Spatiotemporal frequency responses of cat retinal ganglion cells

Spatiotemporal frequency responses were measured at different levels of light adaptation for cat X and Y retinal ganglion cells. Stationary sinusoidal luminance gratings whose contrast was modulated sinusoidally in time or drifting gratings were used as stimuli. Under photopic illumination, when the spatial frequency was held constant at or above its optimum value, an X cell's responsivity was essentially constant as the temporal frequency was changed from 1.5 to 30 Hz. At lower temporal frequencies, responsivity rolled off gradually, and at higher ones it rolled off rapidly. In contrast, when the spatial frequency was held constant at a low value, an X cell's responsivity increased continuously with temporal frequency from a very low value at 0.1 Hz to substantial values at temporal frequencies higher than 30 Hz, from which responsivity rolled off again. Thus, 0 cycles X deg-1 became the optimal spatial frequency above 30 Hz. For Y cells under photopic illumination, the spatiotemporal interaction was even more complex. When the spatial frequency was held constant at or above its optimal value, the temporal frequency range over which responsivity was constant was shorter than that of X cells. At lower spatial frequencies, this range was not appreciably different. As for X cells, 0 cycles X deg-1 was the optimal spatial frequency above 30 Hz. Temporal resolution (defined as the high temporal frequency at which responsivity had fallen to 10 impulses X s-1) for a uniform field was approximately 95 Hz for X cells and approximately 120 Hz for Y cells under photopic illumination. Temporal resolution was lower at lower adaptation levels. The results were interpreted in terms of a Gaussian center-surround model. For X cells, the surround and center strengths were nearly equal at low and moderate temporal frequencies, but the surround strength exceeded the center strength above 30 Hz. Thus, the response to a spatially uniform stimulus at high temporal frequencies was dominated by the surround. In addition, at temporal frequencies above 30 Hz, the center radius increased.     

Fast temporal adaptation of on-off units in the first optic chiasm of the blowfly

1. We recorded from spiking units in the first optic chiasm between lamina and medulla in the brain of the blowfly (Calliphora vicina). Both previously characterized neuron types, on-off units and sustaining units, were encountered. On-off units had a temporal frequency response with a lower cut-off frequency than blowfly photoreceptors. This low cut-off frequency is related to a fast temporal adaptation of the on-off units to trains of short light pulses. Temporal adaptation occurred independently for short on- and off-pulses. 2. On-off units only responded to stimuli of relatively large contrast. Contrasts of less than 10% gave little or no response.     

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.     

Evidence for spatio-temporal selectivity in attentional modulation of the motion aftereffect

An ignored region of the visual field might be monitored by an intermittent full visual analysis or by a more continuous but restricted analysis. We investigated which type of process is more likely in early vision by studying the effects of diverting attention on adaptation to a range of spatial (0.5, 2, 4. and 6 c/deg) and temporal (1.5 and 10 Hz) frequencies. During adaptation, subjects either fixated an unchanging digit (normal attention). or named the sequence of changing digits which formed the fixation point (diverted). The test field was always a static version of the adapting field, and the strength of adaptation was measured through the velocity and duration of subsequent Motion Aftereffects (MAEs). When attention during adaptation was normal MAE durations rose with spatial frequency for the 1.5 Hz stimuli, and declined with spatial frequency for the 10 Hz stimuli. When attention was diverted from the 10 Hz stimuli, MAE durations and velocities fell by a similar amount at all spatial frequencies. However, for the 1.5 Hz stimuli, the effects of diversion were very small at 0.5 c/deg, and rose progressively with spatial frequency, so that MAE reductions were largest at 6 c/deg. It appears that diversion hardly affects the encoding of coarse, slow stimuli, but attenuates the encoding of finer and/or faster stimuli. This is consistent with the idea that during diversion the visual system monitors the scene continuously, but over a restricted range of spatial and temporal scales.     

A unified neural network model of spatiotemporal processing in X and Y retinal ganglion cells

This article makes use of a push-pull shunting network, which was introduced in the companion article, to model certain properties of X and Y retinal ganglion cells. Input to the push-pull network is preprocessed by a nonlinear mechanism for temporal adaptation, which is ascribed here to photoreceptor dynamics. The complete circuit is used to show that a simple change in receptive field morphology within a single model equation can change the network's response characteristics to closely resemble those of either X or Y cells. Specifically, an increase in width of the receptive field center mechanism is sufficient to account for generation of on-off (Y-like) instead of null (X-like) responses to modulated gratings. In agreement with experimental data, the Y cell on-off response is independent of spatial phase. Also, the model accurately predicts that on-off responses can be observed in X cells for particular stimulus configurations. Taken together, the results show how the retina combines individually inadequate modules to efficiently handle the tasks required for accurate spatial and temporal visual information processing. The model is also able to clarify a number of controversial experimental findings on the nature of spatiotemporal visual processing in the retina.     

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.     

Colour and luminance interactions in the visual perception of motion

We sought to determine the extent to which red-green, colour-opponent mechanisms in the human visual system play a role in the perception of drifting luminance-modulated targets. Contrast sensitivity for the directional discrimination of drifting luminance-modulated (yellow-black) test sinusoids was measured following adaptation to isoluminant red-green sinusoids drifting in either the same or opposite direction. When the test and adapt stimuli drifted in the same direction, large sensitivity losses were evident at all test temporal frequencies employed (1-16 Hz). The magnitude of the loss was independent of temporal frequency. When adapt and test stimuli drifted in opposing directions, large sensitivity losses were evident at lower temporal frequencies (1-4 Hz) and declined with increasing temporal frequency. Control studies showed that this temporal-frequency-dependent effect could not reflect the activity of achromatic units. Our results provide evidence that chromatic mechanisms contribute to the perception of luminance-modulated motion targets drifting at speeds of up to at least 32 degrees s(-1). We argue that such mechanisms most probably lie within a parvocellular-dominated cortical visual pathway, sensitive to both chromatic and luminance modulation, but only weakly selective for the direction of stimulus motion.     

On spiking units in the first optic chiasm of the blowfly

We recorded from the spiking sustaining unit in the optic chiasm between lamina and medulla in the brain of the blowfly Calliphora vicina, and investigated both temporal and spatial properties of the light-adapted cell. The sustaining unit fails to follow the highest temporal frequencies followed by the photoreceptor, but its temporal resolution is substantially better than that of the on-off unit. The sustaining unit does not display the fast temporal adaptation as previously described in the on-off unit. As compared with the on-off unit, the sustaining unit has a high sensitivity to small contrasts. Although the sustaining unit continues spiking as long as the light is on, its response is also transient as it adapts rapidly after a change of intensity. The receptive field and the line spread function of the sustaining unit have a similar size and profile: a central lobe with a half-width of approximately 2° surrounded by a circular inhibitory zone located at about 3° off-axis.     

Visual signals in an optomotor reflex: systems and information theoretic analysis

Compensatory optomotor reflexes were examined in crayfish (Procambarus clarkii) with oscillating sine wave gratings and step displacements of a single stripe. A capacitance transducer was used to measure the rotation of the eyestalk about its longitudinal axis. System studies reveal a spatial frequency response independent of velocity and stimulus amplitude and linear contrast sensitivity similar to that of neurons in the visual pathway. The reflex operates at low temporal frequencies (<0.002 Hz to 0.5 Hz) and exhibits a low-pass temporal frequency response with cut-off frequency of 0.1 Hz. Eyestalk rotation increases as a saturable function of the angular stimulus displacement. When compared to the oscillatory response, transient responses are faster, and they exhibit a lower gain for large stimulus displacements. These differences may reflect system nonlinearity and/or the presence of at least two classes of afferents in the visual pathway. Our metric for information transmission is the Kullback-Leibler (K-L) distance, which is inversely proportional to the probability of an error in distinguishing two stimuli. K-L distances are related to differences in responsiveness for variations in spatial frequency, contrast, and angular displacement. The results are interpreted in terms of the neural filters that shape the system response and the constraints that the K-L distances place on information transmission in the afferent visual pathway.     

Superfast vocal muscles control song production in songbirds

Birdsong is a widely used model for vocal learning and human speech, which exhibits high temporal and acoustic diversity. Rapid acoustic modulations are thought to arise from the vocal organ, the syrinx, by passive interactions between the two independent sound generators or intrinsic nonlinear dynamics of sound generating structures. Additionally, direct neuromuscular control could produce such rapid and precisely timed acoustic features if syringeal muscles exhibit rare superfast muscle contractile kinetics. However, no direct evidence exists that avian vocal muscles can produce modulations at such high rates. Here, we show that 1) syringeal muscles are active in phase with sound modulations during song over 200 Hz, 2) direct stimulation of the muscles in situ produces sound modulations at the frequency observed during singing, and that 3) syringeal muscles produce mechanical work at the required frequencies and up to 250 Hz in vitro. The twitch kinematics of these so-called superfast muscles are the fastest measured in any vertebrate muscle. Superfast vocal muscles enable birds to directly control the generation of many observed rapid acoustic changes and to actuate the millisecond precision of neural activity into precise temporal vocal control. Furthermore, birds now join the list of vertebrate classes in which superfast muscle kinetics evolved independently for acoustic communication.     

Characteristics of Gamma-Oscillations in Responses of Neurons of the Cat Lateral Geniculate Body

There were studied characteristics of gamma-oscillations in responses of neurons of the lateral geniculate body (LGB) in cat to exposure in their receptive fields (RF) of half-tone and binary test images. The gamma-oscillations were observed in 38.8% of cases (69 cells). The spectral characteristics (SC) (the band 20–100 Hz) of the neuronal responses to adequate stimuli (on- and off-responses correspondingly of on- and off-neurons) were analyzed. The total of 5930 poststimulus histograms (PSTH) of responses constructed from 177 900 neuronal impulse responses were considered. The mean value of the SC dominant frequencies of the whole sample of the neuronal responses amounted to 44.74 ± 21.46 Hz. In this cell sample, the neurons were revealed, which generated oscillations with markedly different frequencies in response to the same stimuli. Based on this property, three types of neurons were determined, with the mean oscillation frequencies of 26.95 ± 4.35, 52.02 ± 9.05, and 85.79 ± 7.19 Hz. The histograms of distribution of peak frequency values in SC of the neuronal responses and of index values of these oscillation peaks also revealed three maxima that corresponded to the frequencies of the three described types of neurons. The mean values of dominant frequencies of gamma-oscillations in responses of all three types of neurons remained constant (within the limits of dispersion) at changes of spatial-brightness parameters of test stimuli as well as at changes of the neuronal excitation level (the number of impulses in responses). The oscillation index values of dominant frequencies depended on parameters of the test images and correlated with the neuronal excitation level (the coefficient of correlation was 0.78 from data of 5930 CX). The suggestion is made about the existence in the neuronal network of the synchronization mechanisms functioning on the principle of multiple synchronization.      

Influence of sound pressure level on the processing of amplitude modulations by auditory neurons of the locust

Typical features of natural sounds are amplitude changes at different time scales. In many species, amplitude modulations constitute decisive cues to recognize communication signals. Since these signals should be recognizable over a broad intensity range, we investigated how the encoding of amplitude modulations by auditory neurons depends on sound pressure level. Identified neurons that represent different processing stages in the locusts’ auditory pathway were stimulated with sinusoidal modulations of a broad band noise carrier, at different intensities, and characteristic parameters of modulation transfer functions (MTFs) were determined. The corner frequencies of temporal MTFs turned out to be independent of intensity for all neurons except one. Furthermore, for none of the neurons investigated corner frequencies were significantly correlated with spike rate, indicating a remarkable intensity invariance of the upper limits of temporal resolution. The shape of the tMTFs changed with increasing intensity from a low-pass to a band-pass for receptors and local neurons, while no consistent change was observed for ascending neurons. The best modulation frequency depended on intensity and spike rate, especially for receptors and local neurons. Remarkably, the adaptation state of some neurons turned out to be independent of the spike rate during the modulation part of the stimulus.     

Profound contrast adaptation early in the visual pathway

Prior exposure to a moving grating of high contrast led to a substantial and persistent reduction in the contrast sensitivity of neurons in the lateral geniculate nucleus (LGN) of macaque. This slow contrast adaptation was potent in all magnocellular (M) cells but essentially absent in parvocellular (P) cells and neurons that received input from S cones. Simultaneous recordings of M cells and the potentials of ganglion cells driving them showed that adaptation originated in ganglion cells. As expected from the spatiotemporal tuning of M cells, adaptation was broadly tuned for spatial frequency and lacked orientation selectivity. Adaptation could be induced by high temporal frequencies to which cortical neurons do not respond, but not by low temporal frequencies that can strongly adapt cortical neurons. Our observations confirm that contrast adaptation occurs at multiple levels in the visual system, and they provide a new way to reveal the function and perceptual significance of the M pathway.     

Membrane potential synchrony in primary visual cortex during sensory stimulation

When the primary visual cortex (V1) is activated by sensory stimulation, what is the temporal correlation between the synaptic inputs to nearby neurons? This question underlies the origin of correlated activity, the mechanism of how visually evoked activity emerges and propagates in cortical circuits, and the relationship between spontaneous and evoked activity. Here, we have recorded membrane potential from pairs of V1 neurons in anesthetized cats and found that visual stimulation suppressed low-frequency membrane potential synchrony (0-10 Hz), and often increased synchrony at high frequencies (20-80 Hz). The increase in high-frequency synchrony occurred for neurons with similar orientation preferences and for neurons with different orientation preferences and occurred for a wide range of stimulus orientations. Thus, while only a subset of neurons spike in response to visual stimulation, a far larger proportion of the circuit is correlated with spiking activity through subthreshold, high-frequency synchronous activity that crosses functional domains.     

Impact of adaptation currents on synchronization of coupled exponential integrate-and-fire neurons

The ability of spiking neurons to synchronize their activity in a network depends on the response behavior of these neurons as quantified by the phase response curve (PRC) and on coupling properties. The PRC characterizes the effects of transient inputs on spike timing and can be measured experimentally. Here we use the adaptive exponential integrate-and-fire (aEIF) neuron model to determine how subthreshold and spike-triggered slow adaptation currents shape the PRC. Based on that, we predict how synchrony and phase locked states of coupled neurons change in presence of synaptic delays and unequal coupling strengths. We find that increased subthreshold adaptation currents cause a transition of the PRC from only phase advances to phase advances and delays in response to excitatory perturbations. Increased spike-triggered adaptation currents on the other hand predominantly skew the PRC to the right. Both adaptation induced changes of the PRC are modulated by spike frequency, being more prominent at lower frequencies. Applying phase reduction theory, we show that subthreshold adaptation stabilizes synchrony for pairs of coupled excitatory neurons, while spike-triggered adaptation causes locking with a small phase difference, as long as synaptic heterogeneities are negligible. For inhibitory pairs synchrony is stable and robust against conduction delays, and adaptation can mediate bistability of in-phase and anti-phase locking. We further demonstrate that stable synchrony and bistable in/anti-phase locking of pairs carry over to synchronization and clustering of larger networks. The effects of adaptation in aEIF neurons on PRCs and network dynamics qualitatively reflect those of biophysical adaptation currents in detailed Hodgkin-Huxley-based neurons, which underscores the utility of the aEIF model for investigating the dynamical behavior of networks. Our results suggest neuronal spike frequency adaptation as a mechanism synchronizing low frequency oscillations in local excitatory networks, but indicate that inhibition rather than excitation generates coherent rhythms at higher frequencies.     

Adaptation of trigeminal ganglion cells to periodic whisker deflections

Trigeminal ganglion neurons in adult rats adapt to periodic whisker deflections in the range of 1-40 Hz, manifested as a reduction in spike counts to progressively later stimuli in a train of pulsatile or sinusoidal deflections. For high velocity, pulsatile deflections, adaptation is time- and frequency-dependent; as in the case of thalamic and cortical neurons, adaptation is greater at higher stimulus frequencies. With slower velocity, sinusoidal movements, trigeminal ganglion cells differ from central neurons, however, by exhibiting strong adaptation even at low frequencies. For both types of stimuli, effects in trigeminal ganglion neurons were more pronounced in rats maintained during the recording session under neuromuscular blockade than in non-paralysed animals. Results are consistent with previous findings in other systems that frequency-dependent adaptation of cutaneous primary afferent neurons is affected by mechanical properties of the skin. Such effects are likely to vary depending on the nature of the whisker stimuli and physiological states that affect skin viscoelasticity.     

Adaptation of trigeminal ganglion cells to periodic whisker deflections

Trigeminal ganglion neurons in adult rats adapt to periodic whisker deflections in the range of 1–40?Hz, manifested as a reduction in spike counts to progressively later stimuli in a train of pulsatile or sinusoidal deflections. For high velocity, pulsatile deflections, adaptation is time- and frequency-dependent; as in the case of thalamic and cortical neurons, adaptation is greater at higher stimulus frequencies. With slower velocity, sinusoidal movements, trigeminal ganglion cells differ from central neurons, however, by exhibiting strong adaptation even at low frequencies. For both types of stimuli, effects in trigeminal ganglion neurons were more pronounced in rats maintained during the recording session under neuromuscular blockade than in non-paralysed animals. Results are consistent with previous findings in other systems that frequency-dependent adaptation of cutaneous primary afferent neurons is affected by mechanical properties of the skin. Such effects are likely to vary depending on the nature of the whisker stimuli and physiological states that affect skin viscoelasticity.     

Frequency dependence of the action-perception cycle for postural control in a moving visual environment: relative phase dynamics

When standing human subjects are exposed to a moving visual environment, the induced postural sway displays varying degrees of coherence with the visual information. In our experiment we varied the frequency of an oscillatory visual display and analysed the temporal relationship between visual motion and sway. We found that subjects maintain sizeable sway amplitudes even as temporal coherence with the display is lost. Postural sway tended to phase lead (for frequencies below 0.2 Hz) or phase lag (above 0.3 Hz). However, we also observed at a fixed frequency, highly variable phase relationships in which a preferred range of phase lags is prevalent, but phase jumps occur that return the system into the preferred range after phase has begun drifting out of the preferred regime. By comparing the results quantitatively with a dynamical model (the sine-circle map), we show that this effect can be understood as a form of relative coordination and arises through an instability of the dynamics of the action-perception cycle. Because such instabilities cannot arise in passively driven systems, we conclude that postural sway in this situation is actively generated as rhythmic movement which is coupled dynamically to the visual motion. Received: 7 September 1993/Accepted in revised form: 2 May 1994     

Visual capacities of the owl monkey (Aotus trivirgatus): temporal contrast sensitivity.

Aotus monkeys were tested in a forced-choice discrimination task to determine their ability to discriminate sinusoidally flickering lights varying in temporal frequency and luminance contrast. Under conditions of moderate light adaptation this primate is maximally sensitive to lights flickering at 10 Hz while the highest frequency they can discriminate is about 42 Hz. At very low light levels (10(-5) ft L) maximum sensitivity is for 2.2--5 Hz flicker. The highest flicker rate that could be discriminated under these conditons was about 29 Hz. In comparison to humans tested in the same situation. Aotus monkeys show relatively lower sensitivity to temporal flicker under conditions of light adaptation but relatively higher sensitivity at very low light levels.     

Directionality of auditory nerve fiber responses to pure tone stimuli in the grassfrog, Rana temporaria. II. Spike timing

We studied the directionality of spike timing in the responses of single auditory nerve fibers of the grass frog, Rana temporaria, to tone burst stimulation. Both the latency of the first spike after stimulus onset and the preferred firing phase during the stimulus were studied. In addition, the directionality of the phase of eardrum vibrations was measured. The response latency showed systematic and statistically significant changes with sound direction at both low and high frequencies. The latency changes were correlated with response strength (spike rate) changes and were probably the result of directional changes in effective stimulus intensity. Systematic changes in the preferred firing phase were seen in all fibers that showed phaselocking (i.e., at frequencies below 500–700 Hz). The mean phase lead for stimulation from the contralateral side was approximately 140° at 200 Hz and decreased to approximately 100° at 700 Hz. These phaseshifts correspond to differences in spike timing of approximately 2 ms and 0.4 ms respectively. The phaseshifts were nearly independent of stimulus intensity. The phase directionality of eardrum vibrations was smaller than that of the nerve fibers. Hence, the strong directional phaseshifts shown by the nerve fibers probably reflect the directional characteristics of extratympanic pathways. Accepted: 23 November 1996