Receptive Field Properties Of Cells Research Articles

A synaptic signature for ON- and OFF-center parasol ganglion cells of the primate retina.

In the primate retina, parasol ganglion cells contribute to the primary visual pathway via the magnocellular division of the lateral geniculate nucleus, display ON and OFF concentric receptive field structure, nonlinear spatial summation, and high achromatic temporal-contrast sensitivity. Parasol cells may be homologous to the alpha-Y cells of nonprimate mammals where evidence suggests that N-methyl-D-aspartate (NMDA) receptor-mediated synaptic excitation as well as glycinergic disinhibition play critical roles in contrast sensitivity, acting asymmetrically in OFF- but not ON-pathways. Here, light-evoked synaptic currents were recorded in the macaque monkey retina in vitro to examine the circuitry underlying parasol cell receptive field properties. Synaptic excitation in both ON and OFF types was mediated by NMDA as well as α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/kainate glutamate receptors. The NMDA-mediated current-voltage relationship suggested high Mg2+ affinity such that at physiological potentials, NMDA receptors contributed ∼20% of the total excitatory conductance evoked by moderate stimulus contrasts and temporal frequencies. Postsynaptic inhibition in both ON and OFF cells was dominated by a large glycinergic "crossover" conductance, with a relatively small contribution from GABAergic feedforward inhibition. However, crossover inhibition was largely rectified, greatly diminished at low stimulus contrasts, and did not contribute, via disinhibition, to contrast sensitivity. In addition, attenuation of GABAergic and glycinergic synaptic inhibition left center-surround and Y-type receptive field structure and high temporal sensitivity fundamentally intact and clearly derived from modulation of excitatory bipolar cell output. Thus, the characteristic spatial and temporal-contrast sensitivity of the primate parasol cell arises presynaptically and is governed primarily by modulation of the large AMPA/kainate receptor-mediated excitatory conductance. Moreover, the negative feedback responsible for the receptive field surround must derive from a nonGABAergic mechanism.

Visual receptive field properties of cells in the optic tectum of the archer fish

The archer fish is well known for its extreme visual behavior in shooting water jets at prey hanging on vegetation above water. This fish is a promising model in the study of visual system function because it can be trained to respond to artificial targets and thus to provide valuable psychophysical data. Although much behavioral data have indeed been collected over the past two decades, little is known about the functional organization of the main visual area supporting this visual behavior, namely, the fish optic tectum. In this article we focus on a fundamental aspect of this functional organization and provide a detailed analysis of receptive field properties of cells in the archer fish optic tectum. Using extracellular measurements to record activities of single cells, we first measure their retinotectal mapping. We then determine their receptive field properties such as size, selectivity for stimulus direction and orientation, tuning for spatial frequency, and tuning for temporal frequency. Finally, on the basis of all these measurements, we demonstrate that optic tectum cells can be classified into three categories: orientation-tuned cells, direction-tuned cells, and direction-agnostic cells. Our results provide an essential basis for future investigations of information processing in the archer fish visual system.

Anterior-Posterior Direction Opponency in the Superficial Mouse Lateral Geniculate Nucleus

We show functional-anatomical organization of motion direction in mouse dorsal lateral geniculate nucleus (dLGN) using two-photon calcium imaging of dense populations in thalamus. Surprisingly, thesuperficial 75μm region contains anterior and posterior direction-selective neurons (DSLGNs) intermingled with nondirection-selective neurons, while upward- and downward-selective neurons are nearlyabsent. Unexpectedly, the remaining neurons encode both anterior and posterior directions, forming horizontal motion-axis selectivity. A model of random wiring consistent with these results makes quantitative predictions about the connectivity of direction-selective retinal ganglion cell (DSRGC) inputs to the superficial dLGN. DSLGNs are more sharply tuned than DSRGCs. These results suggest that dLGN maintains and sharpens retinal direction selectivity and integrates opposing DSRGC subtypes in a functional-anatomical region, perhaps forming a feature representation for horizontal-axis motion, contrary to dLGN being a simple relay. Furthermore, they support recent conjecture that cortical direction and orientation selectivity emerge in part from a previously undescribed motion-selective retinogeniculate pathway.

GABA inactivation of visual area MT modifies the responsiveness and direction selectivity of V2 neurons in Cebus monkeys

We investigated the contribution of the projections from area MT to the receptive field properties of cells in visual area V2 in anesthetized and paralyzed Cebus apella monkeys. We recorded extracellular single-unit activity using tungsten microelectrodes in three monkeys before and after pressure injection of a 0.25-mol/l GABA solution. The visual stimulus consisted of a single bar moving in one of eight directions. In total, 72 V2 neurons were studied in 18 sessions of GABA injection into area MT. A group of 22 neurons was investigated over a shorter period of time ranging from 15 to 60 min, during which the activity did not return to baseline levels. The remaining 50 neurons were studied over a period of at least 2 h, and no statistical difference was observed in the neuronal response before and long after GABA inactivation. The effects on these 50 neurons consisted of an early (1-20 min) significant general decrease in excitability with changes in either orientation or direction selectivity. The differential decrease in excitability resulted in an intermediate improvement (20-40 min) of the signal-to-noise ratio for the stimulus-driven activity. The inactivation depended on the quantity of GABA injected into area MT and persisted for a period of 2 h. The GABA inactivation in area MT produced inhibition of most cells (72%) and a significant change of direction tuning in the majority (56%) of V2 neurons. Both increases and also decreases in the direction tuning of V2 neurons were observed. These feedback projections are capable of modulating not only the levels of spontaneous and driven activity of V2 neurons but also the V2 receptive field properties, such as direction selectivity.

The effects of aging on the strength of surround suppression of receptive field of V1 cells in monkeys

The surround suppression of the receptive field is important for basic visual information processing, such as orientation specificity. To date, the effects of aging on the strength of surround suppression are not clear. To address this issue, we carried out extracellular single-unit studies of the receptive field properties of cells in the primary visual cortex (area V1) in young and old rhesus ( Macaca mulatta) monkeys. When presented with the oriented central stimulus, we found that cells in old animals showed reduced orientation and direction selectivity compared with those in young animals. When presented with the oriented central stimulus together with the optimal surround stimulus, more selective cells {orientation bias (OB) ≥0.1; a bias of 0.1 is significant at the P<0.005 level} in animals of both ages showed reduced orientation selectivity compared with the experiment that presented only the oriented central stimulus. When presented with the optimal central stimulus together with the oriented surround stimulus, cells in old animals showed reduced orientation and direction selectivity compared with young animals. Moreover, broadly tuned cells (OB<0.1) in old animals exhibited significantly reduced suppression indices that quantified the strength of the surround suppression of the receptive field, when compared with those in young animals. These results suggest that aging may seriously affect the surround suppression of the receptive field of V1 cells. Thus, the decreased strength of surround suppression of the receptive field may be one possible reason for the decreased stimulus selectivity of V1 cells previously found in the senescent brain. This work will contribute to an understanding of the physiological mechanisms mediating surround suppression of the receptive field.

Origins of cortical layer V surround receptive fields in the rat barrel cortex.

Layer IV of the barrel cortex contains an anatomical map of the contralateral whisker pad, which serves as a useful reference in relating receptive field properties of cells to the cortical columns in which they reside. Recent studies have shown that the degree to which the surround receptive fields of layer IV cells are generated intracortically or subcortically depends on whether they lie in barrel or septal columns. To investigate whether this is true for layer V cells, we blocked intracortical activity in the barrel cortex by infusing muscimol from the cortical surface and measuring spike responses to sensory stimulation in the presence of locally iontophoresed bicuculline. Layer V cells beneath barrels had small subcortically generated single- or double-whisker center receptive fields and larger intracortically generated six to seven whisker surround receptive fields. Conversely, septally located cells received multiwhisker input from both subcortical and cortical sources. Most properties of layer Va and layer Vb cells were very similar. However, layer Vb barrel neurons showed a relative lack of phasic inhibition evoked from sensory input compared with layer Va cells. The direct thalamic input to the layer V cells was not sufficient to evoke a sensory response in the absence of input from superficial layers. These findings suggest that despite the apparent overt similarity of layer V receptive fields, barrel and septal subdivisions process different sources of information within the barrel cortex.

Spatio-temporal receptive field properties of cells in the rat superior colliculus

Although the rat is widely used in neurobehavioural research, the spatio-temporal receptive field properties of neurons in superficial layers of the superior colliculus are relatively unknown. Extracellular recordings were carried out in anesthetized Long Evans rats. Neurons in these layers had simple-like and complex-like receptive fields (RFs). Most cells (67%) had RFs showing band-pass and low-pass spatial frequency (SF) tuning profiles. Spatial band-pass profiles showed low optimal SF (mean = 0.03 c/deg), low spatial resolution (mean = 0.18 c/deg) and large spatial bandwidths (mean = 2.3 octaves). More than two-thirds of the RFs (71%) were selective to orientation and only 11% were clearly direction selective. Nearly two-thirds of cells (68%) had band-pass temporal frequency (TF) tuning profiles with narrow bandwidths (mean = 1.7 oct.) whereas the others showed low-pass TF tuning profiles. Temporal band-pass profiles had low optimal TFs (mean = 3.5 c/s). Although some cells showed relatively low contrast thresholds (6%), most cells only responded to high contrast values (mean = 38.2%). These results show that the spatial resolution of collicular cells is poor and that they respond mainly to highly contrasted moving stimuli.

The Synaptic Mechanism of Direction Selectivity in Distal Processes of Starburst Amacrine Cells

Patch-clamp recordings revealed that distal processes of starburst amacrine cells (SACs) received largely excitatory synaptic input from the receptive field center and nearly purely inhibitory inputs from the surround during both stationary and moving light stimulations. The direct surround inhibition was mediated mainly by reciprocal GABA(A) synapses between opposing SACs, which provided leading and prolonged inhibition during centripetal stimulus motion. Simultaneous Ca(2+) imaging and current-clamp recording during apparent-motion stimulation further demonstrated the contributions of both centrifugal excitation and GABA(A/C)-receptor-mediated centripetal inhibition to the direction-selective Ca(2+) responses in SAC distal processes. Thus, by placing GABA release sites in electrotonically semi-isolated distal processes and endowing these sites with reciprocal GABA(A) synapses, SACs use a radial-symmetric center-surround receptive field structure to build a polar-asymmetric circuitry. This circuitry may integrate at least three levels of interactions--center excitation, surround inhibition, and reciprocal inhibitions that amplify the center--surround antagonism-to generate robust direction selectivity in the distal processes.

Functional degradation of extrastriate visual cortex in senescent rhesus monkeys

The receptive field properties of striate cortical (V1) cells degrade in senescent macaque monkeys. We have now carried out extracellular single unit studies of the receptive field properties of cells in extrastriate visual cortex (area V2) in very old rhesus ( Macaca mulatta) monkeys. This study provides evidence that both the orientation and direction selectivities of V2 cells in old monkeys degrade significantly. Decreased selectivity is accompanied by increased visually driven and spontaneous responses. As a result, V2 cells in old animals exhibit markedly decreased signal-to-noise ratios. A significant degradation of neural function in extrastriate cortex may underlie the declines in higher order visual function that accompany normal aging.

Brainstem modulation of visual response properties of single cells in the dorsal lateral geniculate nucleus of cat.

The dorsal lateral geniculate nucleus (dLGN) transmits visual signals from the retina to the cortex. In the dLGN the antagonism between the centre and the surround of the receptive fields is increased through intrageniculate inhibitory mechanisms. Furthermore, the transmission of signals through the dLGN is modulated in a state-dependent manner by input from various brainstem nuclei including an area in the parabrachial region (PBR) containing cholinergic cells involved in the regulation of arousal and sleep. Here, we studied the effects of increased PBR input on the spatial receptive field properties of cells in the dLGN. We made simultaneous single-unit recordings of the input to the cells from the retina (S-potentials) and the output of the cells to the cortex (action potentials) to determine spatial receptive field modifications generated in the dLGN. State-dependent modulation of the spatial receptive field properties was studied by electrical stimulation of the PBR. The results showed that PBR stimulation had only a minor effect on the modifications of the spatial receptive field properties generated in the dLGN. The PBR-evoked effects could be described mainly as increased response gain. This suggested that the spatial modifications of the receptive field occurred at an earlier stage of processing in the dLGN than the PBR-controlled gain regulation, such that the PBR input modulates the gain of the spatially modified signals. We propose that the spatial receptive field modifications occur at the input to relay cells through the synaptic triades between retinal afferents, inhibitory interneurone dendrites, and relay cell dendrites and that the gain regulation is related to postsynaptic cholinergic effects on the relay cells.

Primary afferent input to and receptive field properties of cells in rat lumbar area X.

In this study we examined the primary afferent input to rat area X of Rexed, and characterized sensory receptive fields (RFs) of the cells therein. This poorly understood area contains primary afferent fibres, some of which are arranged into a compact bundle beneath the central canal. Anterograde transport of the B fragment of cholera toxin (CTB) from the sciatic nerve showed a strictly ipsilateral projection to segments in L4 and L5 but both ipsi- and contralateral projections in L6 and more caudal segments. The response of cells in area X to mechanical cutaneous stimuli was recorded through extracellular microelectrodes in decerebrate, decerebrate-spinal, and urethane-anaesthetised preparations. The lateral edge of area X was marked by an abrupt change in the RFs: Lateral to area X in the dorsal horn, they were strictly unilateral and relatively small. At a mean of 90 microm from the midline, there was an abrupt expansion of the RFs to cover at least the entire ipsilateral dermatome. Within area X, 70% of the cells' RFs extended across the midline to include contralateral skin. In 35% of cells recorded in rats with intact spinal cords, the RF extended rostrally onto the forelimb. In a small number of cells, the RF included ear pinnae and nose. The precise function of area X cells remains unknown; although they have been shown to be involved in visceral reflexes, the fact that they receive convergent input from a wide variety of tissues and from local and remote body parts implies a more generalized, integrative function.

Responses to continuously changing optic flow in area MST.

We studied the temporal behavior and tuning properties of medial superior temporal (MST) neurons in response to constant flow-field stimulation and continuously changing flow-field stimulation (transitions), which were obtained by morphing one flow field into another. During transitions, the flow fields resembled the motion pattern seen by an observer during changing ego-motion. Our aim was to explore the behavior of MST cells in response to changes in the flow-field pattern and to establish whether the responses of MST cells are temporally independent or if they are affected by contextual information from preceding stimulation. We first tested whether the responses obtained during transitions were linear with respect to the two stimuli defining the transition. In over half of the transitions, the cell response was nonlinear: the response during the transition could not be predicted by the linear interpolation between the stimulus before and after the transition. Nonlinearities in the responses could arise from a dependence on temporal context or from nonlinearities in the tuning to flow-field patterns. To distinguish between these two hypotheses, we fit the responses during transitions and during continuous stimuli to the predictions of a temporally independent model (temporal-independence test) and we compared the responses during transitions to the responses elicited by inverse transitions (temporal-symmetry test). The effect of temporal context was significant in only 7.2% and 5.5% of cells in the temporal-independence test and in the temporal-symmetry test, respectively. Most of the nonlinearities in the cell responses could be accounted for by nonlinearities in the tuning to flow-field stimuli (i.e., the responses to a restricted set of flow fields did not predict the responses to other flow fields). Tuning nonlinearities indicate that a complete characterization of the tuning properties of MST neurons cannot be obtained by testing only a small number of flow fields. Because the cells' responses do not depend on temporal context, continuously changing stimulation can be used to characterize the receptive field properties of cells more efficiently than constant stimulation. Temporal independence in the responses to transitions indicates that MST cells do not code for second-order temporal properties of flow-field stimuli, i.e., for changes in the flow field through time that can be construed as paths through the environment. Information about ego-motion three-dimensional paths through the environment may either be processed at the population level in MST or in other cortical areas.

Chromatic properties of neurons in macaque area V2.

We recorded from single cells in area V2 of cynomolgus monkeys using standard acute recording techniques. After measuring each cell's spatial and temporal properties, we performed several tests of its chromatic properties using sine-wave gratings modulated around a mean gray background. Most cells behaved like neurons in area V1 and their responses were adequately described by a model that assumes a linear combination of cone signals. Unlike in V1, we found a subpopulation of cells whose activity was increased or inhibited by stimuli within a narrow range of color combinations. No particular color directions were preferentially represented. V2 cells showing color specificity, including cells showing narrow chromatic tuning, were present in any of the stripe compartments, as defined by cytochrome-oxidase (CO) staining. An addition of chromatic contrast facilitated the responses of most neurons to gratings with various luminance contrasts. Neurons in all three CO compartments gave significant responses to isoluminant gratings. Receptive-field properties of cells were generally similar for luminance and chromatically defined stimuli. We found only a small number of cells with a clearly identifiable double-opponent receptive-field organization.

Reorganization in the auditory cortex of the rat induced by intracortical microstimulation: a multiple single-unit study.

Many manipulations are able to change or perturb various aspects of single neuron properties and interneuronal relationships. Changes of cerebral cortex organization have been observed in different cortical areas and at different time scales in relation to peripheral stimulation, peripheral damage, associative learning, and electrical stimulation. Here we describe studies on separable multineuron recordings in the rat's auditory cortex under two different anesthetics. Acoustic stimuli were used as a normal, physiological input, and weak electrical intracortical microstimulation (ICMS) as a perturbation that forces a rapid cortical reorganization. ICMS induced fast changes in the cortical map and in the receptive field properties of cells at the electrically stimulated and adjacent electrodes. In effect there was an enlargement of the cortical domain tuned to the acoustic frequency that had been represented at the stimulating electrode. ICMS also incremented afterdischarge responses; these consisted of an initial response to the auditory stimulus followed by less intense repetitive activity that was stimulus-time locked and had a period of 8-12 Hz, similar to that of the spontaneous synchronous activity. Cortical activity under ketamine differed from that under pentobarbital sodium, although in both situations we observed that cortical neurons were highly synchronous.

Modulation of horizontal cell receptive fields in the light adapted goldfish retina

In the isolated goldfish retina, 700 nm background illumination increases the horizontal cell receptive field size, as measured with 565 nm slits of light, but decreases the receptive field size, when measured with 660 nm slits. These background-induced changes in receptive field size are absent when the depolarizing responses in bi- and triphasic horizontal cells are blocked by lowering the [Ca 2+] in the Ringer's solution from 1.0 to 0.1 mM. These results cannot be explained by the linear properties of the horizontal cell layers, nor by slow adaptational processes, but are consistent with the concept that feedback from horizontal cells to cones modifies the horizontal cell receptive field properties.

Effects of brain stem parabrachial activation on receptive field properties of cells in the cat's lateral geniculate nucleus.

1. The lateral geniculate nucleus is the primary thalamic relay for the transfer of retinal signals to the visual cortex. Geniculate cells are heavily innervated from nonretinal sources, and these modify retinogeniculate transmission. A major ascending projection to the lateral geniculate nucleus arises from cholinergic cells in the parabrachial region of the brain stem. This is an important pathway in the ascending control of arousal. In an in vivo preparation, we used extracellular recordings to study the effects of electrical activation of the parabrachial region on the spontaneous activity and visual responses of X and Y cells in the lateral geniculate nucleus of the cat. 2. We studied the effects of two patterns of parabrachial activation on the spontaneous activity of geniculate cells. Burst stimulation consisted of a short pulse at high frequency (16 ms at 250 Hz). Train stimulation was of longer duration at lower frequency (e.g., 1 s at 50 Hz). The firing rate of almost all geniculate cells was enhanced by either pattern of stimulation. However, the burst pattern of stimulation elicited a short, modulated response with excitatory and inhibitory epochs. We found that the different epochs could differentially modulate the visual responses to drifting gratings. Thus the temporal alignment of the brain stem and visual stimuli was critical with burst stimulation, and varied alignments could dramatically confound the results. In comparison, the train pattern of stimulation consistently produced a relatively flat plateau of increased firing, after a short initial period of more variable effects. We used the less confounding pattern of train stimuli to study the effects of parabrachial activation on visual responses. 3. Our main emphasis was to examine the parabrachial effects on the visual responses of geniculate cells. For most visual stimuli, we used drifting sine wave gratings that varied in spatial frequency; these evoked modulated responses from the geniculate cells. Parabrachial activation enhanced the visual responses of almost all geniculate cells, and this enhancement included both increased depth of modulation and greater response rates. 4. Our results were incorporated quantitatively into a difference-of-Gaussians model of visual receptive fields in order to study the parabrachial effects on the spatial structure of the receptive field. This model fit our data well and provided measures of the response amplitude and radius of the receptive field center (Kc and Rc, respectively) and the response amplitude and radius of the receptive field surround (Ks and Rs, respectively).(ABSTRACT TRUNCATED AT 400 WORDS)

Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex

The receptive field properties of cells in layers 2, 3, and 4 of area 17 (V1) of the monkey were studied quantitatively using colored and broad-band gratings, bars, and spots. Many cells in all regions studied responded selectively to stimulus orientation, direction, and color. Nearly all cells (95%) in layers 2 and 3 exhibited statistically significant orientation preferences (biases), most exhibited at least some color sensitivity, and many were direction sensitive. The degree of selectivity of cells in layers 2 and 3 varied continuously among cells; we did not find discrete regions containing cells sensitive to orientation and direction but not color, and vice versa. There was no relationship between the degree of orientation sensitivity of the cells studied and their degree of color sensitivity. There was also no obvious relationship between the receptive field properties studied and the cells' location relative to cytochrome oxidase-rich regions. Our findings are difficult to reconcile with the hypothesis that there is a strict segregation of cells sensitive to orientation, direction, and color in layers 2 and 3. In fact, the present results suggest the opposite since most cells in these layers are selective for a number of stimulus attributes.

Local intracortical connections in the cat's visual cortex: postnatal development and plasticity.

1. We have studied the nature, development, and plasticity of local intracortical interactions by examining the visual responses from pairs of cells in the visual cortex of anesthetized and paralyzed adult cats and kittens at postnatal age 4 wk. Simultaneous discharge from nearby cells was analyzed by the cross-correlation method to infer three types of neuronal interactions: monosynaptic excitation, monosynaptic inhibition, and polysynaptic excitation. 2. Among cell pairs that exhibit correlated discharge, the nature of these interactions is similar in kittens and adults. For example, the mean monosynaptic delay is the same for cell pairs in the adult cat and the kitten: 0.8 ms. The primary difference in the distribution of neural interactions is the increased prevalence of inhibitory interactions among adult cat cell pairs compared with kitten cell pairs. However, in both age groups and in nearly all laminae, polysynaptic interactions are the most commonly observed type of interaction. 3. Neural interactions revealed by cross-correlation analysis also were studied with respect to the receptive field properties of the cells. The hierarchical theory proposed by Hubel and Wiesel suggests that monosynaptic excitation should be seen from simple to complex cells. It further suggests that complex cells do not provide monosynaptic excitation either to simple or to other complex cells. However, we find no cases of monosynaptic excitation from simple to complex cells in the adult cat. Moreover, we find explicitly antihierarchical connections, i.e., excitatory connections from complex to simple cells, in both kittens and adults. The excitatory influence of complex cells on simple cell receptive field properties is not incorporated into current models of receptive field structure formation. Our results suggest that complex cells might have an important modulatory role in simple cell discharge. 4. Plasticity of intracortical synaptic connections was studied by examining the dynamics of monosynaptic peaks with cross-correlograms. We examined Hebb's seminal hypothesis regarding synaptic plasticity that the excitatory connections between two neurons should strengthen with simultaneous activity. To test directly whether Hebbian plasticity can be rapidly induced by stimulus-evoked activity, the strength of monosynaptic excitation between pairs of neurons was monitored during periods of visual stimulation lasting < or = 2 h. Synaptic strength was computed by summing the cross-correlogram bins containing the monosynaptic peak. Transient increases in monosynaptic peak area are found among cell pairs linked by monosynaptic excitation after 8-15 min of visual stimulation. The duration and amplitude of these changes are similar in adult cats and kittens.(ABSTRACT TRUNCATED AT 400 WORDS)

What Is the Goal of Sensory Coding?

A number of recent attempts have been made to describe early sensory coding in terms of a general information processing strategy. In this paper, two strategies are contrasted. Both strategies take advantage of the redundancy in the environment to produce more effective representations. The first is described as a “compact” coding scheme. A compact code performs a transform that allows the input to be represented with a reduced number of vectors (cells) with minimal RMS error. This approach has recently become popular in the neural network literature and is related to a process called Principal Components Analysis (PCA). A number of recent papers have suggested that the optimal “compact” code for representing natural scenes will have units with receptive field profiles much like those found in the retina and primary visual cortex. However, in this paper, it is proposed that compact coding schemes are insufficient to account for the receptive field properties of cells in the mammalian visual pathway. In contrast, it is proposed that the visual system is near to optimal in representing natural scenes only if optimality is defined in terms of “sparse distributed” coding. In a sparse distributed code, all cells in the code have an equal response probability across the class of images but have a low response probability for any single image. In such a code, the dimensionality is not reduced. Rather, the redundancy of the input is transformed into the redundancy of the firing pattern of cells. It is proposed that the signature for a sparse code is found in the fourth moment of the response distribution (i.e., the kurtosis). In measurements with 55 calibrated natural scenes, the kurtosis was found to peak when the bandwidths of the visual code matched those of cells in the mammalian visual cortex. Codes resembling “wavelet transforms” are proposed to be effective because the response histograms of such codes are sparse (i.e., show high kurtosis) when presented with natural scenes. It is proposed that the structure of the image that allows sparse coding is found in the phase spectrum of the image. It is suggested that natural scenes, to a first approximation, can be considered as a sum of self-similar local functions (the inverse of a wavelet). Possible reasons for why sensory systems would evolve toward sparse coding are presented.

Activity sharpens the regenerating retinotectal projection in goldfish: sensitive period for strobe illumination and lack of effect on synaptogenesis and on ganglion cell receptive field properties.

The regenerating optic nerve of goldfish first reestablishes a rough retinotopic map on the contralateral tectum and then sharpens it. Disruption of visual activity, either by blocking activity with intraocular tetrodotoxin (TTX; Schmidt and Edwards, 1983) or by synchronizing activity with strobe illumination (Schmidt and Eisele, 1985), disrupts the sharpening process: the map is correctly oriented but the multiunit receptive fields at each point average 25-40 degrees in diameter. In order to test whether strobe and TTX interfere with the same mechanism, we have tested whether their sensitive periods are the same, and whether strobe, like TTX treatment, does not affect either ganglion cell receptive field properties or synaptogenesis. In parallel studies, we exposed fish to 2 weeks of either strobe illumination or intraocular TTX beginning at various times after crush and determined via electrophysiological recordings that the periods of sensitivity were nearly identical. There was no effect of either treatment during the first 2 weeks (before the fibers arrive at the tectum), maximal disruption of sharpening between 14 and 50 days (the period of rapid synaptogenesis), decreasing disruption between 50 and 125 days, and no effect beyond that point or in the normal projection. In addition, long strobe exposures of up to 142 days produced no greater disruptions than shorter 2-3-week exposures, indicating no cumulative effect. The reestablishment of synaptic transmission in tectum, assayed by recording field potentials elicited by optic nerve shock, was not affected by stroboscopic illumination. Finally, individual ganglion cells, recorded intraretinally following long-term strobe exposure, had receptive fields that were normal both in size and in their characteristic responses to light-on, to light-off, or to both on and off. These findings support the hypothesis that strobe-like TTX prevents retinotopic refinement by preventing the correction of errors initially made by the ingrowing optic axons (Schmidt et al., 1988).