A rapid evoked potential index of cortical adaptation

Contrast thresholds and acuity limits were measured in 4 observers with the swept visual evoked potential (VEP) technique. In this technique, grating contrast or grating spatial frequency is electronically varied while the subject's evoked response is retrieved in real time (without averaging). Contrast or spatial frequency variation make the stimulus vary in intensity; zero VEP response amplitude indicates the threshold intensity.Large shifts occur in the indicated threshold when stimulus sweep direction is reversed. Thresholds are always relatively elevated when the run begins with the strongest stimulus value. These shifts do not have a technical origin in the delay of the instrument (Nelson et al. 1984b). Here, it is shown that the shifts are due to orientation and spatial frequency selective adaptation, probably of cortical origin.Measurable adaptation is produced by momentary exposure to contrasts as low as 1.25%; nearly maximum adaptation (0.6 log units) is reached with 20% contrast. These findings support the concept of a contrast gain control mechanism in visual cortex, and pose practical problems for visual assessment with the evoked potential.     

抑制性整合野细胞的对比度响应函数研究

采用细胞外记录的方法,在单独刺激经典感受野(classical receptive field,CRF)或同时刺激CRF和感受野外区域(extra-receptive field,ERF)的情况下,测量了猫初级视觉皮层细胞的对比度响应函数。当刺激所用的中心和外周运动光栅的参数一致时,与仅刺激CRF相比,强的ERF抑制使对比度响应函数动态区增加,响应增益和对比度增益降低。当中心和外周光栅的方位相差90度时,与方位参数一致的情况相比,大部分细胞的ERF抑制减弱,对比度响应函数的动态区减小,对比度增益和响应增益增加;少数细胞的ERF对CRF的作用从抑制变为易化,其对比度响应函数的动态区与只刺激CRF相比还要小,而对比度增益和响应增益还要大。揭示了初级视觉皮层细胞的抑制型整合野在CRF和ERF图像的方位及对比度差异检测中的作用机制。     

Adaptation-induced plasticity of orientation tuning in adult visual cortex

A key emergent property of the primary visual cortex (V1) is the orientation selectivity of its neurons. The extent to which adult visual cortical neurons can exhibit changes in orientation selectivity is unknown. Here we use single-unit recording and intrinsic signal imaging in V1 of adult cats to demonstrate systematic repulsive shifts in orientation preference following short-term exposure (adaptation) to one stimulus orientation. In contrast to the common view of adaptation as a passive process by which responses around the adapting orientation are reduced, we show that changes in orientation tuning also occur due to response increases at orientations away from the adapting stimulus. Adaptation-induced orientation plasticity is thus an active time-dependent process that involves network interactions and includes both response depression and enhancement.     

Adaptation to stimulus contrast and correlations during natural visual stimulation

In this study, we characterize the adaptation of neurons in the cat lateral geniculate nucleus to changes in stimulus contrast and correlations. By comparing responses to high- and low-contrast natural scene movie and white noise stimuli, we show that an increase in contrast or correlations results in receptive fields with faster temporal dynamics and stronger antagonistic surrounds, as well as decreases in gain and selectivity. We also observe contrast- and correlation-induced changes in the reliability and sparseness of neural responses. We find that reliability is determined primarily by processing in the receptive field (the effective contrast of the stimulus), while sparseness is determined by the interactions between several functional properties. These results reveal a number of adaptive phenomena and suggest that adaptation to stimulus contrast and correlations may play an important role in visual coding in a dynamic natural environment.     

Attention to stimulus features shifts spectral tuning of V4 neurons during natural vision

Previous neurophysiological studies suggest that attention can alter the baseline or gain of neurons in extrastriate visual areas but that it cannot change tuning. This suggests that neurons in visual cortex function as labeled lines whose meaning does not depend on task demands. To test this common assumption, we used a system identification approach to measure spatial frequency and orientation tuning in area V4 during two attentionally demanding visual search tasks, one that required fixation and one that allowed free viewing during search. We found that spatial attention modulates response baseline and gain but does not alter tuning, consistent with previous reports. In contrast, feature-based attention often shifts neuronal tuning. These tuning shifts are inconsistent with the labeled-line model and tend to enhance responses to stimulus features that distinguish the search target. Our data suggest that V4 neurons behave as matched filters that are dynamically tuned to optimize visual search.     

Visual cells remember earlier applied target: plasticity of orientation selectivity

Background

A canonical proposition states that, in mature brain, neurons responsive to sensory stimuli are tuned to specific properties installed shortly after birth. It is amply demonstrated that that neurons in adult visual cortex of cats are orientation-selective that is they respond with the highest firing rates to preferred oriented stimuli.

Methodology/Principal Findings

In anesthetized cats, prepared in a conventional fashion for single cell recordings, the present investigation shows that presenting a stimulus uninterruptedly at a non-preferred orientation for twelve minutes induces changes in orientation preference. Across all conditions orientation tuning curves were investigated using a trial by trial method. Contrary to what has been previously reported with shorter adaptation duration, twelve minutes of adaptation induces mostly attractive shifts, i.e. toward the adapter. After a recovery period allowing neurons to restore their original orientation tuning curves, we carried out a second adaptation which produced three major results: (1) more frequent attractive shifts, (2) an increase of their magnitude, and (3) an additional enhancement of responses at the new or acquired preferred orientation. Additionally, we also show that the direction of shifts depends on the duration of the adaptation: shorter adaptation in most cases produces repulsive shifts, whereas adaptation exceeding nine minutes results in attractive shifts, in the same unit. Consequently, shifts in preferred orientation depend on the duration of adaptation.

Conclusion/Significance

The supplementary response improvements indicate that neurons in area 17 keep a memory trace of the previous stimulus properties, thereby upgrading cellular performance. It also highlights the dynamic nature of basic neuronal properties in adult cortex since repeated adaptations modified both the orientation tuning selectivity and the response strength to the preferred orientation. These enhanced neuronal responses suggest that the range of neuronal plasticity available to the visual system is broader than anticipated.     

Orientation sensitive properties of visually driven neurons in extrastriate area 21a of cat cortex

Orientation sensitive properties of extrastriate area 21a neurons were investigated. Special attention was paid to the qualitative characteristics of neuron responses to the different orientations of visual stimulus motion across neuron classical receptive fields (CRF). The results of experiments have shown that a group of neurons (31%) in area 21a with specialized responses to moving visual stimuli changed their direction selective (DS) characteristics depending on the orientation of the stimulus movement. Some neurons reveal an abrupt drop of the direction sensitivity index (DI) to certain orientation (58%), and some show significant increase of DI at one of applied orientations of stimulus motion (22%). Detailed investigation of response patterns of non-directional neurons to different orientations of stimulus motion have revealed clear-cut qualitative differences, such as different regularities in the distribution of inter-peak inhibitory intervals in the response pattern in dependence of the orientation of stimulus motion. The investigation of neuron CRF stationary functional organization did not reveal correlations between RF's spatial functional organization, and that of qualitative modulations of neuron response patterns. A suggestion was put forward, that visual information central processing of orientation discrimination is a complex integrative process that includes quantitative as well as qualitative transformations of neuron activity.     

Adaptation accentuates responses of fly motion-sensitive visual neurons to sudden stimulus changes

Adaptation in sensory and neuronal systems usually leads to reduced responses to persistent or frequently presented stimuli. In contrast to simple fatigue, adapted neurons often retain their ability to encode changes in stimulus intensity and to respond when novel stimuli appear. We investigated how the level of adaptation of a fly visual motion-sensitive neuron affects its responses to discontinuities in the stimulus, i.e. sudden brief changes in one of the stimulus parameters (velocity, contrast, grating orientation and spatial frequency). Although the neuron''s overall response decreased gradually during ongoing motion stimulation, the response transients elicited by stimulus discontinuities were preserved or even enhanced with adaptation. Moreover, the enhanced sensitivity to velocity changes by adaptation was not restricted to a certain velocity range, but was present regardless of whether the neuron was adapted to a baseline velocity below or above its steady-state velocity optimum. Our results suggest that motion adaptation helps motion-sensitive neurons to preserve their sensitivity to novel stimuli even in the presence of strong tonic stimulation, for example during self-motion.     

Attention increases sensitivity of V4 neurons

When attention is directed to a location in the visual field, sensitivity to stimuli at that location is increased. At the neuronal level, this could arise either through a multiplicative increase in firing rate or through an increase in the effective strength of the stimulus. To test conflicting predictions of these alternative models, we recorded responses of V4 neurons to stimuli across a range of luminance contrasts and measured the change in response when monkeys attended to them in order to discriminate a target stimulus from nontargets. Attention caused greater increases in response at low contrast than at high contrast, consistent with an increase in effective stimulus strength. On average, attention increased the effective contrast of the attended stimulus by a factor of 1.51, an increase of 51% of its physical contrast.     

Input-output transformation in the visuo-oculomotor loop: comparison of real-time optical imaging recordings in V1 to ocular following responses upon center-surround stimulation

In psychophysics and physiology, it is well established that lateral interactions are crucial mechanisms to constrain response normalization and contextual modulations. To study the cortical mechanisms involved in the contextual modulation of the behavioral contrast response function, we compared in behaving monkeys the Ocular Following Response (OFR) to V1 population activity measured using Optical Imaging of Voltage-Sensitive Dyes (VSD). If contrast response functions (CRF) to a simple local stimulus are similar in V1 and in the OFR, lateral interaction leads however to quite different modulation at those two levels. At the behavioural level, contrast response function is strongly suppressed by lateral interactions, and this suppression is stronger for higher contrasts. In V1, we showed a slow dynamic of facilitation for low contrasts integration and a fast suppression operating on high contrasts. These modulatory interactions influence differently the contrast response functions, interrupting the dynamic increase of contrast sensitivity in OFR, but not in V1 response. The temporal properties of those effects lead us to hypothesize that horizontal and feedback connectivity have differential effect on low and high contrasts integration in V1. V1 provides then an input to MT whose contextual dependency is not totally determined and must be refined before affecting the behavioural OFR.     

Magno- and Parvocellular Contrast Responses in Varying Degrees of Autistic Trait

Autistic tendency has been associated with altered visual perception, especially impaired visual motion sensitivity and global/local integration, as well as enhanced visual search and local shape recognition. However, the neurophysiological mechanisms underlying these abnormalities remain poorly defined. The current study recruited 29 young adults displaying low, middle or high autistic trait as measured by Baron-Cohen''s Autism spectrum Quotient (AQ), and measured motion coherence thresholds psychophysically, with manipulation of dot lifetime and stimulus contrast, as well as nonlinear cortical visual evoked potentials (VEPs) over a range of temporal luminance contrast levels from 10% to 95%. Contrast response functions extracted from the major first order and second order Wiener kernel peaks of the VEPs showed consistent variation with AQ group, and Naka-Rushton fits enabled contrast gain and semi-saturation contrasts to be elicited for each peak. A short latency second order response (previously associated with magnocellular processing) with high contrast gain and a saturating contrast response function showed higher amplitude for the High AQ (compared with Mid and Low groups) indicating poorer neural recovery after rapid stimulation. A non-linearity evoked at longer interaction times (previously associated with parvocellular processing) with no evidence of contrast saturation and lower contrast gain showed no difference between autism quotient groups across the full range of stimulus contrasts. In addition, the short latency first order response and a small, early second order second slice response showed gain and semi-saturation parameters indicative of magnocellular origin, while the longer latency first order response probably reflects a mixture of inputs (including feedback from higher cortical areas). Significant motion coherence (AQ group) * (dot lifetime) interactions with higher coherence threshold for limited dot lifetime stimuli is consistent with atypical magnocellular functioning, however psychophysical performance for those with High AQ is not explained fully, suggesting that other factors may be involved.     

Temporal processing and adaptation in the songbird auditory forebrain

Songbird auditory neurons must encode the dynamics of natural sounds at many volumes. We investigated how neural coding depends on the distribution of stimulus intensities. Using reverse-correlation, we modeled responses to amplitude-modulated sounds as the output of a linear filter and a nonlinear gain function, then asked how filters and nonlinearities depend on the stimulus mean and variance. Filter shape depended strongly on mean amplitude (volume): at low mean, most neurons integrated sound over many milliseconds, while at high mean, neurons responded more to local changes in amplitude. Increasing the variance (contrast) of amplitude modulations had less effect on filter shape but decreased the gain of firing in most cells. Both filter and gain changes occurred rapidly after a change in statistics, suggesting that they represent nonlinearities in processing. These changes may permit neurons to signal effectively over a wider dynamic range and are reminiscent of findings in other sensory systems.     

Attentional modulation strength in cortical area MT depends on stimulus contrast

The attentional modulation of sensory information processing in the visual system is the result of top-down influences, which can cause a multiplicative modulation of the firing rate of sensory neurons in extrastriate visual cortex, an effect reminiscent of the bottom-up effect of changes in stimulus contrast. This similarity could simply reflect the multiplicity of both effects. But, here we show that in direction-selective neurons in monkey visual cortical area MT, stimulus and attentional effects share a nonlinearity. These neurons show higher response gain for both contrast and attentional changes for intermediate contrast stimuli and smaller gain for low- and high-contrast stimuli. This finding suggests a close relationship between the neural encoding of stimulus contrast and the modulating effect of the behavioral relevance of stimuli.     

Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors

Response properties of short-type (R1-6) photoreceptors of the blowfly (Calliphora vicina) were investigated with intracellular recordings using repeated sequences of pseudorandomly modulated light contrast stimuli at adapting backgrounds covering 5 log intensity units. The resulting voltage responses were used to determine the effects of adaptational regulation on signal-to-noise ratios (SNR), signal induced noise, contrast gain, linearity and the dead time in phototransduction. In light adaptation the SNR of the photoreceptors improved more than 100-fold due to (a) increased photoreceptor voltage responses to a contrast stimulus and (b) reduction of voltage noise at high intensity backgrounds. In the frequency domain the SNR was attenuated in low frequencies with an increase in the middle and high frequency ranges. A pseudorandom contrast stimulus by itself did not produce any additional noise. The contrast gain of the photoreceptor frequency responses increased with mean illumination and the gain was best fitted with a model consisting of two second order and one double pole of first order. The coherence function (a normalized measure of linearity and SNR) of the frequency responses demonstrated that the photoreceptors responded linearly (from 1 to 150 Hz) to the contrast stimuli even under fairly dim conditions. The theoretically derived and the recorded phase functions were used to calculate phototransduction dead time, which decreased in light adaptation from approximately 5-2.5 ms. This analysis suggests that the ability of fly photoreceptors to maintain linear performance under dynamic stimulation conditions results from the high early gain followed by delayed compressive feed-back mechanisms.     

Representation of color stimuli in awake macaque primary visual cortex

We investigated the responses of single neurons in primary visual cortex (area V1) of awake monkeys to chromatic stimuli. Chromatic tuning properties, determined for homogeneous color patches presented on a neutral gray background, varied strongly between cells. The continuum of preferred chromaticities and tuning widths indicated a distributed representation of color signals in V1. When stimuli were presented on colored backgrounds, chromatic tuning was different in most neurons, and the changes in tuning were consistent with some degree of sensitivity of the neurons to the chromatic contrast between stimulus and background. Quantitatively, the average response changes matched the magnitudes of color induction effects measured in human subjects under corresponding stimulus conditions.     

Network Adaptation Improves Temporal Representation of Naturalistic Stimuli in Drosophila Eye: I Dynamics

Because of the limited processing capacity of eyes, retinal networks must adapt constantly to best present the ever changing visual world to the brain. However, we still know little about how adaptation in retinal networks shapes neural encoding of changing information. To study this question, we recorded voltage responses from photoreceptors (R1–R6) and their output neurons (LMCs) in the Drosophila eye to repeated patterns of contrast values, collected from natural scenes. By analyzing the continuous photoreceptor-to-LMC transformations of these graded-potential neurons, we show that the efficiency of coding is dynamically improved by adaptation. In particular, adaptation enhances both the frequency and amplitude distribution of LMC output by improving sensitivity to under-represented signals within seconds. Moreover, the signal-to-noise ratio of LMC output increases in the same time scale. We suggest that these coding properties can be used to study network adaptation using the genetic tools in Drosophila, as shown in a companion paper (Part II).     

Stimulus-Response-Outcome Coding in the Pigeon Nidopallium Caudolaterale

A prerequisite for adaptive goal-directed behavior is that animals constantly evaluate action outcomes and relate them to both their antecedent behavior and to stimuli predictive of reward or non-reward. Here, we investigate whether single neurons in the avian nidopallium caudolaterale (NCL), a multimodal associative forebrain structure and a presumed analogue of mammalian prefrontal cortex, represent information useful for goal-directed behavior. We subjected pigeons to a go-nogo task, in which responding to one visual stimulus (S+) was partially reinforced, responding to another stimulus (S–) was punished, and responding to test stimuli from the same physical dimension (spatial frequency) was inconsequential. The birds responded most intensely to S+, and their response rates decreased monotonically as stimuli became progressively dissimilar to S+; thereby, response rates provided a behavioral index of reward expectancy. We found that many NCL neurons'' responses were modulated in the stimulus discrimination phase, the outcome phase, or both. A substantial fraction of neurons increased firing for cues predicting non-reward or decreased firing for cues predicting reward. Interestingly, the same neurons also responded when reward was expected but not delivered, and could thus provide a negative reward prediction error or, alternatively, signal negative value. In addition, many cells showed motor-related response modulation. In summary, NCL neurons represent information about the reward value of specific stimuli, instrumental actions as well as action outcomes, and therefore provide signals useful for adaptive behavior in dynamically changing environments.     

Adaptation to contingencies in macaque primary visual cortex.

We tested the hypothesis that neurons in the primary visual cortex (V1) adapt selectively to contingencies in the attributes of visual stimuli. We recorded from single neurons in macaque V1 and measured the effects of adaptation either to the sum of two gratings (compound stimulus) or to the individual gratings. According to our hypothesis, there would be a component of adaptation that is specific to the compound stimulus. In a first series of experiments, the two gratings differed in orientation. One grating had optimal orientation and the other was orthogonal to it, and therefore did not activate the neuron under study. These experiments provided evidence in favour of our hypothesis. In most cells adaptation to the compound stimulus reduced responses to the compound stimulus more than it reduced responses to the optimal grating, and the responses to the compound stimulus were reduced more by adaptation to the compound stimulus than by adaptation to the individual gratings. This suggests that a component of adaptation was specific to (and caused by) the simultaneous presence of the two orientations in the compound stimulus. To test whether V1 neurons could adapt to other contingencies in the stimulus attributes, we performed a second series of experiments, in which the component gratings were parallel but differed in spatial frequency, and were both effective in activating the neuron under study. These experiments failed to reveal convincing contingent effects of adaptation, suggesting that neurons cannot adapt equally well to all types of contingency.     

Reorganization of Receptive Fields of Cortical Field 21a Neurons and Formation of Responses to Moving Visual Stimuli

Using extracellular recording of spike activity from single neurons of field 21a of the cat neocortex, we examined in detail the spatial organization of receptive fields (RFs) of such cells after conditions of presentation of an immobile blinking light spot (a static RF) and moving visual stimuli (dynamic RFs). As was shown, the excitability of different RF subfields of a group of neurons possessing homogeneous on–off organization of the static RF changes significantly depended on the contrast, shape, dimension, orientation, and direction of movement of the applied mobile visual stimulus. This is manifested in changes in the number of discharge centers and shifts of their spatial localization. A hypothesis on the possible role of synchronous activation of the neurons neighboring the cell under study in the formation of an additional neuronal mechanism providing specialization of neuronal responses is proposed.