The classical receptive fields of simple cells in mammalian primary visual cortex demonstrate three cardinal response properties: (1) they do not respond to stimuli that are spatially homogeneous; (2) they respond best to stimuli in a preferred orientation (direction); and (3) they do not respond to stimuli in other, nonpreferred orientations (directions). We refer to these as the balanced field property, the maximum response direction property, and the zero response direction property, respectively. These empirically determined response properties are used to derive a complete characterization of elementary receptive field functions defined as products of a circularly symmetric weight function and a simple periodic carrier. Two disjoint classes of elementary receptive field functions result: the balanced Gabor class, a generalization of the traditional Gabor filter, and a bandlimited class whose Fourier transforms have compact support (i.e., are zero valued outside of a bounded range). The detailed specification of these two classes of receptive field functions from empirically based postulates may prove useful to neurophysiologists seeking to test alternative theories of simple cell receptive field structure and to computational neuroscientists seeking basis functions with which to model human vision.
© 2009 Optical Society of America
The pioneering work of Hubel and Weisel [1, 2] established that neurons in the mammalian primary visual cortex possessed receptive fields that, unlike the circularly concentric receptive fields of subcortical visual neurons, were spatially oriented. The receptive field of one type of cortical neuron, the simple cell, possessed discrete elongated regions within which stimulation by light evoked either excitation or inhibition. This geometry suggested that simple cells might be especially responsive to visual stimuli consisting of bars or edges. Reinterpreting the presumptive role of simple cells as bar and edge detectors, DeValois and colleagues [3, 4] demonstrated that the periodic structure of simple cell receptive fields rendered them highly selective for stimulus spatial frequency and suggested that they might therefore constitute the basis functions for a piecewise Fourier (or wavelet) encoding of the retinal intensity distribution. Much attention was concurrently devoted to developing a mathematical description of the simple cell receptive field function. The first such descriptions, formulated by Marcelja  and Daugman [6, 7], inspired by the earlier work of Gabor , showed that the spatial sensitivity of simple cells was well described by a 2D Gaussian-damped sine-wave carrier signal, a so-called Gabor function. Owing to some undesirable features of the Gabor function, in particular the fact that it does not integrate to zero for all carrier phases, a variety of competing mathematical formulations have been proposed, which include the difference-of-Gaussians [9, 10], the Laplacian-of-a-Gaussian , the log-Gabor  and the Cauchy function ; see Wallis  for a critical review. However, the Gabor model has withstood the test of repeated physiological [15, 16, 4, 17], and psychophysical [18, 19] verification and has therefore emerged as the most commonly accepted mathematical description of cortical simple cell receptive field structure. Theorists interested in developing mathematical descriptions and computational models of various aspects of human spatial vision therefore frequently employ Gabor filters as basis functions [20, 21, 22, 23, 24].
Experimental studies have established that simple cells show a variety of well-defined behaviors . We are concerned here with three essential properties of simple cell receptive fields: (1) the balanced field property (i.e., spatially homogeneous patterns produce a zero response); (2) the zero response direction (ZRD) property [i.e., there is a direction (viz, stimulus orientation) that elicits a zero response to sinusoidal gratings]; and (3) the maximum response direction (MRD) property [the maximum response decreases monotonically to zero as direction (i.e., stimulus orientation) changes from the optimal direction to a direction perpendicular to the optimal]. Note that we use the term “direction” to describe what vision scientists commonly refer to as “orientation,” where grating direction is orthogonal to grating orientation.
In this paper we use these three empirical response properties of simple cells as postulates, which are themselves independent of any particular receptive field structure, and apply them to obtain a complete classification of elementary receptive field functions, which are defined as the product of a circularly symmetric weight function and a simple periodic carrier. Thus, we describe all possible types of elementary receptive field functions that satisfy these empirical constraints. Two disjoint classes of receptive field functions result. The first class, designated here as balanced Gabor receptive fields, is found to be a natural generalization of the traditional Gabor receptive field model. It includes as its simplest case the simple balanced Gabor. The simple balanced Gabor has a receptive field structure similar to the traditional Gabor receptive field model but integrates to zero for all spatial phases of the periodic carrier function. Balanced Gabor filters possess all of the desirable features of the traditional Gabor model, viz., spatial frequency and orientation (direction) tuning, etc., but correct what is commonly regarded as the chief deficiency of the traditional Gabor, which is that it possesses a nonzero DC response. The second class, designated here as bandlimited receptive fields  also possess well-behaved spatial frequency and orientation response properties but differ sufficiently from balanced Gabor functions in other respects that an empirical determination of which class best describes simple cell receptive field structure may be possible.
This paper presents formulation, terminology, and a complete statement of our results together with examples of elementary receptive field functions. The more extensive mathematical derivations are given as Appendices A, B, C in a separate Supplement together with additional figures . Appendices A and B derive our main results stated in Section 4, and Appendix C contains miscellaneous derivations. Appendices are referenced herein as appropriate.
2. FORMALIZATION OF POSTULATED SIMPLE CELL RECEPTIVE FIELD PROPERTIES
This section states the ZRD and MRD properties and provides a concise mathematical formulation. It should be noted that these three properties are cumulative, not independent; that is, the MRD property mathematically implies the ZRD property, which in turn implies the balanced field property. Although experimental procedure may emphasize the MRD, the ZRD has more immediate theoretical implications, and this cumulative formulation has been found useful for the development of such implications. It is assumed that the integral [Eq. (1) below] describes the interaction of the receptive field with the stimulus, but no assumption about a specific structure of the receptive field is made in this section. Section 3 will make such an assumption in defining an elementary receptive field function and a mathematically rigorous formulation will be given there.
We define the visual field as a plane, described by the Cartesian coordinates (briefly, ). We define visual stimuli, or patterns in the visual field, as nonnegative, bounded, and possibly time-dependent functions on the plane. The receptive field of the simple cell is described with respect to a fixed reference location, its center, taken here to be the origin. The receptive field is modeled by the receptive field function , an absolutely integrable function that is assumed to interact with the stimulus pattern by
The response to a sinusoidal grating stimulus is closely related to the Fourier transform of the receptive field function. Specifically, the Fourier transform of is defined by
Since the response function, that is, the response over all grating directions and wavelengths, determines the Fourier transform of R, sinusoidal grating experiments have fundamental significance for the study of the receptive field. If Eq. (1) completely described the response to a visual stimulus, then the Fourier transform, that is, the response function, would completely determine the receptive field. In practice, the response necessarily includes nonlinear behavior not described by Eq. (1), but it is widely accepted that the equation models a major portion of the response, and the response function determined by sinusoidal grating experiments plays a correspondingly major role. A second reason for the fundamental significance of grating experiments is that simple cells respond in a remarkably well-defined way to sinusoidal grating stimuli, showing a maximum response for an optimum grating direction and optimum grating wavelength, then decreasing steadily as these parameters vary from the optimum with, in particular, a zero response for grating directions perpendicular to the optimum direction. Our postulates are expressed in terms of such observed behavior for the response to sinusoidal gratings.
The first postulated property of simple cells is that spatially homogeneous patterns produce a zero response, i.e., the
Balanced Field Property. The response to a spatially homogeneous pattern is zero.
Such patterns correspond to a zero-contrast grating. The constant scales out, and the mathematical form is
The second postulated property of simple cells is that there is a stimulus direction (i.e., grating orientation) that elicits a zero response, the ZRD property:
ZRD Property (Form 1). There exist values and such that for all sinusoidal gratings p with grating direction and contrast .
The mathematical form is that, for all grating phases and wavelengths ,9) can then hold for all if and only if , the ZRD property is equivalent to the following formulation, which drops all reference to grating contrast and phase:
ZRD Property (Form 2). There exists a value such that, for all ,10) to show that the receptive field is balanced; then Eq. (9) follows for arbitrary contrast. The direction is a ZRD and is determined only up to an additive multiple of π; values differing by multiples of π are equivalent directions, and multiple, that is, nonequivalent, zero response directions may occur.
Incidentally, in modeling the neurophysiological response to excitation and inhibition, the response is sometimes taken to be the positive part of the calculated numerical value since firing rates cannot be negative. Using that convention, a zero response would mean , that is, . That convention is not used here: response means , and a zero response means .
The third postulated property is essentially that the maximum response decreases monotonically to zero as direction (i.e., stimulus orientation) changes from the optimal direction to a direction perpendicular to the optimal, the MRD property:
MRD Property (Form 1). There exists a value such that is not identically zero and a value such that, for all sinusoidal gratings p with contrast and at each fixed wavelength , either the response is zero for all grating directions or it is strictly decreasing to zero (and remains zero) as the grating direction changes from .
The range covers one period of , and the MRD property implies for each wavelength . Thus, the MRD property implies the ZRD property with . The balanced field property therefore holds as well, so that
The MRD Property is equivalent to the following formulation, which drops all reference to grating contrast and phase:
MRD Property (Form 2). For some pair ,
To see that Form 2 implies Form 1, notice that
The direction is a MRD and is determined only up to an additive multiple of π; values differing by multiples of π are equivalent directions (orientations). It should be emphasized that this property refers not only to the existence of a direction (orientation) of maximum response but also to the monotonic decrease in response with increasing angular distance from the optimal direction. Such monotonic behavior implies that a maximum response direction, if it exists, is unique.
It should be noted that the properties are robust with respect to nonlinear processing. For example, if the response defined by Eq. (1) is followed by a nonlinear operation, then the properties will continue to hold for the new result given some mild conditions on the nonlinear operation, such as monotonicity and having zero as a fixed point.
3. ELEMENTARY RECEPTIVE FIELD FUNCTIONS AND HANKEL TRANSFORMS
Receptive fields are typically modeled as a product of a weight function, providing localization of the response, and an oscillatory carrier function, providing directionality (orientation) to the response. This section defines an elementary receptive field function to be the product of a circularly symmetric weight function and a simple periodic carrier. For such receptive field functions, the response to a sinusoidal grating can be expressed in terms of the Hankel transform of the weight function. This section describes the Hankel transform and its use to provide reduced mathematical formulations of the ZRD and MRD properties for elementary receptive field functions. These reduced formulations are the basis for the results of Section 4.
We define an elementary receptive field function (centered at the origin) to be the product of a circularly symmetric weight function q and a simple periodic carrier function, that is,
Section 2 formulated properties of the receptive field in terms of the response to sinusoidal gratings, and then gave mathematical formulations in terms of the Fourier transform . The form (11) for the receptive field is essentially a modulated circularly symmetric function. The 2D Fourier transform of a circularly symmetric function is also a circularly symmetric function, and the relation between these two functions of a single radial variable is given by the Hankel transform:4)]. The transform and the inverse transform are given specifically by12) imply11) are simple modulations of the circularly symmetric weight functions q, the Fourier transform can be expressed in terms of translations of the Fourier transform , which in turn can be expressed in terms of the Hankel transform (see Appendix C in the Supplement ). To express various relations, it will be useful to write and3 noted general relations between the Fourier transform of the receptive field function R and its response to a sinusoidal grating, and the corresponding quantities for an elementary receptive field function therefore reduce to expressions involving the Hankel transform . Specifically, for constant patterns, Eq. (5) becomes6), becomes7), becomes20) in terms of and and is now given by19, 20, 23) are completely general formulas describing, in terms of the Hankel transform , the response of elementary receptive field functions (11) to sinusoidal grating stimuli.
Section 2 formulated the three properties in terms of the Fourier transform of the general receptive field function R. Using Eq. (18), those results now become formulations of the properties for an elementary receptive field function (11) in terms of the Hankel transform .
The first result follows immediately from Eq. (19) and uniquely determines the balancing parameter :
Lemma 1. Let the receptive field function be given by Eq. (11). Let satisfy Eq. (12) [in which case the Hankel transform exists and satisfies Eq. (15)]. Then has the balanced field property if and only if10), Eq. (15), and the representation (18) with :
Lemma 2. Let the receptive field function be given by Eq. (11). Let satisfy Eq. (12) [in which case the Hankel transform exists and satisfies Eq. (15)]. Then has the ZRD property if and only if there exists a value such that the following relations hold for all :
The third result is a direct restatement of the MRD property (Form 2) in terms of the amplitude factor :
Lemma 3. Let the receptive field function be given by Eq. (11). Let satisfy Eq. (12) [in which case the Hankel transform exists and satisfies Eq. (15)]. Then has the MRD property if and only if for some pair and there exists a value such that, at each fixed wavelength , either is zero for all grating directions or it is strictly decreasing to zero (and remains zero) as increases.
Section 2 observed that an MRD, if it exists, is unique. It is evident from Eq. (23) that is an even function of , which implies . Section 2 also observed that the MRD property implies the ZRD property, specifically, that a ZRD is given by .
4. CHARACTERIZATION OF ELEMENTARY RECEPTIVE FIELD FUNCTIONS WITH POSTULATED PROPERTIES
This section first states Theorems A.1 and A.2, which describe elementary receptive field functions with the ZRD property, and then states the main result, Theorem B.1, a complete characterization of elementary receptive field functions with the MRD property for cosine-type and mixed-type receptive fields. Related results for sine-type receptive fields are summarized in the course of discussion as Theorems B.2 and B.3. The proofs for A.1 and A.2 involve a preparatory lemma and are given in Appendix A . The proof for Theorem B.1 builds on Theorems A.1 and A.2 and is given in Appendix B .
Theorem A.1 (Cosine-type and mixed-type receptive field functions). Let the receptive field function be given by Eq. (11). Let satisfy Eq. (12) [in which case the Hankel transform exists and satisfies Eq. (15)]. Assume . Then has the ZRD property if and only if satisfies one of the following cases:
- and where is with and . In this case, there is exactly one ZRD given by .
- and , where is with and . In this case, there is exactly one ZRD given by .
- and on the interval but on no larger interval. In this case, there is a sector of ZRDs and the sector is given by .
Note that Theorem A.1(4) is simply a remaining case, where the theorem does not provide a definitive conclusion. We conjecture that no exists, that is, that the case is vacuous, but we have been unable to settle the conjecture under the sole condition that a ZRD exists. This case is eliminated at the next stage, where the MRD Property is assumed.
Theorem A.2 (Sine-type receptive field functions). Let the receptive field function be given by Eq. (11). Let satisfy Eq. (12) [in which case the Hankel transform exists and satisfies Eq. (15)]. Assume . Then
- has a ZRD given by .
Theorem B.1. Let the receptive field function be given by Eq. (11). Let satisfy Eq. (12) [in which case the Hankel transform exists and satisfies Eq. (15)]. Assume . Then has the MRD property if and only if satisfies one of the following cases:
(1) where , is continuous and positive on the real line, , , and
if , then, for each a, the function
is initially zero on and strictly increasing on ;
if , then, for each a, the function
is strictly increasing on .
In , (that is, is initially zero on a nontrivial interval) if and only if the value a satisfies
For both and :
(a) the MRD is given by ;
(b) the ZRD is unique and given by ;
(c) is positive and strictly decreasing for all y.
(2) is strictly decreasing on and on . In this case:
(a) the MRD is given by ;
(b) there is a sector of ZRDs given by .
The remainder of this section discusses implications of Theorem B.1, in particular, that it leads to two disjoint classes of receptive field functions. A preliminary analysis of the two classes is given. Subsections 5A, 5B, respectively, provide more detailed results for each class as well as explicit analytic examples illustrating those results.
In result (1) of Theorem B.1, parts and can be considered as providing tests for candidate periodic functions in forming the Hankel transform. Notice it is sufficient to test the expressions for since , and thus the given expressions as well, has period 1. However, it is useful to leave the criterion in terms of arbitrary a. Equation (30) says that the strictly decreasing function reduces to a linear function on some intervals. This condition (with ) cannot hold for all a, or even for , because would reduce to a strictly linear function over an interval larger than a period. Consequently, expression (28) must be strictly increasing on for some values of a.
Theorem B.1 completely characterizes elementary receptive field functions (of cosine-type and mixed-type) possessing the MRD property in terms of the Hankel transform of the receptive field weight functions . For the moment, let us refer to weights occurring under result (1) as Type I weights and those under result (2) as Type II weights. These two classes of weight functions are completely disjoint, since the Hankel transform for a Type I weight is positive for all ρ, while the transform for a Type II weight is zero outside a finite interval. The characterization theorem thus results in two disjoint classes of receptive field functions , each possessing the MRD property.
Type I and Type II weights yield quite different formulas for the amplitude response factor given by Eq. (23), and the formulas may be helpful in understanding the results of Theorem B.1. (The formulas continue to hold for sine-type receptive fields.) For Type I weights with Hankel transform where has period one, the factor is32) with result (1) shows that or implies that, for fixed , is strictly decreasing as increases. For Type II weights with Hankel transform vanishing on some interval , the factor is simply
Type II weights are well defined by result (2); in particular, the definition is independent of the receptive field parameters. In contrast, the definition of Type I weights in result (1) depends on the receptive field phase . That is, is a Type I weight if its Hankel transform satisfies the conditions of result (1) for some , and it may be that satisfies the conditions or for some values of and not for others. Roughly speaking, test becomes less restrictive as approaches 0, that is, as the receptive field approaches a sine-type receptive field. This observation suggests that, within the Type I class, cosine-type receptive fields are the most basic type. The following theorem illustrates this idea by showing that cosine-type receptive field functions can be used to construct receptive field functions for both mixed-type and sine-type receptive fields. This theorem is the basis for the definition of balanced Gabor weights in Subsection 5A, the subclass of Type I weights that can be used to define elementary receptive field functions with the MRD Property for arbitrary receptive field phase. Type II weights are precisely the bandlimited weights of Subsection 5B. Notice that Theorem B.2 yields sine-type receptive field functions.
- where , is continuous and positive on the real line, , .
- is positive and strictly decreasing for all y.
- For each a, the function is initially zero on and strictly increasing on .
- In (c), if and only if the value a satisfies on for some constant .
Theorem B.2 follows directly from result (1) of Theorem B.1:
- For cosine-type receptive fields, has the MRD Property because the conditions are simply a restatement of .
- For mixed-type receptive fields, has the property because holds. Conditions (c) and (b) respectively imply that the component of Eq. (29) is increasing and the component is strictly increasing because is strictly increasing.
Theorem A.2 shows that sine-type elementary receptive field functions possessing a ZRD form a much broader class than the corresponding cosine-type and mixed-type receptive field functions described by Theorem A.1. Similarly, sine-type elementary receptive field functions with the MRD property form a broader class than the cosine-type and mixed-type receptive field functions described by Theorem B.1. The following theorem gives partial results for sine-type receptive fields.
- If with and is positive and strictly decreasing for all y, then with has the MRD property. In this case, there is a unique ZRD given by .
- If is strictly decreasing on and on , then with has the MRD property. In this case, there is a sector of ZRDs and the sector is given by .
- has the MRD property and more than one ZRD if and only if satisfies (2) with . In this case, and there is a sector of ZRDs.
5. RECEPTIVE FIELD FUNCTIONS
5A. Balanced Gabor Receptive Field Functions: Discussion and Examples
This subsection defines and discusses the balanced Gabor class of weights and elementary receptive field functions mentioned in Section 4. Two cases are analyzed: the simple balanced Gabor receptive field function, corresponding to the traditional Gabor filter model of the receptive field, and a more general class of balanced Gabor weights, corresponding to elementary receptive fields with weight functions that are not simple Gaussians but that are products of Gaussians and oscillatory components.
5A1. Balanced Gabor Weights and Receptive Fields
Balanced Gabor weights (with exponent ) are weight functions satisfying
- , where is continuous and positive on the real line, , ;
- is strictly decreasing on the real line;
All parameters and independent variables are dimensionless. For each balanced Gabor Hankel transform (and thus for the corresponding weight function), the exponent is uniquely determined. The exponents thus partition or classify both the transforms and the weights. For balanced Gabor weights , is necessarily positive because Eq. (14) reduces to a positive integrand for . Simple balanced Gabor weights refer to the special case . The following subsection discusses these weights and compares them with the traditional Gabor filter model for receptive fields.
Some points should be mentioned with regard to checking conditions (b), (c), and (d) of the definition. In checking (b) for a candidate periodic function , it is necessary to check only that is strictly decreasing over an interval of length one, since shifting this function by a period multiplies it by a constant:
- the condition on for some interval since the expression is 1-periodic in a;
While the sets of balanced Gabor Hankel transforms for different exponents are disjoint, the corresponding sets of periodic components are related:
Closure Lemma. Let26]. Result (3) follows directly from (1) and (2).
Two aspects of the Closure Lemma should be noted. First, the sets of periodic components for different exponents simply increase in extent as increases. Second, new weights can be formed by appropriately interpreted convex combinations of old weights. For example, let , be balanced Gabor weights with corresponding Hankel transforms , , where . Then, by result (2), convex combinations of the form
A balanced Gabor receptive field function (with exponent ) is an elementary receptive field function where the receptive field weight is a balanced Gabor function, that is,4, balanced Gabor weights are precisely the weights that are phase independent in the sense that elementary receptive fields based on these weights have the MRD property for all receptive field phase values .
Balanced Gabor receptive field functions have a unique ZRD given by (Theorem B.1).
The Fourier transform of a balanced Gabor receptive field function , where the weight has Hankel transform , follows from Eq. (18) and is given by20) and is given by5B), although this term is the exponentially dominant component. Consequently, for fixed grating orientation , grating wavelength , and grating contrast , the maximum of the response does not occur at a grating phase that exactly lines up with the receptive field phase .5B). The maximum of the max-response, that is, the max of , occurs at for fixed ; that is, the optimal grating orientation lines up with the receptive field orientation . This is a general consequence of the MRD property, but it can also be seen in the expression for , since the portion is strictly decreasing as increases by part (b) of the definition of balanced Gabor weight and the portion is strictly decreasing by part (c). [Cosine-type filters may decrease to intervals where due to condition (d).] However, examples show that the maximum, for fixed grating orientation , does not necessarily occur at ; that is, the optimal grating spatial wavelength does not necessarily occur at the receptive field spatial wavelength, another difference between the balanced Gabor and bandlimited cases (see examples below and Subsection 5B). Notice that (for ) because
An explicit transform pair for the Hankel transform is
5A2. Example: Simple Balanced Gabor Receptive Field Functions (and Traditional Gabor Filters)
The traditional Gabor filter model for a receptive field function is11). This is a typical normalization of the Gabor filter, where the Gaussian factor has unit volume. Its Fourier transform is2) is4], giving 0.0425 for the exponential term in Eq. (47). That is, for this ratio, the imbalance of a cosine-type filter is about 4% of the Gaussian component’s unit volume and becomes worse as increases, that is, at large bandwidth.
The simple balanced Gabor weight is determined by an exponent . The weight and its Hankel transform are given by37, 38):45, 49) shows that the receptive field function is essentially the Gabor filter corrected to achieve balance. This is, of course, the motivation for the name of this class of weights. The exponent can be considered a dimensionless “shape” parameter that arises naturally in the derivation of these functions and unifies all cases of balanced Gabor weights, or, since matching the Gaussian components of Eqs. (45, 49) gives the relation , can be considered a measure of “reciprocal bandwidth.” Figure 1 illustrates weights and corresponding Hankel transforms for a range of values of . Figure 2 compares the traditional Gabor filter and the corresponding simple balanced Gabor receptive field function with identical Gaussian components, that is, with identical weight functions (“envelopes”). Figure 2 also shows the corresponding Fourier transforms. The imbalance of the traditional Gabor receptive field is shown by the nonzero values of its Fourier transform at the origin.
It will be useful to express our results in terms of the exponent since it provides a common unifying parameter for the entire class of balanced Gabor receptive field functions, both simple and nonsimple (see the following subsection). The typical value gives . Consequently, typical trial values for our plots in this subsection will be (respectively, ) with the value included to indicate trends at more extreme values. Figure 2 shows that the two types of receptive fields essentially merge for large and increasingly diverge for small with as a nominal boundary between the two regimes. The same values will be used in the following subsection for nonsimple balanced Gabor receptive field functions for comparison.
The response of a simple balanced Gabor receptive field function to a sinusoidal grating pattern p is a special case of Eq. (40) and is given by
Similarly, the max-response function amplitude factor is a special case of Eq. (42) and is given by3 . Plots of vs. are given for the optimal orientation . These plots are essentially the same for all receptive field phases at and with maxima essentially at , but they show increasing dependence on the receptive field phase and increasing deviation of the optimal grating wavelength from the receptive field wavelength as decreases. This behavior is quite different from the bandlimited case, where the max-response is completely independent of (Subsection 5B).
For fixed grating wavelength , has a maximum at , that is, where the grating orientation matches the field orientation, due to the MRD property. Figure 3 also shows such plots of response versus grating orientation at optimal grating wavelengths. The increasing dependence of the response on the receptive field phase as decreases is again evident.
5A3. Example: a Class of Nonsimple Balanced Gabor Receptive Field Functions
We define general balanced Gabor weights of order 1 (with exponent ) as those weights given by
In the Hankel transform, notice that is the most general form of periodic function with a single harmonic term that satisfies the definition for a balanced Gabor weight, and it can be shown that the bound on is a necessary and sufficient condition to satisfy parts (a), (b), (c) of that definition (Appendix C ). Part (d) is vacuous for this case. The simple balanced Gabor occurs for and can be considered the “order 0” form. With the Hankel transform determined, the inverse transform follows by the explicit inversion formula (43).
In , notice the oscillatory component is the more slowly decaying component:
The balanced Gabor receptive field function (order 1) is the special case of Eq. (37) given by53). In the same way, the Fourier transform , the response function for sinusoidal grating patterns p, and the max-response amplitude factor are given by formulas combining Eq. (53) with the general formulas (38), (40), and (42), respectively.
The figures show examples of these nonsimple balanced Gabor receptive field functions and their behavior. There are two sets: Figures 4, 5, 6 have and Figs. 7, 8, 9 have . Each plot shows behavior for exponents and for cases of with the coefficient taking the value 0 (that is, the simple balanced Gabor case) and the two most extreme values permitted by the bound (55). Since this bound is small for small , the plots for essentially reduce to the simple balanced Gabor case. As increases, however, the bound also increases, and substantial differences from the simple balanced Gabor are evident at . Specifically, Figs. 4, 7 show the Hankel transforms and weight functions for these parameter values. Notice that the weight functions can become negative, in contrast to the simple balanced Gabor, where the weights are strictly positive. Figures 5, 8 show the corresponding receptive field functions (with the weight functions as envelopes) and Fourier transforms for the receptive field functions (cosine-type receptive fields). Figures 6, 9 show plots of versus at the optimal grating orientation . The optimal grating wavelength is quite different from the receptive field wavelength for small but begins to match it as increases. At the same time, the variation in these curves increases with . That is, as bandwidth decreases and the simple balanced Gabor and traditional Gabor receptive fields become identical (see Fig. 2), the nonsimple balanced Gabor weights and receptive fields show a widening range of behavior. The same figures show plots of versus at optimal wavelengths . The maximum response occurs at , that is, when the grating orientation matches the receptive field orientation, in agreement with the MRD property, and the variation in the response increases with .
5B. Bandlimited Receptive Field Functions: Discussion and Examples
This section defines and discusses the bandlimited class of weights and elementary receptive field functions mentioned in Section 4. A bandlimited class with explicit analytic solutions (Bessel receptive fields) is given as an example.
5B1. Bandlimited Weights and Receptive Fields
Bandlimited weights (with support ) are weight functions satisfying
(a) on ;
(b) is strictly decreasing on with .
All parameters and independent variables are dimensionless. For each bandlimited Hankel transform (and thus for the corresponding weight function), the support value is uniquely determined. The support values thus partition or classify both the transforms and the weights. Since the support is a measure of the width of the Hankel transform and thus of the Fourier transform for the receptive field (see below), it corresponds to a measure of the bandwidth of the bandlimited receptive field function. For bandlimited weights , is necessarily positive [because Eq. (14) reduces to a positive integrand for ]. In contrast to balanced Gabor weights, no explicit analytic structure occurs naturally for bandlimited weights, and no analog for “simple” balanced Gabor weights occurs.
A closure result can be stated for the bandlimited case and takes a simpler form than for the balanced Gabor case:
- The set of bandlimited Hankel transforms and the corresponding set of bandlimited weights for a fixed support value are closed under convex combinations.
- The set of all bandlimited Hankel transforms and the corresponding set of all bandlimited weights are closed under convex combinations.
Both parts follow by a straightforward check of the conditions of the bandlimited definition when applied to convex combinations.
If is a bandlimited weight function with support , it follows directly from the definition that, for an arbitrary c, , the function is a bandlimited weight with support and Hankel transform . That is, scaling maps bandlimited weights with a given support value to weights with other support values. In particular, the equivalence class of weights for a given support value is a scaled copy of any other equivalence class.
A bandlimited receptive field function is an elementary receptive field function where the receptive field weight is a bandlimited function; that is, has been replaced by ,
The support value determines the corresponding sector of ZRDs (possibly reducing to a single line) by . The sector is centered on and is bounded by ; that is, the ZRD sector consists of .
The Fourier transform of a bandlimited receptive field function reduces to
The response of a bandlimited receptive field function to a sinusoidal grating pattern p is given by (assuming )
The max-response of a bandlimited receptive field function to a sinusoidal grating pattern is given by
The simplicity of the formula for provides several results:
- The maximum of the max-response amplitude factor is and occurs for exactly one pair of values, .
- The response function is independent of the receptive field phase .
- If the grating wavelength is fixed, then , where , is required for a nonzero response. A nonzero response occurs only for orientations in the range
The synthesis/analysis formulas for the Hankel transform and the fact that vanishes outside the interval with for the bandlimited class give a general formula for the weights:
5B2. Example: Bessel Receptive Field Functions
An example of the explicit inversion (65) is the following Hankel transform and inverse transform. These functions satisfy the conditions for a bandlimited weight function with support parameter : for ,27]. The function satisfies as , and the condition ensures the absolute integrability of as well as continuity of the Hankel transform.
Scaling gives weight functions with arbitrary support :
This set of scaled functions will be called Bessel weights of order , referring to the order of the corresponding Bessel function. The support parameter determines an equivalence class of weights.
The Bessel receptive field functions are the elementary receptive field functions given by
Formulas and properties for the Fourier transform, response function, and max-response for Bessel receptive fields carry over directly from the general discussion. We note a couple of simplifications. The response function for a sinusoidal grating pattern p reduces to (assuming )
Figures 10, 11, 12 show examples of Bessel receptive field functions and their behavior. Each plot shows curves for orders . Each figure shows plots for support values , corresponding to scaled versions of each other. Figure 10 shows Hankel transforms and corresponding weight functions. Figure 11 shows Fourier transforms and corresponding receptive field functions. Since the balance parameter for the bandlimited case, the receptive field curves always match up with their envelopes and the nodes always match exactly with the zeros of the periodic carrier. Figure 12 shows amplitude factors at optimal orientations and optimal wavelengths . Notice, in contrast to the balanced Gabor case, the max-response is independent of the receptive field phase .
First, we suggest three properties as theoretical postulates for simple-cell receptive fields (Section 2). Experimental studies have established that simple cells show three well-defined properties, formulated here as the balanced field property (spatially homogeneous patterns produce a zero response); the zero response direction (ZRD) property (there is a direction, i.e., stimulus orientation, which elicits a zero response to sinusoidal gratings); and the maximum response direction (MRD) property (the maximum response to sinusoidal gratings decreases monotonically to zero as direction, i.e., stimulus orientation, changes from the optimal direction to a direction perpendicular to the optimal). These properties are directly motivated by well-established experimentally observed behavior [1, 2, 4, 17]. Our analysis complements that of Olshausen and Field [28, 29], who numerically derived spatial structures for linear V1 neurons from natural scenes coupled with a sparse coding constraint. Since our analysis is based on responses to sinusoidal grating stimuli, these properties can be restated in terms of the Fourier transform of the simple cell receptive field function. For the Fourier transform of the receptive field function , the properties are
- Balanced field property: .
- ZRD Property: There exists a direction such that for all real s.
- MRD Property: There exists a direction such that, for each fixed s, either is zero for all α or strictly decreases to zero (and remains zero) as increases.
Second, we demonstrate that these properties can serve as a productive basis for theoretical development. A simple role for such postulates is to provide definite criteria that any proposed receptive field model should satisfy, where such models either should satisfy the criteria or, if not, should possess compensating advantage(s). For example, the traditional Gabor filter is not balanced, but the imbalance is negligible over a certain parameter range, and the filter provides a useful explicit approximation to observed receptive field functions within that range. A deeper role is to provide a catalyst. We have demonstrated such a role by using the properties to completely characterize elementary receptive field functions, that is, to characterize the weight functions q defining such receptive fields for cosine-type and mixed-type receptive fields (Sections 3, 4). This derivation began by obtaining a description of receptive field functions with the ZRD property (Appendix A ), then refining that description to obtain receptive field functions with the MRD property (Appendix B ). The usefulness of this stepwise approach motivates the above formulation of three cumulative properties.
This characterization yields two disjoint classes of elementary receptive field functions, the balanced Gabor class (Subsection 5A) and the bandlimited class (Subsection 5B). The balanced Gabor class appears to be an essentially new class of receptive field models, although its most basic case, the simple balanced Gabor receptive field function, is a straightforward modification of the traditional Gabor filter. Bandlimited models for receptive fields have been proposed , and the bandlimited class derived here is an unexpected connection with that literature. One difference between the classes is that the balanced Gabor class has a unique ZRD (orthogonal to the MRD), while the bandlimited class can have a sector of zero response directions/orientations (centered on an orientation orthogonal to the maximum response orientation, but possibly reducing to a single orientation). Another difference is that the Hankel transform of the weight function q is strictly positive for the balanced Gabor class (although it decays exponentially fast owing to a characteristic Gaussian factor), while for the bandlimited case is nonnegative and is always zero outside some bounded region (i.e., has compact support).
Third, we provide explicit examples and short studies of these two classes of elementary receptive field functions (Subsections 5A, 5B). It should be noticed that the balanced Gabor class has a partially determined analytic structure [the Hankel transform of the weight function is the product of a gaussian and a periodic function]; while equally well defined, the bandlimited class does not imply a comparable analytic form for the Hankel transform.
With regard to further work, the fact that a set of three experimentally based properties leads to two disjoint classes of elementary receptive field functions raises the obvious question of which class better describes the simple cell receptive field. Consequently, the most immediate question raised by this paper is whether experimental study might lead to a decision between these two classes. In addition, there are natural directions for generalizing both the results obtained here and the approach. We set these out under the following suggestions.
Experimental diagnostics for receptive field functions. The two classes of receptive field functions resulting from our analysis necessarily exhibit similar behavior since they both satisfy the three imposed experimentally based response properties to sinusoidal grating stimuli. Not surprisingly, therefore, identifying diagnostic differences in the responses of the two classes of elementary receptive field functions that are both experimentally detectable and empirically conclusive may prove challenging. The construction of explicit examples of receptive field functions of both types, based on the selection of receptive field parameter values that result in physiologically plausible behavior, has suggested some differences which may have experimental significance. We list some of these differences by way of example but note that further study is required:
(a) Bandlimited receptive field functions can have a sector of ZRDs, whereas balanced Gabor receptive fields always possess a unique ZRD. While a narrow range of ZRDs (orientations) may be experimentally indistinguishable from a single ZRD, a broad range of grating orientations yielding zero response points to bandlimited receptive field structure.
(b) Bandlimited receptive field functions have max-response (i.e., tuning) functions with respect to both spatial frequency and orientation that are completely independent of the receptive field phase shift . By contrast, balanced Gabor max-response functions depend on receptive field phase, and max-response values for sine-type receptive field functions are always larger than those for cosine-type receptive field functions. In addition, initial numerical calculations suggest that, for balanced Gabor types, cosine phase receptive field functions are more narrowly tuned for both spatial frequency and orientation than are mixed or sine phase receptive fields (see Figs. 3, 6, 9). Population level surveys of simple cell behavior might be diagnostic if, as a group, simple cell max-responses, orientation, or spatial frequency tuning were found to systematically vary with receptive field phase, since this would contraindicate the bandlimited class of receptive field model for which these response properties are invariant with receptive field phase.
(c) The weight function, q, of the simple balanced Gabor receptive field function is always nonnegative, whereas the weight functions of nonsimple balanced Gabor and bandlimited types may assume negative values. When the weight function changes sign, the phase of the periodic carrier function undergoes an abrupt reversal. Such abrupt carrier phase reversals may be of diagnostic value since discovering simple cells with such receptive field structure would disqualify the simple balanced Gabor receptive field type.
Theoretical diagnostics for evaluating receptive field functions. There may be theoretical grounds, such as minimal energy or other optimality arguments, for preferring one class of elementary receptive field function over the other. We have not extended our analysis to include such considerations, but this may be a fruitful direction for further study.
Further developments of the present analysis. The present analysis has assumed that the weight function, q, of the elementary receptive field function is circularly symmetric and satisfies the regularity conditions described in Eq. (12), in particular that (i.e., that the weight function possesses unit volume), which in turn implies that the Hankel transform satisfies . This is a broad normalization condition since a simple scaling of the weight function can transform any nonzero weight integral to unit value. Several questions regarding further generalizations naturally arise:
(a) What receptive field structures might satisfy the balanced field, ZRD, and MRD constraints if our assumed regularity condition is modified to be the singular condition , in which case the weight function itself must integrate to zero? If valid receptive field functions result, that is, if nontrivial weight functions, q, are discovered that satisfy the constraints imposed by the three postulated response properties, then they would necessarily form a new class of receptive field structures distinct from the two classes described in this paper, since no scaling of independent or dependent variables can convert the singular to the regular condition.
(b) What are the implications for our analysis of receptive field functions if the condition of a circularly symmetric weight function, q, is relaxed to allow for elliptically symmetric weights? Both psychophysical [19, 30, 31] (but see  and physiological observations [17, 32]) indicate that simple cell receptive fields with elliptically symmetric weight functions may commonly occur. This suggests that extending the current analysis to include such receptive field variations would be profitable. This extension of our analysis is, however, beyond the scope of the present paper.
(c) We have defined elementary receptive field functions in Eq. (11) to be the product of a circularly symmetric weight and a simple periodic carrier. The simple periodic carrier corresponds to the first two terms of a Fourier series expansion. Can receptive field functions with a general periodic carrier be characterized? That is, can nonelementary receptive field functions that satisfy our postulated response behaviors be characterized, where the functions have the following form, and is an arbitrary 1-periodic function?
(d) Our approach has been to deduce the mathematical implications of three simple, but generally accepted, properties of the response of simple cells to sinusoidal gratings. Our analysis relies, in part, on the fact that statements about such responses convert directly to statements about the Fourier transform of elementary receptive field functions and on the leverage afforded by the intersection of constraints imposed by these three response properties. It is therefore of interest to ask whether there might be additional properties of simple cells, well defined but perhaps less widely recognized (and not necessarily restricted to sinusoidal grating stimuli) that could be incorporated to supplement the three postulated properties. It should be kept in mind that such properties might be considered of minor or secondary importance from the viewpoint of experimental significance yet might have unexpected power in mathematical terms. For example, the ZRD property might easily be regarded as of secondary importance in comparison with the MRD property, yet studying the implications of the existence of a ZRD provided important initial results for this work. The incorporation of such an additional response property to the present analysis would quite probably determine which class of elementary receptive field function best describes simple cell receptive fields.
Classical versus extraclassical receptive fields. A final caveat is that our analysis is motivated by considering the response properties of the so-called classical receptive field of V1 neurons, which typically demonstrate the balanced field property. A large body of literature suggests that V1 neurons also possess “extraclassical” receptive fields [33, 34], and a sizable proportion of V1 neurons respond to homogeneous luminance modulations if these stimuli extend into the extraclassical region, which may subtend many degrees of visual angle beyond the classical receptive field [35, 36, 37, 38, 39, 40, 41, 42, 43].
This work was supported by grants R01EY014015 from the National Eye Institute (NEI) and NIH P20 RR020151 from the National Center for Research Resources (NCRR). The NEI and the NCRR are components of the National Institutes of Health (NIH). The contents of this report are solely the responsibility of the authors and do not necessarily reflect the official views of the NIH, NCRR, or NEI. Commercial relationships: none.
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