Correction to: Gamma-band-based dynamic functional connectivity in pigeon entopallium during sample presentation in a delayed color matching task.

[This corrects the article DOI: 10.1007/s11571-022-09916-w.].

Gamma-band-based dynamic functional connectivity in pigeon entopallium during sample presentation in a delayed color matching task.

Birds have developed visual cognitions, especially in discriminating colors due to their four types of cones in the retina. The entopallium of birds is thought to be involved in the processing of color information during visual cognition. However, there is a lack of understanding about how functional connectivity in the entopallium region of birds changes during color cognition, which is related to various input colors. We therefore trained pigeons to perform a delayed color matching task, in which two colors were randomly presented in sample stimuli phrases, and the neural activity at individual recording site and the gamma band functional connectivity among local population in entopallium during sample presentation were analyzed. Both gamma band energy and gamma band functional connectivity presented dynamics as the stimulus was presented and persisted. The response features in the early-stimulus phase were significantly different from those of baseline and the late-stimulus phase. Furthermore, gamma band energy showed significant differences between different colors during the early-stimulus phase, but the global feature of the gamma band functional network did not. Further decoding results showed that decoding accuracy was significantly enhanced by adding functional connectivity features, suggesting the global feature of the gamma band functional network did not directly contain color information, but was related to it. These results provided insight into information processing rules among local neuronal populations in the entopallium of birds during color cognition, which is important for their daily life.

Detection of a temporal salient object benefits from visual stimulus-specific adaptation in avian midbrain inhibitory nucleus.

Food and predators are the most noteworthy objects for the basic survival of wild animals, and both are often deviant in both spatial and temporal domains and quickly attract an animal's attention. Although stimulus-specific adaptation (SSA) is considered a potential neural basis of salient sound detection in the temporal domain, related research on visual SSA is limited and its relationship with temporal saliency is uncertain. The avian nucleus isthmi pars magnocellularis (Imc), which is central to midbrain selective attention network, is an ideal site to investigate the neural correlate of visual SSA and detection of a salient object in the time domain. Here, the constant order paradigm was applied to explore the visual SSA in the Imc of pigeons. The results showed that the firing rates of Imc neurons gradually decrease with repetitions of motion in the same direction, but recover when a motion in a deviant direction is presented, implying visual SSA to the direction of a moving object. Furthermore, enhanced response for an object moving in other directions that were not presented ever in the paradigm is also observed. To verify the neural mechanism underlying these phenomena, we introduced a neural computation model involving a recoverable synaptic change with a "center-surround" pattern to reproduce the visual SSA and temporal saliency for the moving object. These results suggest that the Imc produces visual SSA to motion direction, allowing temporal salient object detection, which may facilitate the detection of the sudden appearance of a predator.

Visual Responses to Moving and Flashed Stimuli of Neurons in Domestic Pigeon (Columba livia domestica) Optic Tectum.

Birds can rapidly and accurately detect moving objects for better survival in complex environments. This visual ability may be attributed to the response properties of neurons in the optic tectum. However, it is unknown how neurons in the optic tectum respond differently to moving objects compared to static ones. To address this question, neuronal activities were recorded from domestic pigeon (Columba livia domestica) optic tectum, responsible for orienting to moving objects, and the responses to moving and flashed stimuli were compared. An encoding model based on the Generalized Linear Model (GLM) framework was established to explain the difference in neuronal responses. The experimental results showed that the first spike latency to moving stimuli was smaller than that to flashed ones and firing rate was higher. The model further implied the faster and stronger response to a moving target result from spatiotemporal integration process, corresponding to the spatially sequential activation of tectal neurons and the accumulation of information in time. This study provides direct electrophysiological evidence about the different tectal neuron responses to moving objects and flashed ones. The findings of this investigation increase our understanding of the motion detection mechanism of tectal neurons.

Surround Modulation Properties of Tectal Neurons in Pigeons Characterized by Moving and Flashed Stimuli.

Surround modulation has been abundantly studied in several mammalian brain areas, including the primary visual cortex, lateral geniculate nucleus, and superior colliculus (SC), but systematic analysis is lacking in the avian optic tectum (OT, homologous to mammal SC). Here, multi-units were recorded from pigeon (Columba livia) OT, and responses to different sizes of moving, flashed squares, and bars were compared. The statistical results showed that most tectal neurons presented suppressed responses to larger stimuli in both moving and flashed paradigms, and suppression induced by flashed squares was comparable with moving ones when the stimuli center crossed the near classical receptive field (CRF) center, which corresponded to the full surrounding condition. Correspondingly, the suppression grew weaker when the stimuli center moved across the CRF border, equivalent to partially surrounding conditions. Similarly, suppression induced by full surrounding flashed squares was more intense than by partially surrounding flashed bars. These results suggest that inhibitions performed on tectal neurons appear to be full surrounding rather than locally lateral. This study enriches the understanding of surround modulation properties of avian tectum neurons and provides possible hypotheses about the arrangement of inhibitions from other nuclei, both of which are important for clarifying the mechanism of target detection against clutter background performed by avians.

Entrainment within neuronal response in optic tectum of pigeon to video displays.

The cathode ray tube (CRT) is a common and important tool that has been in use for decades, with which behavioral and visual neuroscientists deliver specific visual images generated by computers. Considering the operating principle of the CRT, the image it presents can flick at a constant rate, which will introduce distractions to the visual experiments on subjects with higher temporal resolutions. While this entrainment has been proved common in recordings of the primary visual cortex of mammals, it is uncertain whether it also exists in the intermediate to deep layers of pigeon's optic tectum, which is relevant to the spatial attention. Here, we present continuous visual stimuli with different refresh rates and luminances couples shown on a CRT to pigeons. The recordings in the intermediate to deep layers of optic tectum were significantly phase locking to the refresh of the CRT, and lower refresh rates of the CRT with higher brightness more likely introduced artifacts in electrophysiological recordings of pigeons, which may seriously damage their visual information perception.

Comparison of pop-out responses to luminance and motion contrasting stimuli of tectal neurons in pigeons.

The emergence of visual saliency has been widely studied in the primary visual cortex and the superior colliculus (SC) in mammals. There are fewer studies on the pop-out response to motion direction contrasting stimuli taken in the optic tectum (OT, homologous to mammalian SC), and these are mainly of owls and fish. To our knowledge the influence of spatial luminance has not been reported. In this study, we have recorded multi-units in pigeon OT and analyzed the tectal response to spatial luminance contrasting, motion direction contrasting, and contrasting stimuli from both feature dimensions. The comparison results showed that 1) the tectal response would pop-out in either motion direction or spatial luminance contrasting conditions. 2) The modulation from motion direction contrasting was independent of the temporal luminance variation of the visual stimuli. 3) When both spatial luminance and motion direction were salient, the response of tectal neurons was modulated more intensely by motion direction than by spatial luminance. The phenomenon was consistent with the innate instinct of avians in their natural environment. This study will help to deepen the understanding of mechanisms involved in bottom-up visual information processing and selective attention in the avian.

Natural image reconstruction on the basis of local field potential signals of pigeon optic tectum neurons.

Reconstruction of visual input through a neuron response helps to understand the information processing mechanism of the visual system. This paper uses the amplitude and phase characteristics of the local field potential signal in the pigeon optic tectum area to reconstruct the visual input from the neuron response data by means of local information accumulation using a linear inverse filter and a back propagation neural network algorithm. The reconstructed results show that the correlation between three reconstructed images and their corresponding stimulus images (tree branches, birds, and eyeglasses) was 0.8461±0.1135 for optimal values of number of channels, response duration, time from stimulus onset, and frequency band. This method of reconstructing the natural image from the pigeon optic tectum area neuron response signal can be applied to coding mechanism analysis of brightness and structural information in the visual system and to feedback from implantable visual prostheses.

Luminance information decoding on the basis of local field potential signals of pigeon optic tectum neurons.

Important aspects of brain information processing can be understood by examining decoding of visual stimuli from neuronal response signals. In this research, the luminance information is decoded from the local field potential signal in the optic tectum region of the pigeon. We designed a luminance visual stimulus model with transient flicker characteristics, recorded multichannel local field potential (LFP) signals using a microelectrode array, extracted LFP Fourier transform energy and phase features, constructed a multivariate linear inverse filter luminance information decoding algorithm, and evaluated decoding effects using a cross-correlation method. We found that LFP signal phase decoding of luminance information yielded better effects than amplitude decoding of luminance information. In the case of optimal frequency band, channels, delay time, and other parameters, the results of phase and amplitude codecoding could reach 0.94±0.02. Comparing the differences between neuronal spike decoding and LFP decoding, we found that LFP signal phase and amplitude codecoding resulted in luminance closer to that of the actual stimulus and required fewer decoding electrode channels.

Dynamic functional connectivity among neuronal population during modulation of extra-classical receptive field in primary visual cortex.

The neuronal activity evoked by stimuli confined in a receptive field can be modulated by surround stimuli of the extra-classical receptive field (eCRF). The surrounding modulation, hypothesized to be the basis of visual feature integration and figure-ground segregation, has drawn much attention in the field of neuroscience and engineering. However, most studies focused on surround modulation of individual neuronal response. In this study, we analyzed surround modulation of the population response recorded from rat primary visual cortex, and further investigated dynamic functional connectivity modulated by the surrounding stimuli. The functional connectivity was estimated using Granger causality (GC) and then determined by thresholding the p-matrix with different significance α values. Four scalar indexes were calculated to describe the functional connectivity of neuronal population: averaged connection strength (mGC), connection density (D), clustering coefficient (C) and path length (L). The statistical results from 5 rats showed that these network characteristics were dynamically changed during modulation of surrounding stimuli, which suggested that the neuronal population may connect in a dynamic way during modulation of eCRF. We further guessed that the neurons may happened to be organized in a more efficient way underlying surrounding modulation conditions, which helps to process larger images efficiently with the same number of neurons. This study provided new insights for a better understanding of the underlying neural mechanisms responsible for surround modulation.

Effect of the small-world structure on encoding performance in the primary visual cortex: an electrophysiological and modeling analysis.

The biological networks have been widely reported to present small-world properties. However, the effects of small-world network structure on population's encoding performance remain poorly understood. To address this issue, we applied a small world-based framework to quantify and analyze the response dynamics of cell assemblies recorded from rat primary visual cortex, and further established a population encoding model based on small world-based generalized linear model (SW-GLM). The electrophysiological experimental results show that the small world-based population responses to different topological shapes present significant variation (t test, p < 0.01; effect size: Hedge's g > 0.8), while no significant variation was found for control networks without considering their spatial connectivity (t test, p > 0.05; effect size: Hedge's g < 0.5). Furthermore, the numerical experimental results show that the predicted response under SW-GLM is more accurate and reliable compared to the control model without small-world structure, and the decoding performance is also improved about 10 % by taking the small-world structure into account. The above results suggest the important role of the small-world neural structure in encoding visual information for the neural population by providing electrophysiological and theoretical evidence, respectively. The study helps greatly to well understand the population encoding mechanisms of visual cortex.

A small-world-based population encoding model of the primary visual cortex.

A wide range of evidence has shown that information encoding performed by the visual cortex involves complex activities of neuronal populations. However, the effects of the neuronal connectivity structure on the population's encoding performance remain poorly understood. In this paper, a small-world-based population encoding model of the primary visual cortex (V1) is established on the basis of the generalized linear model (GLM) to describe the computation of the neuronal population. The model mainly consists of three sets of filters, including a spatiotemporal stimulus filter, a post-spike history filter, and a set of coupled filters with the coupling neurons organizing as a small-world network. The parameters of the model were fitted with neuronal data of the rat V1 recorded with a micro-electrode array. Compared to the traditional GLM, without considering the small-world structure of the neuronal population, the proposed model was proved to produce more accurate spiking response to grating stimuli and enhance the capability of the neuronal population to carry information. The comparison results proved the validity of the proposed model and further suggest the role of small-world structure in the encoding performance of local populations in V1, which provides new insights for understanding encoding mechanisms of a small scale population in visual system.

An information integration model of the primary visual cortex under grating stimulations.

During the course of information processing, a visual system extracts characteristic information of the visual image and integrates the spatial and temporal visual information simultaneously. In this study, we investigate the integration effect of neurons in the primary visual cortex (V1 area) under the grating stimulation. First, an information integration model was established based on the receptive field properties of the extracted features of the visual images features, the interaction between neurons and the nonlinear integration of those neurons. Then the neuropsychological experiments were designed both to provide parameters for the model and to verify its effect. The experimental results with factual visual image were largely consistent with the model's forecast output. This demonstrates that our model can truly reflect the integration effect of the primary visual system when being subjected to grating stimulations with different orientations. Our results indicate the primary visual system integrates the visual information in the following manner: it first extracts visual information through different types of receptive field, and then its neurons interact with each other in a non-linear manner, finally the neurons fire spikes recorded as responses to the visual stimulus.