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.     

Top-Down Inputs Enhance Orientation Selectivity in Neurons of the Primary Visual Cortex during Perceptual Learning

Perceptual learning has been used to probe the mechanisms of cortical plasticity in the adult brain. Feedback projections are ubiquitous in the cortex, but little is known about their role in cortical plasticity. Here we explore the hypothesis that learning visual orientation discrimination involves learning-dependent plasticity of top-down feedback inputs from higher cortical areas, serving a different function from plasticity due to changes in recurrent connections within a cortical area. In a Hodgkin-Huxley-based spiking neural network model of visual cortex, we show that modulation of feedback inputs to V1 from higher cortical areas results in shunting inhibition in V1 neurons, which changes the response properties of V1 neurons. The orientation selectivity of V1 neurons is enhanced without changing orientation preference, preserving the topographic organizations in V1. These results provide new insights to the mechanisms of plasticity in the adult brain, reconciling apparently inconsistent experiments and providing a new hypothesis for a functional role of the feedback connections.     

Integration of local features into global shapes: monkey and human FMRI studies

The integration of local image features into global shapes was investigated in monkeys and humans using fMRI. An adaptation paradigm was used, in which stimulus selectivity was deduced by changes in the course of adaptation of a pattern of randomly oriented elements. Accordingly, we observed stronger activity when orientation changes in the adapting stimulus resulted in a collinear contour than a different random pattern. This selectivity to collinear contours was observed not only in higher visual areas that are implicated in shape processing, but also in early visual areas where selectivity depended on the receptive field size. These findings suggest that unified shape perception in both monkeys and humans involves multiple visual areas that may integrate local elements to global shapes at different spatial scales.     

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.     

Modulation of V1 Spike Response by Temporal Interval of Spatiotemporal Stimulus Sequence

The spike activity of single neurons of the primary visual cortex (V1) becomes more selective and reliable in response to wide-field natural scenes compared to smaller stimuli confined to the classical receptive field (RF). However, it is largely unknown what aspects of natural scenes increase the selectivity of V1 neurons. One hypothesis is that modulation by surround interaction is highly sensitive to small changes in spatiotemporal aspects of RF surround. Such a fine-tuned modulation would enable single neurons to hold information about spatiotemporal sequences of oriented stimuli, which extends the role of V1 neurons as a simple spatiotemporal filter confined to the RF. In the current study, we examined the hypothesis in the V1 of awake behaving monkeys, by testing whether the spike response of single V1 neurons is modulated by temporal interval of spatiotemporal stimulus sequence encompassing inside and outside the RF. We used two identical Gabor stimuli that were sequentially presented with a variable stimulus onset asynchrony (SOA): the preceding one (S1) outside the RF and the following one (S2) in the RF. This stimulus configuration enabled us to examine the spatiotemporal selectivity of response modulation from a focal surround region. Although S1 alone did not evoke spike responses, visual response to S2 was modulated for SOA in the range of tens of milliseconds. These results suggest that V1 neurons participate in processing spatiotemporal sequences of oriented stimuli extending outside the RF.     

Stability of cortical responses and the statistics of natural scenes.

The primary visual cortex (V1) of higher mammals contains maps of stimulus features; how these maps influence vision remains unknown. We have examined the functional significance of an asymmetry in the orientation map in cat V1, i.e., the fact that a larger area of V1 is preferentially activated by vertical and horizontal contours than by contours at oblique orientations. Despite the fact that neurons tuned to cardinal and oblique orientations have indistinguishable tuning characteristics, cardinal neurons remain more stable in their response properties after selective perturbation induced by adaptation. Similarly, human observers report different adaptation-induced changes in orientation tuning between cardinal and oblique axes. We suggest that the larger cortical area devoted to cardinal orientations imposes stability on the processing of cardinal contours during visual perception, by retaining invariant cortical responses along cardinal axes.     

Functional specialization of mouse higher visual cortical areas

The mouse is emerging as an important model for understanding how sensory neocortex extracts cues to guide behavior, yet little is known about how these cues are processed beyond primary cortical areas. Here, we used two-photon calcium imaging in awake mice to compare visual responses in primary visual cortex (V1) and in two downstream target areas, AL and PM. Neighboring V1 neurons had diverse stimulus preferences spanning five octaves in spatial and temporal frequency. By contrast, AL and PM neurons responded best to distinct ranges of stimulus parameters. Most strikingly, AL neurons preferred fast-moving stimuli while PM neurons preferred slow-moving stimuli. By contrast, neurons in V1, AL, and PM demonstrated similar selectivity for stimulus orientation but not for stimulus direction. Based on these findings, we predict that area AL helps guide behaviors involving fast-moving stimuli (e.g., optic flow), while area PM?helps guide behaviors involving slow-moving objects.     

Synaptic integration by V1 neurons depends on location within the orientation map

Neurons in the primary visual cortex (V1) are organized into an orientation map consisting of orientation domains arranged radially around "pinwheel centers" at which the representations of all orientations converge. We have combined optical imaging of intrinsic signals with intracellular recordings to estimate the subthreshold inputs and spike outputs of neurons located near pinwheel centers or in orientation domains. We find that neurons near pinwheel centers have subthreshold responses to all stimulus orientations but spike responses to only a narrow range of orientations. Across the map, the selectivity of inputs covaries with the selectivity of orientations in the local cortical network, while the selectivity of spike outputs does not. Thus, the input-output transformation performed by V1 neurons is powerfully influenced by the local structure of the orientation map.     

Sensitivity profile for orientation selectivity in the visual cortex of goggle-reared mice

It has been widely accepted that ocular dominance in the responses of visual cortical neurons can change depending on visual experience in a postnatal period. However, experience-dependent plasticity for orientation selectivity, which is another important response property of visual cortical neurons, is not yet fully understood. To address this issue, using intrinsic signal imaging and two-photon calcium imaging we attempted to observe the alteration of orientation selectivity in the visual cortex of juvenile and adult mice reared with head-mounted goggles, through which animals can experience only the vertical orientation. After one week of goggle rearing, the density of neurons optimally responding to the exposed orientation increased, while that responding to unexposed orientations decreased. These changes can be interpreted as a reallocation of preferred orientations among visually responsive neurons. Our obtained sensitivity profile for orientation selectivity showed a marked peak at 5 weeks and sustained elevation at 12 weeks and later. These features indicate the existence of a critical period between 4 and 7 weeks and residual orientation plasticity in adult mice. The presence of a dip in the sensitivity profile at 10 weeks suggests that different mechanisms are involved in orientation plasticity in childhood and adulthood.     

Learning strengthens the response of primary visual cortex to simple patterns

Training can significantly improve performance on even the most basic visual tasks, such as detecting a faint patch of light or determining the orientation of a bar (for reviews, see ). The neural mechanisms of visual learning, however, remain controversial. One simple way to improve behavior is to increase the overall neural response to the trained stimulus by increasing the number or gain of responsive neurons. Learning of this type has been observed in other sensory modalities, where training increases the number of receptive fields that cover the trained stimulus. Here, we show that visual learning can selectively increase the overall response to trained stimuli in primary visual cortex (V1). We used functional magnetic resonance imaging (fMRI) to measure neural signals before and after one month of practice at detecting very low-contrast oriented patterns. Training increased V1 response for practiced orientations relative to control orientations by an average of 39%, and the magnitude of the change in V1 correlated moderately well with the magnitude of changes in detection performance. The elevation of V1 activity by training likely results from an increase in the number of neurons responding to the trained stimulus or an increase in response gain.     

初级视皮层神经元响应反应与撤反应的朝向选择性

朝向选择性是初级视皮层(17区或V1)神经元的基本性质,在图形感知中起着关键作用.同时这些神经元对于持续时间大于100 ms的视觉刺激具有清晰的响应反应(Onset responses)和撤反应(Offset responses).以往的研究只关注响应反应的朝向选择性,而忽视了对撤反应的朝向选择性研究.我们比较了响应与撤反应的朝向调谐性质,大多数细胞的撤反应与响应反应基本上具有相似的最优朝向,而撤反应的朝向调谐宽度有窄于响应反应的趋势,撤反应的最优延迟普遍滞后于响应反应的最优延迟.撤反应的朝向选择性略强于响应反应和具有显著长的反应延迟提示,皮层内的反馈输入可能在形成撤反应的朝向选择性中起着作用.本研究揭示了撤反应的朝向选择性在刺激朝向的连续表征和主体在形状知觉的后期对朝向的精细区分中起着作用.     

老年猫视皮层细胞对刺激反应的对比敏感度下降伴随皮层内抑制作用减弱(英文)

对人类和动物的心理学研究证实,老年个体的视觉对比敏感度相对青年个体显著下降。为揭示其可能的神经机制,采用在体细胞外单细胞记录技术研究青、老年猫(Felis catus)初级视皮层(primary visual cortex,V1)细胞对不同视觉刺激对比度的调谐反应。结果显示,老年猫V1细胞对视觉刺激反应的平均对比敏感度比青年猫显著下降,这与灵长类报道的研究结果相一致,表明衰老影响视皮层细胞对视觉刺激反应的对比敏感度是灵长类和非灵长类哺乳动物中普遍存在的现象,并可能是介导老年性视觉对比敏感度下降的神经基础。另外,与青年猫相比,老年猫初级视皮层细胞对视觉刺激的反应性显著增强,信噪比下降,感受野显著增大,表明衰老导致的初级视皮层细胞对视觉刺激反应的对比敏感度下降伴随着皮层内抑制性作用减弱。     

Dietary Restriction Affects Neuronal Response Property and GABA Synthesis in the Primary Visual Cortex

Previous studies have reported inconsistent effects of dietary restriction (DR) on cortical inhibition. To clarify this issue, we examined the response properties of neurons in the primary visual cortex (V1) of DR and control groups of cats using in vivo extracellular single-unit recording techniques, and assessed the synthesis of inhibitory neurotransmitter GABA in the V1 of cats from both groups using immunohistochemical and Western blot techniques. Our results showed that the response of V1 neurons to visual stimuli was significantly modified by DR, as indicated by an enhanced selectivity for stimulus orientations and motion directions, decreased visually-evoked response, lowered spontaneous activity and increased signal-to-noise ratio in DR cats relative to control cats. Further, it was shown that, accompanied with these changes of neuronal responsiveness, GABA immunoreactivity and the expression of a key GABA-synthesizing enzyme GAD67 in the V1 were significantly increased by DR. These results demonstrate that DR may retard brain aging by increasing the intracortical inhibition effect and improve the function of visual cortical neurons in visual information processing. This DR-induced elevation of cortical inhibition may favor the brain in modulating energy expenditure based on food availability.     

Integrate-and-fire vs Poisson models of LGN input to V1 cortex: noisier inputs reduce orientation selectivity

One of the reasons the visual cortex has attracted the interest of computational neuroscience is that it has well-defined inputs. The lateral geniculate nucleus (LGN) of the thalamus is the source of visual signals to the primary visual cortex (V1). Most large-scale cortical network models approximate the spike trains of LGN neurons as simple Poisson point processes. However, many studies have shown that neurons in the early visual pathway are capable of spiking with high temporal precision and their discharges are not Poisson-like. To gain an understanding of how response variability in the LGN influences the behavior of V1, we study response properties of model V1 neurons that receive purely feedforward inputs from LGN cells modeled either as noisy leaky integrate-and-fire (NLIF) neurons or as inhomogeneous Poisson processes. We first demonstrate that the NLIF model is capable of reproducing many experimentally observed statistical properties of LGN neurons. Then we show that a V1 model in which the LGN input to a V1 neuron is modeled as a group of NLIF neurons produces higher orientation selectivity than the one with Poisson LGN input. The second result implies that statistical characteristics of LGN spike trains are important for V1’s function. We conclude that physiologically motivated models of V1 need to include more realistic LGN spike trains that are less noisy than inhomogeneous Poisson processes.     

Mathematical model for self-organization of direction columns in the primate middle temporal area

We attempted to reproduce modular structures for direction selectivity characteristic of the primate middle temporal area (MT) based on our thermodynamic model for the activity-dependent self-organization of neural networks. We assumed that excitatory afferent input to MT neurons arises from V1 and/or V2 neurons which are selective to both orientation of a visual stimulus and direction of its motion, and that such input is modifiable and becomes selectively connected through the process of self-organization. By contrast, local circuit connections within MT are unmodifiable and remain nonselectively connected (isotropic). The present simulations reproduced characteristic patterns of organization in the cortex of MT in that: (1) preferred directions of the afferent input gradually shifted, except for singularity lines where direction abruptly changed by 180°; (2) model MT neurons located between the singularity lines responded to unidirectionally moving stimuli, closely reflecting preferred direction of the afferent input; (3) neurons responding to stimuli moving in two opposite directions were located along the singularity lines; and (4) neurons responding to stimuli moving in any direction were clustered at the ends of the singularity lines. When the strength of the lateral inhibition was decreased, direction selectivity of MT neurons was reduced. Therefore, the lateral inhibition, even if isotropic, strengthens the direction selectivity of MT neurons. Expression of singularities changed depending on a parameter that represents the relative dominance of the direction selectivity to the orientation selectivity of the afferent input. When the direction selectivity was predominant, singularity points were formed, while when the orientation selectivity prevailed, the MT was covered by two-dimensional singularity networks. Line singularities similar to those experimentally observed were reproduced when these two types of selectivity were in balance. Received: 15 October 1992/Accepted in revised form: 27 June 1993     

Effects of Isoflurane Anesthesia on Ensemble Patterns of Ca2+ Activity in Mouse V1: Reduced Direction Selectivity Independent of Increased Correlations in Cellular Activity

Anesthesia affects brain activity at the molecular, neuronal and network level, but it is not well-understood how tuning properties of sensory neurons and network connectivity change under its influence. Using in vivo two-photon calcium imaging we matched neuron identity across episodes of wakefulness and anesthesia in the same mouse and recorded spontaneous and visually evoked activity patterns of neuronal ensembles in these two states. Correlations in spontaneous patterns of calcium activity between pairs of neurons were increased under anesthesia. While orientation selectivity remained unaffected by anesthesia, this treatment reduced direction selectivity, which was attributable to an increased response to the null-direction. As compared to anesthesia, populations of V1 neurons coded more mutual information on opposite stimulus directions during wakefulness, whereas information on stimulus orientation differences was lower. Increases in correlations of calcium activity during visual stimulation were correlated with poorer population coding, which raised the hypothesis that the anesthesia-induced increase in correlations may be causal to degrading directional coding. Visual stimulation under anesthesia, however, decorrelated ongoing activity patterns to a level comparable to wakefulness. Because visual stimulation thus appears to ‘break’ the strength of pairwise correlations normally found in spontaneous activity under anesthesia, the changes in correlational structure cannot explain the awake-anesthesia difference in direction coding. The population-wide decrease in coding for stimulus direction thus occurs independently of anesthesia-induced increments in correlations of spontaneous activity.     

Dynamics of orientation selectivity in the primary visual cortex and the importance of cortical inhibition

To test theories of orientation selectivity in primary visual cortex (V1), we have done experiments to measure the dynamics of orientation tuning of single neurons in the V1 cortex of macaque monkeys. Based on our dynamics results, we propose that a V1 cell's orientation selectivity is generated mainly by both tuned enhancement and global suppression. Enhancement near the preferred orientation is probably caused by feed-forward input from LGN (plus amplification by cortical-cortical interaction). Global suppression could be supplied by cortical inhibition. Additionally, in about 1/3 of V1 neurons (usually the most sharply tuned) there is tuned suppression, centered near the cell's preferred orientation but broader than tuned enhancement. These mechanisms also can explain important features of steady-state selectivity in the V1 neuron population. Furthermore, similar neuronal mechanisms may be used generally throughout the cerebral cortex.     

Contrast adaptation and representation in human early visual cortex

The human visual system can distinguish variations in image contrast over a much larger range than measurements of the static relationship between contrast and response in visual cortex would suggest. This discrepancy may be explained if adaptation serves to re-center contrast response functions around the ambient contrast, yet experiments on humans have yet to report such an effect. By using event-related fMRI and a data-driven analysis approach, we found that contrast response functions in V1, V2, and V3 shift to approximately center on the adapting contrast. Furthermore, we discovered that, unlike earlier areas, human V4 (hV4) responds positively to contrast changes, whether increments or decrements, suggesting that hV4 does not faithfully represent contrast, but instead responds to salient changes. These findings suggest that the visual system discounts slow uninformative changes in contrast with adaptation, yet remains exquisitely sensitive to changes that may signal important events in the environment.     

Motion adaptation distorts perceived visual position

After an observer adapts to a moving stimulus, texture within a stationary stimulus is perceived to drift in the opposite direction-the traditional motion aftereffect (MAE). It has recently been shown that the perceived position of objects can be markedly influenced by motion adaptation. In the present study, we examine the selectivity of positional shifts resulting from motion adaptation to stimulus attributes such as velocity, relative contrast, and relative spatial frequency. In addition, we ask whether spatial position can be modified in the absence of perceived motion. Results show that when adapting and test stimuli have collinear carrier gratings, the global position of the object shows a substantial shift in the direction of the illusory motion. When the carrier gratings of the adapting and test stimuli are orthogonal (a configuration in which no MAE is experienced), a global positional shift of similar magnitude is found. The illusory positional shift was found to be immune to changes in spatial frequency and to contrast between adapting and test stimuli-manipulations that dramatically reduce the magnitude of the traditional MAE. The lack of sensitivity for stimulus characteristics other than direction of motion suggests that a specialized population of cortical neurones, which are insensitive to changes in a number of rudimentary visual attributes, may modulate positional representation in lower cortical areas.     

Role of spike-frequency adaptation in shaping neuronal response to dynamic stimuli

Spike-frequency adaptation is the reduction of a neuron’s firing rate to a stimulus of constant intensity. In the locust, the Lobula Giant Movement Detector (LGMD) is a visual interneuron that exhibits rapid adaptation to both current injection and visual stimuli. Here, a reduced compartmental model of the LGMD is employed to explore adaptation’s role in selectivity for stimuli whose intensity changes with time. We show that supralinearly increasing current injection stimuli are best at driving a high spike count in the response, while linearly increasing current injection stimuli (i.e., ramps) are best at attaining large firing rate changes in an adapting neuron. This result is extended with in vivo experiments showing that the LGMD’s response to translating stimuli having a supralinear velocity profile is larger than the response to constant or linearly increasing velocity translation. Furthermore, we show that the LGMD’s preference for approaching versus receding stimuli can partly be accounted for by adaptation. Finally, we show that the LGMD’s adaptation mechanism appears well tuned to minimize sensitivity for the level of basal input. This article is part of a special issue on Neuronal Dynamics of Sensory Coding.