contrast, in columns in areas 17 and 18 receptive field centers reportedly are dispersed over regions about equal to the largest of the fields (Hubel and Wiesel 1962, 1965, 1974). The scatter of afferents' receptive fields was assessed anatomically by measuring the overlap between patches of different anterograde tracers in LS. These patches represented terminal labeling from two adjacent or overlapping tracer injections in area 17. While a large degree of overlap would be predicted if afferents have substantial scatter, we found the overlap to be small unless the two injection sites themselves were highly overlapping. Scatter in afferents' receptive fields was measured more directly by physiological recording. In previous experiments, cells in LS were silenced by the local injection of kainic acid, and responses were recorded from axon terminals arising from areas 17 and 18 (Sherk 1989). We examined the receptive field scatter in three penetrations made approximately normal to the cortical surface. Scatter was modest, much less than predicted by the size of post-synaptic receptive fields. Because the degree of receptive field scatter for postsynaptic cells in LS was similar to that of inputs from areas 17 and 18, the scatter of these inputs might be entirely responsible for that seen postsynaptically. Postsynaptic receptive field scatter, on the other hand, was too small to explain the reported disorder in the map in LS.

Local precision of visuotopic organization in the middle temporal area (MT) of the macaque.

The representation of the visual field in the middle temporal area (MT) was examined by recording from single neurons in anesthetized, immobilized macaques. Measurements of receptive field size, variability of receptive field position (scatter) and magnification factor were obtained within the representation of the central 25 degree. Over at least short distances (less than 3 mm), the visual field representation in MT is surprisingly orderly. Receptive field size increases as a linear function of eccentricity and is about ten times larger than in V1 at all eccentricities. Scatter in receptive field position at any point in the visual field representation is equal to about one-third of the receptive field size at that location, the same relationship that has been found in V1. Magnification factor in MT is only about one-fifth that reported in V1 within the central 5 degree but appears to decline somewhat less steeply than in V1 with increasing eccentricity. Because the smaller magnification factor in MT relative to V1 is complemented by larger receptive field size and scatter, the point-image size (the diameter of the region of cortex activated by a single point in the visual field) is roughly comparable in the two areas. On the basis of these results, as well as on our previous finding that 180 degrees of axis of stimulus motion in MT are represented in about the same amount of tissue as 180 degrees of stimulus orientation in V1, we suggest that a stimulus at one point in the visual field activates at least as many functional "modules" in MT as in V1.

Visual receptive field properties in the posterior suprasylvian cortex of the cat: A comparison between the areas PMLS and PLLS

Receptive field (RF) properties of single units were examined in two visual areas in the cat's postero-medial and postero-lateral suprasylvian cortex (PMLS/PLLS). Electrophysiological recordings were made in the paralyzed and anesthetized preparation in corresponding regions of the medial and lateral banks of the lateral suprasylvian sulcus (LS). In both areas, cell samples were obtained from within the same range of A/P co-ordinates. In both samples, cells responded best to moving stimuli, had large RF's, and did not differ with respect to the distributions of their ocular dominance. Binocularity was equally high, but units in PLLS showed significantly less binocular summation. Cells in both areas preferred high velocities, and a high percentage was direction selective, with directions up and away from the vertical meridian being most common. While in PMLS the preferred direction of a unit usually could be classified into a “radial” vs a “circular” category when RF position was taken into account, this was not possible in PLLS. Units in PLLS also had significantly higher spontaneous activity, higher optimal velocity, and larger RF sizes. In PLLS the investigation of background-foreground interactions revealed a large variety of phase-dependent responses. This is in contrast to the clear preponderance of in-phase inhibition and antiphase facilitation effects in PMLS. The results indicate important differences of RF properties for the two areas, but do not yet suggest a clear functional differentiation. These differences reflect in some respects the RF properties of cells in the structures that provide the main afferents to the two areas.

Coding of visual information by units in the cat cerebellar vermis.

Extracellular records were made of the responses to precisely controlled stationary or moving visual stimuli of 174 units in the cerebellar vermis of cats anaesthetised with chloralose. Identified Purkinje cells and unidentified units responsed similarly. Responses to ON and to OFF steps of a stationary light bar had different characteristics. Some units showed changes in the form of their ON responses related to different positions of the stimulus in their large receptive fields. In some cases changes in response latency from different field positions were also noted. Some units responded only to binocular stimulation and others gave much larger responses to binocular than to monocular stimulation. In addition, some were sensitive to the relative retinal disparity of images and, of these, several were sensitive to vertical as well as to horizontal retinal disparity. Sinusoidally-moving light bars gave responses consisting of one or two bursts of impulses per cycle; the most effective frequency was about 3 Hz. These responses may represent detection of the instant of maximum velocity. The relatively precise coding of retinal disparity in spite of the large size of receptive fields and the coding of position within these large fields is discussed. A possible function for the disparity-sensitive units in the control of vergence is suggested and the relation of this control to visual depth detection and to the estimation of the absolute distance of objects from the animal is discussed.