Local sensitivity to stimulus orientation and spatial frequency within the receptive fields of neurons in visual area 2 of macaque monkeys.

We used dynamic dense noise stimuli and local spectral reverse correlation methods to reveal the local sensitivities of neurons in visual area 2 (V2) of macaque monkeys to orientation and spatial frequency within their receptive fields. This minimized the potentially confounding assumptions that are inherent in stimulus selections. The majority of neurons exhibited a relatively high degree of homogeneity for the preferred orientations and spatial frequencies in the spatial matrix of facilitatory subfields. However, about 20% of all neurons showed maximum orientation differences between neighboring subfields that were greater than 25 deg. The neurons preferring horizontal or vertical orientations showed less inhomogeneity in space than the neurons preferring oblique orientations. Over 50% of all units also exhibited suppressive profiles, and those were more heterogeneous than facilitatory profiles. The preferred orientation and spatial frequency of suppressive profiles differed substantially from those of facilitatory profiles, and the neurons with suppressive subfields had greater orientation selectivity than those without suppressive subfields. The peak suppression occurred with longer delays than the peak facilitation. These results suggest that the receptive field profiles of the majority of V2 neurons reflect the orderly convergence of V1 inputs over space, but that a subset of V2 neurons exhibit more complex response profiles having both suppressive and facilitatory subfields. These V2 neurons with heterogeneous subfield profiles could play an important role in the initial processing of complex stimulus features.

Activation of projective neurons from the nucleus accumbens to ventral pallidum by a learned aversive taste stimulus in rats: a manganese-enhanced magnetic resonance imaging study.

Conditioned taste aversion (CTA) causes a palatability shift of a taste stimulus (conditioned stimulus, CS) from ingestive to aversive. We previously found that the ventral pallidum (VP) mediates the palatability shift in CTA. Because the VP receives major projections from the nucleus accumbens (NAc), we examined whether the presentation of CS activates the NAc-VP projective neurons after the establishment of CTA, using a manganese-enhanced magnetic resonance imaging technique. Rats were implanted with a guide cannula in the NAc and an intraoral cannula. After the surgery, they received a pairing of 5 mM saccharin solution with an i.p. injection of 0.15 M lithium chloride (CTA group) or saline (sham group). Two days after the conditioning, rats were microinjected with manganese chloride (MnCl2) into the NAc. Thirty minutes later, the rats were presented with saccharin (CTA-CS and sham-CS groups) or water (CTA-DW and sham-DW groups) via the intraoral cannula. Only the CTA-CS group showed a robust aversion to the CS. At 1 and 2 h after the MnCl2 injection, T1-weighted MR images were acquired using an 11.7 T MRI. Imaging analysis showed that significantly more manganese moved toward the VP in the CTA-CS group than in the other groups. These results indicate that the conditioned aversive taste enhanced the activities of the projective NAc-VP neurons and suggest specific involvement of the NAc-VP pathway in the rejection of CS in retrieval of CTA.

The brain mapping of the retrieval of conditioned taste aversion memory using manganese-enhanced magnetic resonance imaging in rats.

Manganese-enhanced MRI (MEMRI) is a newly developed noninvasive imaging technique of brain activities. The signal intensity of MEMRI reflects cumulative activities of the neurons. To validate the use of MEMRI technique to investigate the neural mechanisms of learning and memory, we tried to map brain areas involved in the retrieval of conditioned taste aversion (CTA) memory. CTAs were established to saccharin (conditioned stimulus: CS) by pairing its ingestion with an i.p. injection of LiCl (unconditioned stimulus: US). LiCl solutions (as a robust aversion chemical) of 0.15 M were injected i.p. 15 min after drinking the saccharine solution (CS). After the two times conditionings, these rats showed a robust aversion to the saccharine solution (CS). Rats of the control group were injected saline i.p. instead of LiCl solutions. The MRI signal intensities at the gustatory cortex (GC), the core subregion of the nucleus accumbens (NAcC), the shell subregion of the nucleus accumbens (NAcSh), the ventral pallidum (VP), the central nucleus of amygdala (CeA), the lateral hypothalamus (LH), and the basolateral nucleus of amygdala (BLA) of the conditioned group were higher than those of the control group. There were no significant differences between the conditioned and the control groups in the intensities for other regions, such as the striatum area, motor cortex, cingulate cortex, interstitial nucleus of the posterior limb of the anterior commissure and hippocampus. These indicate that the GC, NAcC, NAcSh, VP, CeA, LH and BLA have important roles in the memory retrieval of CTA.

Beyond the classical receptive field in the visual cortex.

We have investigated the organization of regions outside the classical receptive field (CRF) for neurons in the visual cortex. First, we have determined the incidence and nature of interactions from outside the CRF. We find interaction from regions outside the CRF for a majority of cortical cells and it is almost always of a suppressive nature. Second, we have determined that most interaction is from specific well-defined regions outside the CRF. These regions are generally as effective as what is found for a complete annulus. Third, it is possible to reverse the inhibition from outside the CRF by the addition of a second grating that is orthogonal to the preferred orientation. This disinhibition may completely offset the suppressive influence of the surround. Additional experiments suggest that this process is not necessarily involved in figure/ground analysis.

Neural and perceptual adjustments to dim light.

At reduced luminance levels, the visual system integrates light over extended periods of time. Although the general effects of this process are known, specific changes in the visual cortex have not been identified. We have studied the physiological changes that occur during a transition from high to low luminance by measurements of single neurons in the cat's primary visual cortex. Under low-luminance conditions, we find increased latencies, expanded temporal responses, and a loss of temporal structure. This results in temporal-frequency tuning curves that are peaked at relatively low frequencies. To examine parallel perceptual changes, we compared perceived temporal frequency in human subjects under high- and low-luminance conditions. Low-luminance flickering patterns are perceived to modulate at relatively high rates. This occurs even though peak sensitivity is shifted to relatively low temporal frequencies. To explore further the perceptual component, we measured perceived temporal frequency in human subjects with unilateral optic neuritis for whom optic nerve transmission is known to be relatively slow and generally similar to the normal physiological state under low luminance. These subjects also perceive relatively high modulation rates through their affected eye. Considered together, these results demonstrate an inverse relationship between the physiological and the perceptual consequences of reduced stimulus luminance. This relationship may be accounted for by shifts of neuronal population responses between high- and low-luminance levels.

Joint-encoding of motion and depth by visual cortical neurons: neural basis of the Pulfrich effect.

Motion and stereoscopic depth are fundamental parameters of the structural analysis of visual scenes. Because they are defined by a difference in object position, either over time or across the eyes, a common neural machinery may be used for encoding these attributes. To examine this idea, we analyzed responses of binocular complex cells in the cat striate cortex to stimuli of various intra- and interocular spatial and temporal shifts. We found that most neurons exhibit space-time-oriented response profiles in both monocular and binocular domains. This indicates that these neurons encode motion and depth jointly, and it explains phenomena such as the Pulfrich effect. We also found that the relationship between neuronal tuning of motion and depth conforms to that predicted by the use of motion parallax as a depth cue. These results demonstrate a joint-encoding of motion and depth at an early cortical stage.

Suppression outside the classical cortical receptive field.

The important visual stimulus parameters for a given cell are defined by the classical receptive field (CRF). However, cells are also influenced by visual stimuli presented in areas surrounding the CRF. The experiments described here were conducted to determine the incidence and nature of CRF surround influences in the primary visual cortex. From extracellular recordings in the cat's striate cortex, we find that for over half of the cells investigated (56%, 153/271), the effect of stimulation in the surround of the CRF is to suppress the neuron's activity by at least 10% compared to the response to a grating presented within the CRF alone. For the remainder of the cells, the interactions were minimal and a few were of a facilitatory nature. In this paper, we focus on the suppressive interactions. Simple and complex cell types exhibit equal incidences of surround suppression. Suppression is observed for cells in all layers, and its degree is strongly correlated between the two eyes for binocular neurons. These results show that surround suppression is a prevalent form of inhibition and may play an important role in visual processing.

Contrast gain control in the visual cortex: monocular versus binocular mechanisms.

In this study, we compare binocular and monocular mechanisms underlying contrast encoding by binocular simple cells in primary visual cortex. At mid to high levels of stimulus contrast, contrast gain of cortical neurons typically decreases as stimulus contrast is increased (). We have devised a technique by which it is possible to determine the relative contributions of monocular and binocular processes to such reductions in contrast gain. First, we model the simple cell as an adjustable linear mechanism with a static output nonlinearity. For binocular cells, the linear mechanism is sensitive to inputs from both eyes. To constrain the parameters of the model, we record from binocular simple cells in striate cortex. To activate each cell, drifting sinusoidal gratings are presented dichoptically at various relative interocular phases. Stimulus contrast for one eye is varied over a large range whereas that for the other eye is fixed. We then determine the best-fitting parameters of the model for each cell for all of the interocular contrast ratios. This allows us to determine the effect of contrast on the contrast gain of the system. Finally, we decompose the contrast gain into monocular and binocular components. Using the data to constrain the model for a fixed contrast in one eye and increased contrasts in the other eye, we find steep reductions in monocular gain, whereas binocular gain exhibits modest and variable changes. These findings demonstrate that contrast gain reductions occur primarily at a monocular site, before convergence of information from the two eyes.

Linear and nonlinear contributions to orientation tuning of simple cells in the cat's striate cortex.

Orientation selectivity is one of the most conspicuous receptive-field (RF) properties that distinguishes neurons in the striate cortex from those in the lateral geniculate nucleus (LGN). It has been suggested that orientation selectivity arises from an elongated array of feedforward LGN inputs (Hubel & Wiesel, 1962). Others have argued that cortical mechanisms underlie orientation selectivity (e.g. Sillito, 1975; Somers et al., 1995). However, isolation of each mechanism is experimentally difficult and no single study has analyzed both processes simultaneously to address their relative roles. An alternative approach, which we have employed in this study, is to examine the relative contributions of linear and nonlinear mechanisms in sharpening orientation tuning. Since the input stage of simple cells is remarkably linear, the nonlinear contribution can be attributed solely to cortical factors. Therefore, if the nonlinear component is substantial compared to the linear contribution, it can be concluded that cortical factors play a prominent role in sharpening orientation tuning. To obtain the linear contribution, we first measure RF profiles of simple cells in the cat's striate cortex using a binary m-sequence noise stimulus. Then, based on linear spatial summation of the RF profile, we obtain a predicted orientation-tuning curve, which represents the linear contribution. The nonlinear contribution is estimated as the difference between the predicted tuning curve and that measured with drifting sinusoidal gratings. We find that measured tuning curves are generally more sharply tuned for orientation than predicted curves, which indicates that the linear mechanism is not enough to account for the sharpness of orientation-tuning. Therefore, cortical factors must play an important role in sharpening orientation tuning of simple cells. We also examine the relationship of RF shape (subregion aspect ratio) and size (subregion length and width) to orientation-tuning halfwidth. As expected, predicted tuning halfwidths are found to depend strongly on both subregion length and subregion aspect ratio. However, we find that measured tuning halfwidths show only a weak correlation with subregion aspect ratio, and no significant correlation with RF length and width. These results suggest that cortical mechanisms not only serve to sharpen orientation tuning, but also serve to make orientation tuning less dependent on the size and shape of the RF. This ensures that orientation is represented equally well regardless of RF size and shape.

Asymmetric suppression outside the classical receptive field of the visual cortex.

Areas beyond the classical receptive field (CRF) can modulate responses of the majority of cells in the primary visual cortex of the cat (). Although general characteristics of this phenomenon have been reported previously, little is known about the detailed spatial organization of the surrounds. Previous work suggests that the surrounds may be uniform regions that encircle the CRF or may be limited to the "ends" of the CRF. We have examined the spatial organization of surrounds of single-cell receptive fields in the primary visual cortex of anesthetized, paralyzed cats. The CRF was stimulated with an optimal drifting grating, whereas the surround was probed with a second small grating patch placed at discrete locations around the CRF. For most cells that exhibit suppression, the surrounds are spatially asymmetric, such that the suppression originates from a localized region. We find a variety of suppressive zone locations, but there is a slight bias for suppression to occur at the end zones of the CRF. The spatial pattern of suppression is independent of the parameters of the suppressive stimulus used, although the effect is clearest with iso-oriented surround stimuli. A subset of cells exhibit axially symmetric or uniform surround fields. These results demonstrate that the surrounds are more specific than previously realized, and this specialization has implications for the processing of visual information in the primary visual cortex. One possibility is that these localized surrounds may provide a substrate for figure-ground segmentation of visual scenes.

Neural mechanisms for processing binocular information II. Complex cells.

Complex cells in the striate cortex exhibit extensive spatiotemporal nonlinearities, presumably due to a convergence of various subunits. Because these subunits essentially determine many aspects of a complex cell receptive field (RF), such as tuning for orientation, spatial frequency, and binocular disparity, examination of the RF properties of subunits is important for understanding functional roles of complex cells. Although monocular aspects of these subunits have been studied, little is known about their binocular properties. Using a sophisticated RF mapping technique that employs binary m-sequences, we have examined binocular interactions exhibited by complex cells in the cat's striate cortex and the binocular RF properties of their underlying functional subunits. We find that binocular interaction RFs of complex cells exhibit subregions that are elongated along the frontoparallel axis at different binocular disparities. Therefore responses of complex cells are largely independent of monocular stimulus position or phase as long as the binocular disparity of the stimulus is kept constant. The binocular interaction RF is well described by a sum of binocular interaction RFs of underlying functional subunits, which exhibit simple cell-like RFs and a preference for different monocular phases but the same binocular disparity. For more than half of the complex cells examined, subunits of each cell are consistent with the characteristics specified by an energy model, with respect to the number of subunits as well as relationships between the subunit properties. Subunits exhibit RF binocular disparities that are largely consistent with a phase mechanism for encoding binocular disparity. These results indicate that binocular interactions of complex cells are derived from simple cell-like subunits, which exhibit multiplicative binocular interactions. Therefore binocular interactions of complex cells are also multiplicative. This suggests that complex cells compute something analogous to an interocular cross-correlation of images for a local region of visual space. The result of this computation can be used for solving the stereo correspondence problem.

Neural mechanisms for processing binocular information I. Simple cells.

The visual system integrates information from the left and right eyes and constructs a visual world that is perceived as single and three dimensional. To understand neural mechanisms underlying this process, it is important to learn about how signals from the two eyes interact at the level of single neurons. Using a sophisticated receptive field (RF) mapping technique that employs binary m-sequences, we have determined the rules of binocular interactions exhibited by simple cells in the cat's striate cortex in relation to the structure of their monocular RFs. We find that binocular interaction RFs of most simple cells are well described as the product of left and right eye RFs. Therefore the binocular interactions depend not only on binocular disparity but also on monocular stimulus position or phase. The binocular interaction RF is consistent with that predicted by a model of a linear binocular filter followed by a static nonlinearity. The static nonlinearity is shown to have a shape of a half-power function with an average exponent of approximately 2. Although the initial binocular convergence of signals is linear, the static nonlinearity makes binocular interaction multiplicative at the output of simple cells. This multiplicative binocular interaction is a key ingredient for the computation of interocular cross-correlation, an algorithm for solving the stereo correspondence problem. Therefore simple cells may perform initial computations necessary to solve this problem.

Neural mechanisms for encoding binocular disparity: receptive field position versus phase.

The visual system uses binocular disparity to discriminate the relative depth of objects in space. Because the striate cortex is the first site along the central visual pathways at which signals from the left and right eyes converge onto a single neuron, encoding of binocular disparity is thought to begin in this region. There are two possible mechanisms for encoding binocular disparity through simple cells in the striate cortex: a difference in receptive field (RF) position between the two eyes (RF position disparity) and a difference in RF profiles between the two eyes (RF phase disparity). Although there is evidence that supports each of these schemes, both mechanisms have not been examined in a single study to determine their relative roles. In this study, we have measured RF position and phase disparities of individual simple cells in the cat's striate cortex to address this issue. Using a sophisticated RF mapping technique that employs binary m-sequences, we have obtained left and right eye RF profiles of two or more cells recorded simultaneously. A version of the reference-cell method was used to estimate RF position disparity. We find that RF position disparities generally are limited to values that are not sufficient to encode large binocular disparities. In contrast, RF phase disparities cover a wide range of binocular disparities and exhibit dependencies on RF orientation and spatial frequency in a manner expected for a mechanism that encodes binocular disparity. These results suggest that binocular disparity is encoded mainly through RF phase disparity. However, RF position disparity may play a significant role for cells with high spatial frequency selectivity that are constrained to have only small RF phase disparities.

Functional micro-organization of primary visual cortex: receptive field analysis of nearby neurons.

It is well established that multiple stimulus dimensions (e.g., orientation and spatial frequency) are mapped onto the surface of striate cortex. However, the detailed organization of neurons within a local region of striate cortex remains unclear. Within a vertical column, do all neurons have the same response selectivities? And if not, how do they most commonly differ and why? To address these questions, we recorded from nearby pairs of simple cells and made detailed spatiotemporal maps of their receptive fields. From these maps, we extracted and analyzed a variety of response metrics. Our results provide new insights into the local organization of striate cortex. First, we show that nearby neurons seldom have very similar receptive fields, when these fields are characterized in space and time. Thus, there may be less redundancy within a column than previously thought. Moreover, we show that correlated discharge increases with receptive field similarity; thus, the local dissimilarity between neurons may allow for noise reduction by response pooling. Second, we show that several response variables are clustered within striate cortex, including some that have not received much attention such as response latency and temporal frequency. We also demonstrate that other parameters are not clustered, including the spatial phase (or symmetry) of the receptive field. Third, we show that spatial phase is the single parameter that accounts for most of the difference between receptive fields of nearby neurons. We consider the implications of this local diversity of spatial phase for population coding and construction of higher-order receptive fields.

Mechanisms of stereoscopic vision: the disparity energy model.

The past year has seen significant advances in our understanding of the role played by the primary visual cortex (V1) in stereoscopic vision. Recently, the mechanism by which complex cells in V1 respond to random-dot stereograms has been characterized; it appears that their response properties greatly reduce the complexity of one of the critical links for stereopsis, the correspondence problem.

Binocular cross-orientation suppression in the cat's striate cortex.

When a cortical cell is activated by an optimal sinusoidal grating, its response can be attenuated by a superimposed second grating oriented orthogonally to the optimal stimulus. This effect is known as cross-orientation suppression (COS). In previous work, monocular characteristics have been explored and interocular tests have been conducted in an attempt to locate the origin of the suppression. In this study, we have recorded extracellularly from cortical cells to investigate the binocular characteristics of COS. Our hypothesis is that binocular disparity influences the strength of the effect. Our results do not support this supposition. We find that binocular COS is as strong as monocular COS, but disparity changes are of no consequence. We also conducted interocular tests in which the optimal grating and the orthogonal mask were seen by separate eyes. Although most interocular effects were weak, they were present in almost every cell and spanned a wide range of suppression strengths. We also tested the effect of asynchronous presentation of optimal and orthogonal gratings. These temporal offsets did not affect the strength of COS. We conclude that the suppressive mechanism underlying COS is primarily monocular and acts prior to the convergence of the two monocular streams.

Encoding of binocular disparity by complex cells in the cat's visual cortex.

To examine the roles that complex cells play in stereopsis, we have recorded extracellularly from isolated single neurons in the striate cortex of anesthetized paralyzed cats. We measured binocular responses of complex cells using a comprehensive stimulus set that encompasses all possible combinations of positions over the receptive fields for the two eyes. For a given position combination, stimulus contrast could be the same for the two eyes (2 bright or 2 dark bars) or opposite (1 bright and 1 dark). These measurements provide a binocular receptive field (RF) profile that completely characterizes complex cell responses in a joint domain of left and right stimulus positions. Complex cells typically exhibit a strong selectivity for binocular disparity, but are only broadly selective for stimulus position. For most cells, selectivity for disparity is more than twice as narrow as that for position. These characteristics are highly desirable if we assume that a disparity sensor should exhibit position invariance while encoding small changes in stimulus depth. Complex cells have nearly identical binocular RFs for bright and dark stimuli as long as the sign of stimulus contrast is the same for the two eyes. When stimulus contrast is opposite, the binocular RF also is inverted such that excitatory subregions become suppressive. We have developed a disparity energy model that accounts for the behavior of disparity-sensitive complex cells. This is a hierarchical model that incorporates specific constraints on the selection of simple cells from which a complex cell receives input. Experimental data are used to examine quantitatively predictions of the model. Responses of complex cells generally agree well with predictions of the disparity energy model. However, various types of deviations from the predictions also are found, including a highly elongated excitatory region beyond that supported by a single energy mechanism. Complex cells in the visual cortex appear to provide a next level of abstraction in encoding information for stereopsis based on the activity of a group of simple-type subunits. In addition to exhibiting narrow disparity tuning and position invariance, these cells seem to provide a partial solution to the stereo correspondence problem that arises in complex natural scenes. Based on their binocular response properties, these cells provide a substantial reduction in the complexity of the correspondence problem.

Neural mechanisms underlying binocular fusion and stereopsis: position vs. phase.

The visual system utilizes binocular disparity to discriminate the relative depth of objects in space. Since the striate cortex is the first site along the central visual pathways at which signals from the left and right eyes converge onto a single neuron, encoding of binocular disparity is thought to begin in this region. There are two possible mechanisms for encoding binocular disparity through simple cells in the striate cortex: a difference in receptive field (RF) position between the two eyes (RF position disparity) and a difference in RF profile between the two eyes (RF phase disparity). Although there have been studies supporting each of the two encoding mechanisms, both mechanisms have not been examined in a single study. Therefore, the relative roles of the two mechanisms have not been determined. To address this issue, we have mapped left and right eye RFs of simple cells in the cat's striate cortex using binary m-sequence noise, and then we have estimated RF position and phase disparities. We find that RF position disparities are generally limited to small values that are not sufficient to encode large binocular disparities. In contrast, RF phase disparities cover a wide range of binocular disparities and exhibit dependencies on orientation and spatial frequency in a manner expected for a mechanism that encodes binocular disparity. These results indicate that binocular disparity is mainly encoded through RF phase disparity. However, RF position disparity may play a significant role for cells with high spatial frequency selectivity, which are constrained to small RF phase disparities.

The neural coding of stereoscopic depth.

Stereopsis is a process by which the visual system gauges the relative depth of objects in three-dimensional space by measuring minute positional differences between left and right images. According to the standard notion, this information is thought to be encoded in the primary visual cortex by differences in receptive field (RF) positions for the two eyes. We have developed in alternative model by which stereoscopic information is coded and transformed through a hierarchical chain of processing in the primary visual cortex. Initially, first-order neurons of the visual cortex, simple cells, encode depth information by a scheme based on differences in internal receptive field structure between left and right eyes. Further abstraction of information is achieved by a subset of second-order neurons, complex cells, that are well suited for the detection of depth information in a manner unaffected by positional variations of objects. We review physiological evidence from studies of the cat and monkey that are relevant to the proposed scheme.