Spatial Receptive Fields Research Articles

Auditory Space-Time Receptive Field Dynamics Revealed by Spherical White-Noise Analysis

Numerous studies have investigated the spatial sensitivity of cat auditory cortical neurons, but possible dynamic properties of the spatial receptive fields have been largely ignored. Given the considerable amount of evidence that implicates the primary auditory field in the neural pathways responsible for the perception of sound source location, a logical extension to earlier observations of spectrotemporal receptive fields, which characterize the dynamics of frequency tuning, is a description that uses sound source direction, rather than sound frequency, to examine the evolution of spatial tuning over time. The object of this study was to describe auditory space-time receptive field dynamics using a new method based on cross-correlational techniques and white-noise analysis in spherical auditory space. This resulted in a characterization of auditory receptive fields in two spherical dimensions of space (azimuth and elevation) plus a third dimension of time. Further analysis has revealed that spatial receptive fields of neurons in auditory cortex, like those in the visual system, are not static but can exhibit marked temporal dynamics. This might result, for example, in a neuron becoming selective for the direction and speed of moving auditory sound sources. Our results show that approximately 14% of AI neurons evidence significant space-time interaction (inseparability).

Receptive fields in the rat piriform cortex.

Current models of odor discrimination in mammals involve molecular feature detection by a large family of diverse olfactory receptors, refinement of molecular feature extraction through precise projections of olfactory receptor neurons to the olfactory bulb to form an odor-specific spatial map of molecular features across glomerular layer, and synthesis of these features into odor objects within the piriform cortex. This review describes our recent work on odor and spatial receptive fields within the anterior piriform cortex and compares these fields with receptive fields of their primary afferent, olfactory bulb mitral/tufted cells. The results suggest that receptive fields in the piriform cortex are ensemble in nature, highly dynamic, and may contribute to odor discrimination and odor memory.

Deconstructing the receptive field: Information coding in macaque area MST

When cells respond well to complex stimuli, it is often difficult to determine which aspects of the stimulus are most relevant. We present a technique to describe the encoding of information on many stimulus features by a single cell. Based on the concept of conditional mutual information, we distinguish cells that are mono-, dual- or synergistic encoders, depending on their amount of specialisation for stimulus features. As an application of the technique, we show that cells in the macaque medial superior temporal area encode information on the direction of heading, but simultaneously on local features such as the direction of motion in small parts of their large spatial receptive field.

Reconstruction of Target Speed for the Guidance of Pursuit Eye Movements

We studied how object speed is reconstructed from the responses of motion-selective cells for the generation of a behavior that is tightly linked to the speed of visual motion. In theory, the speed of an object could be estimated either from the speed tuning of the active population of motion-selective cells or from the rate of displacement of activation across the cortical map of visual space. We measured the pursuit eye movements evoked by stimuli containing two conflicting motion components: a local component designed to excite motion-selective cells with a particular speed tuning and a displacement component designed to excite cells with a sequence of spatial receptive fields. Pursuit eye movements were driven primarily by the local-motion component and were affected to only a small degree by the rate of target displacement across visual space. Extracellular single-unit recordings using the same stimuli revealed that the responses of cells in the middle temporal visual area (MT) depended primarily on the local-motion component but were influenced by the displacement component to the same degree as were pursuit eye movements. We conclude that the initiation of pursuit is consistent with a reconstruction of target speed based on the speed tuning of the active population of MT cells.

Auditory spatial receptive fields created by multiplication.

Examples of multiplication by neurons or neural circuits are scarce, although many computational models use this basic operation. The owl's auditory system computes interaural time (ITD) and 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. A multiplication of separate postsynaptic potentials tuned to ITD and ILD, rather than an addition, can account for the subthreshold responses of these neurons to ITD-ILD pairs. Other nonlinear processes improve the spatial tuning of the spike output and reduce the fit to the multiplicative model.

Auditory Cortical Spatial Receptive Fields

Neurons in the primary auditory cortex (AI) of anesthetized cats were studied for their sensitivity to directions of transient sounds in virtual acoustic space under a variety of conditions. An effective transient sound evokes a single spike or short burst of spikes with a precisely timed onset. The aggregate of effective directions forms a spatial receptive field. Typically, spatial receptive fields are large, often occupying a quadrant or more of acoustic space. Within the receptive field onset latency varies systematically with direction thereby providing information about source direction. This receptive field structure is highly robust, remaining relatively stable under conditions of competing sounds. Maximum likelihood analysis suggests that psychophysical spatial acuity can be achieved with a relatively small ensemble of AI neurons with broad receptive fields having response gradients of latency. Using reverse correlation and white-noise analysis receptive fields were mapped in space and time. This analysis revealed that spatial receptive fields of AI neurons need not be static but may exhibit marked temporal dynamics. This suggests a sensitivity for direction and speed of moving sound sources.

Spatial receptive fields of inferior colliculus neurons to auditory apparent motion in free field.

We examined responses from 91 single-neurons in the inferior colliculus (IC) of anesthetized guinea pigs to auditory apparent motion in the free field. Apparent motion was generated by presenting 100-ms tone bursts, separated by 50-ms silent intervals, at consecutive speaker positions in an array of 11 speakers, positioned in an arc +/-112.5 degrees around midline. Most neurons demonstrated discrete spatial receptive fields (SRFs) to apparent motion in the clockwise and anti-clockwise directions. However, SRFs showed marked differences for apparent motion in opposite directions. In virtually all neurons, mean best azimuthal positions for SRFs to opposite directions occurred at earlier positions in the motion sweep, producing receptive fields to the two directions of motion that only partially overlapped. Despite this, overall spike counts to the two directions were similar for equivalent angular velocities. Responses of 28 neurons were recorded to stimuli with different duration silent intervals between speaker presentations, mimicking different apparent angular velocities. Increasing the stimulus OFF time increased neuronal discharge rates, particularly at later portions of the apparent motion sweep, and reduced the differences in the SRFs to opposite motion directions. Consequently SRFs to both directions broadened and converged with decreasing motion velocity. This expansion was most obvious on the outgoing side of the each SRF. Responses of 11 neurons were recorded to short (90 degrees ) partially overlapping apparent motion sweeps centered at different spatial positions. Nonoverlapping response profiles were recorded in 9 of the 11 neurons tested and confirmed that responses at each speaker position were dependent on the preceding response history. Together these data are consistent with the suggestion that a mechanism of adaptation of excitation contributes to the apparent sensitivity of IC neurons to auditory motion cues. In addition, the data indicate that the sequential activation of an array of speakers to produce apparent auditory motion may not be an optimal stimulus paradigm to separate the temporal and spatial aspects of auditory motion processing.

Mathematical models for the spatial receptive-field organization of nonlagged X-cells in dorsal lateral geniculate nucleus of cat.

Spatial receptive fields of relay cells in dorsal lateral geniculate nucleus (dLGN) have commonly been modeled as a difference of two Gaussian functions. We present alternative models for dLGN cells which take known physiological couplings between retina and dLGN and within dLGN into account. The models include excitatory input from a single retinal ganglion cell and feedforward inhibition via intrageniculate interneurons. Mathematical formulas describing the receptive field and response to circular spot stimuli are found both for models with a finite and an infinite number of ganglion-cell inputs to dLGN neurons. The advantage of these models compared to the common difference-of-Gaussians model is that they, in addition to providing mathematical descriptions of the receptive fields of dLGN neurons, also make explicit contributions from the geniculate circuit. Moreover, the model parameters have direct physiological relevance and can be manipulated and measured experimentally. The discrete model is applied to recently published data (Ruksenas et al., 2000) on response versus spot-diameter curves for dLGN cells and for the retinal input to the cell (S-potentials). The models are found to account well for the results for the X-cells in these experiments. Moreover, predictions from the discrete model regarding receptive-field sizes of interneurons, the amount of center-surround antagonism for interneurons compared to relay cells, and distance between neighboring retinal ganglion cells providing input to interneurons, are all compatible with data available in the literature.

Do Simple Cells in Primary Visual Cortex Form a Tight Frame?

Sets of neuronal tuning curves, which describe the responses of neurons as functions of a stimulus, can serve as a basis for approximating other functions of stimulus parameters. In a function-approximating network, synaptic weights determined by a correlation-based Hebbian rule are closely related to the coefficients that result when a function is expanded in an orthogonal basis. Although neuronal tuning curves typically are not orthogonal functions, the relationship between function approximation and correlation-based synaptic weights can be retained if the tuning curves satisfy the conditions of a tight frame. We examine whether the spatial receptive fields of simple cells in cat and monkey primary visual cortex (V1) form a tight frame, allowing them to serve as a basis for constructing more complicated extrastriate receptive fields using correlation-based synaptic weights. Our calculations show that the set of V1 simple cell receptive fields is not tight enough to account for the acuity observed psychophysically.

Modeling place fields in terms of the cortical inputs to the hippocampus.

A model of place-cell firing is presented that makes quantitative predictions about specific place cells' spatial receptive fields following changes to the rat's environment. A place cell's firing rate is modeled as a function of the rat's location by the thresholded sum of the firing rates of a number of putative cortical inputs. These inputs are tuned to respond whenever an environmental boundary is at a particular distance and allocentric direction from the rat. The initial behavior of a place cell in any environment is simply determined by its set of inputs and its threshold; learning is not necessary. The model is shown to produce a good fit to the firing of individual place cells, and populations of place cells across environments of differing shape. The cells' behavior can be predicted for novel environments of arbitrary size and shape, or for manipulations such as introducing a barrier. The model can be extended to make behavioral predictions regarding spatial memory.

Complex cells as linear mechanisms receiving sequential afferents

Complex cells in mammalian visual cortex appear to be non-linear mechanisms lacking a structured receptive field, and different complex cells display mutually inconsistent behaviors. Current models postulate nonlinear interactions among multiple simultaneous afferents, but none explains the diversity of complex cell behaviors. We propose that complex cell inputs are sequential and cyclic. Cells receiving such input behave as if their spatial receptive field changes shape over time. Different putative time-varying receptive fields arise when the number of afferents, their characteristics and/or the sequence of their inputs vary, and simulations show that they exhibit all reported varieties of complex cell behavior. Our results suggest a common functional description for simple and complex cells. Additional non-linearities are unnecessary to explain complex cell behavior.

Probabilistic framework for the adaptation and comparison of image codes

We apply a Bayesian method for inferring an optimal basis to the problem of finding efficient image codes for natural scenes. The basis functions learned by the algorithm are oriented and localized in both space and frequency, bearing a resemblance to two-dimensional Gabor functions, and increasing the number of basis functions results in a greater sampling density in position, orientation, and scale. These properties also resemble the spatial receptive fields of neurons in the primary visual cortex of mammals, suggesting that the receptive-field structure of these neurons can be accounted for by a general efficient coding principle. The probabilistic framework provides a method for comparing the coding efficiency of different bases objectively by calculating their probability given the observed data or by measuring the entropy of the basis function coefficients. The learned bases are shown to have better coding efficiency than traditional Fourier and wavelet bases. This framework also provides a Bayesian solution to the problems of image denoising and filling in of missing pixels. We demonstrate that the results obtained by applying the learned bases to these problems are improved over those obtained with traditional techniques.

Signals and noise in the elasmobranch electrosensory system

Analyzing signal and noise for any sensory system requires an appreciation of the biological and physical milieu of the animal. Behavioral studies show that elasmobranchs use their electrosensory systems extensively for prey detection, but also for mate recognition and possibly for navigation. These biologically important signals are detected against a background of self-generated bioelectric fields. Noise-suppression mechanisms can be recognized at a number of different levels: behavior, receptor anatomy and physiology, and at the early stages of sensory processing. The peripheral filters and receptor characteristics provide a detector with permissive temporal properties but restrictive spatial characteristics. Biologically important signals probably cover the range from direct current to 10 Hz, whereas the bandwidth of the receptors is more like 0.1-10 Hz. This degree of alternating current coupling overcomes significant noise problems while still allowing the animal to detect external direct current signals by its own movement. Self-generated bioelectric fields modulated by breathing movement have similar temporal characteristics to important external signals and produce very strong modulation of electrosensory afferents. This sensory reafference is essentially similar, or common-mode, across all afferent fibers. The principal electrosensory neurons (ascending efferent neurons; AENs) of the dorsal octavolateralis nucleus show a greatly reduced response to common-mode signals. This suppression is mediated by the balanced excitatory and inhibitory components of their spatial receptive fields. The receptive field characteristics of AENs determine the information extracted from external stimuli for further central processing.

Respiratory Airflow Pattern at the Rat’s Snout and an Hypothesis Regarding Its Role in Olfaction

Respiratory airflow outside the external nares of the rat was mapped by monitoring temperature fluctuations with a thermistor and simultaneous piezoelectric monitoring of respiration-associated chestwall movement. The results demonstrated that both exhalation and inhalation airflow were directed laterally. Relatively little air exchange occurred anterior to the nares. These results suggest that the two nares of the rat take independent, bilateral samples of the odor environment. Combined with recent descriptions of laterally specific, spatial receptive fields in piriform cortical neurons, an hypothesis is outlined describing a mechanism of odor orientation in the rat involving comparisons of timing or intensity of bilateral odor stimulation.

A neuronal representation of the location of nearby sounds.

Humans can accurately perceive the location of a sound source-not only the direction, but also the distance. Sounds near the head, within ducking or reaching distance, have a special saliency. However, little is known about this perception of auditory distance. The direction to a sound source can be determined by interaural differences, and the mechanisms of direction perception have been studied intensively; but except for studies on echolocation in the bat, little is known about how neurons encode information on auditory distance. Here we describe neurons in the brain of macaque monkeys (Macaca fascicularis) that represent the auditory space surrounding the head, within roughly 30 cm. These neurons, which are located in the ventral premotor cortex, have spatial receptive fields that extend a limited distance outward from the head.

Structure and dynamics of receptive fields in the visual cortex of the cat (area 18) and the influence of GABAergic inhibition.

Receptive fields (RFs) in the visual cortex are characterized by spatiotemporal profiles that have been described in detail for area 17 simple cells. In this study, we analyse spatial and temporal RF properties of simple and complex cells in layer II/III of area 18 of the anaesthetized adult cat, using the reverse correlation method with brief 50 ms presentations of flashing bright and dark bars. Stimuli were presented with preferred orientation as previously determined by moving bars. Simple cell RFs were characterized by spatially and temporally separable ON and OFF subfields, while in complex cells ON and OFF subfields were superimposed. To discriminate possible contributions of GABAergic inhibition to RF structure and response dynamics in area 18, we have used three-barrelled micropipettes for single cell recordings and microiontophoresis, and have documented ON and OFF responses before, during and after application of bicuculline methiodide for blockade of GABAA receptors. During blockade of GABAergic inhibition, the stimulus-induced and resting discharge frequency increased, and in about 50% of the cells both ON and OFF subfields changed significantly in space and/or time in a reversible manner. In space, blockade of inhibition widened RF subfields, whereas in time, it shortened the duration of the excitatory cell response in simple and complex cells. ON and OFF subfields separated in space and time (simple cells), or time (complex cells) became less isolated or even superimposed. The results indicate substantial local inhibitory processing contributing to spatiotemporal RF properties in layers II/III of area 18 of the cat.

Modeling of auditory spatial receptive fields with spherical approximation functions.

A spherical approximation technique is presented that affords a mathematical characterization of a virtual space receptive field (VSRF) based on first-spike latency in the auditory cortex of cat. Parameterizing directional sensitivity in this fashion is much akin to the use of difference-of-Gaussian (DOG) functions for modeling neural responses in visual cortex. Artificial neural networks and approximation techniques typically have been applied to problems conforming to a multidimensional Cartesian input space. The problem with using classical planar Gaussians is that radial symmetry and consistency on the plane actually translate into directionally dependent distortion on spherical surfaces. An alternative set of spherical basis functions, the von Mises basis function (VMBF), is used to eliminate spherical approximation distortion. Unlike the Fourier transform or spherical harmonic expansions, the VMBFs are nonorthogonal, and hence require some form of gradient-descent search for optimal estimation of parameters in the modeling of the VSRF. The optimization equations required to solve this problem are presented. Three descriptive classes of VSRF (contralateral, frontal, and ipsilateral) approximations are investigated, together with an examination of the residual error after parameter optimization. The use of the analytic receptive field model in computational models of population coding of sound direction is discussed, together with the importance of quantifying receptive field gradients. Because spatial hearing is by its very nature three dimensional or, more precisely, two dimensional (directional) on the sphere, we find that spatial receptive field models are best developed on the sphere.

Sparse coding with an overcomplete basis set: A strategy employed by V1?

The spatial receptive fields of simple cells in mammalian striate cortex have been reasonably well described physiologically and can be characterized as being localized, oriented, and bandpass, comparable with the basis functions of wavelet transforms. Previously, we have shown that these receptive field properties may be accounted for in terms of a strategy for producing a sparse distribution of output activity in response to natural images. Here, in addition to describing this work in a more expansive fashion, we examine the neurobiological implications of sparse coding. Of particular interest is the case when the code is overcomplete--i.e., when the number of code elements is greater than the effective dimensionality of the input space. Because the basis functions are non-orthogonal and not linearly independent of each other, sparsifying the code will recruit only those basis functions necessary for representing a given input, and so the input-output function will deviate from being purely linear. These deviations from linearity provide a potential explanation for the weak forms of non-linearity observed in the response properties of cortical simple cells, and they further make predictions about the expected interactions among units in response to naturalistic stimuli.

Receptive field dimensions of lateral geniculate cells in the common marmoset ( Callithrix jacchus)

We measured the spatial receptive field dimensions of cells in the lateral geniculate nucleus (LGN) of the common marmoset ( Callithrix jacchus) using a bipartite field stimulus in which the two halves of the field were modulated identically but in countrphase. Horizontal and vertical edges between the two fields were positioned at different locations in the receptive field. By assuming that centers and surrounds have gaussian profiles, we were able to obtain a satisfactory mathematical description of the data. Receptive field centers were about a factor 1.6 larger than those of macaque LGN cells, in accordance with the smaller marmoset eye. There was a limited correspondence with dendritic tree dimensions of marmoset retinal ganglion cells. We further found that center and surround gaussians were not always concentric, and that the centers of some cells were elongated. This might allow some direction or orientation biases in LGN cells.

Binaral interactions in the rat piriform cortex.

Single-unit recordings were made from layer II/III anterior piriform cortex (aPCX) neurons in adult Wistar rats to examine odor response patterns to unilaterally and bilaterally delivered stimuli. Isoamyl acetate odor stimulation was presented either unilaterally through tubes inserted into the external nares, or bilaterally during unilateral olfactory bulb lidocaine infusions. Olfactory bulb multiunit or slow-wave activity was recorded simultaneously bilaterally to monitor selectivity of unilateral odor stimulation. The results demonstrate that 1) commissural input to aPCX neurons is sufficient to drive odor responses, and 2) aPCX neurons can be classified on the basis of spatial receptive field type. These receptive fields include cells that respond 1) selectively to ipsilateral stimulation, 2) selectively to contralateral stimulation, 3) to either ipsilateral or contralateral stimulation, and 4) selectively to bilateral stimulation. The potential functions of binaral convergence in the piriform cortex are discussed, and may include enhancement of perceived odor intensity and bilateral access to olfactory memory.