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D Ferster

Publications and source records attributed to D Ferster.

At least 19 recordsLinked to original sources

Membrane potential and conductance changes underlying length tuning of cells in cat primary visual cortex.

Spike responses for many cells of cat primary visual cortex are optimized for the length of a drifting grating stimulus. Stimuli that are longer or shorter than this optimal length elicit submaximal spike responses. To investigate the mechanisms responsible for this length tuning, we have recorded intracellularly from visual cortical neurons in the cat while presenting drifting grating stimuli of varying lengths. We have found that the membrane potential responses of the cells also exhibit length tuning, but that the suppression of spike responses at lengths longer than the preferred is 30-50% stronger than the corresponding suppression of the membrane potential responses. This difference may be attributed to the effects of spike threshold. Furthermore, using steady injected currents, we have measured changes in the excitatory and inhibitory components of input conductance evoked by stimuli of different lengths. We find that, compared with optimal stimuli, long stimuli evoke both an increase in inhibitory conductance and a decrease in excitatory conductance. These two mechanisms differ in their contrast sensitivity, resulting in stronger end stopping and shorter optimal lengths for high-contrast stimuli. These patterns suggest that response suppression for long stimuli is generated by a combination of active inhibition from stimuli outside the excitatory receptive field, as well as decreased excitation from other cortical cells that are themselves end-inhibited.

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Sleeper's wake.

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Prediction of orientation selectivity from receptive field architecture in simple cells of cat visual cortex.

From the intracellularly recorded responses to small, rapidly flashed spots, we have quantitatively mapped the receptive fields of simple cells in the cat visual cortex. We then applied these maps to a feedforward model of orientation selectivity. Both the preferred orientation and the width of orientation tuning of the responses to oriented stimuli were well predicted by the model. Where tested, the tuning curve was well predicted at different spatial frequencies. The model was also successful in predicting certain features of the spatial frequency selectivity of the cells. It did not successfully predict the amplitude of the responses to drifting gratings. Our results show that the spatial organization of the receptive field can account for a large fraction of the orientation selectivity of simple cells.

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Dynamics of the orientation-tuned membrane potential response in cat primary visual cortex.

Neurons in the primary visual cortex are highly selective for stimulus orientation, whereas their thalamic inputs are not. Much controversy has been focused on the mechanism by which cortical orientation selectivity arises. Although an increasing amount of evidence supports a linear model in which orientation selectivity is conferred upon visual cortical cells by the alignment of the receptive fields of their thalamic inputs, the controversy has recently been rekindled with the suggestion that late cortical input--delayed by multiple synapses--could lead to sharpening of orientation selectivity over time. Here we used intracellular recordings in vivo to examine temporal properties of the orientation-selective response to flashed gratings. Bayesian parameter estimation demonstrated that both preferred orientation and tuning width were stable throughout the response to a single stimulus.

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The contribution of noise to contrast invariance of orientation tuning in cat visual cortex.

Feedforward models of visual cortex appear to be inconsistent with a well-known property of cortical cells: contrast invariance of orientation tuning. The models' fixed threshold broadens orientation tuning as contrast increases, whereas in real cells tuning width is invariant with contrast. We have compared the orientation tuning of spike and membrane potential responses in single cells. Both are contrast invariant, yet a threshold-linear relation applied to the membrane potential accurately predicts the orientation tuning of spike responses. The key to this apparent paradox lies in the noisiness of the membrane potential. Responses that are subthreshold on average are still capable of generating spikes on individual trials. Unlike the iceberg effect, contrast invariance remains intact even as threshold narrows orientation selectivity. Noise may, by extension, smooth the average relation between membrane potential and spike rate throughout the brain.

Action Potentials↗

Membrane potential and firing rate in cat primary visual cortex.

We have investigated the relationship between membrane potential and firing rate in cat visual cortex and found that the spike threshold contributes substantially to the sharpness of orientation tuning. The half-width at half-height of the tuning of the spike responses was 23 +/- 8 degrees, compared with 38 +/- 15 degrees for the membrane potential responses. Direction selectivity was also greater in spike responses (direction index, 0.61 +/- 0.35) than in membrane potential responses (0.28 +/- 0.21). Threshold also increased the distinction between simple and complex cells, which is commonly based on the linearity of the spike responses to drifting sinusoidal gratings. In many simple cells, such stimuli evoked substantial elevations in the mean potential, which are nonlinear. Being subthreshold, these elevations would be hard to detect in the firing rate responses. Moreover, just as simple cells displayed various degrees of nonlinearity, complex cells displayed various degrees of linearity. We fitted the firing rates with a classic rectification model in which firing rate is zero at potentials below a threshold and grows linearly with the potential above threshold. When the model was applied to a low-pass-filtered version of the membrane potential (with spikes removed), the estimated values of threshold (-54.4 +/- 1.4 mV) and linear gain (7.2 +/- 0.6 spikes. sec(-1). mV(-1)) were similar across the population. The predicted firing rates matched the observed firing rates well and accounted for the sharpening of orientation tuning of the spike responses relative to that of the membrane potential. As it was for stimulus orientation, threshold was also independent of stimulus contrast. The rectification model accounted for the dependence of spike responses on contrast and, because of a stimulus-induced tonic hyperpolarization, for the response adaptation induced by prolonged stimulation. Because gain and threshold are unaffected by visual stimulation and by adaptation, we suggest that they are constant under all conditions.

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Stimulus dependence of two-state fluctuations of membrane potential in cat visual cortex.

Membrane potentials of cortical neurons fluctuate between a hyperpolarized ('down') state and a depolarized ('up') state which may be separated by up to 30 mV, reflecting rapid but infrequent transitions between two patterns of synaptic input. Here we show that such fluctuations may contribute to representation of visual stimuli by cortical cells. In complex cells of anesthetized cats, where such fluctuations are most prominent, prolonged visual stimulation increased the probability of the up state. This probability increase was related to stimulus strength: its dependence on stimulus orientation and contrast matched each cell's averaged membrane potential. Thus large fluctuations in membrane potential are not simply noise on which visual responses are superimposed, but may provide a substrate for encoding sensory information.

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Neural mechanisms of orientation selectivity in the visual cortex.

The origin of orientation selectivity in the responses of simple cells in cat visual cortex serves as a model problem for understanding cortical circuitry and computation. The feed-forward model posits that this selectivity arises simply from the arrangement of thalamic inputs to a simple cell. Much evidence, including a number of recent intracellular studies, supports a primary role of the thalamic inputs in determining simple cell response properties, including orientation tuning. This mechanism alone, however, cannot explain the invariance of orientation tuning to changes in stimulus contrast. Simple cells receive push-pull inhibition: ON inhibition in OFF subregions and vice versa. Addition of such inhibition to the feed-forward model can account for this contrast invariance, provided the inhibition is sufficiently strong. The predictions of "normalization" and "feedback" models are reviewed and compared with the predictions of this modified feed-forward model and with experimental results. The modified feed-forward and the feedback models ascribe fundamentally different functions to cortical processing.

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Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex.

The input conductance of cells in the cat primary visual cortex (V1) has been shown recently to grow substantially during visual stimulation. Because increasing conductance can have a divisive effect on the synaptic input, theoretical proposals have ascribed to it specific functions. According to the veto model, conductance increases would serve to sharpen orientation tuning by increasing most at off-optimal orientations. According to the normalization model, conductance increases would control the cell's gain, by being independent of stimulus orientation and by growing with stimulus contrast. We set out to test these proposals and to determine the visual properties and possible synaptic origin of the conductance increases. We recorded the membrane potential of cat V1 cells while injecting steady currents and presenting drifting grating patterns of varying contrast and orientation. Input conductance grew with stimulus contrast by 20-300%, generally more in simple cells (40-300%) than in complex cells (20-120%), and in simple cells was strongly modulated in time. Conductance was invariably maximal for stimuli of the preferred orientation. Thus conductance changes contribute to a gain control mechanism, but the strength of this gain control does not depend uniquely on contrast. By assuming that the conductance changes are entirely synaptic, we further derived the excitatory and inhibitory synaptic conductances underlying the visual responses. In simple cells, these conductances were often arranged in push-pull: excitation increased when inhibition decreased and vice versa. Excitation and inhibition had similar preferred orientations and did not appear to differ in tuning width, suggesting that the intracortical synaptic inputs to simple cells of cat V1 originate from cells with similar orientation tuning. This finding is at odds with models where orientation tuning in simple cells is achieved by inhibition at off-optimal orientations or sharpened by inhibition that is more broadly tuned than excitation.

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Synchronous membrane potential fluctuations in neurons of the cat visual cortex.

We have recorded intracellularly from pairs of neurons less than 500 microm distant from one another in V1 of anesthetized cats. Cross-correlation of spontaneous fluctuations in membrane potential revealed significant correlations between the cells in each pair. This synchronization was not dependent on the occurrence of action potentials, indicating that it was not caused by mutual interconnections. The cells were synchronized continuously rather than for brief epochs. Much weaker correlations were found between the EEG and intracellular potentials, suggesting local, rather than global, synchrony. The highest correlation occurred among cells with similar connectivity from the LGN and similar receptive fields. During visual stimulation, correlations increased when both cells responded to the stimulus and decreased when neither cell responded.

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Strength and orientation tuning of the thalamic input to simple cells revealed by electrically evoked cortical suppression.

Is thalamic input to the visual cortex strong and well tuned for orientation, as predicted by Hubel and Wiesel's (1962) model of orientation selectivity in simple cells? We directly measured the size of the thalamic input to single simple cells intracellularly by combining electrical stimulation of the cortex with a briefly flashed visual stimulus. In nearby cells, the electrical stimulation evoked a long-lasting inhibition that prevented them from firing in response to the visual stimulus. The visually evoked excitatory postsynaptic potentials (EPSPs) recorded during the period of cortical suppression, therefore, reflected largely the thalamic input. In 16 neurons that received monosynaptic input from the thalamus, cortical suppression left 46% of normal visual response on average (12%-86% in range). In those cells tested, this remaining visual response was as well tuned for orientation as the normal response to the visual stimulus alone. We conclude that the thalamic input to cortical simple cells with monosynaptic input from the thalamus is strong and well tuned in orientation, and that the intracortical input does not appear to sharpen orientation tuning in these cells.

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A tonic hyperpolarization underlying contrast adaptation in cat visual cortex.

The firing rate responses of neurons in the primary visual cortex grow with stimulus contrast, the variation in the luminance of an image relative to the mean luminance. These responses, however, are reduced after a cell is exposed for prolonged periods to high-contrast visual stimuli. This phenomenon, known as contrast adaptation, occurs in the cortex and is not present at earlier stages of visual processing. To investigate the cellular mechanisms underlying cortical adaptation, intracellular recordings were performed in the visual cortex of cats, and the effects of prolonged visual stimulation were studied. Surprisingly, contrast adaptation barely affected the stimulus-driven modulations in the membrane potential of cortical cells. Moreover, it did not produce sizable changes in membrane resistance. The major effect of adaptation, evident both in the presence and in the absence of a visual stimulus, was a tonic hyperpolarization. Adaptation affects a class of synaptic inputs, most likely excitatory in nature, that exert a tonic influence on cortical cells.

Adaptation, Physiological↗

Direction selectivity of synaptic potentials in simple cells of the cat visual cortex.

Direction selectivity of synaptic potentials in simple cells of the cat visual cortex. J. Neurophysiol. 78: 2772-2789, 1997. The direction selectivity of simple cells in the visual cortex is generated at least in part by nonlinear mechanisms. If a neuron were spatially linear, its responses to moving stimuli could be predicted accurately from linear combinations of its responses to stationary stimuli presented at different positions within the receptive field. In extracellular recordings, this has not been found to be the case. Although the extracellular experiments demonstrate the presence of a nonlinearity, the cellular process underlying the nonlinearity, whether an early synaptic mechanism such as a shunting inhibition or simply the spike threshold at the output, is not known. To differentiate between these possibilities, we have recorded intracellularly from simple cells of the intact cat with the whole cell patch technique. A linear model of direction selectivity was used to analyze the synaptic potentials evoked by stationary sine-wave gratings. The model predicted the responses of cells to moving gratings with considerable accuracy. The degree of direction selectivity and the time course of the responses to moving gratings were both well matched by the model. The direction selectivity of the synaptic potentials was considerably smaller than that of the intracellularly recorded action potential, indicating that a nonlinear mechanism such as threshold enhances the direction selectivity of the cell's output over that of its synaptic inputs. At the input stage, however, the cells apparently sum their synaptic inputs in a highly linear fashion. A more constrained test of linearity of synaptic summation based on principal component analysis was applied to the responses of direction-selective cells to stationary gratings. The analysis confirms that the summation in these cells is highly linear. The principal component analysis is consistent with a model in which direction selectivity in cortical simple cells is generated by only two subunits, each with a different receptive-field position and response time course. The response time course for each of the two subunits is derived for four analyzed cells. Each derived subunit is linear in spatial summation, suggesting that the neurons that comprise each subunit are either geniculate X-cells or receive their primary synaptic input from X-cells. The amplitude of the response of each subunit is linearly related to the contrast of the stimulus. The subunits are nonlinear in the time domain, however: the response to a stationary stimulus whose contrast is modulated sinusoidally in time is nonsinusoidal. The principal component analysis does not exclude models of direction selectivity based on more than two subunits, but such higher-order models would have to include the constraint that the extra subunits form a smooth continuum of interpolation between the properties derived from the two subunit solution.

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Orientation selectivity of thalamic input to simple cells of cat visual cortex.

More than 30 years after Hubel and Wiesel first described orientation selectivity in the mammalian visual cortex, the mechanism that gives rise to this property is still controversial. Hubel and Wiesel proposed a simple model for the origin of orientation tuning, in which the circularly symmetrical receptive fields of neurons in the lateral geniculate nucleus that excite a cortical simple cell are arranged in rows. Since this model was proposed, several experiments and neuronal simulations have suggested that the connectivity between the lateral geniculate nucleus and the cortex is not well organized in an orientation-specific fashion, and that orientation tuning arises instead from extensive interactions within the cortex. To test these models we have recorded visually evoked synaptic potentials in simple cells while cooling the cortex, which largely inactivates the cortical network, but leaves geniculate synaptic input functional. We report that the orientation tuning of these potentials is almost unaffected by cooling the cortex, in agreement with Hubel and Wiesel's original proposal.

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Linearity of synaptic interactions in the assembly of receptive fields in cat visual cortex.

Recent extra- and intracellular recordings from simple cells in the striate cortex have led to the development of detailed models of how novel receptive field properties are generated by the neuronal circuitry of the cortex. The first stage in assembling simple receptive fields appears to be a linear combination of visual inputs. The output of the linear stage is then normalized by a contrast gain control mechanism. Finally, a threshold and expansive nonlinearity in the spike-generating mechanism enhances selectivity for stimulus features such as orientation, direction, and spatial frequency.

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