Spatial Receptive Fields Research Articles

Receptive-Field Modification in Rat Visual Cortex Induced by Paired Visual Stimulation and Single-Cell Spiking

Experience-dependent plasticity of visual cortical receptive fields (RFs) involves synaptic modifications in the underlying neural circuits, but the site and mechanism of these modifications remain to be elucidated. Using in vivo whole-cell recordings, we show that pairing visual stimulation at a given retinal location with spiking of a single neuron in developing rat visual cortex induces rapid RF modifications. The time course of the response to the visual stimulus at the paired RF location is altered, with an enhancement of the response preceding the spike time and a reduction following the spike. Such bidirectional modification is consistent with spike timing-dependent plasticity. Response modification also occurs at nearby locations, the direction and magnitude of which are correlated with the change at the paired location. In addition, changes at unpaired locations show a negative correlation with the initial strength of the response, which may facilitate rapid modification of the spatial RF profile.

Functional Organization of Ganglion Cells in the Salamander Retina

Recently, we reported a novel technique for recording all of the ganglion cells in a retinal patch and showed that their receptive fields cover visual space roughly 60 times over in the tiger salamander. Here, we carry this analysis further and divide the population of ganglion cells into functional classes using quantitative clustering algorithms that combine several response characteristics. Using only the receptive field to classify ganglion cells revealed six cell types, in agreement with anatomical studies. Adding other response measures served to blur the distinctions between these cell types rather than resolve further classes. Only the biphasic off type had receptive fields that tiled the retina. Even when we attempted to split these classes more finely, ganglion cells with almost identical functional properties were found to have strongly overlapping spatial receptive fields. A territorial spatial organization, where ganglion cell receptive fields tend to avoid those of other cells of the same type, was only found for the biphasic off cell. We further studied the functional segregation of the ganglion cell population by computing the amount of visual information shared between pairs of cells under natural movie stimulation. This analysis revealed an extensive mixing of visual information among cells of different functional type. Together, our results indicate that the salamander retina uses a population code in which every point in visual space is represented by multiple neurons with subtly different visual sensitivities.

Interaural Timing Cues Do Not Contribute to the Map of Space in the Ferret Superior Colliculus: A Virtual Acoustic Space Study

In this study, we used individualized virtual acoustic space (VAS) stimuli to investigate the representation of auditory space in the superior colliculus (SC) of anesthetized ferrets. The VAS stimuli were generated by convolving broadband noise bursts with each animal's own head-related transfer function and presented over earphones. Comparison of the amplitude spectra of the free-field and VAS signals and of the spatial receptive fields of neurons recorded in the inferior colliculus with each form of stimulation confirmed that the VAS provided an accurate simulation of sounds presented in the free field. Units recorded in the deeper layers of the SC responded predominantly to virtual sound directions within the contralateral hemifield. In most cases, increasing the sound level resulted in stronger spike discharges and broader spatial receptive fields. However, the preferred sound directions, as defined by the direction of the centroid vector, remained largely unchanged across different levels and, as observed in previous free-field studies, varied topographically in azimuth along the rostrocaudal axis of the SC. We also examined the contribution of interaural time differences (ITDs) to map topography by digitally manipulating the VAS stimuli so that ITDs were held constant while allowing other spatial cues to vary naturally. The response properties of the majority of units, including centroid direction, remained unchanged with fixed ITDs, indicating that sensitivity to this cue is not responsible for tuning to different sound directions. These results are consistent with previous data suggesting that sensitivity to interaural level differences and spectral cues provides the basis for the map of auditory space in the mammalian SC.

Analyzing Functional Connectivity Using a Network Likelihood Model of Ensemble Neural Spiking Activity

Analyzing the dependencies between spike trains is an important step in understanding how neurons work in concert to represent biological signals. Usually this is done for pairs of neurons at a time using correlation-based techniques. Chornoboy, Schramm, and Karr (1988) proposed maximum likelihood methods for the simultaneous analysis of multiple pair-wise interactions among an ensemble of neurons. One of these methods is an iterative, continuous-time estimation algorithm for a network likelihood model formulated in terms of multiplicative conditional intensity functions. We devised a discrete-time version of this algorithm that includes a new, efficient computational strategy, a principled method to compute starting values, and a principled stopping criterion. In an analysis of simulated neural spike trains from ensembles of interacting neurons, the algorithm recovered the correct connectivity matrices and interaction parameters. In the analysis of spike trains from an ensemble of rat hippocampal place cells, the algorithm identified a connectivity matrix and interaction parameters consistent with the pattern of conjoined firing predicted by the overlap of the neurons' spatial receptive fields. These results suggest that the network likelihood model can be an efficient tool for the analysis of ensemble spiking activity.

RECEPTIVE FIELD PROPERTIES OF NEAR NEIGHBOR ORIENTATION SELECTIVE NEURONS IN THE VISUAL CORTEX: A MODELING STUDY

The primary visual cortex is organized into clusters of cells having similar receptive fields (RFs). A purely feedforward model has been shown to produce realistic simple cell receptive fields. The modeled cells capture a wide range of receptive field properties of orientation selective cortical cells. We have analyzed the responses of 78 nearby cell pairs to study which RF properties are clustered. Orientation preference shows strongest clustering. Orientation tuning width (hwhh) and tuning height (spikes/sec) at the preferred orientation are not as tightly clustered. Spatial frequency is also not as tightly clustered and RF phase has the least clustering. Clustering property of orientation preference, orientation tuning height and width depend on the location of cells in the orientation map. No such location dependence is observed for spatial frequency and RF phase. Our results agree well with experimental data.

Human sound localization at near-threshold levels

Physiological studies of spatial hearing show that the spatial receptive fields of cortical neurons typically are narrow at near-threshold levels, broadening at moderate levels. The apparent loss of neuronal spatial selectivity at increasing sound levels conflicts with the accurate performance of human subjects localizing at moderate sound levels. In the present study, human sound localization was evaluated across a wide range of sensation levels, extending down to the detection threshold. Listeners reported whether they heard each target sound and, if the target was audible, turned their heads to face the apparent source direction. Head orientation was tracked electromagnetically. At near-threshold levels, the lateral (left/right) components of responses were highly variable and slightly biased towards the midline, and front vertical components consistently exhibited a strong bias towards the horizontal plane. Stimulus levels were specified relative to the detection threshold for a front-positioned source, so low-level rear targets often were inaudible. As the sound level increased, first lateral and then vertical localization neared asymptotic levels. The improvement of localization over a range of increasing levels, in which neural spatial receptive fields presumably are broadening, indicates that sound localization does not depend on narrow spatial receptive fields of cortical neurons.

A neuronal correlate of the precedence effect is associated with spatial selectivity in the barn owl's auditory midbrain.

Sound localization in echoic conditions depends on a precedence effect (PE), in which the first arriving sound dominates the perceived location of later reflections. Previous studies have demonstrated neurophysiological correlates of the PE in several species, but the underlying mechanisms remain unknown. The present study documents responses of space-specific neurons in the barn owl's inferior colliculus (IC) to stimuli simulating direct sounds and reflections that overlap in time at the listener's ears. Responses to 100-ms noises with lead-lag delays from 1 to 100 ms were recorded from neurons in the space-mapped subdivisions of IC in anesthetized owls (N2O/isofluorane). Responses to a target located at a unit's best location were usually suppressed by a masker located outside the excitatory portion of the spatial receptive field. The least spatially selective units exhibited temporally symmetric effects, in that the amount of suppression was the same whether the masker led or lagged. Such effects mirror the alteration of localization cues caused by acoustic superposition of leading and lagging sounds. In more spatially selective units, the suppression was often temporally asymmetric, being more pronounced when the masker led. The masker often evoked small changes in spatial tuning that were not related to the magnitude of suppressive effects. The association of temporally asymmetric suppression with spatial selectivity suggests that this property emerges within IC, and not at earlier stages of auditory processing. Asymmetric suppression reduces the ability of highly spatially selective neurons to encode the location of lagging sounds, providing a possible basis for the PE.

Visual response properties in the dorsal lateral geniculate nucleus of mice lacking the beta2 subunit of the nicotinic acetylcholine receptor.

We present a quantitative description of single-cell visual response properties in the dorsal lateral geniculate nucleus (dLGN) of anesthetized adult mice lacking the beta2 subunit of the nicotinic acetylcholine receptor (beta2-/-) and compare these response properties with data from wild-type animals. Some response features, including all spatial receptive field characteristics and bursting behavior, are entirely normal in beta2-/- dLGN cells. In other respects, the responses of beta2-/- dLGN cells are quantitatively abnormal: the mutation is associated with higher spontaneous and visually evoked firing rates, faster visual response latencies, a preference for higher temporal frequencies, and a trend toward greater contrast sensitivity. The normal response properties in the beta2-/- dLGN show that none of the many effects of the mutation, including disrupted geniculate functional organization and abnormal cholinergic transmission, have any effect on spatial response characteristics and bursting behavior in dLGN neurons. The abnormal response characteristics in the beta2-/- dLGN are most interesting in that they are no worse than normal; any visual processing deficits found in studies of the beta2-/- visual cortex must therefore arise solely from abnormalities in cortical processing.

A preference for phase-based disparity in a neuromorphic implementation of the binocular energy model.

The relative depth of objects causes small shifts in the left and right retinal positions of these objects, called binocular disparity. This letter describes an electronic implementation of a single binocularly tuned complex cell based on the binocular energy model, which has been proposed to model disparity-tuned complex cells in the mammalian primary visual cortex. Our system consists of two silicon retinas representing the left and right eyes, two silicon chips containing retinotopic arrays of spiking neurons with monocular Gabor-type spatial receptive fields, and logic circuits that combine the spike outputs to compute a disparity-selective complex cell response. The tuned disparity can be adjusted electronically by introducing either position or phase shifts between the monocular receptive field profiles. Mismatch between the monocular receptive field profiles caused by transistor mismatch can degrade the relative responses of neurons tuned to different disparities. In our system, the relative responses between neurons tuned by phase encoding are better matched than neurons tuned by position encoding. Our numerical sensitivity analysis indicates that the relative responses of phase-encoded neurons that are least sensitive to the receptive field parameters vary the most in our system. We conjecture that this robustness may be one reason for the existence of phase-encoded disparity-tuned neurons in biological neural systems.

Neural responses to free field and virtual acoustic stimulation in the inferior colliculus of the guinea pig.

Virtual auditory space (VAS) stimuli based on outer ear transfer functions became increasingly important in spatial hearing research. However, few studies have investigated the match between responses of auditory neurons to VAS and free-field (FF) stimulation. This study validates acoustic spatial receptive fields (SRFs) of 183 individual midbrain units using both VAS and FF stimuli. The first-spike latency, which varied systematically across SRFs, was 14.9 +/- 8.3 (SD) ms in FF, and 15.1 +/- 8.3 ms in VAS. Spike-count-based SRFs measured 0-20 dB above the neural threshold covered on average 44.5 +/- 18.0% of the recorded sphere in FF and 45.5 +/- 18.7% in VAS. The average deviation of the centroid position of SRFs using FF and VAS stimuli was 7.4 degrees azimuth and 3.3 degrees elevation. The average spike rate remained unchanged. The SRF overlap recorded using FF and VAS stimuli (mean: 71.3 +/- 12.6%) or repeated FF stimuli (70.2 +/- 14.2%) was high and strongly correlated (r = 0.96; P < 0.05). The SRF match observed with FF and VAS stimuli was not significantly altered over a range of stimulus levels (paired t-test P = 0.51; n = 6). Randomized VAS barely affected SRF sizes, centroids, or maximum spike count but decreased the average minimum response to 59% compared with sequential stimulation (paired t-test; P = 0.05; n = 26). SRF recordings in VAS excluding the acoustic distortions of the recording equipment differed from those in VAS incorporating the equipment (paired t-test P = 0.01; n = 5). In conclusion, neurophysiological recordings demonstrate that individualized VAS stimuli provided a good simulation of a FF environment.

Spatiotemporal receptive fields maximizing temporal coherence in natural image sequences

The relationship between the structure and functionality of the visual system and the properties of natural visual stimuli is an active research topic in computational visual neuroscience. It has previously been shown that maximization of temporal coherence of activity levels is one computational principle which leads to the emergence of simple-cell-like spatial receptive fields from natural image sequences. In this paper we extend previous results by examining the case of spatiotemporal receptive fields. We show that application of the same principle of temporal coherence in the spatiotemporal case yields receptive fields which are not only localized, oriented and multiscale, as in the spatial case, but also share some important temporal characteristics with spatiotemporal simple-cell receptive fields. Quantitative measurements of the properties of the resulting receptive fields are also provided, and these are compared against similar results obtained with independent component analysis.

Dynamic analysis of neural encoding by point process adaptive filtering.

Neural receptive fields are dynamic in that with experience, neurons change their spiking responses to relevant stimuli. To understand how neural systems adapt their representations of biological information, analyses of receptive field plasticity from experimental measurements are crucial. Adaptive signal processing, the well-established engineering discipline for characterizing the temporal evolution of system parameters, suggests a framework for studying the plasticity of receptive fields. We use the Bayes' rule Chapman-Kolmogorov paradigm with a linear state equation and point process observation models to derive adaptive filters appropriate for estimation from neural spike trains. We derive point process filter analogues of the Kalman filter, recursive least squares, and steepest-descent algorithms and describe the properties of these new filters. We illustrate our algorithms in two simulated data examples. The first is a study of slow and rapid evolution of spatial receptive fields in hippocampal neurons. The second is an adaptive decoding study in which a signal is decoded from ensemble neural spiking activity as the receptive fields of the neurons in the ensemble evolve. Our results provide a paradigm for adaptive estimation for point process observations and suggest a practical approach for constructing filtering algorithms to track neural receptive field dynamics on a millisecond timescale.

Spatiotemporal receptive fields maximizing temporal coherence in natural image sequences

The relationship between the structure and functionality of the visual system and the properties of natural visual stimuli is an active research topic in computational visual neuroscience. It has previously been shown that maximization of temporal coherence of activity levels is one computational principle which leads to the emergence of simple-cell-like spatial receptive fields from natural image sequences. In this paper we extend previous results by examining the case of spatiotemporal receptive fields. We show that application of the same principle of temporal coherence in the spatiotemporal case yields receptive fields which are not only localized, oriented and multiscale, as in the spatial case, but also share some important temporal characteristics with spatiotemporal simple-cell receptive fields. Quantitative measurements of the properties of the resulting receptive fields are also provided, and these are compared against similar results obtained with independent component analysis.

Goal-Related Activity in V4 during Free Viewing Visual Search: Evidence for a Ventral Stream Visual Salience Map

Natural exploration of complex visual scenes depends on saccadic eye movements toward important locations. Saccade targeting is thought to be mediated by a retinotopic map that represents the locations of salient features. In this report, we demonstrate that extrastriate ventral area V4 contains a retinotopic salience map that guides exploratory eye movements during a naturalistic free viewing visual search task. In more than half of recorded cells, visually driven activity is enhanced prior to saccades that move the fovea toward the location previously occupied by a neuron's spatial receptive field. This correlation suggests that bottom-up processing in V4 influences the oculomotor planning process. Half of the neurons also exhibit top-down modulation of visual responses that depends on search target identity but not visual stimulation. Convergence of bottom-up and top-down processing streams in area V4 results in an adaptive, dynamic map of salience that guides oculomotor planning during natural vision.

Binaural processing in the synthesis of auditory spatial receptive fields.

The owl's auditory system computes interaural time (ITD) and interaural level (ILD) differences to create a two-dimensional map of auditory space. Space-specific neurons are selective for combinations of ITD and ILD, which define, respectively, the horizontal and vertical dimensions of their receptive fields. ITD curves for postsynaptic potentials indicate that ICx neurons integrate the results of binaural cross correlation in different frequency bands. However, the difference between the main and side peaks is slight. ICx neurons further enhance this difference in the process of converting membrane potentials to impulse rates. Comparison of subthreshold postsynaptic potentials (PSPs) and spike output for the same neurons showed that receptive fields measured in PSPs were much larger than those measured in spikes in both ITD and ILD dimensions. A multiplication of separate postsynaptic potentials tuned to ITD and ILD can account for the combination sensitivity of these neurons to ITD-ILD pairs.

Representation of Auditory Space by Cortical Neurons in Awake Cats

We evaluated the spatial selectivity of auditory cortical neurons in awake cats. Single- and multiunit activity was recorded in primary auditory cortex as the animals performed a nonspatial auditory discrimination or sat idly. Their heads were unrestrained, and head position was tracked. Broadband sounds were delivered from locations throughout 360 degrees on the horizontal plane, and source locations were expressed in head-centered coordinates. As in anesthetized animals, the firing rates of most units were modulated by sound location, and most units responded best to sounds in the contralateral hemifield. Tuning was sharper than in anesthetized cats, in part because of suppression at nonoptimal locations. Nonetheless, spatial receptive fields typically spanned 150-180 degrees. Units exhibited diverse temporal response patterns that often depended on sound location. An information-theoretic analysis showed that information transmission was reduced by approximately 10% when the precision of spike timing was disrupted by 16-32 msec, and by approximately 50% when all location-related variation of spike timing was removed. Spikes occurring within 60 msec of stimulus onset transmitted the most location-related information, but later spikes also carried information. The amount of information transmitted by ensembles of units increased with the number of units, indicating some degree of mutual independence in the spatial information transmitted by various units. Spatial tuning and information transmission were changed little by an increase in sound level of 20-30 dB. For the vast majority of units, receptive fields showed no significant change with the cat's head position or level of participation in the auditory task.

Prediction of auditory spatial acuity from neural images on the owl's auditory space map.

The owl can discriminate changes in the location of sound sources as small as 3 degrees and can aim its head to within 2 degrees of a source. A typical neuron in its midbrain space map has a spatial receptive field that spans 40 degrees--a width that is many times the behavioural threshold. Here we have quantitatively examined the relationship between neuronal activity and perceptual acuity in the auditory space map in the barn owl midbrain. By analysing changes in firing rate resulting from small changes of stimulus azimuth, we show that most neurons can reliably signal changes in source location that are smaller than the behavioural threshold. Each source is represented in the space map by a focus of activity in a population of neurons. Displacement of the source causes the pattern of activity in this population to change. We show that this change predicts the owl's ability to detect a change in source location.

Spatial tuning to virtual sounds in the inferior colliculus of the guinea pig.

How do neurons in the inferior colliculus (IC) encode the spatial location of sound? We have addressed this question using a virtual auditory environment. For this purpose, the individual head-related transfer functions (HRTFs) of 18 guinea pigs were measured under free-field conditions for 122 locations covering the upper hemisphere. From 257 neurons, 94% responded to the short (50-ms) white noise stimulus at 70 dB sound pressure level (SPL). Out of these neurons, 80% were spatially tuned with a receptive field that is smaller than a hemifield (at 70 dB). The remainder responded omnidirectionally or showed fractured receptive fields. The majority of the neurons preferred directions in the contralateral hemisphere. However, preference for front or rear positions and high elevations occurred frequently. For stimulation at 70 dB SPL, the average diameter of the receptive fields, based on half-maximal response, was less than a quarter of the upper hemisphere. Neurons that preferred frontal directions responded weakly or showed no response to posterior directions and vice versa. Hence, front/back discrimination is present at the single-neuron level in the IC. When nonindividual HRTFs were used to create the stimuli, the spatial receptive fields of most neurons became larger, split into several parts, changed position, or the response became omnidirectional. Variation of absolute sound intensity had little effect on the preferred directions of the neurons over a range of 20 to 40 dB above threshold. With increasing intensity, most receptive fields remained constant or expanded. Furthermore, we tested the influence of binaural decorrelation and stimulus bandwidth on spatial tuning. The vast majority of neurons with a low characteristic frequency (<2.5 kHz) lost spatial tuning under stimulation with binaurally uncorrelated noise, whereas high-frequency units were mostly unaffected. Most neurons that showed spatial tuning under broadband stimulation (white noise and 1 octave wide noise) turned omnidirectional when stimulated with 1/3 octave wide noise.

The Receptive-Field Organization of Simple Cells in Primary Visual Cortex of Ferrets under Natural Scene Stimulation

The responses of simple cells in primary visual cortex to sinusoidal gratings can primarily be predicted from their spatial receptive fields, as mapped using spots or bars. Although this quasilinearity is well documented, it is not clear whether it holds for complex natural stimuli. We recorded from simple cells in the primary visual cortex of anesthetized ferrets while stimulating with flashed digitized photographs of natural scenes. We applied standard reverse-correlation methods to quantify the average natural stimulus that invokes a neuronal response. Although these maps cannot be the receptive fields, we find that they still predict the preferred orientation of grating for each cell very well (r = 0.91); they do not predict the spatial-frequency tuning. Using a novel application of the linear reconstruction method called regularized pseudoinverse, we were able to recover high-resolution receptive-field maps from the responses to a relatively small number of natural scenes. These receptive-field maps not only predict the optimum orientation of each cell (r = 0.96) but also the spatial-frequency optimum (r = 0.89); the maps also predict the tuning bandwidths of many cells. Therefore, our first conclusion is that the tuning preferences of the cells are primarily linear and constant across stimulus type. However, when we used these maps to predict the actual responses of the cells to natural scenes, we did find evidence of expansive output nonlinearity and nonlinear influences from outside the classical receptive fields, orientation tuning, and spatial-frequency tuning.

Frequency-Specific Interaural Level Difference Tuning Predicts Spatial Response Patterns of Space-Specific Neurons in the Barn Owl Inferior Colliculus

Space-specific neurons in the barn owl's inferior colliculus have spatial receptive fields (RFs) because of sensitivity to interaural time difference and frequency-specific interaural level difference (ILD). These neurons are assumed to be tuned to the frequency-specific ILDs occurring at their spatial RFs, but attempts to assess this tuning with traditional narrowband stimuli have had limited success. Indeed, tuning assessed in this manner, when processed via a linear model of spectral integration, typically explains only approximately half the variance in spatial response patterns. Here we report our findings that frequency-specific ILD tuning of space-specific neurons, when assessed from responses to broadband stimuli, predicted nearly 75% of the variance in spatial responses, using a linear model of spectral integration (p < 0.0001; n = 97 neurons). Furthermore, when we tested neurons using only those frequencies we found to be spatially relevant, we saw that their responses were similar to those elicited by broadband stimuli. When we used frequencies not identified as spatially relevant, such similarity was lacking. Furthermore, spectral components that elicited high firing rates when presented as narrowband stimuli were found in several cases to be irrelevant for or detrimental to the definition of spatial RFs. Thus, neurons achieved sharp spatial tuning by selecting for ILDs of a subset of spectral components in noise, some of which were not identified using narrowband stimuli.