Spatio-temporal organization of receptive fields of the cat striate cortex

The responses of cortical cells to gratings and bars were compared. The excitatory and inhibitory on-and off-zones of a simple cell are composed of on- and off-subfields of CGL. Any zone is formed by an opponent pair of subfields one of which gives an excitatory effect, the other — inhibitory. Such organization assumes the linear properties of a simple field. The deviations from linearity are due to spatial dis-placements of the subfields, heterogeneity of subfields, or the absence of one subfield in the opponent pair. Subfields may be both phasic and tonic, even in the same RF. Analysis of the most common type of a complex cell with modulated responses against unmodulated background shows that a mask eliminating stimulation of any half of the RF causes (according to the theory of filtres) increasing the bandwidth due to the increase or the appearance of responses to side low and high frequencies. The modulated components of the responses from both halves of the RF are out of phase. Analysis of this fact and the responses to thin bars suggests that a complex field is formed by linear and nonlinear subsystems converging onto output neuron. Other types of complex fields are organized by different combinations of subsystems. Limited in area by masking the RF responds to much higher spatial frequencies than the whole RF. The optimal frequency in two-dimensional spatial frequency characteristics of the RF does not change with orientation. Simple RFs and a part of complex RF calculate the amplitude and the phase of the stimulus, the other part of complex RFs (with unmodulated response) calculate only amplitude. Given all this, the RFs are grating filters of spatial frequency.     

Structure of the simple receptive field of the cat visual cortex

Comparison of unit responses of simple receptive fields of the cat visual cortex (area 17) to presentation of sinusoidal gratings and thin light and dark bars showed that excitatory and inhibitory on- and off-zones of the field are composed of on- and off-subfields of the lateral geniculate body converging on the cortical neuron. Each zone is formed by a pair of opposing subfields, activation of one of which gives an excitatory, and the other, an inhibitory effect. This organization is evidence that the simple field has linear properties. However, a real simple field is not a linear system because of deviations from the ideal organization described above, namely displacement of the subfields relative to each other, nonhomogeneity of the properties of the subfields, and absence of an antagonistic subfield in one of the zones. Even within the same field phasic and tonic subfields may be present.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 13, No. 4, pp. 339–344, July–August, 1981.     

Symmetry between the visual B- and D-systems and equivalence of center and surround: Studies of light increment and decrement in retinal and geniculate neurons of the cat

The dual center surround organization of retinal and geniculate neurons in two antagonistic subsystems B and D, having on-center or off-center receptive fields and signalling brightness or darkness respectively, has been studied by local light increments and decrements. Intensity response functions obtained by the introduction and withdrawal of small center spots either brighter or darker than a common homogeneous field are similar in a given neuron, but the phasic responses are stronger in on-center neurons than in off-center neurons. Center size increments and decrements, however, lead to equal excitations in the B- and D-system, respectively, provided that both luminance steps start from the same level and are of equal size on a linear scale. Decrementing and incrementing the surrounding luminance of the same optimal center spots lead to equal surround responses in the two subsystems if the two luminance steps terminate at the same level. This lateral activation is elicited by light decrement in the B-system and by light increment in the D-system. Center and surround responses within a given subsystem are of comparable amplitude, but generally slightly stronger responses are elicited by optimal center increments (decrements) than by the equivalent surround decrements (increments) which lead to the same spatial contrast for B-(D-) neurons. The symmetry relations between the B- and D-system and the equivalence relations between center and surround in each subsystem hold for retinal and geniculate neurons. The difference between center and surround response latencies is about 9 ms in both subsystems at the retinal and 14 ms at the geniculate level. Stimulus response functions of on- and off-center neurons are unified on the basis of linear relative luminance scales.     

Are receptive fields of the visual cortex detectors or spatial frequency filters?

Besides its principal maximum, the spatial frequency characteristic curve of the complex visual cortical receptive field of curarized cats also has additional maxima and also negative regions, as predicted by the theory of piecewise Fourier analysis. Comparison of responses of the complex receptive field to sinusoidal gratings completely and incompletely contained in the field and comparison of responses to sinusoidal and square-wave gratings indicate that the receptive field, as a spatial frequency filter, has linear properties. The response of the complex receptive field rises with an increase in the number of periods of the sinusoidal grating. Several periods of optimal frequency match the complex field. Receptive fields tuned to a broad band of spatial frequencies were found in neuron columns. The results confirm the view that complex receptive fields are spatial frequency filters and not detectors.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 11, No. 5, pp. 403–411, September–October, 1979.     

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.     

Spatial distribution and interaction of responses in receptive fields of cat lateral geniculate neurons

Responses of lateral geniculate neurons to local photic stimulation and to adaptation of the central, antagonistic, and disinhibiting zones of their receptive fields were compared in unanesthetized cats immobilized with D-tubocurarine. Under most conditions of local adaptation, activation of on- and off-responses of neurons occurred after stimulation of the peripheral zones and inhibition of responses after stimulation of the central zone of the receptive field. As a result most neurons acquired the ability to generate a considerable on- and off-signal in response to stimulation. Comparison of this fact with the properties of on-off neurons [7] supports the view that under light-adaptation conditions the processing of large volumes of visual information and the more sophisticated performance of visual functions are connected with activation of responses from peripheral zones of circular receptive fields. It is concluded that local adaptation to light can extend the functional capacity of circular receptive fields.Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 15, No. 5, pp. 451–456, September–October, 1983.     

Bifurcation of orbits and synchrony in inferior olive neurons

Inferior olive neurons (IONs) have rich dynamics and can exhibit stable, unstable, periodic, and even chaotic trajectories. This paper presents an analysis of bifurcation of periodic orbits of an ION when its two key parameters (a, μ) are varied in a two-dimensional plane. The parameter a describes the shape of the parabolic nonlinearity in the model and μ is the extracellular stimulus. The four-dimensional ION model considered here is a cascade connection of two subsystems (S(a) and S(b)). The parameter plane (a - μ) is delineated into several subregions. The ION has distinct orbit structure and stability property in each subregion. It is shown that the subsystem S(a) or S(b) undergoes supercritical Poincare-Andronov-Hopf (PAH) bifurcation at a critical value μ(c)(a) of the extracellular stimulus and periodic orbits of the neuron are born. Based on the center manifold theory, the existence of periodic orbits in the asymptotically stable S(a), when the subsystem S(b) undergoes PAH bifurcation, is established. In such a case, both subsystems exhibit periodic orbits. Interestingly when S(b) is under PAH bifurcation and S(a) is unstable, the trajectory of S(a) exhibits periodic bursting, interrupted by periods of quiescence. The bifurcation analysis is followed by the design of (i) a linear first-order filter and (ii) a nonlinear control system for the synchronization of IONs. The first controller uses a single output of each ION, but the nonlinear control system uses two state variables for feedback. The open-loop and closed-loop responses are presented which show bifurcation of orbits and synchronization of oscillating neurons.     

Receptive fields of neurons in the lateral suprasylvian area of the cat

The structure of receptive fields of single neurons in the lateral suprasylvian area of the cat's cortex was studied. Receptive fields of neurons in this area are larger (up to 2000 deg² or more) than those of the visual projection cortex. A difference was found in the sizes of these fields of the same neuron when measured by presentation of a black object and spot of light. Experimental results showed that most neurons of the area (104 of 148) that are sensitive to visual stimulation respond clearly to flashes of a stationary spot of light. Because of this feature the structure of the receptive fields of the neurons were studied by point by point testing of their whole surface. Intensities of on- and off-components of on-off neurons were found to differ. Only 16% of receptive fields had equal numbers of discharges in on- and off-components of the on-off response. Dominance of one component was observed in 84% of on-off neurons. Receptive fields with several discharge centers are a characteristic feature of neurons in this area. A concentric organization of the receptive fields was found in 11% of neurons.L. A. Orbeli Institute of Physiology, Academy of Sciences of the Armenian SSR, Erevan, Translated from Neirofiziologiya, Vol. 14, No. 3, pp. 278–283, May–June, 1982.     

Color sensitivity in the receptive fields of neurons of the squirrel visual cortex

Color-opponent properties in neurons of the primary visual cortex were investigated in the squirrel. All neurons responded to the presentation of both black and white visual stimuli and of colored stimuli — mainly to blue and green. In 65% of test neurons a response only occurred when blue and green stimuli were applied while the remaining cells partially responded to red. Neurons were divided into groups according to how they responded to the presentation of stimuli composed of black and white: whether nonselective, directionally selective, or orientationally selective (simple or complex). No color-opponent properties were found in any of these groups at receptive field level. The whole or parts of the receptive field responded similarly to the presentation of white, blue, or green stimuli of the same shape. The way in which the receptive fields were divided into on- and off-regions and between directional and orientational selectivity does not depend on the color of the visual stimuli. Findings are discussed with regard to the presence of opponent-color cells in squirrel retina and lateral geniculate body.A. N. Severtsov Institute of Evolutionary Morphology and Animal Ecology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 17, No. 6, pp. 764–770, November–December, 1985.     

Rabbit visual cortical neurons with simple and complex receptive fields

Receptive fields of neurons of the rabbit visual cortex selective for stimulus orientation were investigated. These receptive fields were less well differentiated than those of the analogous neurons of the cat visual cortex (large in size and circular in shape). Two mechanisms of selectivity for stimulus orientation were observed: inhibition between on and off zones of the receptive field (sample type) and oriented lateral inhibition within the same zone of the receptive field (complex type). Lateral inhibition within the same zone of the receptive field also took place in unselective neurons; "complex" selective neurons differed from them in the orientation of this inhibition. A combination of both mechanisms was possible in the receptive field of the same neuron. It is suggested that both simple and complex receptive fields are derivatives of unselective receptive fields and that "complex" neurons are not the basis for a higher level of analysis of visual information than in "simple" neurons.A. N. Severtsov Institute of Evolutionary Morphology and Ecology of Animals, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 10, No. 1, pp. 13–21, January–February, 1978.     

Electrophysiological investigation of medullary neurons connected with lateral line organs of the catfish (Ictalurus nebulosus)

Unit responses in the acoustic-lateral region of the medulla to electrical and mechanical stimulation of the lateral line organs were investigated in acute experiments on curarized catfish. Of the total number of neurons 70% possessed spontaneous activity. An electrical stimulus evoked a tonic response both in spontaneously active and in "silent" cells. Three main types of firing pattern of the neurons were distinguished: fast-adapting, slow-adapting, and grouped. As regards the relation of the neurons to polarity of the stimulus they were subdivided into two groups. The thresholds of unit responses to electrical stimulation varied considerably: from 2.5·10^–9 to 5·10^–12 A/mm². The effect of intensity of the electrical stimulation on unit responses in the medulla is analyzed. The precise dependence of on- and off-responses of each neuron on stimulus intensity of any polarity was determined. The neurons were shown to be sensitive to both electrical and mechanical stimuli. It is postulated that this phenomenon is due to convergence of impulses from electrical and mechanical receptors of the lateral line on the neurons. The properties of the central neurons are compared with those of the peripheral electroreceptor system in catfish.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 5, No. 2, pp. 156–163, March–April, 1973.     

Orientation-selective neurons in the squirrel visual cortex

The organization of receptive fields of neurons sensitive to orientation of visual stimuli was investigated in the squirrel visual cortex. Neurons with mutually inhibitory on- and off-areas of the receptive field, with partially and completely overlapping excitatory and inhibitory mechanisms, were distinguished. Neurons of the second group are most typical. They exhibit orientation selectivity within the excitatory area of the receptive field because, if the stimulus widens in the zero direction, perpendicular to the preferred direction, lateral inhibition is much stronger than if it widens in the preferred direction. Additional inhibitory areas (outside the excitatory area) potentiate this inhibition and increase selectivity. It is suggested that there is no strict separation of simple (with separate excitatory and inhibitory mechanisms in the receptive field) and complex (with overlapping of these mechanisms) neurons in the squirrel visual cortex.A. N. Severtsov Institute of Evolutionary Morphology and Ecology of Animals, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 11, No. 6, pp. 540–549, November–December, 1979.     

Dynamic and static receptive field characteristics of single neurons in the lateral suprasylvian area in cats

Static and dynamic properties of receptive fields of neurons in the lateral suprasylvian area of the cat cerebral cortex were studied. Neurons with different dynamic characteristics may have an identical static organization of their receptive fields; strict correlation is thus not found between these two characteristics of neurons in this area. Most black-sensitive neurons were found to have a receptive field with off-response. Stimulus contrast reversal tests showed that generation of responses to presentation of both black and light stimuli takes place as a result of excitation of the same area of the receptive field and is not due to spatially different on- and off-zones.L. A. Orbeli Institute of Physiology, Academy of Sciences of the Armenian SSR, Erevan. Translated from Neirofiziologiya, Vol. 16, No. 1, pp. 116–123, January–February, 1984.     

Reciprocal Interaction of On- and Off-Systems as a Mechanism of Sensitivity of Visual Neurons to The Orientation of the Vector of the Brightness Gradient in Cats

An experimental study has been performed on neuronal mechanisms of sensitivity of cat visual neurons (lateral geniculate body) to the value and orientation of the vector of brightness gradient in a test stimulus. With changes of the value and orientation of the brightness gradient vector, there exists an optimal (preferred) orientation of the gradient vector, at which the neuronal response is maximal. The sensitivity of neurons to the brightness gradient at shifts of the gradient vector towards the preferred orientation increases not due to an increased excitation in neuronal reactions, but due to a reduction of reciprocal (on- and off-) inhibition, affecting this neuron, of adjacent neurons in neuronal pools. The reciprocal inhibitory interaction of on- and off-systems is enhanced by inhibiting the response of the antagonistic neuron at shifts of the brightness gradient vector in the stimulus from the preferred to the non-preferred orientation. This reciprocal inhibitory interaction is clearly seen in pairs of on- and off-neurons with superposed receptive fields (RF) at their simultaneous analysis of on- and off-responses at a change of the orientation of the brightness gradient vector by 180 degrees. Dependencies of the parameters (duration and intensity of inhibitory phases in responses) of reciprocal inhibitory interaction on orientation of the brightness gradient vector in RF of neurons are determined. Dependencies of responses of the total sample of neurons, which are plotted for on- and off-neurons, to their adequate and inadequate (on- and off-) stimuli on the orientation of the brightness gradient vector are inversely proportional.     

“Irregular” visual receptive fields of neurons of the cat lateral geniculate body

Using point-to-point testing, the spatial organization of receptive fields (RF) of the neurons of the lateral geniculate body (LGB) was studied in cats with pretrigeminally transected brainstcm (without general anesthesia). In 60% of studied neurons (96 units of 160 examined), configuration of their RF considerably differed from round or ellipsoid. The shape of such RF was frequently rather complex, and they were qualified as irregular receptive fields (IRF). Presentation of the stable flickering spot throughout the entire surface of 60 IRF (63%) evoked qualitatively similar responses of a neuron, i.e., these IRF were homogeneous. In 29 cells the responses were of theon-off type, 22 neurons generatedoff responses, andon responses were observed in 9 cells. In the rest of the IRF (37%), it was possible to differentiate the subfields, whose stimulation evoked generation of different types of responses, i.e., these IRF were heterogeneous. In the case of moving stimuli, the neurons with homogeneous IRF showed no directional selectivity, while such selectivity was observed in most units with heterogeneous IRF.Neirofiziologiya/Neurophysiology, Vol. 28, No. 1, pp. 7–16, January–February, 1996.     

Vestibular integrator neurons have quadratic functions due to voltage dependent conductances

The nonlinear properties of the dendrites of the prepositus hypoglossi nucleus (PHN) neurons are essential for the operation of the vestibular neural integrator that converts a head velocity signal to one that controls eye position. A novel system of frequency probing, namely quadratic sinusoidal analysis (QSA), was used to decode the intrinsic nonlinear behavior of these neurons under voltage clamp conditions. Voltage clamp currents were measured at harmonic and interactive frequencies using specific nonoverlapping stimulation frequencies. Eigenanalysis of the QSA matrix reduces it to a remarkably compact processing unit, composed of just one or two dominant components (eigenvalues). The QSA matrix of rat PHN neurons provides signatures of the voltage dependent conductances for their particular dendritic and somatic distributions. An important part of the nonlinear response is due to the persistent sodium conductance (g_NaP), which is likely to be essential for sustained effects needed for a neural integrator. It was found that responses in the range of 10 mV peak to peak could be well described by quadratic nonlinearities suggesting that effects of higher degree nonlinearities would add only marginal improvement. Therefore, the quadratic response is likely to sufficiently capture most of the nonlinear behavior of neuronal systems except for extremely large synaptic inputs. Thus, neurons have two distinct linear and quadratic functions, which shows that piecewise linear?+?quadratic analysis is much more complete than just piecewise linear analysis; in addition quadratic analysis can be done at a single holding potential. Furthermore, the nonlinear neuronal responses contain more frequencies over a wider frequency band than the input signal. As a consequence, they convert limited amplitude and bandwidth input signals to wider bandwidth and more complex output responses. Finally, simulations at subthreshold membrane potentials with realistic PHN neuron models suggest that the quadratic functions are fundamentally dominated by active dendritic structures and persistent sodium conductances.     

Modeling convergent ON and OFF pathways in the early visual system

For understanding the computation and function of single neurons in sensory systems, one needs to investigate how sensory stimuli are related to a neuron’s response and which biological mechanisms underlie this relationship. Mathematical models of the stimulus–response relationship have proved very useful in approaching these issues in a systematic, quantitative way. A starting point for many such analyses has been provided by phenomenological “linear–nonlinear” (LN) models, which comprise a linear filter followed by a static nonlinear transformation. The linear filter is often associated with the neuron’s receptive field. However, the structure of the receptive field is generally a result of inputs from many presynaptic neurons, which may form parallel signal processing pathways. In the retina, for example, certain ganglion cells receive excitatory inputs from ON-type as well as OFF-type bipolar cells. Recent experiments have shown that the convergence of these pathways leads to intriguing response characteristics that cannot be captured by a single linear filter. One approach to adjust the LN model to the biological circuit structure is to use multiple parallel filters that capture ON and OFF bipolar inputs. Here, we review these new developments in modeling neuronal responses in the early visual system and provide details about one particular technique for obtaining the required sets of parallel filters from experimental data.     

Characteristics of poststimulus and lateral inhibition in neurons of cat primary auditory cortex

Experiments using intracellular recording of potentials from neurons of the primary auditory cortex of cats anesthetized with pentobarbital showed that under the influence of tones of characteristic frequency for the neuron under test, or of electrical stimulation of nerve fibers of the spiral ganglion, innervating the center of the receptive field of the neuron, transient excitation of the latter is followed by the development of prolonged (20–250 msec) inhibition. The cause of this inhibition is an IPSP arising in the neuron after the action potential. On the basis of data showing a close connection between inhibition and the preceding spike it is concluded that it arises through the participation of a mechanism of recurrent inhibition. During the action of tones of uncharacteristic frequency or electrical stimulation of the peripheral part of the receptive field of the neuron, a response consisting of EPSP-IPSP arises in the neuron. This IPSP is accompanied by inhibition of spontaneous activity of the neuron and its responses to testing stimulation. It has been shown that this inhibition is lateral in its genesis. Characteristics of these two types of inhibition are given.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 16, No. 2, pp. 194–201, March–April, 1984.     

Organization of receptive fields of motion-senstitive neurons in the cat pulvinar

The distribution of 70 visually sensitive neurons in the cat pulvinar sensitive to motion in the receptive fields was studied. The experimental results showed that components with directional characteristics are present in the structure of these fields of both direction-selective and unselective neurons. In the receptive fields of direction-selective neurons the directional elements of the substructure have identical preferred directions, which coincide with the preferred directions of response to stimulus movement over the entire receptive field. The organization of receptive fields of direction-selective neurons of the visual association structure thus does not differ significantly from that of analogous fields of visual projection neurons. Directional elements of the receptive fields of direction-unselective neurons were found to have different preferred directions, thereby providing a basis for organization of the nondirectional response of the neuron to a stimulus moving across the entire receptive field.L. A. Orbeli Institute of Physiology, Academy of Sciences of the Armenian SSR, Erevan. Translated from Neirofiziologiya, Vol. 14, No. 4, pp. 339–346, July–August, 1982.     

Identification of head motions by central vestibular neurons receiving linear and angular input

Most naturally occurring displacements of the head in space, due to either an external perturbation of the body or a self-generated, volitional head movement, apply both linear and angular forces to the head. The vestibular system detects linear and angular accelerations of the head separately, but the succeeding control of gaze and posture often relies upon the combined processing of linear and angular motion information. Thus, the output of a secondary neuron may reflect the linear, the angular, or both components of the head motion. Although the vestibular system is typically studied in terms of separate responses to linear and angular acceleration of the head, many secondary and higher-order neurons in the vestibular system do, in fact, receive information from both sets of motion sensors. The present paper develops methods to analyze responses of neurons that receive both types of information, and focuses on responses to sinusoidal motions composed of a linear and an angular component. We show that each neuron has a preferred motion, but a single neuron cannot code for a single motion. However, a pair of neurons can code for a motion by the relative phases of firing-rate modulation. In this way, information about motion is enhanced by neurons combining information about linear and angular motion. Received: 5 November 1998 / Accepted in revised form: 19 March 1999