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.     

Development of direction selectivity in mouse cortical neurons

Previous studies of the ferret visual cortex indicate that the development of direction selectivity requires visual experience. Here, we used two-photon calcium imaging to study the development of direction selectivity in layer 2/3 neurons of the mouse visual cortex in vivo. Surprisingly, just after eye opening nearly all orientation-selective neurons were also direction selective. During later development, the number of neurons responding to drifting gratings increased in parallel with the fraction of neurons that were orientation, but not direction, selective. Our experiments demonstrate that direction selectivity develops normally in dark-reared mice, indicating that the early development of direction selectivity is independent of visual experience. Furthermore, remarkable functional similarities exist between the development of direction selectivity in cortical neurons and the previously reported development of direction selectivity in the mouse retina. Together, these findings provide strong evidence that the development of orientation and direction selectivity in the mouse brain is distinctly different from that in ferrets.     

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.     

Similarity of visual selectivity among clonally related neurons in visual cortex

Neurons in rodent visual cortex are organized in a salt-and-pepper fashion for orientation selectivity, but it is still unknown how this functional architecture develops. A recent study reported that the progeny of single cortical progenitor cells are preferentially connected in the postnatal cortex. If these neurons acquire similar selectivity through their connections, a salt-and-pepper organization may be generated, because neurons derived from different progenitors are intermingled in rodents. Here we investigated whether clonally related cells have similar preferred orientation by using a transgenic mouse, which labels all the progeny of single cortical progenitor cells. We found that preferred orientations of clonally related cells are similar to each other, suggesting that cell lineage is involved in the development of response selectivity of neurons in the cortex. However, not all clonally related cells share response selectivity, suggesting that cell lineage is not the only determinant of response selectivity.     

A Postnatal Critical Period for Orientation Plasticity in the Cat Visual Cortex

Orientation selectivity of primary visual cortical neurons is an important requisite for shape perception. Although numerous studies have been previously devoted to a question of how orientation selectivity is established and elaborated in early life, how the susceptibility of orientation plasticity to visual experience changes in time remains unclear. In the present study, we showed a postnatal sensitive period profile for the modifiability of orientation selectivity in the visual cortex of kittens reared with head-mounted goggles for stable single-orientation exposure. When goggle rearing (GR) started at P16-P30, 2 weeks of GR induced a marked over-representation of the exposed orientation, and 2 more weeks of GR consolidated the altered orientation maps. GR that started later than P50, in turn, induced the under-representation of the exposed orientation. Orientation plasticity in the most sensitive period was markedly suppressed by cortical infusion of NMDAR antagonist. The present study reveals that the plasticity and consolidation of orientation selectivity in an early life are dynamically regulated in an experience-dependent manner.     

Development of stimulus selectivity and functional organization in the suprasylvian visual cortex of the cat

We have recorded from single neurons in the medial bank of the middle suprasylvian sulcus (PMLS) of anaesthetized and paralysed cats aged between nine days and eight weeks. Visual responses were assessed qualitatively, by using conventional projected stimuli, and quantitatively for drifting, high-contrast gratings of optimum spatial and temporal frequencies, but varying in orientation and direction of drift. At 9 days of age, some cells in the PMLS were spontaneously active but in three long penetrations only one visually responsive neuron was isolated. Between 9 and 15 days there was a rapid increase in the proportion of responsive units, which first appeared in small clusters in the lower layers (IV, V, VI). During the second and third postnatal weeks, spontaneous activity and the strength of visual responses increased to adult levels, and the proportion of cells showing rapid habituation to visual stimulation decreased. Even before two weeks of age, at least 85% of responsive cells in the PMLS were selective, by quantitative criteria, for image motion along one particular axis, and a majority of these were clearly direction-selective (responding to movement in one direction significantly more strongly than to that in the opposite). By the end of the third postnatal week the proportion of units with strong direction preference reached adult levels. The selective cells were initially more broadly 'tuned', on average, for the direction of motion of a grating (mean half-width in animals of 10-12 days was 32.6 degrees), but the sharpness of tuning improved to reach the adult level (ca. 23 degrees) during the third postnatal week. In animals younger than three weeks a slightly smaller proportion of cells than in adults (but always more than one third of all visually responsive cells) responded to stationary, contrast-modulated gratings. The majority of these cells showed clear selectivity for the orientation of a flashed grating. A few 'non-selective' cells were found in the youngest animals but by the end of the third postnatal week virtually all cells responsive to stationary gratings displayed orientation selectivity. There was always good agreement between the preferred orientations for stationary and drifting gratings. Even before two weeks of age, when responsive cells occurred only in small clusters, there was a clear tendency for neighbouring neurons to have similar or opposite preferred directions, just as in adult cats. By 2-3 weeks of age there were clear progressive shifts in stimulus preference along oblique or tangential tracks.(ABSTRACT TRUNCATED AT 400 WORDS)     

Selective sensitivity of the cat striate neurons to cruciform and angular figures of various orientations

Selectivity and invariability of tuning were studied in 51 neurons of the primary visual cortex (area 17); cruciform and angular figures (CF and AF, respectively) of different configurations and orientations were presented in their receptive fields. Twenty-three neurons, or 45% of the studied cells, demonstrated selective sensitivity to these figures. Their responses considerably (2.38±0.36 times, on average) increased, as compared with those evoked by presentation of a single bar of preferred orientation. In the examined group, 2 cells demonstrated sensitivity both to the CF and AF. A wide range of detector properties related to the CF and AF analysis was found in the analyzed neuronal population. Detectors of configuration of these figures are described. Selective sensitivity to the angle between branches of these figures was observed in 17 neurons, and responses of 2 neurons among them showed invariability to orientation of these figures. Four cells were selective for orientation and were insensitive to configuration, and 4 other cells showed no specific sensitivity to either of these properties, but were sensitive to the appearance of a CF itself in their receptive field (these cells were regarded as invariant detectors of crossing nodes). Data inconsistent with the hierarchic principle of detection of the above properties are presented. Possible mechanisms and functional significance of selective sensitivity of striate neurons to the CF and AF are discussed.Neirofiziologiya/Neurophysiology, Vol. 27, No. 5/6, pp. 403–412, September–December, 1995.     

Visual cortical detector neurons in the Siberian chipmunkEutamias sibiricus

Three functional classes of neurons are described in the visual cortex of the Siberian chipmunk: neurons not selective for direction of movement and orientation, neurons selective for movement in a particular direction, and neurons selective for orientation. Unselective and directionally-selective neurons were activated maximally at speeds of movement of 100–500 deg/sec or more, most orientation-selective neurons at speeds of 10–50 deg/sec. For all three classes of neurons clear correlation was observed between selectivity for velocity of movement and character of responses to presentation of stimuli stationary in the receptive field. With reference to this sign the neurons were divided into two groups: phasic (fast) and tonic (slow). Phasic (fast) neurons predominate in the visual cortex ofEutamias sibiricus.A. N. Severtsov Institute of Evolutionary Morphology and Ecology of Animals, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 16, No. 6, pp. 807–814, November–December, 1984.     

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.     

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.     

Postnatal development of functional properties of the visual cortical cells of area 18 in kittens raised with or without visual experience

866 units were recorded extracellularly in area 18 of anaesthetized and paralysed kittens from 13 to 66 days of age. The development of their receptive field properties was studied in normally (EN) and dark-reared (EO) kittens. In addition to orientation selective (S) and non-selective (NS) cells, we found a number of non-selective units whose receptive field was surrounded by a peripheral zone (NSp) where stationary stimuli were effective. In EN kittens, the orientation selectivity developed with age and concomitantly, NS and NSp cells disappeared. Ocular dominance distribution was also gradually modified from a contralateral monocular dominance at 13 days of age to an adult-like binocularity at 58 days. In EO kittens, the early orientation selectivity began to decrease at the 5th week. From then on, the process of despecification started and progressed until nearly all cells were NS. Absence of visual experience also delayed the development of mature binocularity. In 6 week old EO kittens, a 6 hrs. visual exposure induced a fast but uncomplete specification with decrease of both NS and NSp cells and a slight modification of the ocular dominance distribution. The comparison of these results with those obtained in area 17 shows that functional properties vary more slowly in area 18 than in area 17.     

Spontaneous symmetry-breaking energy functions and the emergence of orientation selective cortical cells

The mammalian visual cortex is comprised of hypercolumns of orientation selective cells. The developmental process by which cells are generated with receptive fields tuned to a variety of orientations has so far remained a mystery. We present a model for the production of orientation selective cells that requires no external stimuli and a minimum of input parameters. The process involves spontaneous symmetry-breaking in an energy function that governs the maturation of the cortical cells in a multi-layer network of Hebb-type feedforward neurons. An important feature is that the symmetry breaking occurs for each cell separately and is not due to global organizing effects. We present examples of receptive field profiles calculated with the symmetry-breaking procedure and note that the results seem robust and may be useful in the study of development in several types of cortical cells. The inclusion of long range lateral (intra-layer) correlations in the energy function could result in the development of cell groups with correlated preferred orientations that resemble the hypercolumns seen in the visual cortex.     

Horizontal organization of orientation-sensitive cells in primate visual cortex

In the visual cortex of the monkey the horizontal organization of the preferred orientations of orientation-selective cells follows two opposing rules:(1) neighbors tend to have similar orientation preferences, and(2) many different orientations are observed in a local region. We have described a classification for orientation maps based on the types of topological singularities and the spacing of these singularities relative to the cytochrome oxidase blobs. Using the orientation drift rate as a measure we have compared simulated orientation maps to published records of horizontal electrode recordings.     

猫前内侧上雪氏区视神经元对运动随机线条的反应

对于运动信息在脑内的加工,一种观点认为分两阶段进行,低级视皮层只对运动图形内部成分的取向进行调谐,高级视皮层整合低级视皮层的输入,对图形整体的运动方向敏感。用网格（plaid）作为刺激的实验表明,在较低级皮层区,细胞多表现为成分方向选择性（Component-motion Selectivity),即对刺激中的取向因素敏感：而较高视皮层的细胞多表现为整体方向选择性（Pattern-motion Selecitivity),对运动整体的方向敏感,从而支持运动信息加工的“两阶段”理论。实验中,用一系列运动随机线条刺激（random line patterns)。研究猫前内侧上雪氏区（Anteriormedial lateral suprasylvian area,AMLS)神经元的方向调谐特性。结果表明多数细胞为整体方向选择性,且随线长增加此类细胞比例下降,而成分方向选择性细胞的比例有所增加,呈现由整体方向选择性向中间类型（Unclassified),由中间类型向成分方向选择性变化的趋势,提示整体或成分方向选择性可能并非细胞的固有特性,而是可以随刺激取向因素的变化而改变的。     

Emergence of Functional Specificity in Balanced Networks with Synaptic Plasticity

In rodent visual cortex, synaptic connections between orientation-selective neurons are unspecific at the time of eye opening, and become to some degree functionally specific only later during development. An explanation for this two-stage process was proposed in terms of Hebbian plasticity based on visual experience that would eventually enhance connections between neurons with similar response features. For this to work, however, two conditions must be satisfied: First, orientation selective neuronal responses must exist before specific recurrent synaptic connections can be established. Second, Hebbian learning must be compatible with the recurrent network dynamics contributing to orientation selectivity, and the resulting specific connectivity must remain stable for unspecific background activity. Previous studies have mainly focused on very simple models, where the receptive fields of neurons were essentially determined by feedforward mechanisms, and where the recurrent network was small, lacking the complex recurrent dynamics of large-scale networks of excitatory and inhibitory neurons. Here we studied the emergence of functionally specific connectivity in large-scale recurrent networks with synaptic plasticity. Our results show that balanced random networks, which already exhibit highly selective responses at eye opening, can develop feature-specific connectivity if appropriate rules of synaptic plasticity are invoked within and between excitatory and inhibitory populations. If these conditions are met, the initial orientation selectivity guides the process of Hebbian learning and, as a result, functionally specific and a surplus of bidirectional connections emerge. Our results thus demonstrate the cooperation of synaptic plasticity and recurrent dynamics in large-scale functional networks with realistic receptive fields, highlight the role of inhibition as a critical element in this process, and paves the road for further computational studies of sensory processing in neocortical network models equipped with synaptic plasticity.     

Processing of Feature Selectivity in Cortical Networks with Specific Connectivity

Although non-specific at the onset of eye opening, networks in rodent visual cortex attain a non-random structure after eye opening, with a specific bias for connections between neurons of similar preferred orientations. As orientation selectivity is already present at eye opening, it remains unclear how this specificity in network wiring contributes to feature selectivity. Using large-scale inhibition-dominated spiking networks as a model, we show that feature-specific connectivity leads to a linear amplification of feedforward tuning, consistent with recent electrophysiological single-neuron recordings in rodent neocortex. Our results show that optimal amplification is achieved at an intermediate regime of specific connectivity. In this configuration a moderate increase of pairwise correlations is observed, consistent with recent experimental findings. Furthermore, we observed that feature-specific connectivity leads to the emergence of orientation-selective reverberating activity, and entails pattern completion in network responses. Our theoretical analysis provides a mechanistic understanding of subnetworks’ responses to visual stimuli, and casts light on the regime of operation of sensory cortices in the presence of specific connectivity.     

Electrophysiological investigation of effect of pulvinar stimulation of caudate nucleus neurons that react to visual stimulation

Responses of caudate neurons to electrical stimulation of the afferent input from thepulvinar thalamic nucleus and to visual stimuli of various orientations were studied extracellularly in awake chronic cats. Activation responses dominated among reactions of these neurons. The response latencies have ranged from 4 to 85 msec for units with primary activation and from 20 to 150 msec for inhibited ones. The values are indicative of both rapidly and slowly conducting afferent pathways. A possibility of monosynaptic transmission in thepulvinarcaudate projections is also revealed.Pulvinar stimulation is found to be efficient for a significant (more than 50 percent) number of caudate neurons responding to visual stimuli, including orientation-selective cells. The mode of influences from other structures of the visual system (optic tract, area 17, the Clare-Bishop area) on caudate neurons responding topulvinar stimulation is described. The data are discussed with respect to the possible role of cortical and subcortical projections of the visual system in the creation of sensory specific responses of the caudate nucleus.A. A. Bogomolets Physiology Institute, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 23, No. 5, pp. 520–529, September–October, 1991.     

Orientation selectivity of visual cortical neurons at different stimulus intensities in cats

Orientation selectivity of 24 neurons in area 17 of the visual cortex at different intensities of test bars of light, flashing against a constant light background in the center of the receptive field, was investigated in acute experiments on immobilized cats. Five neurons were invariant in orientation tuning to stimulus intensity (contrast): Although the magnitude of the response and acuteness of orientation selectivity were modified, preferential orientation was unchanged. More than half of the cells studied (13) were classed as noninvariant, for their preferential orientation was significantly shifted by 22–90° with a change in contrast. Small shifts of the peak of orientation selectivity, not statistically significant, were observed for the other neurons. Invariant neurons, unlike noninvariant, were characterized by preferential horizontal and vertical orientation, a lower frequency of spontaneous and evoked discharges, and the more frequent presence of receptive fields of simple type. The mechanisms of the change of orientation selectivity during contrast variation and also the different use of the two types of cells in orientation detection operations are discussed.     

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.     

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.