Receptive field properties of neurons in the electrosensory lateral line lobe of the weakly electric fish, <Emphasis Type="Italic">Gnathonemus petersii</Emphasis>

The receptive field of a sensory neuron is known as that region in sensory space where a stimulus will alter the response of the neuron. We determined the spatial dimensions and the shape of receptive fields of electrosensitive neurons in the medial zone of the electrosensory lateral line lobe of the African weakly electric fish, Gnathonemus petersii, by using single cell recordings. The medial zone receives input from sensory cells which encode the stimulus amplitude. We analysed the receptive fields of 71 neurons. The size and shape of the receptive fields were determined as a function of spike rate and first spike latency and showed differences for the two analysis methods used. Spatial diameters ranged from 2 to 36 mm (spike rate) and from 2.45 to 14.12 mm (first spike latency). Some of the receptive fields were simple consisting only of one uniform centre, whereas most receptive fields showed a complex and antagonistic centre-surround organisation. Several units had a very complex structure with multiple centres and surrounding-areas. While receptive field size did not correlate with peripheral receptor location, the complexity of the receptive fields increased from rostral to caudal along the fish's body.     

Synaptic inputs to the ganglion cells in the tiger salamander retina

The postsynaptic potentials (PSPs) that form the ganglion cell light response were isolated by polarizing the cell membrane with extrinsic currents while stimulating at either the center or surround of the cell's receptive field. The time-course and receptive field properties of the PSPs were correlated with those of the bipolar and amacrine cells. The tiger salamander retina contains four main types of ganglion cell: "on" center, "off" center, "on-off", and a "hybrid" cell that responds transiently to center, but sustainedly, to surround illumination. The results lead to these inferences. The on-ganglion cell receives excitatory synpatic input from the on bipolars and that synapse is "silent" in the dark. The off-ganglion cell receives excitatory synaptic input from the off bipolars with this synapse tonically active in the dark. The on-off and hybrid ganglion cells receive a transient excitatory input with narrow receptive field, not simply correlated with the activity of any presynaptic cell. All cell types receive a broad field transient inhibitory input, which apparently originates in the transient amacrine cells. Thus, most, but not all, ganglion cell responses can be explained in terms of synaptic inputs from bipolar and amacrine cells, integrated at the ganglion cell membrane.     

A dynamic model of the vertebrate retina

In this paper a mathematical model of the retina was proposed to clarify the spatio-temporal information processing mechanism in the retina of vertebrates. In order to explain spatio-temporal characteristics of an on-center receptive field of a ganglion cell, excitatory and inhibitory cell layers were introduced of which time lags increased with the lateral distance from a point of stimulation. The characteristics of this model were found to agree well with the physiological data: e.g., this model shows on-response to the input stimulus given on the center, off-response to the input on the surround, and on-off response to the input on the border between on- and off-response regions of the on-center field.     

A Feedback Model of Attention Explains the Diverse Effects of Attention on Neural Firing Rates and Receptive Field Structure

Visual attention has many effects on neural responses, producing complex changes in firing rates, as well as modifying the structure and size of receptive fields, both in topological and feature space. Several existing models of attention suggest that these effects arise from selective modulation of neural inputs. However, anatomical and physiological observations suggest that attentional modulation targets higher levels of the visual system (such as V4 or MT) rather than input areas (such as V1). Here we propose a simple mechanism that explains how a top-down attentional modulation, falling on higher visual areas, can produce the observed effects of attention on neural responses. Our model requires only the existence of modulatory feedback connections between areas, and short-range lateral inhibition within each area. Feedback connections redistribute the top-down modulation to lower areas, which in turn alters the inputs of other higher-area cells, including those that did not receive the initial modulation. This produces firing rate modulations and receptive field shifts. Simultaneously, short-range lateral inhibition between neighboring cells produce competitive effects that are automatically scaled to receptive field size in any given area. Our model reproduces the observed attentional effects on response rates (response gain, input gain, biased competition automatically scaled to receptive field size) and receptive field structure (shifts and resizing of receptive fields both spatially and in complex feature space), without modifying model parameters. Our model also makes the novel prediction that attentional effects on response curves should shift from response gain to contrast gain as the spatial focus of attention drifts away from the studied cell.     

Investigation of functional organization of receptive fields in the cat visual cortex

Receptive fields of neurons in Area 17 of the visual cortex were investigated in cats. Concentrically shaped fields, fields responding selectively to orientation of a strip or edge, and fields which can be regarded as intermediate between the first two types are described. The boundary between zones of summation and of lateral inhibition coincides in some receptive fields with the boundary between central and peripheral zones with opposite forms of response, while in other fields they do not coincide. For some cells there is no peripheral zone or it may disappear with worsening of the state of function. Cells were observed for which an increase in area of the stimulus in the central zone inhibits the response reaction. Analysis of these data suggests that several cells of the geniculate ganglion converge on some cortical neurons, and several cortical cells on others. An effect of adaptive inhibition was found in which constant illumination of an area in the center of the receptive field inhibits the response in another part. It is shown that this effect is unconnected with the action of scattered light. Constant illumination of the peripheral part of the receptive field deinhibits adaptive inhibition. The boundary between the zones of summation and of lateral inhibition coincides with the boundary between the zones of adaptive inhibition and deinhibition.I. V. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 1, No. 1, pp. 90–100, July–August, 1969.     

Receptive field mechanisms of cat X and Y retinal ganglion cells

We investigated receptive field properties of cat retinal ganglion cells with visual stimuli which were sinusoidal spatial gratings amplitude modulated in time by a sum of sinusoids. Neural responses were analyzed into the Fourier components at the input frequencies and the components at sum and difference frequencies. The first-order frequency response of X cells had a marked spatial phase and spatial frequency dependence which could be explained in terms of linear interactions between center and surround mechanisms in the receptive field. The second-order frequency response of X cells was much smaller than the first-order frequency response at all spatial frequencies. The spatial phase and spatial frequency dependence of the first-order frequency response in Y cells in some ways resembled that of X cells. However, the Y first-order response declined to zero at a much lower spatial frequency than in X cells. Furthermore, the second-order frequency response was larger in Y cells; the second-order frequency components became the dominant part of the response for patterns of high spatial frequency. This implies that the receptive field center and surround mechanisms are physiologically quite different in Y cells from those in X cells, and that the Y cells also receive excitatory drive from an additional nonlinear receptive field mechanism.     

Responses of nervous elements of the visual cortex of the chipmunk Eutamias sibiricus to moving and stationary stimuli]

The receptive field organization of cortical units has been studied in experiments with testing by moving and stationary light spots. The size of the receptive fields varied from 3 degrees to 10 degrees. Receptive fields which were tested by a stationary light spot exhibited various types of organization. Some of the neurons produced extensive excitatory on- and off-responses to stimulation by a light spot. Neuronal excitation evoked by light decreased if the stimulus was near the field boundary. Some of the neurons produced either on- or off-responses in any point of the receptive field. A small part of neurons had receptive fields with on- and off-reactions in the center, and either on- or off-responses at the peripheral zones. Most of the neurons exhibited specialization with respect to high-speed motion.     

Nonlinear characteristics in the Frog's visual system

The receptive fields of retinal fibers in the visual tectum of the frog are mapped with different techniques and the spatial summation characteristics are examined, by presenting stimuli of various shapes and sizes in the center of the receptive field. When the size is increased gradually from the center of the stimulus, for constant stimulus intensity, the maximum response is obtained for stimuli of approximately the size of the most responsive part of the RF. Using a clustering technique to obtain stimuli that are part of the RF and combinations of these parts, it is evident that the spatial summation characteristics are not linear. A model is developed that describes the nonlinear form of these results, based on a power law.     

Orientation tuning of motion-sensitive neurons shaped by vertical-horizontal network interactions

We measured the orientation tuning of two neurons of the fly lobula plate (H1 and H2 cells) sensitive to horizontal image motion. Our results show that H1 and H2 cells are sensitive to vertical motion, too. Their response depended on the position of the vertically moving stimuli within their receptive field. Stimulation within the frontal receptive field produced an asymmetric response: upward motion left the H1/H2 spike frequency nearly unaltered while downward motion increased the spike frequency to about 40% of their maximum responses to horizontal motion. In the lateral parts of their receptive fields, no such asymmetry in the responses to vertical image motion was found. Since downward motion is known to be the preferred direction of neurons of the vertical system in the lobula plate, we analyzed possible interactions between vertical system cells and H1 and H2 cells. Depolarizing current injection into the most frontal vertical system cell (VS1) led to an increased spike frequency, hyperpolarizing current injection to a decreased spike frequency in both H1 and H2 cells. Apart from VS1, no other vertical system cell (VS2-8) had any detectable influence on either H1 or H2 cells. The connectivity of VS1 and H1/H2 is also shown to influence the response properties of both centrifugal horizontal cells in the contralateral lobula plate, which are known to be postsynaptic to the H1 and H2 cells. The vCH cell receives additional input from the contralateral VS2-3 cells via the spiking interneuron V1.     

Response dynamics and receptive-field organization of catfish ganglion cells [published erratum appears in J Gen Physiol 1995 Aug;106(2):following 388]

Responses from catfish retinal ganglion cells were evoked by a spot or an annulus of light and were analyzed by a procedure identical to the one used previously to study catfish amacrine cells (Sakai H. M., and K.-I. Naka, 1992. Journal of Neurophysiology. 67:430-442.). In two- input white-noise experiments, a response evoked by simultaneous stimulation of the center and surround was decomposed into the components generated by the center and surround through a process of cross-correlation. The center and surround responses were also decomposed into their linear and nonlinear components so that the response dynamics of the linear and nonlinear components could be measured. We found that the concentric organization of the receptive field was determined by linear components, i.e., the first-order kernels generated by the center and surround were of opposite polarity. Both the center and surround generated second-order kernels with similar signatures, i.e., the second-order components formed a monotonic receptive field. The peak response time of the first- and second-order kernels from the surround was longer by approximately 20 ms than that of the center. Except for the DC potential present in the intracellular responses, almost identical first- and second-order kernels for the center and surround were obtained from both the intracellular response and spike discharges. Thus, information on concentric organization of a receptive field is translated into spike discharges with little loss of information. A train of spike discharges carries, simultaneously, at least four kinds of information: two linear and two nonlinear components, which originate in the receptive field center and the surround. A spike train is not a simple signaling device but is a carrier of complex and multiple signals. Victor, J. D., and R. M. Shapley (1979. Journal of General Physiology. 74:671-687.) discovered similarly that, in the cat retina, static second-order nonlinearity is encoded into spike trains. Results obtained in this study support the thesis that signals generated by the preganglionic cells are translated into spike discharges without major modification and that those signals can be recovered from the spike trains (Sakuranaga, M., Y. Ando, and K.-I. Naka. 1987. Journal of General Physiology. 90:229-259.; Korenberg, M. J., H. M. Sakai, and K.-I. Naka. 1989. Journal of Neurophysiology. 61:1110-1120.). Current injection studies have shown that such signal transmission is possible (Sakai, H. M., and K.-I. Naka, 1988a. Journal of Neurophysiology. 60:1549-1567.; 1990. Journal of Neurophysiology. 63:105-119.).     

Visual cortical unit responses to photic stimulation of different zones of the receptive fields in cats

In acute experiments on unanesthetized curarized cats the intensity functions, response thresholds, inhibition thresholds, and differential sensitivity of 96 neurons in the primary visual projection cortex were investigated by extracellular recording of unit activity during central and peripheral stimulation of their receptive fields. In darkness the neurons had wide threshold and above-threshold reliefs (3–30°). The threshold reliefs of the receptive fields of some cells were found to be V-shaped, whereas others were marked by alternation of zones of increased and reduced excitability. Sensitivity of both excitatory and inhibitory inputs of the receptive field as a rule was greatest in the center. Inhibitory inputs of different cortical neurons were much more standard and less sensitive to light, and they were mainly activated within the intermediate (mesoptic) range of brightnesses. During light adaptation the threshold contour of the receptive field narrows sharply, mainly because of the fall in sensitivity of its peripheral inputs. Compared with the lateral geniculate body and retina, the relative number of low-threshold elements, sensitivity in the system of inhibitory elements, and differential brightness sensitivity are greater in the cortex. The mechanisms of formation of receptive fields of cortical neurons and their modification during changes in the level of adaptation, and also the role of excitatory and inhibitory inputs of the cell in these effects are discussed.Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 11, No. 3, pp. 227–235, May–June, 1979.     

Thalamic center for the lateral line system in the catfish Ictalurus nebulosus: Evoked potential evidence

By means of evoked potential methods, a lateral line center in the thalamus of the bullhead catfish is here identified. The locus of this lateral line center corresponds to the mechanoreceptive thalamic zone and/or torothalamic tract identified by anatomical means. The thalamic lateral line area responds to acoustic stimuli as well as lateral line nerve shock but fails to respond to electroreceptor inputs that do cause responses in their special part of the midbrain torus semicircularis. The latency of the first peak of response to lateral line nerve shock, which is also the main response peak, is 30 ms for the thalamic zone compared to 15 ms for the earliest peak response in the mechanoreceptive part of the torus semicircularis. The thalamic response fatigues much more quickly than the toral response and has different dynamic properties to closely spaced stimulus pairs as well.     

Inhibitory components in the neuronal response of the lateral suprasylvian cortical area in the cat

Inhibitory components in the response evoked by presentation of mobile visual stimuli in neurons belonging to the lateral suprasylvian area of the cerebral cortex were investigated in cats. It was demonstrated by comparing poststimulus histograms of neuronal response to movement in two opposite directions that the location of discharge centers within the receptive fields changed in relation to movement direction. No spatial area giving rise to the inhibitory component of response could be found in any of the neurons with monotone stationary structure of their receptive fields. Findings from experiments involving techniques of stimulating a test area of the receptive field separately indicated that inhibitory components of response in neurons of the lateral suprasylvian area with monotone organization of the receptive field could represent inhibitory after-response following the neuronal excitation produced by the visual stimulus traveling across this field.L. A. Orbeli Institute of Physiology, Academy of Sciences of the Armenian SSR, Erevan. Translated from Neirofiziologiya, Vol. 19, No. 3, pp. 299–308, May–June, 1987.     

Multiple Representations of the Body and Input-Output Relationships in the Agranular and Granular Cortex of the Chronic Awake Guinea Pig

The organization of somatosensory input and the input-output relationships in regions of the agranular frontal cortex (AGr) and granular parietal cortex (Gr) were examined in the chronic awake guinea pig, using the combined technique of single-unit recording and intracortical microstimulation (ICMS). AGr, which was cytoarchitectonically subdivided into medial (AGrm) and lateral (AGrl) parts, also can be characterized on a functional basis. AGrl contains the head, forelimb, and most hindlimb representations; only a small number of hindlimb neurons are confined in AGrm. Different distributions of submodalities exist in AGr and Gr: AGr receives predominantly deep input (with the exception of the vibrissa region, which receives cutaneous input), whereas neurons of Gr respond almost exclusively to cutaneous input. The cutaneous or deep receptive field (RF) of each neuron was determined by natural peripheral stimulation. All studied neurons were activated by small RFs, with the exception of lip, nose, pinna, and limb units of lateral Gr (Grl), for which the RFs were larger.

Microelectrode mapping experiments revealed the existence of three spatially separate, incomplete body maps in which somatosensory and motor representations overlap. One body map, with limbs medially and head rostrolaterally, is contained in AGr. A second map, comparable to the first somatosensory cortex (SI) of other mammals, is found in Gr, with hindlimb, trunk, forelimb, and head representations in an orderly mediolateral sequence. An unresponsive zone separates the head area from the forelimb region. A third map, with the forelimb rostrally and the hindlimb caudally, lies adjacent and lateral to the SI head area. This limb representation, which is characterized by an upright and small size compared to that found in SI, can be considered to be part of the second somatosensory cortex (SII). A distinct head representation was not recognized as properly belonging to SII, but the evidence that neurons of the SI head region respond to stimulation of large RFs located in lips, nose, and pinna leads us to hypothesize that the SII face area overlaps that of SI to some extent, or, alternatively, that the two areas are strictly contiguous and the limits are ambiguous, making them difficult to distinguish.

The input-output relationships were based on the results of RF mapping and ICMS in the same electrode penetration. The intrinsic specific interconnections of cortical neurons whose afferent input and motor output is related to identical body regions show a considerable degree of refinement. The input-output correspondence is especially pronounced for neurons with small RFs. This study confirms and extends similar data recently reported for other rodents.     

A multi-stage model for fundamental functional properties in primary visual cortex

Many neurons in mammalian primary visual cortex have properties such as sharp tuning for contour orientation, strong selectivity for motion direction, and insensitivity to stimulus polarity, that are not shared with their sub-cortical counterparts. Successful models have been developed for a number of these properties but in one case, direction selectivity, there is no consensus about underlying mechanisms. We here define a model that accounts for many of the empirical observations concerning direction selectivity. The model describes a single column of cat primary visual cortex and comprises a series of processing stages. Each neuron in the first cortical stage receives input from a small number of on-centre and off-centre relay cells in the lateral geniculate nucleus. Consistent with recent physiological evidence, the off-centre inputs to cortex precede the on-centre inputs by a small (～4 ms) interval, and it is this difference that confers direction selectivity on model neurons. We show that the resulting model successfully matches the following empirical data: the proportion of cells that are direction selective; tilted spatiotemporal receptive fields; phase advance in the response to a stationary contrast-reversing grating stepped across the receptive field. The model also accounts for several other fundamental properties. Receptive fields have elongated subregions, orientation selectivity is strong, and the distribution of orientation tuning bandwidth across neurons is similar to that seen in the laboratory. Finally, neurons in the first stage have properties corresponding to simple cells, and more complex-like cells emerge in later stages. The results therefore show that a simple feed-forward model can account for a number of the fundamental properties of primary visual cortex.     

Strongly pH-buffered ringer's solution expands the receptive field size of horizontal cells in the carp retina

By intracellular recordings, we studied the effects of pH buffering on the size of the receptive field and the extent of dye coupling of horizontal cells (HCs) in the light-adapted carp retina. These parameters were compared between data obtained in fortified Ringer's solution and those obtained in control bicarbonate Ringer's of the same pH (7.60). In Ringer's fortified with 10 mM HEPES or 15 mM Tris, the dye-coupling ratio of HCs increased by 71% and 70%, respectively. These fortified Ringer's solutions also depolarized the dark membrane potential and increased the light-evoked response. The HC receptive field profile could be described by the exponential decline in peak response amplitude to a slit of light moved tangentially from the recording electrode. Thus, the receptive field size was determined as a space constant proportional to (gj/gm)(1/2), where gj and gm denote gap and non-gap-junctional conductances. The HEPES- or Tris-fortified Ringer's significantly increased the space constant by 43% and 41%, respectively. Since dye coupling was increased in the fortified Ringer's, it is likely that gj increased more than gm as a result of alkalinization of the cytosol. Since HEPES has an aminosulfonate moiety, it has been assumed to close the hemi-channels of connexin 26, but the pH-buffering effects were essentially the same as those of Tris that has no aminosulfonate moiety. Therefore, it is unlikely that the closure of connexin 26 hemichannels is responsible for the change in the receptive field size of HCs.     

Receptive field dynamics of neurons in the cat visual cortex and lateral geniculate body

Spike responses of single neurons in the primary visual cortex and lateral geniculate body to random presentation of local photic stimuli in different parts of the receptive field of the cell were studied in acute experiments on curarized cats. Series of maps of receptive fields with time interval of 20 msec obtained by computer enabled the dynamics of the excitatory and inhibitory zones of the field to be assessed during development of on- and off-responses to flashes. Receptive fields of all cortical and lateral geniculate body neurons tested were found to undergo regular dynamic reorganization both after the beginning and after the end of action of the photic stimulus. During the latent period of the response no receptive field was found in the part of the visual field tested, but later a small zone of weak responses appeared only in the center of the field. Gradually (most commonly toward 60–100 msec after application of the stimulus) the zone of the responses widened to its limit, after which the recorded field began to shrink, ending with complete disappearance or disintegration into separate fragments. If two bursts of spikes were generated in response to stimulation, during the second burst the receptive field of the neuron changed in the same way. The effects described were clearly exhibited if the level of background illumination, the intensity of the test bars, their contrast with the background, duration, angles subtended, and orientation were varied, although the rate and degree of reorganization of the receptive field in this case changed significantly. The functional importance of the effect for coding of information about the features of a signal by visual cortical neurons is discussed.Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 14, No. 6, pp. 622–630, November–December, 1982.     

Physiological response properties of cat retinal ganglion cells projecting to suprachiasmatic nucleus

The aim of this experiment was to characterize the physiological properties of cat retinal ganglion cells that project to the suprachiasmatic nucleus (SCN). Retrogradely labeled SCN-projecting ganglion cells were recorded extracellularly in vitro. For the first time, this study provides crucial information on visual response properties of ganglion cells in the entrainment circuitry. All recorded cells gave sustained responses (n = 9). Although most of the cells (n = 8) had an "on" center receptive field, one cell showed "on-off" center receptive field properties. The range of receptive field sizes was 2 to 5 deg. For most of the cells tested, the spectral wavelength that evoked peak responses was 500 nm (3 out of 5 cells). All recorded cells (n = 9) preferred still or extremely slow-moving stimuli (3.3 deg/s). These results indicate that cat SCN-projecting cells receive inputs from conventional photoreceptors. The hypothesis that both conventional and cryptochromic photoreceptors are involved in transferring photic signals is discussed.     

Spatial resolution and nonlinearities of simple cells in the cat visual cortex measured with parallel line pairs

The spatial resolution of simple cells in cat visual cortex was measured by stimulation with pairs of 6 wide parallel light bars of various spacings. These double lines were moved across the receptive field and were taken as resolved if there was a 10% deflection between the double peak responses of cells. As a control, recordings were also made from several geniculate fibers. The smallest bar separations resolved by simple cells were larger than those which have been found for cells of the lateral geniculate nucleus (LGN), although the smallest cortical receptive field centers were as small as those of LGN-cells. The correlation between optimal resolving power of a cell and the width of its excitatory receptive field was much weaker in cortical simple cells than in LGN cells. In contrast to the LGN, the double line responses of most simple cells differ markedly from an additive superposition of two single line responses spaced according to the actual interline distance. As possible mechanisms underlying these nonlinearities three different connectivity schemes were investigated. Two of these models were based on receptive field concepts; the third one used intracortical circuits. Only the latter model could explain all the nonlinear effects seen in the neurophysiological experiments.     

Transformation of Stimulus Correlations by the Retina

Redundancies and correlations in the responses of sensory neurons may seem to waste neural resources, but they can also carry cues about structured stimuli and may help the brain to correct for response errors. To investigate the effect of stimulus structure on redundancy in retina, we measured simultaneous responses from populations of retinal ganglion cells presented with natural and artificial stimuli that varied greatly in correlation structure; these stimuli and recordings are publicly available online. Responding to spatio-temporally structured stimuli such as natural movies, pairs of ganglion cells were modestly more correlated than in response to white noise checkerboards, but they were much less correlated than predicted by a non-adapting functional model of retinal response. Meanwhile, responding to stimuli with purely spatial correlations, pairs of ganglion cells showed increased correlations consistent with a static, non-adapting receptive field and nonlinearity. We found that in response to spatio-temporally correlated stimuli, ganglion cells had faster temporal kernels and tended to have stronger surrounds. These properties of individual cells, along with gain changes that opposed changes in effective contrast at the ganglion cell input, largely explained the pattern of pairwise correlations across stimuli where receptive field measurements were possible.