V1 Neurons In Cats Research Articles

Top-down influence of areas 21a and 7 differently affects the surround suppression of V1 neurons in cats.

Surround suppression (SS) is a phenomenon whereby a neuron's response to stimuli in its central receptive field (cRF) is suppressed by stimuli extending to its surround receptive field (sRF). Recent evidence show that top-down influence contributed to SS in the primary visual cortex (V1). However, how the top-down influence from different high-level cortical areas affects SS in V1 has not been comparatively observed. The present study applied transcranial direct current stimulation (tDCS) to modulate the neural activity in area 21a (A21a) and area 7 (A7) of cats and examined the changes in the cRF and sRF of V1 neurons. We found that anode-tDCS at A21a reduced V1 neurons' cRF size and increased their response to visual stimuli in cRF, causing an improved SS strength. By contrast, anode-tDCS at A7 increased V1 neurons' sRF size and response to stimuli in cRF, also enhancing the SS. Modeling analysis based on DoG function indicated that the increased SS of V1 neurons after anode-tDCS at A21a could be explained by a center-only mechanism, whereas the improved SS after anode-tDCS at A7 might be mediated through a combined center and surround mechanism. In conclusion, A21a and A7 may affect the SS of V1 neurons through different mechanisms.

Mechanisms of Surround Suppression Effect on the Contrast Sensitivity of V1 Neurons in Cats.

Surround suppression (SS) is a phenomenon that a neuron's response to visual stimuli within the classical receptive field (cRF) is suppressed by a concurrent stimulation in the surrounding receptive field (sRF) beyond the cRF. Studies show that SS affects neuronal response contrast sensitivity in the primary visual cortex (V1). However, the underlying mechanisms remain unclear. Here, we examined SS effect on the contrast sensitivity of cats' V1 neurons with different preferred SFs using external noise-masked visual stimuli and perceptual template model (PTM) analysis at the system level. The contrast sensitivity was evaluated by the inverted threshold contrast of neurons in response to circular gratings of different contrasts in the cRF with or without an annular grating in the sRF. Our results showed that SS significantly reduced the contrast sensitivity of cats' V1 neurons. The SS-induced reduction of contrast sensitivity was not correlated with SS strength but was dependent on neuron's preferred SF, with a larger reduction for neurons with low preferred SFs than those with high preferred SFs. PTM analysis of threshold versus external noise contrast (TvC) functions indicated that SS decreased contrast sensitivity by increasing both the internal additive noise and impact of external noise for neurons with low preferred SFs, but improving only internal additive noise for neurons with high preferred SFs. Furthermore, the SS effect on the contrast-response function of low- and high-SF neurons also exhibited different mechanisms in contrast gain and response gain. Collectively, these results suggest that the mechanisms of SS effect on neuronal contrast sensitivity may depend on neuronal populations with different SFs.

Top-down influence affects the response adaptation of V1 neurons in cats

The visual system lowers its perceptual sensitivity to a prolonged presentation of the same visual signal. This brain plasticity, called visual adaptation, is generally attributed to the response adaptation of neurons in the visual cortex. Although well-studied in the neurons of the primary visual cortex (V1), the contribution of high-level visual cortical regions to the response adaptation of V1 neurons is unclear. In the present study, we measured the response adaptation strength of V1 neurons before and after the top-down influence of the area 21a (A21a), a higher-order visual cortex homologous to the primate V4 area, was modulated with a noninvasive tool of transcranial direct current stimulation (tDCS). Our results showed that the response adaptation of V1 neurons enhanced significantly after applying anode (a-) tDCS in A21a when compared with that before a-tDCS, whereas the response adaptation of V1 neurons weakened after cathode (c-) tDCS relative to before c-tDCS in A21a. By contrast, sham (s-) tDCS in A21a had no significant impact on the response adaptation of V1 neurons. Further analysis indicated that a-tDCS in A21a significantly increased both the initial response (IR) of V1 neurons to the first several (five) trails of visual stimulation and the plateau response (PR) to the prolonged visual stimulation; the increase in PR was lower than in IR, which caused an enhancement in response adaptation. Conversely, c-tDCS significantly decreased both IR and PR of V1 neurons; the reduction in PR was smaller than in IR, which resulted in a weakness in response adaptation. Furthermore, the tDCS-induced changes of V1 neurons in response and response adaptation could recover after tDCS effect vanished, but did not occur after the neuronal activity in A21a was silenced by electrolytic lesions. These results suggest that the top-down influence of A21a may alter the response adaptation of V1 neurons through activation of local inhibitory circuitry, which enhances network inhibition in the V1 area upon an increased top-down input, weakens inhibition upon a decreased top-down input, and thus maintains homeostasis of V1 neurons in response to the long-presenting visual signals.

Contrast coding in the primary visual cortex depends on temporal contexts.

Contrast response function in the primary visual cortex (V1) has long been described as following a sigmoid curve. However, this is mainly based on measuring neural responses to drifting contrast grating in a stable stimulation, a model that does not consider the effects of motion or length of stimulus presentation. During natural viewing, the visual system can obtain sufficient information for identifying the shapes defined by contrast from a single glance; acquiring greater knowledge of the neuronal response properties to contrast in such a short timescale is necessary to understand the underlying mechanisms. We investigated responses of cat V1 neurons to contrast presented by static grating for 40ms without pause compared to drifting grating presented continuously for 2000ms. The neuronal response to transiently presented contrast could be well described by a linear function. Further examination of the effects of motion and presentation duration on contrast responses demonstrated that motion increased response sensitivity in the low-contrast range, while brief presentation increased response sensitivity in the high-contrast range. Motion and prolonged presentation (adaptation) together resulted in an asymptotic sigmoid curve with a saturation response in the high-contrast range. These results suggest that motion mainly enhance the neural response sensitivity to low-contrast objects, while short and rapid presentation mainly enhance the neural sensitivity to high-contrast stimulus. Our findings indicate that multiple factors influence the properties of contrast response functions, suggesting that V1 neuron contrast coding is flexible and depends on the temporal contexts.

Comparative effects of adaptation on layers II-III and V-VI neurons in cat V1.

V1 is fundamentally grouped into columns that descend from layers II-III to V-VI. Neurons inherent to visual cortex are capable of adapting to changes in the incoming stimuli that drive the cortical plasticity. A principle feature called orientation selectivity can be altered by the presentation of non-optimal stimulus called 'adapter'. When triggered, LGN cells impinge upon layer IV and further relay the information to deeper layers via layers II-III. Using different adaptation protocols, neuronal plasticity can be investigated. Superficial neurons in area V1 are well acknowledged to exhibit attraction and repulsion by shifting their tuning peaks when challenged by a non-optimal stimulus called 'adapter'. Layers V-VI neurons in spite of partnering layers II-III neurons in cortical computation have not been explored simultaneously toward adaptation. We believe that adaptation not only affects cells specific to a layer but modifies the entire column. In this study, through simultaneous multiunit recordings in anesthetized cats using a multichannel depth electrode, we show for the first time how layers V-VI neurons (1000-1200μm) along with layers II-III neurons (300-500μm) exhibit plasticity in response to adaptation. Our results demonstrate that superficial and deeper layer neurons react synonymously toward adapter by exhibiting similar behavioral properties. The neurons displayed similar amplitude of shift and maintained equivalent sharpness of Gaussian tuning peaks before and the following adaptation. It appears that a similar mechanism, belonging to all layers, is responsible for the analog outcome of the neurons' experience with adapter.

Silent suppressive surrounds and optimal spatial frequencies of single neurons in cat V1

The receptive fields of the clear majority of neurons in the primary visual cortex (V1) of cats contain silent surround regions beyond the classical receptive field (CRF). When stimulated on their own, the silent surround regions do not generate action potentials (spikes); instead, they modulate (and usually partially suppress) spike responses to stimuli presented in the CRF. In the present study, we subdivided our sample of single V1 neurons recorded from anesthetized cats into two distinct categories: surround-suppressive (SS) cells and surround-non-suppressive (SN) cells. Consistent with previous reports, we found a negative correlation between the size of the CRF and the optimal spatial frequency (SF) of circular patches of achromatic gratings presented in the cells’ receptive fields. Furthermore, we found a positive correlation between the strength of the surround suppression and the optimal spatial frequency of the achromatic gratings presented in the cells’ receptive fields. The correlation between the strength of surround suppression and the optimal spatial frequency was stronger in neurons with suppressive regions located in the so-called ‘end’ zones. The functional implications of these relationships are discussed.

Neurons in cat V1 show significant clustering by degree of tuning.

Neighboring neurons in cat primary visual cortex (V1) have similar preferred orientation, direction, and spatial frequency. How diverse is their degree of tuning for these properties? To address this, we used single-tetrode recordings to simultaneously isolate multiple cells at single recording sites and record their responses to flashed and drifting gratings of multiple orientations, spatial frequencies, and, for drifting gratings, directions. Orientation tuning width, spatial frequency tuning width, and direction selectivity index (DSI) all showed significant clustering: pairs of neurons recorded at a single site were significantly more similar in each of these properties than pairs of neurons from different recording sites. The strength of the clustering was generally modest. The percent decrease in the median difference between pairs from the same site, relative to pairs from different sites, was as follows: for different measures of orientation tuning width, 29-35% (drifting gratings) or 15-25% (flashed gratings); for DSI, 24%; and for spatial frequency tuning width measured in octaves, 8% (drifting gratings). The clusterings of all of these measures were much weaker than for preferred orientation (68% decrease) but comparable to that seen for preferred spatial frequency in response to drifting gratings (26%). For the above properties, little difference in clustering was seen between simple and complex cells. In studies of spatial frequency tuning to flashed gratings, strong clustering was seen among simple-cell pairs for tuning width (70% decrease) and preferred frequency (71% decrease), whereas no clustering was seen for simple-complex or complex-complex cell pairs.

Contrast-dependent OFF-dominance in cat primary visual cortex facilitates discrimination of stimuli with natural contrast statistics.

Both theoretical and experimental studies suggest that response properties in the visual system are shaped by signals in the natural environment. Recent studies showed that, in the primary visual cortex (V1), neurons preferring light decrements (OFF stimuli) outnumber those preferring light increments (ON stimuli). However, it is not clear whether the OFF-dominance in V1 neurons is related to the contrast statistics in natural images. By analysing the distribution of negative and positive contrasts in natural images at several spatial scales, we showed that optimal coding of the natural contrast signals would lead to a contrast-dependent OFF-dominant response, with a stronger degree of OFF-dominance at a higher contrast. Using bright and dark stimuli at various contrast levels to measure the receptive fields of neurons in cat V1, we found an increasing degree of OFF-dominance of the neuronal population as the contrast was increased. By modeling receptive fields exhibiting OFF- and ON-dominance, we found that contrast-dependent OFF-dominance facilitated the discrimination of stimuli with natural contrast distribution. Thus, by matching contrast-dependent OFF-dominance to the statistics of contrast distribution in natural images, V1 neurons may better discriminate contrast information in natural scenes.

The spatial summation characteristics of three categories of V1 neurons differing in non-classical receptive field modulation properties

The spatial summation of excitation and inhibition determines the final output of neurons in the cat V1. To characterize the spatial extent of the excitatory classical receptive field (CRF) and inhibitory non-classical receptive field (nCRF) areas, we examined the spatial summation properties of 169 neurons in cat V1 at high (20-90%) and low (5-15%) stimulus contrasts. Three categories were classified based on the difference in the contrast dependency of the surround suppression. We discovered that the three categories significantly differed in CRF size, peak firing rate, and the proportion of simple/complex cell number. The classification of simple and complex cells was determined at both high and low contrasts. While the majority of V1 neurons had stable modulation ratios in their responses, 10 cells (6.2%) in our sample crossed the classification boundary under different stimulus contrasts. No significant difference was found in the size of the CRF between simple and complex cells. Further comparisons in each category determined that the CRFs for complex cells were significantly larger than those for simple cells in category type I neurons, with no significant differences between simple and complex cells in category type II and type III neurons. In addition, complex cells have higher peak firing rates than simple cells.

The Detection of Orientation Continuity and Discontinuity by Cat V1 Neurons

The orientation tuning properties of the non-classical receptive field (nCRF or “surround”) relative to that of the classical receptive field (CRF or “center”) were tested for 119 neurons in the cat primary visual cortex (V1). The stimuli were concentric sinusoidal gratings generated on a computer screen with the center grating presented at an optimal orientation to stimulate the CRF and the surround grating with variable orientations stimulating the nCRF. Based on the presence or absence of surround suppression, measured by the suppression index at the optimal orientation of the cells, we subdivided the neurons into two categories: surround-suppressive (SS) cells and surround-non-suppressive (SN) cells. When stimulated with an optimally oriented grating centered at CRF, the SS cells showed increasing surround suppression when the stimulus grating was expanded beyond the boundary of the CRF, whereas for the SN cells, expanding the stimulus grating beyond the CRF caused no suppression of the center response. For the SS cells, strength of surround suppression was dependent on the relative orientation between CRF and nCRF: an iso-orientation grating over center and surround at the optimal orientation evoked strongest suppression and a surround grating orthogonal to the optimal center grating evoked the weakest or no suppression. By contrast, the SN cells showed slightly increased responses to an iso-orientation stimulus and weak suppression to orthogonal surround gratings. This iso-/orthogonal orientation selectivity between center and surround was analyzed in 22 SN and 97 SS cells, and for the two types of cells, the different center-surround orientation selectivity was dependent on the suppressive strength of the cells. We conclude that SN cells are suitable to detect orientation continuity or similarity between CRF and nCRF, whereas the SS cells are adapted to the detection of discontinuity or differences in orientation between CRF and nCRF.

Adaptation maintains population homeostasis in primary visual cortex

Sensory systems exhibit mechanisms of neural adaptation, which adjust neuronal activity based on recent stimulus history. In primary visual cortex (V1), in particular, adaptation controls the responsiveness of individual neurons and shifts their visual selectivity. What benefits does adaptation confer to a neuronal population? We measured adaptation in the responses of populations of cat V1 neurons to stimulus ensembles with markedly different statistics of stimulus orientation. We found that adaptation serves two homeostatic goals. First, it maintains equality in the time-averaged responses across the population. Second, it maintains independence in selectivity across the population. Adaptation scales and distorts population activity according to a simple multiplicative rule that depends on neuronal orientation preference and on stimulus orientation. We conclude that adaptation in V1 acts as a mechanism of homeostasis, enforcing a tendency towards equality and independence in neural activity across the population.

GABA increases stimulus selectivity of neurons in primary visual cortices of cats chronically treated with morphine

Chronic exposure to opiates leads to maladaptive changes in various functions of the mammalian brain, including properties of neuronal response in the visual pathway. In the present study, we used multibarreled microelectrodes to study the effects of electrophoretic application of GABA or the GABAA receptor antagonist bicuculline on the properties of individual V1 neurons in cats which were chronically treated with morphine (MTCs) or saline (STCs). The results showed that the application of either GABA or bicuculline significantly altered spontaneous activity as well as orientation selectivity and signal-to-noise ratios of visually evoked responses in both MTCs and STCs. While administration of bicuculline exerted a much stronger effect on neuronal responses of V1 neurons of the STCs, administration of GABA resulted in improved visual function mainly in MTCs. Most importantly, GABA-treated cells in area V1 of the MTCs displayed similar responses to those in STCs. These results are consistent with the idea that: (1) there is a decrease in GABA-mediated inhibition in area V1 of cats exposed chronically to morphine, and (2) this decrease contributes strongly to the apparent degradation of neuronal function observed in animals exposed chronically to morphine.

Chronic morphine exposure affects contrast response functions of V1 neurons in cats

Opiates disrupt neural functions in many brain areas, including visual cortex. Previous studies have indicated substantial changes of many neuronal response properties induced by chronic morphine exposure in the visual information processing system. However, it remains unclear whether neuronal contrast coding is also affected. To investigate this issue, we measured the contrast response functions (CRFs) of V1 neurons in chronic morphine-treated and saline-treated cats by using extra-cellular single-unit recording techniques. Our results indicated significantly lower contrast sensitivity in morphine-treated cats than in saline-treated cats and V1 neurons in morphine-treated cats exhibited enhanced maximum visual responses, higher baseline responses and lower signal-to-noise ratios compared with saline-treated cats. These findings provide some neurobiological evidence for the morphine-mediated degenerations of the visual cortex, which could underlie the opiate-induced deficits in visual function.

Prediction of spatiotemporal patterns of neural activity using a higher-order Markov representation of instantaneous pairwise maximum entropy model

Maximum entropy (MaxEnt) models have been suggested to fit the spatiotemporal patterns of simultaneously observed neuronal spike trains. To build such models, the distribution, px(X), needs to be determined, where X is a sequence of neural patterns formed from the vector X1,…,Xn for n time samples, where Xi is a sample of the spike train of a population at time i . Each neural pattern itself is a binary sequence, for which one represents a spike, and zero otherwise. MaxEnt models are constructed by matching the moments between neuronal constituents with the analogous empirical estimates from the distribution px(X). MaxEnt models that incorporate the first and second order interactions among neurons, also referred to as the instantaneous pairwise MaxEnt model or the Ising model, are expressed as where the individual, hi, and coupling, Jij, terms are parameters associated with the first and second order interactions, respectively, and Z is a normalization factor to insure . This model was shown to be effective in representing almost 90 percent of the information in small populations (less than 20 neurons) [1,2]. The main disadvantage of this model, however, is that it ignores the temporal correlation that represents the effect of the history of spiking activity on the current population state. Extending the width of neural patterns has been proposed as a method to incorporate spiking history. It destroys, however, the information in precise spike timings [3]. To incorporate the history term without compromising information in spike times, a higher-order Markov model is constructed in which patterns from different time samples are added. An example first-order Markov representation is expressed as where and are the individual, and , and are the coupling terms among the neuronal elements. This spatiotemporal model is more general than the representation introduced in Marre et al [4] to account for history terms , but at the expense of increasing the number of parameters. We evaluated the performance of the extended MaxEnt model in predicting the activity pattern of cat V1 neurons in response to drifting grating stimuli. A population of 21 neurons was recorded with 5 tetrodes. We compared the prediction power of this model with the instantaneous pairwise MaxEnt model, as well as the independent model. We show that the iterative scaling algorithm makes the extended model converge faster compared to [4], and also reduces the Kullback-Leibler divergence between the estimated and true distributions by 20 percent. Taken together, these results suggest the importance of accounting for temporal correlations in predicting the spatiotemporal patterns.

Perceptual Learning Improves Contrast Sensitivity of V1 Neurons in Cats

Perceptual learning has been documented in adult humans over a wide range of tasks. Although the often-observed specificity of learning is generally interpreted as evidence for training-induced plasticity in early cortical areas, physiological evidence for training-induced changes in early visual cortical areas is modest, despite reports of learning-induced changes of cortical activities in fMRI studies. To reveal the physiological bases of perceptual learning, we combined psychophysical measurements with extracellular single-unit recording under anesthetized preparations and examined the effects of training in grating orientation identification on both perceptual and neuronal contrast sensitivity functions of cats. We have found that training significantly improved perceptual contrast sensitivity of the cats to gratings with spatial frequencies near the "trained" spatial frequency, with stronger effects in the trained eye. Consistent with behavioral assessments, the mean contrast sensitivity of neurons recorded from V1 of the trained cats was significantly higher than that of neurons recorded from the untrained cats. Furthermore, in the trained cats, the contrast sensitivity of V1 neurons responding preferentially to stimuli presented via the trained eyes was significantly greater than that of neurons responding preferentially to stimuli presented via the "untrained" eyes. The effect was confined to the trained spatial frequencies. In both trained and untrained cats, the neuronal contrast sensitivity functions derived from the contrast sensitivity of the individual neurons were highly correlated with behaviorally determined perceptual contrast sensitivity functions. We suggest that training-induced neuronal contrast gain in area V1 underlies behaviorally determined perceptual contrast sensitivity improvements.

Dynamics of orientation tuning in cat V1 neurons depend on location within layers and orientation maps

Analysis of the timecourse of the orientation tuning of responses in primary visual cortex (V1) can provide insight into the circuitry underlying tuning. Several studies have examined the temporal evolution of orientation selectivity in V1 neurons, but there is no consensus regarding the stability of orientation tuning properties over the timecourse of the response. We have used reverse-correlation analysis of the responses to dynamic grating stimuli to re-examine this issue in cat V1 neurons. We find that the preferred orientation and tuning curve shape are stable in the majority of neurons; however, more than forty percent of cells show a significant change in either preferred orientation or tuning width between early and late portions of the response. To examine the influence of the local cortical circuit connectivity, we analyzed the timecourse of responses as a function of receptive field type, laminar position, and orientation map position. Simple cells are more selective, and reach peak selectivity earlier, than complex cells. There are pronounced laminar differences in the timing of responses: middle layer cells respond faster, deep layer cells have prolonged response decay, and superficial cells are intermediate in timing. The average timing of neurons near and far from pinwheel centers is similar, but there is more variability in the timecourse of responses near pinwheel centers. This result was reproduced in an established network model of V1 operating in a regime of balanced excitatory and inhibitory recurrent connections, confirming previous results. Thus, response dynamics of cortical neurons reflect circuitry based on both vertical and horizontal location within cortical networks.

Temporal properties of surround suppression in cat primary visual cortex

The responses of neurons in primary visual cortex (V1) are suppressed by stimuli presented in the region surrounding the receptive field. There is debate as to whether this surround suppression is due to intracortical inhibition, is inherited from lateral geniculate nucleus (LGN), or is due to a combination of these factors. The mechanisms involved in surround suppression may differ from those involved in suppression within the receptive field, which is called cross-orientation suppression. To compare surround suppression to cross-orientation suppression, and to help elucidate its underlying mechanisms, we studied its temporal properties in anesthetized and paralyzed cats. We first measured the temporal resolution of suppression. While cat LGN neurons respond vigorously to drift rates up to 30 Hz, most cat V1 neurons stop responding above 10-15 Hz. If suppression originated in cortical responses, therefore, it should disappear above such drift rates. In a majority of cells, surround suppression decreased substantially when surround drift rate was above approximately 15 Hz, but some neurons demonstrated suppression with surround drift rates as high as 21 Hz. We then measured the susceptibility of suppression to contrast adaptation. Contrast adaptation reduces responses of cortical neurons much more than those of LGN neurons. If suppression originated in cortical responses, therefore, it should be reduced by adaptation. Consistent with this hypothesis, we found that prolonged exposure to the surround stimulus decreased the strength of surround suppression. The results of both experiments differ markedly from those previously obtained in a study of cross-orientation suppression, whose temporal properties were found to resemble those of LGN neurons. Our results provide further evidence that these two forms of suppression are due to different mechanisms. Surround suppression can be explained by a mixture of thalamic and cortical influences. It could also arise entirely from intracortical inhibition, but only if inhibitory neurons respond to somewhat higher drift rates than most cortical cells.

Standing Waves and Traveling Waves Distinguish Two Circuits in Visual Cortex

The visual cortex represents stimuli through the activity of neuronal populations. We measured the evolution of this activity in space and time by imaging voltage-sensitive dyes in cat area V1. Contrast-reversing stimuli elicit responses that oscillate at twice the stimulus frequency, indicating that signals originate mostly in complex cells. These responses stand clear of the noise, whose amplitude decreases as 1/frequency, and yield high-resolution maps of orientation preference and retinotopy. We first show how these maps are combined to yield the responses to focal, oriented stimuli. We then study the evolution of the oscillating activity in space and time. In the orientation domain, it is a standing wave. In the spatial domain, it is a traveling wave propagating at 0.2-0.5 m/s. These different dynamics indicate a fundamental distinction in the circuits underlying selectivity for position and orientation, two key stimulus attributes.

Contrast-dependency of spatial summation property of neurons in cat V1 and LGN

Contrast-dependency of spatial summation property of neurons in cat V1 and LGN

Chronic morphine exposure affects the visual response properties of V1 neurons in cat

Chronic opiate exposure leads to maladaptive changes in brain function. In view of the localization of opiate receptors in mammalian visual system, chronic opiate exposure is likely to affect the visual responses properties of V1 neurons. Using in vivo single-unit recording, we here showed that chronic morphine treatment resulted in the functional abnormality of primary visual cortical cells. When compared with saline-treated (as control) cats, cortical neurons in morphine-treated cats exhibited higher spontaneous activity, lower signal-to-noise ratios and weaker orientation and direction selectivity. However, re-exposure with morphine could significantly improve the function of V1 neurons in morphine-treated cats. These findings demonstrated that chronic morphine treatment could significantly degrade the response properties of V1 neurons and may lead to a function dependence on morphine in visual cortical cells.